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Marine Biological Laboratory Library

Woods Hole, Massachusetts

Plant Morphogenesis

McGRAW-HILL PUBLICATIONS IN
THE BOTANICAL SCIENCES

Edmund W. Sinnott, Consulting Editor

Arnold An Introduction to Paleobotany

Curtis and Clark An Introduction to Plant Physiology

Eames Morphology of Vascular Plants

Eames and MacDaniels An Introduction to Plant Anatomv

Haupt An Introduction to Botany

Haupt Laboratory Manual of Elementary Botany

Haupt Plant Morphology

Hill Economic Botany

Hill, Overholts, Popp, and Grove Botany

Johansen Plant Microtechnique

Kramer Plant and Soil Water Relationships

Kramer and Kozlowski Physiology of Trees

Lilly and Barnett Physiology of the Fungi

Maheshwari An Introduction to the Embryology of the Angiosperms

Miller Plant Physiology

Pool Flowers and Flowering Plants

Sharp Fundamentals of Cytology

Sinnott Plant Morphogenesis

Sinnott, Dunn, and Dobzhansky Principles of Genetics

Sinnott and Wilson Botany: Principles and Problems

Smith Cryptogamic Botany

Vol. I. Algae and Fungi

Vol. II. Bryophytes and Pteridophytes
Smith The Fresh-water Algae of the United States
Swingle Textbook of Systematic Botany
Weaver and Clements Plant Ecology

There are also the related series of McGraw-Hill Publications in the Zoological
Sciences, of which E. J. Boell is Consulting Editor, and in the Agricultural
Sciences, of which R. A. Brink is Consulting Editor.

5 5^
ex

PLANT MORPHOGENESIS

Edmund W. Sinnott

STERLING PROFESSOR OF BOTANY, EMERITUS
YALE UNIVERSITY

McGRAW-HILL BOOK COMPANY, INC.

New York Toronto London

1960

PLANT MORPHOGENESIS

Copyright © I960 by the McGraw-Hill Book Company, Inc. Printed in
the United States of America. All rights reserved. This book, or parts
thereof, may not be reproduced in any form without permission of
the publishers. Library of Congress Catalog Card Number 60-6984

II

57585

To the Memory of
HERMANN VOCHTING

PIONEER IN PLANT MORPHOGENESIS

Preface

The present volume is an outcome of the author's concern with the
problems of plant morphogenesis for over 40 years. During that time he
has followed the literature in this field with some care and has seen the
subject grow from a relatively minor aspect of botanical science to a much
wider recognition as one of the central concerns of biology. New tech-
niques and fields of work have developed in it over the years, and its con-
tacts with other sciences have grown much closer. Few discussions of the
subject as a whole have appeared, however, and no extensive synthesis of
its content has been made. The book that follows is an attempt to do
this and to organize the field of plant morphogenesis so that it can be
studied and taught as an integrated discipline.

This is no simple task, and botanists will doubtless disagree as to
how it should be accomplished. The method adopted here is first to
discuss plant growth, emphasizing descriptive and experimental work
on cells and meristems. This is followed by a survey of the various
categories of morphogenetic phenomena— correlation, polarity, differen-
tiation, and the rest— mobilizing under each the major facts that are
known about it and the work of the chief contributors to the field. This
portion is largely descriptive and serves to pose problems for considera-
tion. It is followed by a third section that discusses the major factors
operative in the control of plant development and is primarily concerned
with physiological and genetic questions. It touches these broad sub-
jects, however, only so far as they are concerned with morphogenetic
problems and then only in a brief and rather summary fashion. Too
frequent repetition of material in the three sections is avoided by numer-
ous cross references.

Throughout the book no attempt is made to go at all completely into
most of the topics. From the vast literature on subjects of concern to
plant morphogenesis, however, a considerable bibliography has been
compiled by means of which the reader is introduced to the more im-
portant publications where detailed information may be found. In this
bibliography many important earlier papers of general and historical
interest have been cited, but emphasis has been placed on relatively
recent ones. Where available, review papers have been cited. There is

vii

Preface viii

some unavoidable repetition of material but this has been reduced by fre-
quent use of cross references. The book is designed primarily for reference,
though by means of such a presentation more teachers may be encouraged
to offer courses in this field.

To many individuals the author is indebted for good counsel and as-
sistance in many ways. His thanks are due especially to his former col-
league Dr. Robert Bloch, who for some years collaborated with him in
the present project. Professor Ralph H. Wetmore has read a portion
of the manuscript and made valuable suggestions, as has the author's
colleague Prof. Arthur W. Galston for the chapter on Growth Substances.
Various problems have been discussed with many others, and to all
these the author is grateful. For the positions taken on particular issues
and the opinions expressed, however, he assumes full responsibility, as
he does for any errors of fact, attribution, or citation which may appear
and which are hard to eliminate completely from a book of this sort.

For several years Mrs. Charlotte Reeder has assisted in compiling
information, in abstracting papers, and, through her genius for orderli-
ness, in keeping the project from bogging down under the sheer weight
of its material. To her the author is greatly indebted. Other assistants have
been associated with the work from time to time, and their help is
here thankfully acknowledged.

For financial assistance, and especially for grants from the Eugene
Higgins Trust, the author wishes to express his gratitude to Yale Uni-
versity and its Provost, Edgar S. Furniss.

The illustrations have been taken from the work of many individuals.
In every case the source from which they come has been acknowledged
in the caption, but the author here offers his further thanks for the privi-
lege of using them. For specific figures he is indebted to the editors of
Endeavour, the authorities of the Boyce Thompson Institute for Plant
Research, the Department of Plant Pathology of the University of Wis-
consin, Triarch Botanical Products, the W. Atlee Burpee Company, Dr.
G. R. Zundel, and Rutherford Piatt.

This book has been a long time in the making. It proved to be such a
time-consuming task that the author was not able to bring it to com-
pletion until his retirement from academic duties a few years ago. He
hopes that this long period of ripening may have improved its quality
and increased its value to those who use it.

Edmund W. Sinnott

Contents

Preface vii

Chapter 1. Introduction 1

PART ONE. GROWTH

Chapter 2. Growth in General H

Chapter 3. The Cellular Basis of Growth 23

Cell division — Cell size — Experimental studies — Plane of cell division -
Cell shape.

Chapter 4. Meristems 55

Apical meristems — The shoot apex — Experimental studies on the shoot
apex — The root apex — Lateral meristems — Meristems in determinate
growth.

PART TWO. THE PHENOMENA OF MORPHOGENESIS

Chapter 5. Correlation 95

Physiological correlations — Genetic correlations.

Chapter 6. Polarity 116

Polarity as expressed in external structure — Polarity as expressed in internal
structure — Polarity in isolated cells — Polarity in plasmodia and coenocytes
- Physiological manifestations of polarity - Polarity and developmental
pattern.

Chapter 7. Symmetry 147

Inorganic and organic symmetries — Radial symmetry — Bilateral symmetry —
Dorsi ventral symmetry — Development of symmetry — Symmetry and form.

Chapter 8. Differentiation 181

Growth and differentiation — Differentiation as expressed in structure — Ex-
ternal differentiation - Internal differentiation - Differentiation during
ontogeny —Differentiation in relation to environment — Physiological dif-
ferentiation — Differentiation without growth.

Chapter 9. Regeneration -30

Regeneration in the lower plants — Regeneration in the higher plants —
Reconstitution — Restoration — Reproductive regeneration.

ix

x Contents

Chapter 10. Tissue Mixtures 258

Stock-scion interrelations — Chimeras — Somatic mutations.

Chapter 11. Abnormal Growth 275

Abnormal development of organs — Production of new types of organized
structures — Amorphous structures.

PART THREE. MORPHOGENETIC FACTORS

Chapter 12. Introduction to Factors 303

Chapter 13. Light 308

Intensity of light — Quality of light - Duration of light — Relation to other
factors.

Chapter 14. Water 324

Xeromorphy — Experimental work — Effect of the transpiration stream.

Chapter 15. Temperature 337

Thermoperiodism — Vernalization — Other temperature effects.

Chapter 16. Various Physical Factors 345

Tension — Compression — Bending and swaying — Ultrasonics — Gravity —
Tissue tension — Absolute size — Bioelectrical factors.

Chapter 17. Chemical Factors in General 363

Elements — More complex substances.
Chapter 18. Growth Substances 374

Types of growth substances — Growth substances and plant growth — Growth
substances and correlation — Growth substances and the determination of
structure — Growth substances and internal differentiation — Other formative
effects — Mechanism of action.

Chapter 19. Genetic Factors 415

Genes — Cytoplasm — Chromosomes.
Chapter 20. Organization 449

Bibliography 461

Name Index 527

Subject Index 538

CHAPTER 1

Introduction

A study of the form and structure of living things has a perennial interest,
not only for biologists but for everyone. It appeals to the aesthetic in us.
Philosophers have been concerned with it since the time of Plato, who
distinguished between matter and form and believed that spirit was
inherent in the latter. Most naturalists owe their first interest in animals
and plants to the almost infinite variety of forms which these display
and which make possible their identification. Although morphology
(Goethe's term), the science that deals with form, has lost the command-
ing position it once held, following the advent of physiology and the
disciplines that connect biology with the physical sciences, it still remains
the foundation for any thorough knowledge of living things. We must
all be morphologists before we can be biologists of any other sort.

In a famous sentence Charles Darwin paid tribute to morphology by
calling it the very soul of natural history. How curious it is, he remarked,
that the hand of a man and of a mole, the leg of a horse, the paddle of
a porpoise, and the wing of a bat, despite the great difference in their
functions, should all be formed on the same basic pattern. Specific
bodily forms and structures had long been used to distinguish the major
groups of plants and animals and were also the basis of that "idealistic"
morphology which so intrigued Goethe and the biologists of his day.
Darwin, however, saw in the science of comparative morphology some-
thing far more significant— a strong support for the doctrine of evolution,
for only by assuming a common ancestry for each of the groups that show
a common pattern of bodily form could these similarities be explained.
Form was widely acknowledged as the most distinctive character on
which the phylogenetic relationships of organisms could be based and a
truly natural system of classification constructed.

The study of organic form, however, poses a problem deeper still, and
one concerned with the very character of life itself. From the facts of
embryology it is evident that in the development of an individual there
occurs as regular a progression of changes in form as has taken place in
evolution. Indeed, the theory of recapitulation called attention to some

1

2 Introduction

interesting parallels between the two. In a study of form in organic de-
velopment the biologist has the great advantage of dealing with a process
that is going on under his eyes and is thus susceptible to experimental at-
tack. An organism is not static but displays a continually unfolding
series of changes during its life. It has been well described as a "slice of
space-time." As knowledge about organic development increased, biol-
ogists came to realize that development is not only an orderly unfolding
but that in this process all parts of the growing individual are closely
correlated with the rest so that an organized and integrated system, the
organism, is produced. Differences in rate of growth and in character of
the structures developed are evident, but these various changes do not
occur independently. They keep in step with one another. When form
changes, it does so in a regular and predictable fashion. Still more sig-
nificant, the experimental embryologist is able to show not only that these
relationships are to be seen in normal development but that they per-
sistently tend to be restored if development is disturbed. An organism is
an essentially fluid system through which matter is continually moving
but which nevertheless maintains a constant form much as does a candle
flame or a waterfall.

In the various physiological activities of the living organism there is
evident the same coordination so manifest in bodily development. What
occurs in an individual is not simply a series of unrelated metabolic
processes, but these are tied together in such a precise fashion that the
life of the organism is maintained in a steady state. Just as the normal
progress of development tends to be restored if it is disturbed, so the
normal state of physiological organization tends to be maintained at a
constant level. This regulatory process of homeostasis is recognized as
one of the major facts of physiology.

Organic form is thus the visible expression of an inner relatedness
characteristic of life at every level. This can be most simply designated
as biological organization and is the most important problem that con-
fronts students of the life sciences. Form may be thought of not only as
the soul of natural history in the sense that it provides a measure of evo-
lutionary relationship but as the soul of all biology, since it provides the
most obvious and easily accessible manifestation of the basic character-
istic of life.

Biological organization is to be seen most distinctly in bodily develop-
ment. It is obvious that, to produce an individual with a specific form
and structure, growth must be more rapid in some directions than in
others and must form tissues and organs of different character in different
places. Embryology has shown how precisely the activities in one part of
the developing individual are related to those in every other part. Few
happenings in nature are as fascinating to watch as the unfolding and

Introduction 3

growth of a leaf or a flower from a tiny primordium, especially when this
is speeded up to our eyes by time-lapse photography. Every step is co-
ordinated with all the others as though a craftsman were molding it ac-
cording to a plan. Within the whole, the cells and other subordinate
parts do not develop independently but all are knit together into an
organized system.

How all this is accomplished and a specifically formed organism pro-
duced is not yet understood, although specific parts of the process are
now well known. Most metabolic activities are yielding to biochemical
analysis; students of gene action find that specific substances are produced
by specific genes, and the nucleic acids, with their remarkable properties,
are recognized as being at the very foundation of life itself. How all the
various metabolic and developmental activities are related in such an
orderly fashion, however, and proceed without interference or confusion
so that, step by step, an organism is produced poses a problem of a very
different kind. Relations, not chemical changes, are the facts to be ex-
plained. The problem must be approached experimentally but one should
recognize that this may require the development of techniques and ideas
not yet explored.

The biological science concerned with this dynamic and causal aspect
of organic form is evidently different from either morphology, physi-
ology, or embryology, though partaking of all three. It deserves a
name of its own. The Germans usually call it Entwicklungsmechanik, a
name proposed by Wilhelm Roux. This great zoologist is looked upon as
the father of the science of zoological morphogenesis. He founded the
Archiv fiir Entwicklungsmechanik der Organismen, a journal which now
occupies 16 feet of library shelf and contains a vast amount of material,
chiefly on the animal side. Elsewhere this science has often been termed
experimental morphology or experimental embryology. Rritish biologists
sometimes refer to it as causal morphology. In recent years it has generally
been given a more appropriate name than any of these— morphogenesis.
The derivation of this word is obvious— the origin of form. Who first used
it is not certainly known but Ernst Haeckel employed the cognate form
morphogeny (Morphogenie) in 1859. Some have employed this term in
a strictly descriptive sense, essentially as synonymous with developmental
morphology. More commonly and properly, however, it includes, in addi-
tion to a discussion of purely descriptive facts as to the origin of form, a
study of the results of experimentally controlled development and an
analysis of the effects of the various factors, external and internal, that
determine how the development of form proceeds. In other words, it
attempts to get at the underlying formativeness in the development of
organisms and especially to reach an understanding of the basic fact of
which form is the most obvious manifestation— biological organization

4 Introduction

itself. It is in these senses that the term morphogenesis will be used in
the present volume.

Each of the major biological subsciences is intimately related to the
others. One cannot study genetics apart from physiology, for example,
or physiology from morphology, or taxonomy and evolution from all
these. It may well be maintained, however, that morphogenesis, since it is
concerned with the most distinctive aspect of life— organization— is the
crossroads where all the highways of biological exploration tend to con-
verge. Its subject matter deals with some of the most elusive and intract-
able phenomena in science, but it is here that the greatest discoveries of
the future are likely to be made. These will be significant not only
for biological problems but for many others that man faces. Even
philosophy, long concerned with problems of form, is still gaining
from this source fresh insights into its chief task, an understanding of
life.

More study has been given to morphogenetic problems with animals
than with plants. A great advantage of animal material is that in many
groups the egg is discharged into water and the embryo develops there,
at least through its earlier stages, and is thus easily accessible for obser-
vation and experiment. Among higher plants, on the contrary, all the early
development of the embryo takes place within the ovule, surrounded by
many layers of tissue and relatively inaccessible. The result has been that,
save for rather special material like the egg of Fucus which can be
treated much like that of an animal, very little morphogenetic work has
been done on plant embryos. Modern techniques, however, by which
it is possible to grow the embryos of some higher plants to maturity in
culture, are making the science of experimental plant embryology a more
fruitful one.

Workers with plants have a number of advantages, however. In plants,
permanently embryonic regions, the meristems, are available for study.
At the tip of shoot and root and in the cambial layers these are inde-
terminate and produce new plant structures almost indefinitely. Such
meristems are usually numerous or extensive on the same plant so that
ample material for the study of development, identical in genetic con-
stitution, is available. Growth and differentiation in the development of
a plant are thus continuing processes and not limited to a single and
often brief life cycle.

Organs such as leaves, flowers, and fruits, which are determinate in
growth, pass through a cycle closely comparable to that of individual
animals, and morphogenetic problems can also often profitably be studied
in them. The fact that they are usually produced in abundance on a
single plant is a further advantage, for here the investigator need not be
concerned about genetic diversity in his material but can study strictly

Introduction 5

comparable organic forms under a wide range of environmental condi-
tions.

Another important difference between botanical and zoological ma-
terial is concerned with the behavior of individual cells during develop-
ment. In animal embryos many cells are relatively free to move about so
that certain morphogenetic changes are due to movements of cells or cell
groups rather than to differences in relative growth. In plants above the
simplest types, on the contrary, cells are almost always attached firmly
to their neighbors so that morphogenetic movements have no part in de-
velopment. Changes of form are the result of differences in the location
or orientation of cell divisions or in the size or the shape to which the
individual cells grow. This makes the study of morphogenetic problems
somewhat simpler in plants because development leaves a record of its
course in the structure of the growing system itself.

Most plant cells have rather firm walls as compared with animal cells,
and the structures that they produce are therefore not as soft and plastic
as in many animals. A plant part tends to hold its form rather well and
can thus be measured more easily and accurately. Its anatomical struc-
ture is also less fluid. Certain organs, such as woody stems and hard-
shelled fruits, retain their form when dead and dry and can then be kept
for study without the necessity for special preservative treatment.

Plant material is generally more tractable than that of animals, is easily
grown, and lends itself readily to experiment. Because of their stationary
habit, plants are more susceptible to changes in environmental influences,
notably water and light, than are animals, and the morphogenetic effects
of such factors may be studied more easily in them.

The organization of a plant, too, is much looser than that of most ani-
mals. The individual organism is less sharply marked and specific, and
its powers of regeneration are far greater. Its structural plan is simpler,
for the stationary habit of most plants renders unnecessary several organ
systems found in animals, notably a digestive tract, excretory organs,
musculature, and a nervous system. Morphogenetic problems can there-
fore be studied in plants uncomplicated by the physiological complexi-
ties inseparable from animal life. The absence of a nervous system, which
has such an important role in animal development, is of particular ad-
vantage, for developmental processes in plants are under the control of
relatively unspecialized protoplasm, and they may thus be studied most
directly and at their simplest level. There is no reason to believe that
the fundamental phenomena of the development of form are not as
manifest in these relatively simple systems as in the more complex ones
of animals.

What is now called morphogenesis came first into prominence in the
late decades of the nineteenth century after the early enthusiasm over

6 Introduction

the idea of evolution had given place to a more sober realization that it
did not provide a solution for all the problems about living things. The
list of men working primarily with animal material includes some of the
most brilliant names in the science of zoology. In plant morphogenesis,
most of those who made important early contributions were chiefly en-
gaged in other fields, especially morphology, physiology, and pathology.
Here are remembered the classical studies of Hanstein on meristems and
their derivatives, of Winkler on chimeras, of Haberlandt on plant hor-
mones, of Kiister on abnormal growth, of Klebs on the effects of the
environment, of Goebel on the general area to which he gave the name
of organography, and many others.

It is to Herman Vochting, however, long Professor of Botany at the
University of Bonn, that botanists owe the first thoughtful discussion of
such problems as polarity, differentiation, and regeneration. His "Organ-
bildung im Pflanzenreich," published in 1878, is a classic and may be
said to have founded a new field of botanical investigation. It deserves
to be read by all students of development even today. About the turn of
the century the zoologist Hans Driesch stated his often-quoted aphorism,
"The fate of a cell is a function of its position," which in a few words
sums up a central fact of biological organization. What few botanists
know is that Vochting, in a book written 20 years earlier, said the same
thing in almost the same words.1 Other botanists also made important
contributions here. Much of the work of men such as van Tieghem, Jost,
Sachs, Pfeffer, Schwendener, and Strasburger was on problems that we
should now call morphogenetic.

Most studies in plant morphogenesis have been made with vascular
plants— pteridophytes, gymnosperms, and angiosperms. It should be
remembered, however, that many of these problems can be approached
more directly through work on the lower ones. Polarity, for example, is
manifest in its simplest form in some of the filamentous algae. The very
beginnings of differentiation are to be seen in the lower thallophytes.
Almost every cell in some of the bryophytes may easily be induced to
regenerate. The problem of the development of form is nowhere posed
more directly than in the formation of the remarkable fruiting bodies of
some of the myxomycetes and of the higher fungi. These more primitive
plants are proving to be ideal material for the study of many problems
in physiology and genetics, and although they have been rather neglected
in morphogenesis, they offer abundant opportunities for fruitful work
in this field.

The science of plant morphogenesis has never received a comprehen-

1 Die jeweilig zu verrichtende Function einer Zelle wird in erster Linie durch den
morphologischen Ort bestimmt, den sie an der Lebenseinheit einnimmt. Organ-
bildung im Pflanzenreich, 1878, p. 241.)

Introduction <

sive formulation. To bring together in a single volume a discussion of
the various phenomena that distinguish it and of the factors that have
been found to affect the development of plants, together with a bibliog-
raphy of some of the most important publications dealing with the sub-
ject, should help to give it recognition as a distinctive botanical disci-
pline. To attempt this is the purpose of the present volume.

Morphogenesis is such an immense subject, however, covering most of
the territory of biology, that to organize its facts and its problems in a
logical and reasonably compact fashion is a matter of much difficulty.
The method used here is to divide the subject into three parts. First is
presented a brief discussion of plant growth as a necessary introduction
to morphogenesis proper, placing particular emphasis on its cellular basis
and on the activities of the meristems. The remaining subject matter is
then divided into two sections: first, the various phenomena of plant
morphogenesis and the more important studies that have been made on
them and, second, a brief account of the morphogenetic factors that have
been found to affect the development and form of plants. In the first
there are chapters on Correlation, Polarity, Symmetry, Differentiation,
Regeneration, Tissue Mixtures, and Abnormal Growth. In the second are
discussed the effects of light, water, temperature, and other physical fac-
tors; inorganic and organic substances (especially growth substances);
and finally the various genetic factors. There is a concluding chapter on
the problem of Biological Organization.

At the end of the book is a selected list of references to some of the
more important books and papers on the subject. This obviously must be
far from complete since the literature is enormous and scattered through
most of the fields of botany. An attempt has been made to include, both
in text and references, some of the important early work, not alone for
its intrinsic but also its historical value. In the more rapidly advancing
fields, where many of the results from older studies have now been
superseded, only a relatively few of the earlier papers are mentioned,
and there is considerable representation of recent work. Aside from
bringing the subject up to date, these later papers through their
bibliographies will give the student a means of entry into the literature
of a given field. Opportunities for further research, particularly in areas
now less popular than in the past, are so numerous that the author has
felt justified in calling attention to some of them from time to time.

The problem of deciding which pieces of work to include in a discus-
sion of this sort and which to omit has been very difficult. Among those
mentioned there are doubtless some that will be regarded by many read-
ers as relatively unimportant. The omission of others will be criticized.
It is hoped, however, that the papers chosen will provide a fair picture of
accomplishment in plant morphogenesis. A considerable number of

g Introduction

review papers are cited which help summarize results in particular fields.
No one person, and certainly not the present writer, is competent to give
a thoroughly informed and authoritative judgment on the relative worth
of the wide variety of investigations here discussed. It is hoped, how-
ever, that one service of the book will be to introduce its readers to the
subjects of these studies even though in some cases a piece of work can
be given little more than mention.

Since there is no sharp line between morphogenesis and its neighbor-
ing fields of morphology, physiology, genetics, and the chemical and
physical sciences, much of the advance in it will doubtless be made, as
in the past, by men whose chief concern is with one of these other disci-
plines; but as morphogenesis becomes better organized and as more op-
portunities for training and research in it are offered by our colleges and
universities, there will be more students whose primary interests are
directed to it. More than other biological sciences, perhaps, morpho-
genesis will need to maintain close contact with a wide variety of other
fields, for few can hope to be competent in its entire area. To develop
this comprehensive subject fruitfully will require the active cooperation
of many sciences, and by this means the morphogenetic point of view
can thus help to integrate all of biology.

PART ONE

Growth

CHAPTER 2

Growth in General

The process of organic development, in which are posed the chief prob-
lems for the science of morphogenesis, occurs in the great majority of
cases as an accompaniment of the process of growth. The association be-
tween these two activities is not an invariable one, for there are a few
organisms in which growth is completed before development and dif-
ferentiation are finished, but far more commonly the form and structure
of a living thing change while it grows. Knowledge about growth is
therefore necessary for an understanding of development, and any dis-
cussion of morphogenetic problems in plants should be preceded by a
discussion of plant growth in general. This is the purpose of the first
few chapters of the present volume.

Definition of Growth. The term "growth" has been variously defined
by biologists. For some (Hammett, 1936) 1 it includes not only increase
but also the accompanying phenomena of progressive differentiation.
Most regard this definition as too inclusive and would limit it in one re-
spect or another. Since much of the increase in volume is brought about
merely by gain in amount of water, increase in dry weight might seem to
be the best measure of growth, but sprouting seeds kept in the dark will
"grow" into large, etiolated seedlings through intake of water though
their dry weight actually decreases. In one sense these sprouts have
grown, but in another they have not. The fundamental fact in all growth,
of course, is the self-multiplication of living material, a process of much
biological significance. For this reason, growth might best be defined
as increase in amount of protoplasm. Even if we could agree, however,
as to what constitutes protoplasm (whether vacuoles, for example, are
parts of it), it would be impossible, as a practical matter, to measure
this. Furthermore, in every organism, and particularly in every plant,
there is much material ( such as cell walls and starch grains ) which is an
integral part of the organism but which presumably is not living, and it
seems illogical not to regard increase in such material as part of growth.

1 For bibliographic information concerning books and papers referred to in the text,
see Bibliography, pp. 461 ff.

11

12 Growth

In most multicellular organisms growth is accomplished chiefly by cell
multiplication, and to some observers this process seems to be an essen-
tial part of growth. In the cleavage of many animal eggs and in similar
processes in plants, however, there is a great increase in cell number
but none in the actual material which constitutes the "growing" structure,
and whether such cellular increase should be regarded as growth is a
question. In the case of the female gametophyte in the megaspore of
Selaginella, and especially of the young embryo which develops there,
growth of an organized structure by cell multiplication certainly occurs,
but at the expense of material stored in the spore. Where an entire mass
is cut up into cells, as in the development of a male gametophyte in a
microspore, one may doubt as to whether this should be called growth
at all. What definition of growth one adopts depends on the particular
problem with which he is concerned.

For the study of morphogenesis, the most important aspect of growth
is the permanent increase in volume of an organ or organism, regardless
of how it is accomplished, and this is the sense in which the term will
here be used. The ultimate problem-the self-multiplication of living ma-
terial-is one primarily for the student of physiology and reproduction,
but it is the gross and geometrical result of such growth with which
morphogenesis is chiefly concerned.

Growth in Plants. In most plants, the process of growth is different in
one important respect from that in animals. The typical mature plant
cell is surrounded by a relatively stout cellulose wall which under ordi-
nary conditions prevents any further cell division or growth save in ex-
ceptional circumstances. The cells are rather firmly cemented together
and thus unable to move about or migrate. Plant tissues are therefore in-
capable of growth and renewal except through the activity of thin-walled,
relatively undifferentiated embryonic regions, or meristems, where occur
the divisions that produce new cells and the changes by which these at-
tain their final size. These meristems are rather sharply localized. In plant
axes where growth is continuous and often indeterminate, growth in
length is controlled chiefly by the activity of meristems at the tip of each
root or stem. The older portion of the axis, having once attained maturity,
does not make further growth in length. A tree increases in height only
at the tips of its twigs and not elsewhere. In the stems of some mono-
cotyledons, however, growth of the stem in length may continue for a time
by the activity of intercalary meristematic regions at the base of each
internode. Perennially growing roots and stems increase in thickness
through the activity of a lateral meristem, or cambium, situated between
xylem and phloem, by which the growth of both these tissues is accom-
plished. There are other sharply localized meristematic regions, such as
the phellogen, or cork cambium.

Growth in General 13

In organs which (unlike the axes) have a limited or determinate
growth, such as leaves, flowers, or fruits, the meristems are usually not
localized but are diffuse, so that the whole organ, or most of it, is grow-
ing throughout and not at any particular point. Such structures have a
growth cycle of their own, much as does an animal body, and when they
reach maturity all their tissues stop growing and there is no embryonic
region set apart by which further growth may be accomplished.

Graphical and Mathematical Analysis of Growth. One of the most
obvious facts which a study of growth reveals is that it does not proceed
at a constant rate. Many factors influence this rate, but under normal
and favorable conditions a growing organ or organism undergoes a
characteristic course of increase, first growing slowly, then with increas-
ing speed, and finally slowing down again until growth stops entirely.

It is possible to picture this graphically in various ways. In Table 2-1
are presented the data for the increase in diameter of a gourd fruit from
its early state as a small ovary primordium until maturity. If these diam-
eters are plotted as ordinates against time in days, the growth curve
shown in Fig. 2-1 results. This is an S-shaped, or sigmoid, curve and is
typical of most growing organisms, both plant and animal, though it is
subject to much variation. It presents the changing size of the growing
organ throughout its course but does not give a very clear picture of the
changing amounts of daily growth. If daily increments are plotted in the
same way against time, the curve in Fig. 2-2 results. These increments
are small at first, then progressively larger, and then smaller again.

Such graphical representations of growth have long interested biol-
ogists and mathematicians, who have endeavored to analyze them in
mathematical terms and thus obtain clues as to the character of the
growth process itself. In many cases such analyses have proved helpful
in providing a simple statement of the course of growth, but there are so
many variables involved in growing organisms that one can hardly expect
to express their increase completely in an equation.

Table 2-1. Growth of a Gourd Fruit from a Small Primordium to Maturity

Diameter, Diameter,

Date mm. Date mm.

July 30 2.4 Aug. 9 30.0

" 31 3.1 " 10 35.2

Aug. 1 3.9 " 11 40.0

" 2 5.1 " 12 43.8

" 3 6.5 "13 46.0

" 4 8.4 " 14 47.0

" 5 11.0 " 15 47.5

" 6 14.0 " 16 47.9

" 7 18.0 " 17 48.0

" 8 23.5 " 18 48.0

14

Growth

Time in days
Fig. 2-1. Sigmoid growth curve. Fruit diameters in Table 2-1 plotted against time in
days.

The first period of growth, in the most typical instances, shows the
regular acceleration of a mass increasing, so to speak, at compound in-
terest, the growth during any period being a constant proportion or per-
centage of the amount already present, and the "interest" being com-
pounded continuously. In Table 2-1 it will be observed that for the first 10
days the increase in diameter each day is an approximately constant
proportion of the diameter of the day before, though the daily incre-

Time in days
Fig. 2-2. Graph of daily increments in fruit diameter, from Table 2-1.

Growth in General 15

ments themselves continually increase. The equation for "compound-
interest" growth is the familiar one

?i = P0ert

where Pi is the size at any time t; P0 the size at the beginning of growth;
e the base of the natural logarithms, 2.18; and r the rate of growth (in-
terest or exponential rate). This can be expressed, by using common
logarithms, as

logP1 = logP0 + loge(rt)

To find r for the first 10 days in Table 2-1, we substitute in this equa-
tion as follows:

1.4771 = 0.3802 + 0.4343 X lOr

1.4771 - 0.3802

r =

= 0.25

10 X 0.4343

This is the rate of diameter increase per day at which, continuously com-
pounded, this fruit is growing, expressed as a per cent of its previous
growth. If the logarithms of the successive size of gourd fruits in Table 2-1
are plotted against time (or the data plotted on semilogarithmic paper)
the graph in Fig. 2-3 results. Here the growth for the first 10 days is seen

E
E

O

Time in days

Fig. 2-3. Curve of the logarithm of fruit diameter in Table 2-1 plotted against time in
days.

16 Growth

to fall along an essentially straight line, showing that the fruit was growing
at a constant exponential rate. The slope of the line is a measure of this

rate.

The resemblance between such organic growth and compound-interest
increase has long been noted, but it was particularly emphasized by
V. H. Blackman (1919). He proposed the term efficiency index for the
"interest rate" in such growth. That living things in the early stages of
their development should grow in this way is not surprising, for if
embryonic material is self-multiplicative, the increase per unit of time
should be proportional to the growing mass.

To explain the rest of the growth curve is more difficult. Evidently
growth cannot proceed in any organism at a continually accelerating rate,
if for no other reason than that building material would soon be used up.
The gradual slowing down and final cessation of growth are far too
regular a process, however, to be due to mere exhaustion of materials. A
plant or animal provided with a superabundance of nutrients will rarely
exceed the size characteristic for its species. Each organ or body has a
specific growth cycle through which it passes, and the second part of
this cycle, in which growth is falling off in rate, is much like the first part
in reverse, so that the entire growth curve thus tends to be symmetrical.
In such a case the periodic increments form a curve (Fig. 2-2) which
much resembles the so-called normal curve, or curve of probability. This
relationship has been observed and discussed by various workers,
especially Pearl and his school (1915), but any causal relationship be-
tween the two types of curves is not easy to see.

The similarity between growth and the chemical phenomenon of auto-
catalysis, in which the products of a catalytic process accelerate the
process itself, has been noted by many observers. Robertson ( 1923 ) and
his followers have attempted to analyze the whole growth curve as a sim-
ple ( monomolecular ) autocatalytic reaction by which an enzyme breaks
down a mass of substrate. During the first part of the process, growth will
therefore accelerate, but when the amount of substrate becomes seriously
reduced, rate of growth will also be reduced, and when the substrate is
exhausted, growth will cease.

Robertson derives the typical sigmoid curve from the equation for
autocatalysis:

l^A^x = k{t~tl}

where x is the volume of the organic structure (amount grown) at any
time t; A the final size of the structure; U the time at which it attains half
its final size; and k is a specific growth constant, or exponential growth
rate.

Growth in General

17

The essential feature of this growth equation is that the rate of growth
is determined by the amount of growth which is yet to occur. This im-
plies that the final size is established at the start of growth, either by the
amount of available building material or in some other way. If only one
"master reaction" were concerned, the course of growth might well fol-
low Robertson's equation, but there are evidently many substances in-
volved and many processes going on simultaneously which probably
make the growth process too complex to be analyzed by any one reac-
tion.

Growth curves for certain organs and organisms fit Robertson's equa-
tion fairly well (Reed, 1927). For others the fit is not so close. In a struc-
ture which in its growth fits the equation perfectly, the rate of exponential

E

-3i

Fig. 2-4. Growth of large and of small fruits in Cucurhita. Log of fruit volume plotted
against time in days. Early growth in all races is at a constant rate (straight line) the
slope of which here is the same in large and small races. Solid circle, time of flowering.
( From Sinnott. )

growth will constantly decrease (since it is proportional to the amount
yet to grow, which is decreasing) so that the curve of the logarithm of
size against time will be convex from the beginning. When the rate is
relatively low the difference between this and the straight line of con-
stant exponential growth at first is not great, since the absolute amount
of growth in these early time intervals is slight. In many growth curves,
such as those of fruits of various races of cucurbits presented by Sinnott
( 1945b ) , the early growth is at a constant exponential rate and shows no
indications of convexity of line (Fig. 2-4). Furthermore, large and small
fruits which are here compared grow at essentially the same rates but
for very different durations. Under these conditions, Robertson's formula
would require that the length of time between half size and maturity

18 Growth

should be the same for all races, but actually in the small-fruited races
this period is much less than in the large-fruited ones.

The mathematical analysis of growth involves many complexities and
has been developed in much greater detail than is possible in the present
brief discussion. For a fuller treatment of this subject the reader is re-
ferred to the work of Pearl ( 1939 ) , D'Arcy Thompson ( 1942 ) , Erickson
(1956), and others.

It is evident that no single mathematical statement will express all types
of growth nor perhaps any of them with complete exactness. Growth is
a very complex process involving many variables, and it is not to be ex-
pected that it can be compressed into a single equation. Even if it could
be, this would not tell us a great deal for, as D'Arcy Thompson well says,
a formula "which gives a mere coincidence of numbers may be of little
use or none, unless it go some way to depict and explain the modus
operandi of growth." That growth under some conditions proceeds as at
compound interest and at others like an autocatalytic process is of some
importance in providing a clue to the mechanism of growth, but so far
mathematical analysis has added comparatively little to our understand-
ing of the fundamental character of growth itself. For this we must look
to a more concrete study of the growth process in terms of genetics, bio-
chemistry, and physiology.

Variation in Growth. Many structures do not show the simple sigmoid
growth discussed in the preceding section. Just as the smooth course of
growth in mammals is interrupted by birth and by puberty, it is modified
in various ways in plants. In fruits of peach and cherry, for example,
Tukey and Young (1939) and others have shown that after these struc-
tures are partly grown there is then for some time no increase in volume.
This is the period in which the endocarp, or "stone," is being formed.
Later the fruit begins to enlarge again, so that a curve like that in Fig.
2-5 results. Duncan and Curtis ( 1942 ) have shown a somewhat similar
growth curve in the fruit of certain orchids where one epoch of growth is
associated with meiosis and a later one with seed maturity. In vegetative
structures, aside from annual periods, there are also sometimes discon-
tinuous cycles, as in the pear shoots studied by Reed ( 1927 ) , where there
may be three such in one season. The dandelion scape shows a some-
what similar growth pattern (Chao, 1947). It is rapid during flower de-
velopment, much slower after the flower opens, and then accelerates
greatly as the fruit becomes mature.

Borriss ( 1934a ) reports that etiolated stipes of Coprinus show a marked
periodicity of growth with maxima 3.5 to 4.5 hours apart. This and similar
cases may be manifestations of endogenous rhythms such as have fre-
quently been reported in other processes ( p. 322 ) .

Growth in General

19

In many plants, particularly herbaceous ones, growth is not evenly
distributed throughout the length of the stem. Thus in tobacco (Wolf,
1947) and in maize (Heimsch and Stafford, 1952) the internodes are
progressively longer from the base to about half way up the axis and
then are progressively shorter to the apex. The distribution of growth in
a developing leaf blade also shows local differences (Avery, 1935). Many
alterations in form arise from local changes in growth.

Determinate and Indeterminate Growth. In most animals, growth is
part of a definite life cycle and produces a determinate structure. In many
plants, on the other hand, the growth of the body is essentially indetermi-

A |0

FULL BLOOM

DAYS

Fig. 2-5. Intermittent curves of growth of a cherry fruit from flowering to maturity.
( From L. D. Tukey. )

nate and, within certain limits, may go on indefinitely through the activity
of terminal and lateral meristems. Even such theoretically unlimited
growth (such as that of a tree in height or a vine in length), however,
usually reaches a limit and in its growth follows a curve which is S-
shaped. In some plants, such as the sunflower and most grasses, height
is not indeterminate but is limited by a terminal inflorescence, and stem
growth in such cases is typically sigmoid. Lateral organs, such as leaves
and fruits, which do not grow by localized meristems have still more
definite growth cycles and are quite comparable to single animal indi-
viduals and show similar growth curves. Examples of these are fruits
(Fig. 2-1), leaves (Wolf, 1947), and ovules and embryos (Rietsma et al,

20

Growth

1955 ) . Plants provide examples of all types of growth from that in loosely
organized, essentially indeterminate structures to highly organized and
sharply determinate ones and therefore are particularly good material
for a study of the mechanism by which growth, presumably free and
continuous in primitive organisms, becomes controlled and molded into
a definite cycle or pattern. Such cyclical, controlled growth is one mani-
festation of the general phenomenon of biological organization.

Growth and Size. The size that an organism attains is often an im-
portant factor in determining the character of its development, and size
is intimately related to growth. Differences in ultimate size may be due

cm.

8

7

- / /

6

/ /

5

-

4

/

3

- / /

2

1

0

Fig. 2-6. Diagram of growth of stipe and pileus of the common mushroom, Agaricus
campestris. Homologous points are connected by lines. Growth is most active in the
region intermediate between base and apex. (From Bonner, Kane, and Levey.)

to differences in rate or in duration of growth or in both of these. Little
is known in plants as to the relation between growth and size. The in-
creased size of heterozygous corn plants is apparently associated with a
higher growth rate (Whaley, 1950), and this may be true rather gen-
erally for size difference in indeterminate structures. In determinate
ones such as the fruit, however, rate may not be important. The great size
differences between small-fruited and large-fruited cucurbits of the same
species studied by Sinnott (1945b) are due in almost every case to differ-
ences in duration of growth, for growth rate is essentially the same in all
of them ( Fig. 2-4 ) . This difference in duration applies to all recognizable

Growth in General 21

parts of the growth cycle— from primordium to flowering, from flowering
to the end of exponential growth, and from this point to growth cessation.

Growth in plants has usually been studied in the higher forms because
of their generally larger size and the greater ease with which observations
can be made upon them. Some lower plants, however, offer good oppor-
tunities for growth studies. Borriss (1934a) found that growth is not
evenly distributed in the sporophore stalk of Coprinus but is progressively
more rapid toward the apex. This has been confirmed by Bonner, Kane,
and Levey (1956; Fig. 2-6), who find that, after the early stage, growth is
accomplished chiefly by elongation of the cells of the hyphae. By dusting
the tips of young sporangiophores of Phycomyces with starch grains and
recording changes photographically, Castle ( 1958 ) has analyzed the
distribution of growth here, both as to longitudinal and circumferential
increase. The ratio between these two components is not constant but
changes with location on the sporangiophore.

Brown, Reith, and Robinson ( 1952 ) examined the mechanism of growth
in plant cells, both in intact organs and by culture of isolated fragments.
Lindegren and Haddad (1954) found that in yeast cells growth rate is
constant and that it begins and ends abruptly, thus differing from growth
in most higher organisms.

Physiology of Growth. The essential fact in growth is the increase in
amount of the various components of the organism. This results from the
self-multiplication of its essential portions, the genes and their basic
constituents, the nucleic acids. Everywhere syntheses are involved. This
general field is closer to physiology than to morphogenesis. Also essen-
tially physiological are problems concerning the rate and duration of
growth. These traits may be affected by many factors, some in the genetic
constitution of the plant and others coming from its environment, such
as temperature, light, water, and chemical substances of many kinds. To
consider these aspects of growth would require much space and is outside
the purpose of the present volume. The physiology of plant growth has
been frequently discussed, as by Thimann ( 1954 ) .

It is not growth itself that is of morphogenetic importance but its
relative distribution, for this is what determines form. Richards and
Kavanagh (1945a) call attention to the fact that a study of growth by
geometrical changes alone, as is commonly done, does not tell the whole
story. Density (mass per unit volume) and volume may be increasing at
different rates in different regions. The forces of stretching and compres-
sion that result may affect the distribution of growth. Under the discus-
sion of various factors in the latter part of this book, growth and its con-
trol will from time to time be mentioned, but as part of a larger problem.
This problem is the development of a specifically formed and organized

22 Growth

plant body. One of the leading students of morphogenesis has recently
expressed this well:

I think, after we have surveyed the facts, that the whole subject of growth
will seem bigger than the chemistry of synthesis, and that it will be more likely
that this latter will seem a small (although important) part of a larger scheme
in which growth is used here and there, sometimes encouraged, sometimes dis-
couraged, and in such a way that a consistent, whole, individual organism is
created in an orderly and masterful fashion. (J. T. Bonner, 1952a, p. 61.)

CHAPTER 3

The Cellular Basis of Growth

One of the great biological generalizations of the nineteenth century is
the cell theory, commonly attributed to the botanist Schleiden and the
zoologist Schwann and formally stated in 1839. This was a recognition of
the fact that all organisms are composed of living units, the cells. The
theory provided a common foundation for a study not only of structure
but of growth (cell multiplication) and development (cell differentia-
tion ) . It has served as a unifying concept for all biology, somewhat com-
parable to the atomic theory in the physical sciences.

The implications of the cell theory for morphogenesis are important.
In the minds of those who promulgated it, it meant that the cell is the
true biological individual and that an organism is the result of the ac-
tivities of its constituent cells. That the cell is thus the primary agent of
organization is the opinion of some biologists today. In such a view the
organism is looked on as a sort of cellular state, built by the cooperative
efforts of its citizens among whom, as in a human society, there is a high
degree of division of labor. In support of this idea are cited cases such
as that of certain of the slime molds, where some thousands of individual
cells (myxamoebae), entirely independent in the early stages of the life
cycle, become aggregated into a cellular mass and then by their mutual
interactions build up a fruiting body of a specific size and form (p. 223).

Other biologists, however, believe that the true individual is the
organism, essentially a mass of protoplasm divided into cellular units.
Such division has the advantage that it makes possible the differentiation
of parts and the segregation of various physiological activities within
particular cells. The organism may thus be said to make the cells rather
than the cells to make the organism. In this conception the multicellular
plant body is to be thought of as having arisen not through the aggrega-
tion of individual cells, originally separate, but by cellular multiplica-
tion.

That this organismal theory gives a better picture of the growth and
activities of plants and animals is suggested by the high degree of co-
ordination and self-regulation that exists in a living thing. The produc-
tion of individuals essentially alike by a variety of developmental routes

23

24 Growth

in regeneration is difficult to explain as a result of the interaction of essen-
tially independent units. The cellular society, if it is one, must have a
strong central government which regulates the activities of its individual
members. A certain amount of self-differentiation undoubtedly exists, in
which a given organ or structure, once its development has begun,
proceeds more or less independently of the rest, but the parts are usually
interdependent. The problem of organization, the central one for biology,
can be attacked more hopefully by a study of organized systems as
wholes than simply of the units of which these are composed.

There are obviously considerable differences in the degree and level of
organization. In plants with indeterminate growth, especially in some of
the lower groups, the "individual" is little more than a colony of cellular
individuals, which are so nearly independent that if isolated they
will produce new plants directly. Among higher forms it is much more
closely organized. Even here one can hardly tell, in types such as straw-
berries and many grasses, for example, which spread by stolons or
rootstocks, how much should be regarded as a single individual. In many
cases, however, growth is determinate, the number of parts is relatively
constant, and the individual is a distinct and specific thing. In no plants
does it reach the high level of organization that most animals display.

In support of the concept that the organism is the developmental unit,
one may point to the many cases in plants where, as in the alga Caulerpa,
a very considerable degree of differentiation occurs into "roots," "stems,"
and "leaves" but where there are no cellular boundaries at all. The whole
plant is a coenocyte, a simple mass of cytoplasm in which great numbers
of free nuclei are embedded or move about. In other algae where the
general character of the plant body seems to be similar to this, some
species have uninucleate cells, others multinucleate ones, and others are
entirely coenocytic, with no cell walls save where reproductive organs
are formed. In most of the true molds, or Phycomycetes, the hyphae are
multinucleate and not divided into cells, and this is true of certain of the
higher fungi also. In some other algae and fungi the partitions across the
filaments are incomplete and have a central perforation through which
cytoplasm can flow, so that there is no true cellular structure. In the
developing endosperm of the higher plants there is usually at first a
large number of free nuclei in a mass of cytoplasm, but these gradually
become separated from each other by the growth of walls.

The difference between these two views of the relation between the
cell and the organism is of much importance for morphogenetic theory.
The individual cells are certainly significant, particularly in physiol-
ogy, and their presence makes possible much useful analysis of de-
velopmental processes, but just how a group of cells develops into an
organism still remains the central problem.

The Cellular Basis of Growth

25

CELL DIVISION

Growth of plants and animals, in the last analysis, is an increase in
amount of living stuff in them, but this growth is almost always accom-
panied by an increase in the number of their cells. This takes place by
the process of cell division, which thus assumes much significance for
problems of growth and differentiation. The precise method by which
new cells are formed was not understood for some time after the cell
theory was established. In the seventies of the last century a number
of botanists and zoologists, Strasburger prominent among them, made
clear the mechanism of mitosis and the leading part played by the
nucleus in cell division.

Division does not take place in all parts of the plant individual. In
higher forms it is limited chiefly to apical and lateral meristems and to

1

§3

- J

1

->

1

r

Fig. 3-1. Division of a vacuolate cell showing the development of the phragmosome,
which precedes the cell plate. ( From Sinnott and Bloch. )

the growing regions of determinate organs, though there may be cell
division under certain conditions in other parts of the plant.

Division is usually studied in small-celled meristematic regions where
the cells are not vacuolate or have only small vacuoles. In many cases,
however, particularly in the rib meristems of root and shoot and below
wounds, cells that are relatively large and in which a vacuole occupies
the bulk of the cell may continue to divide. In such cases the nucleus
moves from near the wall to a position in the center of the cell, where it
is held by strands of cytoplasm. Here it undergoes mitosis. The position
where the cell plate, and later the cell wall, will form is usually indi-
cated early bv a plate of cytoplasmic strands, the phragmosome, which
extends across the cell and in which the nucleus is embedded (Sinnott
and Bloch, 1941; Figs. 3-1, 3-2). The cell plate itself is laid down later
by the phragmoplast, a group of fibers which are a continuation of the
fiber system between the nuclei at telophase. This spreads across the cell,
following the course of the phragmosome where the latter is present. In

26

Growth

side view, as in the dividing cambium cells figured by Bailey (1920«),
the phragmoplast appears in section as two spindles at the edge of the
developing cell plate. In face view it looks like a cytoplasmic "halo." The
phragmosome and the phragmoplast, and the function of each in cell
division, have sometimes been confused. The difference is made clear by
Esau ( 1953£>, her Fig. 3-10 ) . In some dividing vacuolate cells, such as
those of the cambium, the phragmosome is either absent or has not
been observed.

Fig. 3-2. Phragmosomes in various cells, a-c, normal tissue; c, in face view showing
anastomosing strands; d, e, mature cells near wound face beginning to divide. (From
Sinnott and Bloch. )

The significance of the cytoplasm in cell division has been emphasized
by Muhldorf ( 1951 ) . The general problems of cell division in plants are
treated at length in Tischler's monumental book ( 1951 ) .

The factors that determine whether a cell will divide or not are various
and have been much discussed. The size of the cell itself is evidently
one of these factors. In actively meristematic regions, the dividing cells
are usually of about the same size. This means that each daughter cell,
after division, enlarges until it reaches the size at which its mother cell
divided, and then itself divides. After division ceases, the cells usually
expand considerably.

Size in dividing cells is by no means always constant, however. Wagner

The Cellular Basis of Growth 27

( 1937), studying the distribution of mitoses in root tips, found that these
occurred not only in the small cells at the apex but in the progressively
larger ones back from this until division ceased. Incidentally, he reported
that in many cases dividing cells are not evenly distributed through the
meristematic region but tend to occur in several waves, moving backward
from the tip (Fig. 3-3).

In developing cucurbit ovaries during the period of cell division there is
a progressive increase in the size of the dividing cells in each region
(epidermis to placental region), and this increase is greater in successive
tissues from the epidermis inward ( Sinnott, 1939; Fig. 3-4 ) . The daughter
cells from a division must therefore increase to a size somewhat greater
than that at which their mother cell divided before they themselves di-
vide again. The largest cells to divide were many times the volume of
the smallest ones.

Fig. 3-3. Changes in cell length in microns (lower line) and frequency of mitoses
(upper line) at successive distances from the root tip (at left) in periblem of onion
root. ( From Wagner. )

Another factor in division, emphasized especially by zoologists, is the
ratio of nucleus to cytoplasm (the nucleoplasmic ratio). R. Hertwig
( 1908 ) believed that, as a cell grows, the cytoplasm increases faster than
the nucleus so that a tension is set up which is finally relieved by the
division of the cell. This restores the equilibrium of nucleus and cyto-
plasm, since presumably the size of the nucleus is at once restored. Popoff
( 1908 ) was able to remove some of the cytoplasm from certain cells by
micropipette and found that these divided more slowly than their un-
treated sister cells, as one would expect on Hertwig's theory. There is
little evidence from meristematic plant cells that a changing nucleo-
plasmic ratio is significant in cell division, though perhaps it may be. In
larger and vacuolate plant cells it is difficult to measure the cytoplasm
since it is distributed in a thin layer lining the wall. The cytonuclear
ratio (volume of cell to volume of nucleus), however, can be de-
termined. In vacuolate cells of progressively larger size the volume of

28

Growth

the nucleus tends to keep pace with the surface of the cell and thus
perhaps with the volume of the cytoplasm if the thickness of the cyto-
plasmic layer is constant (Trombetta, 1939; Fig. 3-5). This suggests a
relationship which in earlier stages may have a bearing on cell division.
An important element in growth and development is the rate at which
cell division takes place. This is essentially a physiological problem and

60 80 100

OVARY DIAMETER mm

OVARY

20

DIAMETER mm

Fig. 3-4. Relation of cell diameter to fruit diameter in Cucurbita pepo. TA, small-
fruited race. CF, large pumpkin. In early development, cell size increases less rapidly
than fruit size, showing that division is occurring. Later growth is by cell enlargement.
Solid circles, cell diameter (in microns) at last division. Final cell diameter at end of
each line. Lowest curve, epidermis; next higher, outer wall; next, middle wall; next,
inner wall; uppermost, placental region. (From Sinnott.)

involves various internal and external factors, some of which will later be
discussed. There are certain techniques by which it can be measured,
however, which are of importance for the student of morphogenesis.

Root tips are especially favorable material for this. Brumfield (1942)
recorded the rate of division in the apical meristems of small roots by
photographing the surface cells at measured intervals of time, and this
has since been done by others ( p. 78 ) . A method for measuring rate of in-
crease in cell number by macerating the root meristem and counting the

The Cellular Basis of Growth

29

,3.Jr

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TOMATO HAIRS

1 - PLANT 7 DAYS OLD

2 - 28

3- " MATURE

CELL VOLUME
Fig. 3-5. Logarithmic graph of relation of nuclear volume to cell volume in cells of
stem hairs of tomato. Nucleus increases about two-thirds as fast as cell. ( From Trom-
betta. )

numbers of cells at intervals has been developed by Brown and his stu-
dents (p. 41). Erickson (1956) has analyzed mathematically the rate of
division in certain root tips.

In growing gourd fruits Sinnott (1942) determined cell number by
dividing tissue volume by cell volume and found that increase in cell
number takes place at approximately the same rate in epidermis, outer
wall, inner wall, and placental region, regardless of the marked differences
in cell size in the four. Cell division in the epidermis takes place at the
rate necessary to maintain a constant cell size, and this tissue may thus
serve in a sense as a pacemaker for division in the whole ovary primor-
dium. Jahn (1941) has made a detailed study of the localization and
degree of cell division and cell expansion in the epidermis of growing in-
ternodes of Vicia faba.

CELL SIZE

The size of plant cells is obviously an important element in growth,
differentiation, and other morphogenetic problems. Cells are relatively
small objects, presumably because the ratio of surface to volume, and thus
the ease of exchange of material between a cell and its environment, is
inversely proportional to its size. Cells with high metabolic rates tend to
be very small, and large cells are relatively inactive. Rapidly dividing
cells, for example, are much smaller than those of storage parenchyma.
There is a wide range in cell size among various tissues of a plant. In meri-
stematic regions they are often as small as 1,000 cu. microns or less but in
pulp of watermelon may be almost a million times this volume. Stras-

30 Growth

burger ( 1893 ) believed that the nucleus has a certain "working sphere"
and that this limits the size to which a particular cell will grow.

Studies of comparative cell size have often been made but chiefly on
mature cells. This problem, however, is one that must be attacked devel-
opmentally. Two processes are involved in it: the rate and amount of
growth or increase in size in a given region and the rate and duration of
cell division there. Cell size is the result of the relationship between these.
The faster the cells divide, in proportion to the total amount of growth,
the smaller will they be, and vice versa.

At the end of a cell division each daughter cell is about half the volume
of its mother cell. At this time it begins to enlarge, and if it is in a meri-
stematic region it will soon divide again. Where division rate is relatively
rapid, the cells may divide before they have time to enlarge to the size of
their mother cells, and cell volume decreases, as in some early embryos.
Sometimes the new cells do not expand at all and a process of cleavage
takes place, much as in the first stages of many animal embryos, where
the egg is cut up into a mass of smaller and smaller cells. In plants such
cleavage may be seen in endosperm formation; in the development of the
female gametophyte within a megaspore; in the renewal of meristematic
activity in large, mature cells during regeneration; and elsewhere. Where
cell enlargement is relatively rapid, the cells will become larger than their
mother cells before they divide again and cell size in the meristematic
region will increase. Thus in growing gourd ovaries, where the tissues are
still meristematic and the cells all start from a very small size, they gradu-
ally enlarge, though not as fast as the ovary itself. In most roots, dividing
cells increase in size with increasing distance from the root tip.

In their detailed analysis of the growth of the oat coleoptile, Avery and
Burkholder ( 1936 ) found that in the outer epidermis cell division ceased
after the organ was first initiated, so that during all later growth cells here
elongated greatly, sometimes becoming 150 times as long as at the begin-
ning. The inner tissues, however, grew in part by cell multiplication until
the coleoptile was 10 to 20 mm. long. There were progressively fewer
divisions from the subepidermis inward. Thus at maturity the longest cells
were in the outer epidermis, the shortest in the layer next below it, and
the cells then increased in length toward the inner layers (Fig. 3-6).

In some meristems, especially the vascular cambium, the size of divid-
ing initials may undergo permanent increase. Sanio ( 1873 ) and others
since his time have found that xylem cells in trees have different lengths
at different distances from the center of the trunk or from the ground and
that these differences are mainly established in the fusiform initials in the
cambium from which the mature cells develop.

Most increase in cell size, however, comes after the final division. In
plants, as contrasted with animals, this increase may be very great. Usually

The Cellular Basis of Growth

31

it is related to the absorption of water and increase in size of the vacuole.
Differences among tissues in mature cell size are very considerable and
are one of the most important aspects of differentiation. In tissues where
division persists relatively late there is little time for cell expansion before
maturity is reached, and the cells remain small, as is often the case in the
epidermis. Where division ceases early, as in storage parenchyma, the cells
grow to a much greater size. In many axial structures there is a gradient
from without inward, the cells becoming progressively larger toward the
center either because of more rapid increase or earlier cessation of divi-

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140

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FOURTH LAYER

INNER EPIDERMIS

-o OUTER EPIDERMIS

10 20 30

COLEOPTILE LENGTH IN MM.

40

50

Fig. 3-6. Number of cells, lengthwise, in various cell layers of the oat coleoptile at six
stages in its growth. There is evidently no division in the outer epidermis after the
coleoptile begins its development, and division ceases early in the other layers, though
there are differences among them in the frequency of division. ( From Avery and Burk-
holder. )

sion. This is not always the case, for the epidermis may have larger cells
than the other tissues, as Avery and Burkholder found in the Avena
coleoptile.

There is a question as to just where in the cycle of cell division growth
actually occurs. Abele (1936) distinguishes between Teilungswachstum,
growth during division itself, and Streckungswacristum, growth after divi-
sion has ceased. There is certainly a considerable visible increase in size
during prophase but not much more until telophase. Of course the dura-
tion of these phases must be taken into account. It is probable that non-
aqueous material increases at a constant rate throughout growth. Sinnott
( 1945a ) found that in gourds there was no change in rate of growth of the

32

Growth

ovary, as measured by gain in dry weight, at the time when cell division
ceased and cell expansion began (Fig. 3-7).

Cell Size and Organ Size. There are several important implications of
the problem of cell size for morphogenesis. One is that of the relation be-
tween the size of an organ or body and the size of the cells that compose
it. Is a body large because its cells are large or because they are more
numerous? This problem was discussed by Gregor Kraus in 1869 in con-
nection with his work on structural changes during etiolation, but Sachs
(1893) and his student Amelung (1893) seem to have been the first to
attack it directly. Sachs called attention to the fact that the size of a cell

Time in Days

Fig. 3-7. Relation of cell division and cell enlargement to growth. Logarithm of ovary
volume plotted against time for three races of Cucurbita differing in fruit size. The
period between the vertical bars is that during which cell division ceases. To the left
of it, growth is by cell division; to the right, by cell enlargement. Despite this change,
the rate of growth at this period remains constant. ( From Sinnvtt. )

must be closely related to its physiological activity and that cells of a par-
ticular tissue should thus be expected to be of about the same size. If this
is so, size in a plant would be related to the number rather than the size
of its cells. His measurements supported this conclusion. Amelung made
a much larger series of measurements and found the same general result,
although he observed a good many cases where cell sizes differed consid-
erably between comparable plants or tissues.

The problem is not quite as simple, however, as these early workers
thought. It is true that most of the size differences between plants, espe-
cially those in the indeterminate axial structures, result from differences
in cell number. In determinate organs, on the other hand, notably in bulky

The Cellular Basis of Growth 33

structures such as tubers and fruits, the greater size is due to an increase
in both the number and the size of their cells. Lehmann (1926) found a
positive correlation between the size of a potato tuber and that of its cells.
Since the increase in cell size was by no means proportional to that in
tuber size, it was evident that large tubers have more as well as larger
cells. The same relations are found in tomatoes (Houghtaling, 1935). A
more detailed study of this problem, in large-fruited and small-fruited
races of gourds, was made by Sinnott (1939; Fig. 3-4). Here cell size in-
creases in the young ovary but much less rapidly than organ size, showing
that cell division is taking place. During this period there is more increase
in cell size in the larger races. The size at which the cells divide steadily
increases. At about the time of flowering, however, division in most of the
young fruit ceases, first in the central region and then progressively out-
ward, so that nearly all later fruit growth is by cell expansion. In large-
fruited races the period of cell division and that of cell expansion are both
longer than in small-fruited ones, so that the greater size of the former is
due to both more and larger cells. This general developmental pattern
was found by Riley and Morrow ( 1942) in Iris ovaries and fruits, by W. H.
Smith (1950) in apple fruits, by Ashby and Wangermann in leaves (p.
210), and by others. In avocado fruits, however, cell division in the fruit
wall continues to some extent until maturity ( Schroeder, 1953b ) . In gen-
eral, larger fruit size results from an extension, so to speak, of all parts of
the developmental history.

In several genera Ullrich (1953) studied the relation between epider-
mal cell size and leaf size in the series of successive leaves up the stem.
He found that the size of the cells decreases steadily whereas that of the
leaves increases for several nodes and then decreases. Thus there is no
close relationship, at least in this tissue, between cell size and organ size.
Under unfavorable conditions, however, both tend to decrease together.
A somewhat similar variation in the correlation between cell and organ
size has been reported in wheat (Nilson, Johnson, and Gardner, 1957).

It is noteworthy that tissues differ considerably in the relation of the
size of their cells to that of the organ of which they are a part. This rela-
tion is usually closest in storage parenchyma and least in the epidermis. In
general, as Sachs pointed out, cells that are physiologically important, like
most of those in the leaf blade, are relatively constant in size and show
little relation to the size of the organ. In mosses, unlike higher plants, cell
size and leaf size are usually rather closely proportional to each other,
cell number being much more constant.

Size relationships sometimes extend below the level of the cell. The
ratio of cell size to nuclear size has already been mentioned here. Both
Budde ( 1923 ) and Schratz ( 1927 ) found a rather close correlation be-
tween the total surface area of the plastids and the volume of the cell.

34 Growth

Mobius (1920), however, observed no relation, in 215 species, between
chloroplast size and that of cells or organs. Irmak (1956) confirmed this.
There are other complications in the problem of cell size, some of which
are of morphogenetic significance. One involves the dwarfing of plant
structures. This has been discussed in a number of early papers, among
others by Gauchery (1899), Sierp (1913), Oehm (1924), Sinoto (1925),
and Abbe (1936). It is generally agreed that where dwarfing is the result
of unfavorable environmental conditions cell size is reduced, though not
equally in all structures. A scanty water supply chiefly affects the second
phase of cell enlargement in which considerable quantities of water nor-
mally are absorbed. The problem is complicated by the fact that dwarfing
is often the result of genetic as well as environmental influences.

o 30

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°0 ,0 20 30 40 50 60 70 80 90 100 110 120 130 140

NUMBER OF CELLS FROM APEX

Fig. 3-8. Relation of cell size to plant height. Length of successive cells along the
terminal meristematic region of a dwarf race (above) and a tall one (below) of to-
mato. Cells of the dwarf are somewhat longer because they attain maturity, and thus
stop dividing, at an earlier stage. The tall plants have many more cells. (From Bind-
loss. )

Genetic Factors. The relation of genetic factors to cell and body size is
complex and will be discussed more fully in a later chapter (Chap. 19).
Genetic analyses of size differences in plants have been made repeatedly
but the histological effects of gene and chromosome differences are widely
various. Most genetically large plants are so because of more rather than
larger cells. Thus in the tall races of Lycopersicon and Zinnia studied by
Bindloss (1942) there are many more cells, lengthwise, than in dwarf
races, though the cells are somewhat shorter (Fig. 3-8). In other cases,
however, cell size is involved. Thus the difference between large-leaved
sugar beets and small-leaved vegetable beets is due chiefly to the greater
cell size of the former. What is inherited here is evidently the amount of
postmitotic expansion, for the meristem cells are the same size in both.
Von Maltzahn ( 1957 ) found that the difference in size of vegetative struc-
tures between large and small races of Cucurbita was related to both cell
size and cell number.

The Cellular Basis of Growth 35

Some "giant" races, however, owe their large size to larger cells. The
first instance of this was reported by Keeble (1912) in a mutant of
Primula sinensis. Tischler (1918) found a similar case in the reed Phrag-
mites communis, and here large cell size was accompanied by larger than
normal chromosome size, a fact reported by others ( Schwanitz and Pirson,
1955). Much more commonly, giant forms with large cells result from
polyploidy ( p. 436 ) . The first case of this to be observed was Oenothera
gigas of de Vries, which was found to be a tetraploid. Many similar ex-
amples are now known. Tetraploids are not always giant in character,
however, and many polyploid series in nature show no difference in body
size or cell size. Sinnott and Franklin ( 1943 ) found that in young tetra-
ploid gourd fruits the gigas condition, both as to ovary and cells, is pres-
ent until after flowering but that later growth is reduced so that at matu-
rity there are no great size differences between diploid and tetraploid (p.
439). A diploid giant moss race reported by von Wettstein (p. 437)
returned to normal size of cell and organ after a few years of vegetative
propagation.

The increased cell size due to polyploidy is not uniform but is consid-
erably greater in some tissues than in others. In the diploid moss races
produced by von Wettstein ( 1924 ) the ratio of size increase from the In
to the 2nwas found to be characteristic for each race (p. 437). In general,
the increase of organ size due to polyploidy is not as great as the increase
in cell size, since cell number tends to be somewhat reduced.

Increased cell size may also result from increased number or bulk of
chromosomes (p. 445), quite apart from polyploidy (Navashin, 1931; Lor-
beer, 1930), and from extra or accessory chromosomes (Randolph, 1941;
Miintzing and Akdik, 1948). Particular chromosomes, when present in
trisomies, have different effects on cell size (and on other characters),
presumably because of the specific genes which they contain (p. 447).
Geitler ( 1940 ) observed that chromosome volume was correlated with
nuclear volume and that in some tissues the chromosomes were more than
four times as large as in others. In species of four genera, Mrs. Sax ( 1938 )
found that cell size was correlated with the chromosome number of the
species but that in three others there was no such correlation. Somatic
polyploidy or polysomaty ( p. 441 ) is a factor of importance both for cell
size and for differentiation.

Cell size has been found to be inherited in a number of lower plants,
as in yeast (Townsend and Lindegren, 1954).

Heterosis is usually not related to an increase in cell size (Kostoff and
Arutiunova, 1936).

Cell Size and Position. Many workers have found a great variation in
size among comparable cells in the same plant. Often this is not ran-
dom but follows a certain pattern. The problem has been studied most

36

Growth

intensively in the size (chiefly length) of cells in the xylem of woody
plants.

Sanio ( 1872, 1873), working with pine, was the first to attack this prob-
lem intensively. He came to several general conclusions, the more impor-
tant of which are the following:

1. Tracheids increase in length from the center of the trunk or branch
toward the outside through a number of annual rings but finally reach a
constant size.

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Age in years

40

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925
900

875

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825 I5
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800 5
775
750
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Fig. 3-9. Relation of vessel diameter and fiber length to annual increment and age in
trunk of Acer pseudoplatanus. ( From Desch. )

2. This final tracheid size increases from the base of the trunk upward
to a maximum at a specific height and then decreases somewhat.

3. The final size of tracheids in a branch is less than in the trunk but
depends to some extent on the position of the branch.

Sanio's "laws" have been confirmed by most workers since his time
(Kribs, 1928, and others). Bailey and Shepard (1915), however, found
that, although the length of tracheids increases from the pith outward in

The Cellular Basis of Growth 37

a number of conifers, it does not reach a constant size but fluctuates rather
widely, falling and rising in cycles, perhaps climatic ones. Laing (1948),
Bissett, Dadswell, and Wardrop (1951), and Bannan (1954) report that
tracheid length tends to be less where the growth of the tree in diameter
is rapid, presumably because of the more frequent pseudotransverse divi-
sions of the cambial initials. Tracheid length is largely determined by
length of the cambial initials ( Bailey, 1920fr ) .

Dicotyledonous woods follow the same general pattern as conifers but
the situation is more complex because of the greater variety of cell types
(Desch, 1932; Fig. 3-9; Kaeiser and Stewart, 1955). Fibers may increase
considerably in length over their cambial initials (Chattaway, 1936) but
vessel segments do not (Chalk and Chattaway, 1935). In storied woods
neither fibers nor parenchyma cells show any tendency to increase in
length from the pith outward (Chalk, Marstrand, and Walsh, 1955). In
all growth rings of pine, Echols (1955) finds a close correlation between
the fibrillar angle in the cell wall and tracheid length. The subject of fiber
length in woody plants has been reviewed by Spurr and Hyvarinen
(1954b).

EXPERIMENTAL STUDIES

The division and enlargement of cells are essentially problems in the
physiology of growth, a subject too extensive to discuss here in any detail.
Much experimental work has been done, however, on certain aspects of
cell growth which are of particular morphogenetic interest and which it
will be profitable to review briefly.

The role of growth substances (Chap. 18) is particularly important.
Auxin was first recognized because of its stimulation of cell enlargement,
and in many cases it also affects cell division. Other substances are effec-
tive here. Jablonski and Skoog ( 1954 ) observed that the cells of tobacco
pith tissue in culture did not divide even under optimum amounts of
auxin unless extracts from vascular tissue, coconut milk, or certain other
things were added. This suggested that a substance specific for cell divi-
sion but different from auxin was here operative, and such substances,
the kinins, are now recognized. Gibberellin especially influences cell size.
Wound hormones induce division in many mature cells. The presence of
vitamin C seems to be related to cell expansion (Reid, 1941). Lutman
(1934) assembled a mass of data on the effects of various inorganic sub-
stances on cell size. The stimulating and inhibiting influences of these vari-
ous chemical factors are key problems in the physiology of develop-
ment.

Metabolic factors are also important. Oxygen consumption is related to
cell division (Beatty, 1946). Interesting observations here have been re-

38

Growth

ported by Transeau ( 1916 ) for the seasonal distribution of various species
of Spirogyra. These differ markedly in the size of their cells, those of the
largest being about 150 times the volume of the smallest. The small-celled
forms are the first to appear in the spring, when temperatures are low,
and the larger-celled ones come on progressively as the season grows
warmer. This presumably is because of the higher metabolic rate of the
smaller cells which results from their greater ratio of surface to volume.

Progressive physiological changes (p. 210) seem also to be involved. In
successively higher leaves on the stem of Ipomoea, Ashby and Wanger-
mann (1950; Fig. 3-10) found that the cells became smaller and suggest

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Fig. 3-10. Relation between area of epidermal cells and of leaf lamina in developing
leaves of Ipomoea caerulea, plotted logarithmically. Solid circles, second leaves;
crosses, fifth leaves; empty circles, eighth leaves. Early growth is chiefly by cell di-
vision, since cell size increases little. Later growth is by cell enlargement since cells
and lamina grow at the same rate. Compare with Fig. 3-4. Cell size becomes smaller
in successive leaves. (From Ashby and Wangermann.)

that this is symptomatic of a process of aging in the apical meristem. This
problem of possible senescence in plants has other implications for cell
size. Benedict ( 1915 ) presented evidence that in a number of vegetatively
propagated plants, notably Vitis, cell size tends progressively to decrease
with the age of the clone, a fact interpreted by him as the result of
senescence. He believed that the "running out" of certain varieties was
due to this cause, but it has now been shown that in many cases such a
change is due to virus infection. Benedict's results have had some con-
firmation, notably by Tellefsen ( 1922) and Bergamaschi ( 1926) in studies
of cuttings from trees of different ages. Ensign (1921), however, found

The Cellular Basis of Growth 39

no correlation between age of plant and vein-islet area (and thus cell

size).

Even growth habit may involve differences in cell size, for H. B. Smith
( 1927 ) reports that annual sweet clover has considerably larger cells than
does the biennial race.

Correlation (p. 95), a sufficiently vague term to describe certain phe-
nomena about which we understand little, also affects cell size. In various
growth compensations, removal of an organ results in greater growth of
another one and often in larger cells there. In "topped" tobacco plants
(where the terminal flower cluster has been removed) Avery (1934)
found that the leaves on the upper third of the stalk grew larger and that
much of this extra growth was due to increase in cell size (Fig. 3-11).
Lindemuth (1904) removed and rooted mature begonia leaves and ob-

Fig. 3-11. Effect of topping a tobacco plant. Portion of the vein network in the
twentieth leaf from the tip. At left, untopped; at right, topped. The leaves from topped
plants are larger and have more space between the veins because of increased cell
size. ( From Avery. )

served that they then increased considerably in size, chiefly because of
cell enlargement. While they were attached to the plant this presumably
was prevented by "correlative inhibition." Similar results have been re-
ported by others. In linden leaves, however, which had been induced to
grow much larger than their normal size by the removal of other leaves,
Ewart ( 1906 ) found the increase to be due chiefly to a larger number
of cells.

Factors within the cell itself are doubtless related to the onset of its
division. Cytoplasmic viscosity generally rises in prophase, falls in meta-
phase, and rises again in telophase. Mole-Bajer ( 1953 ) has explored the
effect of artificially increased viscosity of cytoplasm in slowing down the
rate of mitotic division. Gustafsson ( 1939 ) found that the difference
between meiotic and mitotic division was related to the degree of hydra-

40 Growth

tion of the nucleus. The effect of dehydration in checking mitosis has also
been reported by Mole-Bajer (1951).

Osmotic concentration of the cell sap was observed by Becker ( 1931 )
to be inversely proportional to cell size and to number of chromosome
sets in polyploid moss protonemata.

Various external factors are important both for the division and the
enlargement of cells. Light frequently tends to check division, and ultra-
violet radiation may inhibit it. The hypothetical mitogenetic rays of Gur-
witsch (1926) and his school were thought to stimulate mitosis. The effect
of light on cell size has been emphasized by Straub (1948). Most of the
elongation of etiolated plants (p. 309) is due to increase in cell length.
Giese (1947) has reviewed 300 papers dealing with the effects of various
kinds of radiation on the induction of nuclear division.

Temperature, so important in many protoplasmic processes, has an
effect on mitosis. P. C. Bailey (1954) has shown that in Trillium the
maximum rate of cell division takes place at considerably lower tempera-
tures than does the maximum rate of increase in root length. Burstrom
(1956) reports that under higher temperatures the final cell length in
roots is less because of the shorter period of cell elongation.

Wagner (1936) found evidence that gravity influences mitosis. In root
tips placed horizontally he observed that after about an hour there was a
marked increase of mitoses on the upper side, so that the very tip of the
root bent down. After 4 hours mitoses were equally distributed, and after
10 to 12 hours they were more abundant on the lower side and the tip
straightened out again. These changes were quite independent of the geo-
tropic bending due to auxin and cell expansion, which was evident much
farther back from the tip. When plants were grown on a clinostat. Brain
(1939) observed in lupine seedlings that cells of the cortex, endodermis,
and pith in the hypocotyl were larger than those of upright plants but
that in the radicle they were smaller.

In some cases pressure stimulates division, as can be seen in the cortical
tissues through which a lateral root pushes its way ( Tschermak-Woess
and Dolezal, 1953).

Water is of marked influence in determining cell size. The amount of it
available often determines how much a cell can expand (Thimann, 1951).
Zalenski and others (p. 325) have observed that at successively higher
levels on a plant the cells of the leaves are smaller, presumably because
of their inability to become fully turgid while they were expanding. Water
may have other effects. Funke (1937-1939) found that if some water
plants are put into deep water their petioles elongate rapidly by cell ex-
pansion, sometimes lengthening tenfold in 2 days.

The role of the wall in cell growth has been much discussed. Does the
wall merely stretch under the pressure of an expanding vacuole or does

The Cellular Basis of Growth 41

it grow independently of this? Burstrom ( 1957 and earlier papers ) pre-
sents evidence that cell elongation is not primarily a matter of water
uptake but is due to growth of the cell wall. He believes that this occurs
in two steps, the first a plastic stretching of the wall and the second the
production and deposition of new wall material. Auxin promotes the first
but probably inhibits the second. Others believe that auxin, known to
stimulate cell enlargement, directly increases the plasticity of the wall and
thus its extensibility (Heyn, 1940). This view has found recent support
(p. 412).

It obviously is necessary to know just how the wall grows and particu-
larly whether this is by apposition of new material on its inner face or by
intussusception throughout. Green (1958), using techniques for measur-
ing radioactivity, treated elongating Nitelh cells with tritium (HH) and
found by test that the inner part of the wall became radioactive. The
outer portion, which was not, grew thinner as the cell lengthened, thus
suggesting that new cell wall material was being laid down only on the
inside and not throughout.

Rate of wall thickening sometimes has a direct effect on plant size. Thus
in a dwarf mutant of Aquilegia (Anderson and Abbe, 1933) this trait was
found to be due to the precocious thickening of its cell walls (p. 426).

The important problem of the relation of deoxyribonucleic acid to
cell division has often been investigated. Grundmann and Marquardt
( 1953) determined the content of DNA in successive phases in the mitotic
cycle of the nuclei of periblem cells of the root tip of Vicia. This increases
steadily throughout the interphase. It is reduced at telophase since it is
roughly proportional to nuclear volume.

Brown and his students have used various modern techniques for a
study of the problems of the multiplication and growth of cells. Brown
and Rickless (1949), for example, cut off Cucurbita root tips of equal
length (1.6 mm.) and grew them in culture for 3 days, taking samples
every 12 hours. These tips were macerated, and in a haemacytometer the
total number of cells and the number of nonvacuolate cells were counted.
From these counts, together with a measurement of the length of each
root examined, it was possible to determine the rate of cell division and
the index of extension ( ratio of root length to number of vacuolate cells ) .
This method is subject to a number of errors, particularly from the as-
sumption that only the nonvacuolate cells were dividing. However, it
gave consistent results, and these were in general agreement with the
more laborious method of measuring cell size and volume from microtome
sections. The authors found that there was no division in the absence of
sugar in the culture medium and that the rate of division increased with
the addition of sugar and inorganic salts and even more with the addi-
tion of yeast extract. At 15° C the rate of division was higher than at 5 or

42

Growth

25°. The greatest increase in cell size was with sugar and mineral salts.
Yeast extract tended to decrease extension.

Brown and Wightman ( 1952 ) grew root tips of pea 3.0, 6.0, and 10.0
mm. long in sterile culture and found that the peak rate of division occurs
later and that its peak value is greater the shorter the initial tip. They
conclude that cell division in the meristem depends partly on synthesis of
metabolites there and partly on a supply of metabolites from more mature
regions of the root.

I 3 5 7 9 II

DISTANCE FROM APEX(MMS)

Fig. 3-12. Changes in protein (circles) and water content (crosses) of bean-root cells
at increasing distances from the root apex. ( From Brown and Robinson. )

A basic problem in this field is that of protein synthesis. Brown and
Broadbent ( 1950) sliced a series of root tips into segments 0.2 to 0.8 mm.
thick and in each successive section determined the number of cells, the
protein content, the dry weight, and the amount of respiration. During
development from the meristematic to the fully extended state the average
cell volume increased thirtyfold and there was an increase in protein con-
tent and in respiration (Fig. 3-12).

Genetic factors are concerned in cell activities in many ways. Beadle
( 1931 ) , for example, found a gene for supernumerary divisions in maize;

The Cellular Basis of Growth 43

Moewus (1951), one for cell division in Protosiphon which is linked to
sex manifestation; and Nickerson and Chung (1954), one in yeast that
seems to block the sulphydryl mechanism of division. Dorries-Ruger
(1929) grew protonemata from the spores of plants produced by various
combinations of genome and plasmon in mosses, among races developed
in Wettstein's laboratory. She cut off and cultured the tip cells of these
protonemata and recorded marked differences in the rate of cell division
in the filaments growing from them, thus comparing the effects of dif-
ferent genotypes under the same environment.

PLANE OF CELL DIVISION

Cell size and cell number are important elements in growth and differ-
entiation, but the problem of form is primarily dependent not on these
factors but on the relative directions in which growth occurs. These, in
turn, are closely related to the planes of cell division in the developing
tissues. Whatever determines the position of the new cell wall between
two daughter cells will determine the direction in which these cells ex-
pand, since this direction will normally be at right angles to the new wall.
At the time of cell division, therefore, the direction of growth in this par-
ticular region of the meristem is determined. If plant cells could change
their relative positions, as is possible in many animal tissues, the deciding
factor in the direction of growth would often be cell movement rather
than plane of cell division.

The position of the cell plate at telophase, and thus of the new cell wall,
follows the position which the equatorial plate of chromosomes finally
assumes at metaphase. The mitotic figure may roll around somewhat be-
fore it settles down to a permanent position, but there must be something
that determines that position. This raises the question as to whether the
plane of division is controlled by whatever decides the final orientation
of the mitotic figure or whether this, in turn, is itself determined by other
factors. That the latter may be the case is suggested by the way in which
vacuolate cells divide. In such cells a series of cytoplasmic strands forms
a loose diaphragm, the phragmosome, across the cell, and in the middle
of this the nucleus is supported. In tissues where the plane of division
can be predicted, observation shows that the position of this diaphragm
is the one which the future cell wall will occupy. The diaphragm is laid
down considerably before the nucleus enters metaphase, and the meta-
phase plate of chromosomes may not at first lie parallel to the diaphragm,
though it finally does. This seems to indicate that the plane of division is
determined early and for the cell as a whole rather than by factors acting
on the mitotic figure alone. There is also evidence that the mother cell,
before division, begins to elongate at right angles to the direction in

44 Growth

which it will divide. All this raises the fundamental question as to whether
morphogenetic factors operate directly on each dividing cell or whether
relative directions of growth, and thus form, are determined by factors
affecting the entire growing organ, the whole mass of living stuff, and that
the degree and manner in which this is cut up into cells are a secondary
result. This is simply another aspect of the main problem raised by the
cell theory.

Factors Determining the Plane of Cell Division. Many suggestions have
been made as to the factors that determine the position of a new cell wall.
Years ago Hofmeister ( 1863 ) stated the general rule which bears his
name, that growth precedes division and that the new wall is at right
angles to the long axis of the mother cell. There are many cases, espe-
cially in parenchymatous tissue, where this rule holds, but frequent ex-
ceptions to it occur in which the new wall is parallel to the long axis. An
extreme example of this is the longitudinal division of very long cambial
initials. Sachs (1878) noted that in most dividing cells the new wall meets
the old one at an angle of 90°, even though this requires that the new
wall be curved, and proposed this as a rule for cell division.

About a decade later a number of biologists were impressed by the
close resemblance between many cell configurations and masses of soap
bubbles. The behavior of molecules in liquids and the principle of surface
tension were then being worked out by physicists. One of the implications
of surface tension is that, because of molecular forces acting at their sur-
faces, liquids tend to pull themselves into forms with the smallest possible
surface area. This is why drops of liquid, for example, or soap bubbles are
spherical. The principle of least surfaces was applied to liquid film sys-
tems by the physicist Plateau (1873), who showed that in a mass of
bubbles the partition walls in every case arrange themselves so that they
have the least possible area. He also observed that where walls intersect
there are only three at a given point and that the angles between them
tend to be 120°, the point at which surface forces are in equilibrium.

The biologists Berthold (1886) and Errera (1888) applied this prin-
ciple to young cell walls, assuming that these walls in the beginning are
essentially weightless liquid films. The rather striking resemblance often
observed between a mass of cells and a mass of bubbles on this assump-
tion is easy to understand. Some interesting implications of the principle
of least surfaces for the problem of cell division have been developed by
D'Arcy Thompson (1942).

Only a few examples need be cited here. If, in a cubical box, the sides
of which are liquid films, a film partition extends across the middle, the
partition will be flat. If it is gradually moved toward one of the sides so
that the two "cells" become more and more unequal in size, it will sud-
denly shift to a position across a corner of the box and, as seen in section,

The Cellular Basis of Growth

45

Fig. 3-13. Hypothetical cube of film
with a film partition moving from left
to right across it. When a position is
reached 31.8 per cent of the distance
from the right-hand side, this partition
slips into the corner and becomes
curved, as shown. ( From D'Arcy
Thompson. )

will now be curved instead of straight as it was before (Fig. 3-13). The
point where this shift occurs is the point where the wall, now ( in section )
a quarter of the circumference of a circle, has the same length that the
flat partition wall had, for the wall will have the least possible area that
will enclose the volume of the smaller "cell," the latter now being part
of a cylinder. If this smaller cell is then made still smaller, the wall that
separates it from the larger one will continue to be curved and to be less
than any other wall area that could bound the volume of the smaller cell.
Just where the point of shift from flat wall to curved will occur can be
calculated by determining the point at which (before the shift) the length
of a curved wall (a quarter of the circumference of a circle) across the
corner will be the same as that of the flat partition wall. Both will enclose
the same area. If it is assumed that each side of the cube, and thus the
length of the flat partition, equals 1, then

2irr

= 1 %rr = 4 and r = ^- = 0.637

Ait

The area of a quarter circle with this radius is tt( 0.637 )2/4 = 0.318. This
also is the area of the smaller rectangular cell just before the shift. Thus
the distance from the partition wall to the side wall, when it shifts from
straight to curved, is 0.318 of the diameter of the cube. Experiments with
films essentially confirm this theoretical expectation. In cases of unequal
division of actual cells, such as the formation of companion cells in sieve
tubes, the new cell is usually cut out of a corner of the old one, as this
theory of least surfaces requires.

Many dividing cells in plants and animals are spherical, and here the

46

Growth

application of the liquid film theory is particularly interesting. In the di-
vision of an egg into two equal cells, for example, the position of the
wall between the two daughter cells, if they behave like soap bubbles,
can be determined. This new wall should form an angle of 120° with the
tangent to the circumference of each daughter cell at the point where
these meet the partition wall, since this is the position where the sur-
face forces will be in equilibrium and where the film system thus is stable.
It is obvious geometrically that this wall is in such a position that the
distance between the centers of the two new cells is equal to their radii
(Fig. 3-14). When a single spherical cell, such as an egg or an algal cell,
divides thus equally, the position of the two daughter cells relative to
each other is approximately what this theory demands.

Fig. 3-14. Stable partition and walls of minimum surface assumed by two equal
bubbles which are in contact. Angles OPQ and OPR are 120°. The distance between
the centers equals the radii. ( From D'Arcy Thompson. )

Where such a divided bubble divides again but now by a partition at
right angles to the plane of the first one, these two walls usually do not
meet at an angle of 90° but there is a readjustment in the film system so
that they meet at 120°, the stable position. Arrangements like that of
Fig. 3-15d may thus result, which resembles a group of actual cells. Any-
one familiar with cellular structure and who draws a bit of it comes almost
instinctively to make the cell walls intersect at angles of about 120°,
much as they would if they were liquid films.

Where a spherical bubble is divided unequally, the curvature of the
partition wall can be calculated. Since the pressure is inversely propor-
tional to the radius of curvature, a small bubble pulls itself together, so
to speak, more strongly than a larger one. Thus P = 1/R, where P is the
pressure and R the radius. The pressure that determines the radius of the

The Cellular Basis of Growth 47

partition wall between unequal bubbles is thus the difference between
the pressure of the smaller bubble and that of the larger one. If R equals
the radius of the partition wall, / that of the smaller bubble, and r that
of the larger one, then 1/R = 1// — 1/r, or R = rr7(r - r'). In other
words, the radius of the partition wall is the product of the two bubble
radii divided bv their difference. If two bubbles have radii of 3 and 5, for
example, that of the partition wall will be 7.5. In spherical cells of un-
equal size which are dividing, the new wall does tend to have this theo-
retical radius.

Where the dividing cell has a relatively firm wall, however, as in micro-
spores within which a small prothallial cell is cut off, the situation is
different, since only the new dividing wall now acts as a liquid film. It
will be curved and will occupy a position such that it intersects the old
wall at the stable position of 90°. If the linear distance between the two

Fig. 3-15. Plate of eight cells (or
bubbles) assuming a position of equi-
librium where cell surfaces are of mini-
mum area. (From D'Arcy Thompson.)

points of intersection (as seen in section) and the radius of the large
cell are known, the radius of curvature of the new wall can readily be
calculated.

There are other cases of division walls, notably in "rib" meristems
where the cells are in parallel rows and growth is strongly polar, which
may also be interpreted on the liquid-film theory even though the re-
semblance to a bubble system is much less close. In such rows of cells
it can be observed that the new cross walls, even in the phragmosome
stage, always tend to avoid a position that would put them opposite a
cross wall in an adjacent row ( Fig. 3-16 ) and would thus bring four walls
together, unstably, at a point. The walls are always "staggered," like
bricks in a wall. This often prevents a new wall taking its natural posi-
tion, which would divide the cell into two equal parts. The angles be-
tween the walls are larger than 90° but do not reach the theoretical 120°.
It may be that surface forces are operative in pulling the new wall away

48

Growth

from the intersection point with an old one and thus tending to form an
angle of 120°, even though the longitudinal walls, which are relatively
firm, remain essentially straight and the theoretical angle cannot be

attained.

The theory that the position and curvature of dividing cells are what
they would be if the walls were liquid films lends itself to some interest-
ing geometrical analyses, for which the reader is referred to Thompson's
book. Giesenhagen's work (1905, 1909) also has a discussion of the
theory and its applications. Various experiments with actual liquid films
have been reported by van Iterson and Meeuse (1942), and Matzke
(1946) has discussed the role of surface forces in determining cell shape.
There is no doubt that the configurations of the cells in an actively grow-
ing mass often do resemble a system of bubbles, for there are usually no
more than three walls intersecting at a point and the angles between them
tend to approximate 120°. The young walls are at least semiliquid, so that

-f #

Fig. 3-16. Walls in dividing cells (as shown by position of phragmosome) tend to avoid
continuity with adjacent partition walls. ( From Sinnott and Block. )

surface forces are doubtless operative to some extent in determining their
position. In any morphogenetic analysis the least-surface theory therefore
must certainly be taken into account. It greatly oversimplifies the prob-
lem, however, and fails to explain some facts with which the student of
plant development is confronted. Among the chief objections to it are the
following:

1. The theory in its simplest form is applicable only to weightless
liquid films, and young cell walls obviously are not such, though they
mav approach this condition. To account for their position the theory
would require correction.

2. Many division walls are formed in positions different from those
which the theory demands. Often the new walls are parallel to the longer
axis of the cell instead of at right angles to it. The most extreme case of
this occurs in dividing fusiform initials at the cambium which are 50 times
or more as long as wide but which nevertheless divide lengthwise.

The Cellular Basis of Growth 49

3. The early wall formed by the cell plate, and certainly the phragmo-
some which precedes it in vacuolate cells, are not at first continuous films
and would thus not follow the law of least surfaces.

4. In many cases, as often in the unequal division that cuts off a
stomatal mother cell, the new wall is at first straight instead of curved
and becomes curved only later, as the turgor of the cell increases.

5. Frequently, as in growing cork layers, the new division wall is laid
down exactly opposite a partition wall in an adjacent cell so that four
walls do come together at a point (p. 195). This also happens in tissue
which is to form aerenchyma and in which the cells are in regular rows
with cross walls opposite. Here, however, at the point where the four
walls meet, a small air space (which later may enlarge) is commonly
formed by the pulling apart of the walls so that the wall angles do tend
to reach the theoretical 120°.

6. In a system of film bubbles increasing in number by the formation
of new walls, the equilibrium least-surface configuration is reached by a
shifting of the wall positions within the film system. This involves some
gliding or sliding of the bubbles in relation to each other. Such a change
could happen in animal tissues where the cells are free to move about, at
least to some degree, but would be impossible in most plant tissues, where
they are cemented to one another.

For these reasons it is clear that the theory of surface forces alone is by
no means sufficient to explain all the facts as to the position of new cell
walls and the planes of cell division. Other physical factors are doubtless
involved in determining these events. Among them pressure is important.
Kny ( 1902 ) found that pressure applied to a dividing cell forced the
mitotic figure into a position in which its long axis was oriented at right
angles to the direction of the pressure, and the new wall consequently
was parallel to this direction. This fact, incidentally, makes an important
contribution to our knowledge of the character of the cytoplasm, at least
at this time in the history of the cell. If the cytoplasm were essentially
fluid, pressure from without should not change the orientation of struc-
tures in it but would do so if the cytoplasm had a structural framework.
Other evidence for the conclusion that walls are formed parallel to pres-
sure on the cell can be found in the cortex of the young stems of many
woody plants. Here the cells tend to be elongated tangentially, presum-
ably because of the pressure exerted by the expansion of the vascular
cylinder below through cambial activity. If these cells divide again,
radial walls, parallel to the direction of cambium pressure, are often to be
seen. As Kny points out, however, in cambial cells, which are presumably
under radial pressure, division is chiefly periclinal (at right angles to the
pressure) instead of anticlinal. This he attributes to "inner factors." In the

50

Growth

case of radial divisions in the phellogen, Bouygues (1930) concludes that
pressure is not a factor.

The plane of division is evidently related to the polarity of the cell and
is further discussed under this topic (p. 131 ). It has been studied particu-
larly in the egg of Fucus. Here centrifugal force, light, electricity, and
gradients in concentration of various substances have been found to affect
this plane.

In certain colonial blue-green algae and flagellates, in pollen mother
cells, and in some other cases where division in all the cells is simul-
taneous and in the same plane, the planes of each successive division tend

o°

45°

CL

90°

0°

45°
103

90°

Fig. 3-17. Distribution of angles between mitotic spindles and longitudinal axis of the
ovary in an elongate type of cucurbit fruit ( above ) and an isodiametric one ( below ) .
There is evidently a higher proportion of divisions nearly at right angles to the axis
(spindles with low angles) in the former. In the latter, divisions are approximately
equal at all angles. (From Sinnott.)

to be at right angles to each other so that a regular pattern of cells in
twos, fours, eights, sixteens, and so on, all in one plane, is produced. Be-
tween divisions the cells tend to grow but not enough to make them
isodiametric, so that the next division is at right angles to the longer axis
of the cell, as it would be in a least-surface configuration (Geitler,
1951). Division in three planes sometimes occurs, producing cubical
colonies.

In many instances there is no obvious explanation for the particular
plane in which a cell divides, and we are forced to attribute this to genetic

The Cellular Basis of Growth 51

factors. Steward (1958) finds that in cells freely suspended in culture the
planes of division are highly irregular and unpredictable, since such cells
are not subject to the organizing restraints that are operative in the nor-
mal plant body.

The forms of most plant structures are presumably related to the planes
in which their constituent cells divide. In a few cases this relationship has
been demonstrated. Thus in ovary primordia of elongate gourds such as
Trichosanthes and the "club" variety of Lageruiria, Sinnott ( 1944 ) meas-
ured in the growing ovary the angles between the mitotic spindles and
the longitudinal axis of the primordium and found that there were many

45°
Anaphase

0°

O.

45°
Telophase

90°

Fig. 3-18. Angles between mitotic spindle and ovary axis in metaphases, anaphases,
and telophases in Trichosanthes, the snake gourd, where the great preponderance of
divisions are transverse and thus predictable as to orientation. The mitotic figure evi-
dently becomes more stabilized in direction as mitosis proceeds. ( From Sinnott. )

52 Growth

more of them parallel to the primordium axis, in the direction of growth
in length, than at right angles to it, in the direction of growth in width.
In isodiametric ovaries, however, spindle angles were almost equally
distributed between 0 and 90° to the axis (Fig. 3-17).

The question arises as to just what determines the plane of cell division
in cases like this. It cannot be simply the orientation of the mitotic spin-
dle, for this can be shown to change during mitosis. Thus in the fruit of
Trichosanthes, which is very long and narrow, practically all the divisions
are transverse to the long axis and their orientation can thus be predicted.
The spindles in metaphase, however, are by no means all parallel to the
axis but vary considerably. In anaphase the variation is much less, and
in telophase the cell plates are almost all transverse ( Fig. 3-18 ) . Evidently
the spindle rolls about somewhat during mitosis (as it has been seen to
do in living material of other forms ) but finally settles into position. What
this position will be seems to be determined by the cytoplasmic body
since, in vacuolate cells, the phragmosome is formed at prophase in the
position of the final cell wall (p. 25).

Something certainly controls not only the plane of cell division but the
distribution of divisions and the amount and character of cell expansion.
Whatever this may prove to be, it is concerned with the origin of organic
form. If one looks at a section through a young and growing plant struc-
ture, such as an ovary primordium, he sees a mass of cells of various
shapes and dividing in many planes. Here chaos seems to reign. When he
observes how such a structure develops, however, and finds that it is
growing in a very precise fashion, each dimension in step with all the
others, he comes to realize that this is not the seat of chaos but of an
organizing control so orderly that a specific organic form is produced.
This realization is one of the most revealing experiences a biologist can
have and poses for him the major problem that his science has to face.

CELL SHAPE

One of the simplest manifestations of organic form is in the shape of
individual cells. This obviously involves plane of cell division, cell size,
polarity, microstructure of the wall, genetic constitution, and other fac-
tors.

Since the cell, at least at first, is a fluid system, its natural shape, other
things being equal, is that of a sphere, for this has the least surface in
proportion to its volume. Most cells, however, are parts of tissues and
thus are closely packed against neighboring cells on all sides. This re-
sults in a modification of the basic spherical shape to that of a polyhedron
with flattened sides, each representing a plane of contact with an adja-
cent cell. How many faces should such a cell have, and what sorts of

The Cellular Basis of Growth 53

polygons should these faces be? At first it was believed that cells were
12-sided figures, since when spheres are stacked together like cannon
balls, each touches 12 others. Lord Kelvin (1887, 1894), approaching the
problem mathematically, showed that when space is divided into similar
units, each with a minimum area of partition and with stable angles,
each unit will be a 14-faced figure or a tetrakaidecahedron and that eight
of its faces will be hexagons and six will be squares. This, he thought,
was what the shape of a cell in pith or similar tissues theoretically
should be. F. T. Lewis ( 1923 and others ) found that the average number
of faces in such cells was, indeed, close to 14 but that only very rarely
did a cell with this number of faces show eight hexagons and six squares.

This problem has been studied with particular care by Matzke and
his students and reported in a series of papers. The results have been
briefly reviewed by Matzke (1950), who cites the more important papers
from his laboratory. The general conclusion is that parenchyma cells do
tend to have 14 sides but that "ideal" ones, conforming to Lord Kelvin's
rule, occur very infrequently. Matzke points out that many factors other
than mathematically ideal space-filling are involved in determining cell
shape, among them pressure, surface forces, differences in cell size, direc-
tion of cell division, unequal growth, and genetic constitution. The prob-
lem is being attacked developmentally by an analysis of cell shapes at the
meristem (Matzke and Duffy, 1956). In dividing cells, the number of
faces here rises to about 17 and in daughter cells drops at first to be-
tween 12 and 13. The total cell population has an average number of
about 14 faces.

In more specialized tissues there is a wide variety of cell shapes.
Palisade cells are elongated at right angles to the leaf surface. Most cells
of the vascular and conducting tissues are elongated parallel to the axis.
Hairs and glandular cells have many forms. Some cells expand equally
on all sides. Others, like root hairs, grow only at one point. Still others,
such as the more fantastic sclereids, have many growing regions ( Foster,
1955, and others ) . Galston, Baker, and King ( 1953 ) found that benzimida-
zole promotes the transverse as opposed to the longitudinal extension of
cortex cells in the pea epicotyl. Doubtless the polarity, or polarities, of the
cell and the plasticity, elasticity, and microstructure of its walls are in-
volved in shape differences.

Tenopyr ( 1918 ) found that in leaves of different shapes the shapes and
sizes of cells were constant. Riidiger ( 1952 ) , however, observed that in
tetraploid plants the subepidermal cells of leaves, hypocotyls, and other
organs were not only absolutely but relatively wider than in diploids, a
fact which he relates to the greater relative width found in most tetra-
ploid organs as compared with diploid ones.

Even in microorganisms where the cells are free from contact with

54 Growth

others, they often display shapes by no means spherical. Many unicellular
green algae and the simpler fungi are examples of this. Von Hofsten and
von Hofsten (1958) have explored the effect of various factors on cell
shape and thus on vegetative characters in the ascomycete Ophiostoma.
In the development of cell shape genetic factors are doubtless impor-
tant, and these appear to control cytoplasmic patterns, wall differences,
and other factors. Cell shape is one aspect of the more general problem
of differentiation.

Much of morphogenetic significance can be learned from a study of
individual cells. A knowledge of their relations to each other, and par-
ticularly of the way in which they form cell aggregates, is still more im-
portant. This involves the general problem of meristematic activity, the
subject of the next chapter.

CHAPTER 4

Meristems

In many of the morphogenetic problems which they present, plants and
animals are very similar. The fundamental physiological differences that
distinguish these two groups of living things, however, produce a number
of developmental differences between them. Among these, that in method
of growth is conspicuous. Because of their ability to synthesize food from
inorganic substances, plants have developed, in all forms but the smallest
and simplest, a body which is nonmotile and anchored to the soil or other
substratum. This doubtless resulted, during the course of evolution, from
the fact that motility in a plant is not necessary for obtaining food, as it is
in animals.

The motility of animals requires that their skeletons be jointed and
the rest of their bodies relatively soft and plastic. Plants, however, gain
the necessary rigidity not by a specially differentiated skeleton but by a
thickening of the walls of most of the cells. This is especially conspicuous
in the fibrovascular system of higher plants but it occurs in other tissues.
The plant cell wall, because cellulose is characteristically deposited in it,
is a much firmer structure than the rather tenuous membrane which sur-
rounds typical animal cells. As a result, plant tissues themselves are also
firmer, save in exceptional cases such as certain short-lived floral parts.
As a consequence of this distinctive character, most plant cells, as soon
as their final size is reached, become locked up, so to speak, in a firm box
of cellulose. Such a cell ordinarily does not divide further, or if it does
its daughter cells cannot expand, so that mature plant tissue usually grows
no more. In almost every part of the soft-celled animal body, on the
contrary, growth occurs not only during development but in the restora-
tion and repair of tissues throughout the life of the individual. It should
be remembered, however, that under certain conditions a plant cell or a
group of cells may become embryonic again and begin to divide (p. 232),
setting up a new growing region. There is no doubt that most cells— per-
haps all— are potentially able to do this. What prevents it is not simply
mechanical confinement by the wall but so-called correlative factors that
limit each cell to the development appropriate for its particular place in
the organism.

55

56 Growth

If a plant is to grow, this must be accomplished by allowing some of
its cells to escape the general fate and remain capable of division, pro-
gressively forming new tissues but preserving a remnant that persists in
a perpetually embryonic condition. The plant body grows in size by the
activity of such localized growing points or regions, the meristems, which
are centers of cell division and cell expansion.

The axis of the plant grows in length by a meristem at the apex of stem
and root, and in width by a sheath of lateral meristem, or cambium. De-
terminate organs such as leaves, however, rarely have sharply localized
meristems but enlarge throughout much of their extent, as an animal body
does, until growth ceases. Meristems are obviously of much interest to
the student of plant morphogenesis. They provide, in a sense, a con-
tinuous embryology for the plant and offer an important point of attack
on the problems of plant development.

APICAL MERISTEMS

In the simplest plants, the lower algae and fungi, growth is hardly
localized at all. Cells capable of division are either present throughout
the plant body or in considerable portions of it, and nothing which might
be called a meristem is to be found. In Spirogyra, for example, growth
in length of the filament is produced by cell division almost anywhere in
it. In such a membranous type as Ulva, growth results from divisions at
right angles to the surface throughout most of its area. In coenocytic
forms, the whole thallus enlarges, and growth is not related to cell di-
vision at all.

In some of the simpler filamentous brown algae, however, growth in
length is limited to the tip of the filament, which is occupied by a single
large cell. This divides transversely, and a series of daughter cells is thus
produced from its basal face. They and their daughter cells divide a few
more times, but division finally ceases. The only permanently embryonic
cell is the apical one, which thus dominates the development of the plant
body. Branches originate by the lengthwise division of this apical cell
(Fig. 4-1).

In types like Fucus, with larger and more complex plant bodies, growth
still originates by the activity of an apical cell, which occupies the base
of a terminal notch in the thallus. This cell cuts off daughter cells from
its two lateral faces. From these and their descendants are formed the i
various tissues of the thallus. A fern prothallium grows in much the same
way, developing under the control of the meristematic region in the
notch. This control may be relaxed, however, and almost any cell in the
structure may begin to divide. Many prothallia never form the typical
heart-shaped structure.

Meristems

57

Fig. 4-1. Terminal portion of the alga Sphacelaria,
showing how thallus is produced by activity of the
apical cell and its descendants and how a branch
originates. ( From Haberlandt. )

Throughout the bryophytes, the ferns, the horsetails, and many of the
lycopods, growth of the plant body is governed by the activity of apical
cells, one at the apex of the shoot and the other at the apex of the root.
These cells are usually pyramidal with the base of the pyramid outward,
and division takes place parallel to the three inner sides of the pyramid.
Most growth of tissues results from the later division of these daughter
cells and their descendants, but growth seems to be initiated and domi-
nated by the apical cell (Figs. 4-2, 4-3). It is not clear, however, just
what the function of the apical cell is. Wetmore ( communication to the
author ) states that he has very rarely seen an apical cell dividing and he
suggests that these cells may function as do the groups of large cells just
below the apex of root and shoot in angiosperms, which are thought to
be centers of metabolic activity. Most of the actual cell division in the
meristems of these lower vascular plants takes place in the cells just be-

Fig. 4-2. Longitudinal section through apex of a fern root, showing origin of tissues
from the apical cell. ( From Sacfis. )

58

Growth

side or below the apical cell. In ferns, lycopods, and horsetails this con-
siderable body of embryonic cells at the apex of the axis somewhat re-
sembles the terminal meristems of higher plants.

Among bryophytes, the origin and arrangement of the leaves and the
structure of the various tissues can usually be traced back to precise
divisions of the apical cell and its daughter cells so that there is a very
definite pattern of cell lineage in the plant body. This is especially
diagrammatic in such a form as Sphagnum, where the two markedly
different types of cells in the leaves can be seen to originate in differen-
tial cell divisions. Such a precise cell lineage is less conspicuous in higher

Fig. 4-3. Longitudinal section of shoot apex Fig. 4-4. Selaginella wildenovii. Me-
of Equisetum, showing apical cell and its dian longitudinal section of young
derivatives. ( From Golub and Wetmore. ) shoot, showing apical cell and its de-

rivatives. ( From Barclay. )

forms but often can still be traced even there. In one species of
Selaginella (Barclay, 1931), for example, the derivation of the epidermis,
cortex, pericycle, endodermis, and vascular cylinder can be traced back
to direct descendants of the apical cell (Fig. 4-4).

Although the distribution of the leaves and the general organization
of the shoot are determined in many of the lower forms by the activity
of the apical cell and the arrangement of its derivatives, Golub and
Wetmore (1948) found that in Equisetum there is no relation be-
tween the cellular pattern of the apex and that of the mature axis derived
from it.

Meristems 59

In a few of the lower vascular plants, notably Lycopodium, no single
apical cell can be distinguished, and the same is true of most gymno-
sperms and angiosperms. Instead, the meristem at the tip of both root
and shoot consists of a considerable group of embryonic cells. Many of
these divide actively during the growth of the plant, and they produce
all the tissues of the axis (save those formed by later cambial growth)
as well as the leaves and branches.

Much attention has been paid in recent years to the structure, organiza-
tion, and activity of apical meristems, particularly in the ferns and seed
plants. These regions of persistent embryonic character have often been
compared to animal embryos. Botanists have tried to find a correspond-
ence between their structure and that of the parts that grow from them
so that the developing plant might be analyzed in terms of embryonic
regions, as zoologists have been able to do by using the germ layers
established in the animal embryo. A wide variety of plant meristems
have been studied and compared, but differentiation into layers as pre-
cise in their fate as ectoderm, mesoderm, and entoderm seems rarely to
occur. Some botanists, however, do regard meristematic layers as true
germ layers (Satina, Blakeslee, and Avery, 1940).

Although these apical meristems do not provide a precise classification
of plant tissues, much information of importance for morphogenesis may
be derived from them. Observation of the way in which meristems have
produced the various tissues and organs of plants has been of service in
the solution of problems in growth, differentiation, and phyllotaxy. Plant
meristems offer the great advantage that a single plant may produce
many of these embryonic regions, which are thus genetically identical.
Though small, meristems are open to direct experimental investigation,
and this has already provided results of much morphogenetic significance.

The apical meristems of shoot and root, though alike in many respects,
show certain characteristic differences, and further consideration of their
structure and activity will be more profitable if each is considered by
itself.

THE SHOOT APEX

The length of the growing region in the shoot is considerably greater
than in the root and may often extend over a region of several centi-
meters. Cell division persists longer in some tissues than in others and
usually stops first in the pith. No very sharp line is to be found between
the developing region and the mature portion behind it. The strictly
meristematic zone, however, where cell division chiefly occurs, is usually
limited to a few millimeters or less, and most growth of the stem in length
results from cell elongation back of this.

60

Growth

The tip of the meristem in seed plants is usually a rounded, dome-
shaped mass of cells around the base of which the leaf primordia appear
in succession (Fig. 4-5). Some earlier investigators reported the presence
of apical cells here but later work did not confirm this. Newman (1956),
however, finds dividing cells in the very center of the apical dome in
Tropaeolum and Coleus and believes that they are to be regarded as
true apical cells. A similar situation has been reported in certain roots.

\<-l

b 4"'" •'■ ?w W>. "• •

; ■ '

-„ <%~ - -\V< r- - - r t ■"..:' ••■.. v;

fc

"••V f

Fig. 4-5. Longitudinal section through shoot apex of Coleus, showing meristem, leaf
primordia, and two bud meristems. (Courtesy Triarch Botanical Products.)

Much attention has been paid to the structure of the dome itself.
Hanstein (1868) was the first to give careful study to the shoot meri-
stem. He noted the presence in it of well-marked layers of cells and
distinguished three regions, or histogens, each of which, he believed,
gave rise to a particular tissue or tissues of the stem. The outermost,
or dermatogen, is a single layer and produces the epidermis. Under this,
several layers thick, is the periblem, giving rise to the cortex. The inner-
most core, or plerome, without well-marked layers, forms the vascular
cylinder and pith ( Fig. 4-6 ) .

This hypothesis would have important implications for morphogenesis

Meristems

61

Fig. 4-6. Diagram of shoot apex according to Hanstein's interpretation. D, dermatogen;
Pe, periblem; PI, plerome. (After Buvat.)

if it could be supported. There is now much evidence, however, that no
constant relation exists, valid for all plants, between these "histogens"
and the structures formed by them. Some of this evidence comes from
direct observation, as in Schoute's (1902) studies on the origin of the
vascular cylinder. Some is derived from the structure of periclinal chi-
meras (p. 268) in which the layer or layers derived from one graft com-
ponent can be distinguished by the size of their cells from those coming
from the other, a distinction that persists in the mature structures and is a

Fig. 4-7. Vinca minor. Longitudinal section through shoot apex, showing three-layered
tunica and unlayered corpus beneath it. ( From Schmidt. )

62 Growth

useful means of determining their particular meristematic origin. Evidence
from these sources shows that a particular tissue may come from one
meristematic layer in one plant and from another in another plant.

Hanstein's histogen theory has largely been superseded by another,
first proposed by Schmidt (1924; Fig. 4-7). This recognizes an outer zone
of layered cells, usually from one to four cells thick, the tunica, covering
a core of unlayered cells, the corpus. The tunica-corpus theory does not
maintain that either of these regions produces specific organs or tissues
but describes the common type of organization of the shoot apex (see
Reeve, 1948).

The significance of layering in the meristem has often been overem-
phasized. Whether or not a layer is formed depends on the plane of di-
vision of the meristematic cells. When the apical initials always divide

Fig. 4-8. Longitudinal section of shoot apex of Torreya californica, showing almost
complete absence of layering. ( From Johnson. )

anticlinally they obviously will produce a layer, and its growth will be
entirely growth in surface. Where divisions occur in other planes or ir-
regularly, layers are not produced. Specific factors such as mechanical
pressure (p. 49) which influence plane of division may thus determine the
presence and number of layers. If the central region of the meristem
is growing faster than the surface, the latter will be subjected to pres-
sure, its cells will tend to divide parallel to the direction of that pressure,
and a layer will be formed. Perhaps this is the only real significance of
the layered structure. It is noteworthy that the shoot meristems of many
gymnosperms (Korody, 1938, and others; Fig. 4-8) show little or no
layering but that they produce structures in a perfectly normal fashion.
Layering as such, in the sense of marking out particular regions of the
meristem that are significant morphogenetically, seems to be of much
less importance than many workers have regarded it.

Meristems

63

Fig. 4-9. At left, shoot apex of Abies pectinata, semidiagrammatic. At right, diagram
of confocal parabolas as postulated by Sachs from such an apex as that of Abies.
( From Sachs. )

Even though layering may not be of primary significance, the general
pattern formed by the planes of cell division in the meristem is of in-
terest. Reinke (1880) and Sachs (1878) many years ago called attention
to the fact that the divisions approximately at right angles to the surface
of the meristem and axis and those parallel to it tend, if extended, to
form two sets of essentially parabolic curves with a common focus
just below the apex of the meristem ( Fig. 4-9 ) . This somewhat diagram-
matic interpretation of the situation has largely been neglected by
recent writers. Such a pattern can be found both in shoots and roots,
however, though it is often inconspicuous in small meristems. Foster
( 1943 ) called attention to the observations of these early workers in his
study of the broad apices of certain cycads; and Schuepp, both in his
volume on meristems ( 1926 ) and in a later paper ( 1952 ) , has emphasized
it. The pattern made by these two series of curves is modified as they

V^2

Fig. 4-10. Diagram of longitudinal section of broad apical shoot meristem of Micro-
cycas. 1, initiation zone; 2, central mother-cell zone; 3, peripheral zone; 4, zone of rib
meristem. Arrows represent lines of convergence of cells. (From Foster.)

64

Growth

suffer displacement, transversely and longitudinally, if growth is more
rapid in some regions and directions than in others. In such broad
apices as those of Microcycas, the normal pattern has been greatly
modified and the tip flares out in a fan-like fashion (Fig. 4-10). What
these facts mean morphogenetically we do not know, but they show that
the growing apex has a pattern of organization which develops in a pre-
cise fashion.

The shoot meristem is by no means homogeneous or structureless in
other particulars. In recent years many students have come to recognize
a rather uniform series of zones within it, distinguished not primarily by
layers or planes of cell division but by differences in the character of
their cells. A general survey of zonation in vascular plants has been
made by Popham ( 1951 ) , who, from his own work and a long series of
published descriptions of meristems, has grouped them into seven classes.

Fig. 4-11. Diagram of zonation in the shoot apex of Chrysanthemum morifolium. 1,
mantle layer; 2, central mother-cell zone; 3, zone of cambium-like cells; 4, rib meri-
stem; 5, peripheral zone. (From Popham and Chun.)

In the vascular cryptogams there are one or more apical cells or a sur-
face meristem, with tissues below sometimes differentiating into a cen-
tral and a peripheral meristem. Among seed plants, four or five zones
can be seen (Fig. 4-11). These are a surface zone, or mantle, including
two to several cell layers and corresponding roughly to the tunica; a
zone of subapical mother cells, irregular in shape, often rather highly
vacuolate and dividing less rapidly than the surrounding ones; a central
zone giving rise to the rib meristem and pith; and a peripheral zone just
outside this, producing cortex and procambial tissue. In some plants,
just below the mother-cell zone there is a somewhat cup-shaped arc of
cells stretching across the axis, the cambium-like zone. Popham and
Chan ( 1950 ) and Popham ( 1958 ) have described a typical case of this
last type. The particular functions of these zones are not well understood

Meristems 65

but they doubtless differ physiologically. The subapical mother-cell zone
is perhaps comparable to a somewhat similar region in the root (p. 78)
where the rate of protein synthesis is lower than in surrounding cells.

An attempt to follow cellular changes at the surface of living shoot
apices has been made by Newman ( 1956), using Tropaeolum and Coleus.
By an ingenious technique he was able to follow and draw, for as long
as 9 days, the divisions of individual surface cells. At the very tip of the
meristem he observed that divisions were frequent and believes that in
this region there is a small group of cells that may be regarded as apical
cells. His results fail to confirm those of Lance (1952), who reported
that divisions were infrequent at the very apex, as Plantefol's theory
(p. 156) assumes.

There is a considerable literature dealing with the structure of the shoot
meristem in particular plants and under different conditions. Much of
this has morphogenetic interest. Cutter (1955), for example, finds that
the organization of shoot apices in eight saprophytic and parasitic species
of angiosperms is essentially like that in plants with normal nutrition.
Boke in a series of papers (1955 and earlier) described the stem apices
and shoot histogenesis in a series of xerophytes, especially Cactaceae.
Stant ( 1954 ) compared the shape of the shoot meristem in five species
of monocotyledons and found a relationship between this character and
the growth habit of the plant. In general, where the meristem is long
and narrow, as in Elodea, the plant has well-developed internodes. Where
it is relatively short and wide, as in Narcissus, the stem is much reduced
and the internodes very short. The size of the apical dome is essentially
the same in cucurbits with large fruits as in those with small fruits, and
differences in organ size do not appear until a short distance below the
tip of the meristem (von Maltzahn, 1957). The difference between the sin-
gle-gene maize mutant "corn grass" and normal corn arises in the
meristem, the mutant having a relatively larger meristem and a more
rapid production of leaf primordia (Whaley and Leech, 1950). Bouffa
and Gunckel (1951) examined 54 species of Bosaceae but found no sig-
nificant relation between the number of tunica layers and the taxonomic
position of the plant. The development of the shoot meristem from its
early appearance in the embryo has been studied by various workers
(Beeve, 1948; Spurr, 1949; and others).

The implications of results from the study of the shoot apex for
morphological problems, especially the nature of the leaf, have been
considered by various observers. Philipson (1949) believes that the evi-
dence from this source supports the idea that the leaf is an enation and
not a consolidated branch system.

Leaf primordia are formed in regular sequence below the dome of the
shoot apex, and it is here that many of the structural characters of the

66

Growth

plant seem to be determined. The period between the initiation of two
primordia (or two pairs, if the leaves are opposite) is termed a plasto-
chron (Askenasy, 1880; Schmidt, 1924). These periodic changes in the
meristem can be seen best in opposite-leaved forms. As the two primordia
begin to appear, the apical dome between them becomes relatively flat.
When they have developed further but before another pair appears, the
dome bulges upward again and reaches its maximal surface area. In the
lower vascular plants the primordium arises from one or more of the
surface cells of the meristem but in the higher ones it develops as a
swelling on the side of the apex at the base of the dome, generally as
the result of periclinal divisions in one or more layers below the surface
one. The term plastochron index, for the interval between corresponding
stages of successive leaves, has been proposed (Erickson and Michelini,

Shoot Tip during Rutmg Prion

Shoot Tip during Second Growth Phatt

Fig. 4-12. Diagram of shoot tip of Abies concolor. At left, during resting phase. At
right, during second growth phase. That portion of the shoot apex above plane abed,
which marks the level of the youngest leaf primordium, has a very different zonal
topography in the two stages. 1, zone of apical initials; 2, mother-cell zone; 3,
peripheral zone; 4, zone of central tissue. ( From Parke. )

1957 ) as a better measure of the stage of development of a growing shoot
than is its chronological age. In many plants the shape and structure of
the meristem change somewhat with the season (Parke, 1959; Fig. 4-12).

The phyllotaxy of a shoot is determined by the arrangement of the
leaf primordia around the axis. This phyllotactic pattern has been studied
developmentally in the meristem, both through observation and experi-
ment, by a number of workers (Chap. 7). The regularity and precision
with which the leaf primordia arise at the shoot apex are evidence that
this region has a high degree of organization.

Branches are formed from meristems arising in the axils of the leaf
primordia. They are at first much smaller than the main apical meristem
but do not differ essentially from it. Whether the potentially meristematic
tissue here will grow into buds and whether these buds will produce
branches are dependent in most cases on the stimulatory or inhibitory

Meristems

67

influence of auxin or other growth substances (p. 386). The development
of axillary buds has been discussed by Sharman (1945) and by Garrison
(1955), who finds that they originate from a region of residual meristem.
After the organization of an apical meristem in the bud, the procambial
strands develop acropetally into the leaf primordia, as does the phloem.
Xylem forms at several loci and develops in both acropetal and basipetal

directions (p. 204).

When the shoot is producing leaves, the meristematic dome is relatively
low and rounded but when flower buds begin to be formed it becomes
steeper and more elongate. Flowers arise as modified branches, and the
floral parts develop from a series of primordia (Fig. 4-13). In the forma-

<2

Fig. 4-13. Longitudinal section through young inflorescence, showing stages in de-
velopment of floral primordia. i, bract; t, trace to primordium; v, procambial strand.
Most active meristematic areas are stippled. (From Philipson.)

tion of more complex inflorescences, however, the meristem changes
markedly. Since growth in length usually ceases at this time, what is
formed is essentially a determinate structure rather than an indeterminate
one like that of the vegetative shoot. What its character will be is de-
cided by the size and number of the flowers and the character of the
inflorescence. Various factors, notably the carbohydrate-nitrogen ratio
and the photoperiod, determine whether the meristem forms vegetative
or reproductive structures (p. 184). For accounts of the development of
the reproductive apex, see papers by Gregoire (1938), Philipson (1948),
Gifford and Wetmore (1957), and others.

The shoot meristem is not constant in size but changes during de-
velopment. In the young embryo it is very small, and it enlarges as the

68 Growth

plant grows. At the onset of reproductive maturity or at the end of the
life cycle it often becomes reduced again in size. In maize, a plant
essentially determinate in its growth, Abbe and his colleagues (1951a,
1951b, 1954) have studied the size of the apical shoot meristem (above
the first leaf primordia) and the size and number of its cells as these
change with time. In plastochrons 7 to 14 (the seedling stage until just
before flowering) the apex increases by a constant amount in each
plastochron but the duration of the plastochron decreases exponentially,
from a length of 4.7 days to one of 0.5 day. Cell size is essentially con-
stant throughout, so that all growth is by cell multiplication. The growth
rate per plastochron accelerates exponentially. In the five or six plasto-
chrons during early embryogeny, on the contrary, the duration of suc-
cessive plastochrons increases and the growth rate of the apex decreases.

Sunderland and Brown (1956) have determined the cell number and
average cell volume in the meristematic dome and the first seven
primordia and internodes, back from the apex, in the shoot of Lupinus.
The primordia increase exponentially in successive plastochrons but there
is little increase in cell volume in the internodes.

Cell shape in the shoot apex of Anacharis (Elodea) has been studied
by Matzke and Duffy (1955) with particular reference to the number
of faces. These range from 9 to 21 and are in general agreement with
the shape of cells in other undifferentiated tissues.

For a statement of conditions in the apical meristem of the shoot in
ferns the reader is referred to Wardlaw (1945). This author has also
published an extensive series of papers on experimental and analytical
studies of pteridophytes, many of which are cited in his books (1952«,
1952&) and in later papers by himself and his colleagues. The shoot
meristems of gymnosperms are described by Camefort (1956) and John-
son ( 1951 ) . General accounts of this region in the angiosperms, with re-
views of the literature, have been written by Foster ( 1939, 1949 ) , Sif ton
(1944), Philipson (1949, 1954), Popham (1951), Buvat (1952), and
Gifford (1954).

The ontogeny of a typical shoot apex (Xanthium) has been described
in detail by Millington and Fisk (1956).

EXPERIMENTAL STUDIES ON THE SHOOT APEX

Early work on the shoot apex was primarily descriptive, and much of
this still continues. It has been concerned with apical cells, planes of
division, cell lineages, layering, zonation, and the relations of the meri-
stem to differentiation and organ formation. This work has been of great
value morphogenetically for it has provided a fund of information as to
the structure and developmental activity of this determinative region

Meristems 69

of the plant, but it has yielded little knowledge of the meristem as a
living and functioning center of morphogenetic activity.

In recent years, however, an increasing number of workers have used
experimental methods to attack the problems of the meristem with
techniques like those which have proved so fruitful in the experimental
embryology of animals (Wetmore and Wardlaw, 1951). This part of the
plant is a perpetually embryonic region and thus offers many advantages
for work of this sort. Most shoot meristems are minute, however, and so
enfolded by protective structures that experimental work upon them has
had to await the development of specialized techniques. Means for direct
operative attack on the meristem have now been developed and have
begun to yield valuable results. In this work the Snows, Wardlaw, Ball,
Wetmore, and their colleagues have been particularly active. The methods
of tissue culture have recently added a wealth of information. Biochemi-
cal analysis by means of experiments with growth substances, chromato-
graphic techniques, and other methods is yielding further knowledge
of meristem physiology. This experimental work has powerfully supple-
mented earlier descriptive studies.

Direct operations on the meristem involve procedures of much delicacy
and are performed under a lens by tiny scalpels. Pilkington ( 1929 ) seems
to have been the first to do such work. She split the meristem of Lupinus
down the middle and found that each half regenerated a normal meri-
stem so that the original axis was now divided into two branches. Ball
( 1948 ) , also using Lupinus, divided the meristem into four parts
longitudinally and each of the four, by regenerative development, was
able to produce a normal shoot. Later ( 1952a ) he went still further and
split the meristem into six strips. Each of these, unless it was below a
minimum size, regenerated a new meristem and shoot, though leaf for-
mation was somewhat delayed and vascular tissue was poorly differen-
tiated until leaves had developed.

A major problem here is to find to what extent the meristematic tip is
autonomous and thus independent from the tissues below it in develop-
ment. In a fern, Dryopteris, Wardlaw (1947 and other papers) isolated
the apical meristem from the adjacent leaf primordia by four longi-
tudinal incisions (Fig. 4-14). It was thus continuous with the rest of the
plant only by the parenchyma of the pith below it, all the vascular tissue
having been severed. Despite this isolation, the meristem continued to
grow and to produce leaf primordia and leaves. Whatever material en-
tered it came through undifferentiated parenchyma. Provascular tissue
was developed below the tip but this did not make connection with the
vascular bundles in the stem below.

Ball ( 1948 ) did much the same thing in Lupinus, isolating the central
axis of the meristem by four deep incisions. In this axis, however (unlike

70

Growth

all cases studied in the ferns), vascular bundles were regenerated in the
former pith tissue and became connected basipetally with the vascular
system of the axis below. A normal shoot was thus restored. Similar
results were obtained by Wardlaw (1950) with Primula. Furthermore,
Ball ( 1946 ) succeeded in growing complete plants from isolated apices
in sterile culture, and this has now been done repeatedly in other cases,
both with ferns and seed plants ( see Wetmore, 1954 ) .

As a result of such experiments it is now generally agreed that the
shoot apex is totipotent and independent of the rest of the plant. This is
hardly surprising since many— perhaps all— cells are totipotent under
favorable conditions. The subjacent tissue must have some influence on
the apex, however, since from below there come into it not only water

Fig. 4-14. Longitudinal median section through the stem apex of Dryopteris, show-
ing how the region around the apical cell ( a ) has been isolated by deep cuts extend-
ing through the vascular tissue (v.t. ). (From Wardlaw.)

and nutrient materials but specific substances of morphogenetic im-
portance. The induction of flower buds at the meristem, for example,
results from a hormone brought thither from the leaves. There evidently
must be a reciprocal relation between the shoot meristem and the axis
below it for both are parts of the same integrated organic system.

The shoot apex has a morphogenetic role which goes beyond regenera-
tion, however, for it exerts a strong influence on the differentiation of
tissues and organs in the region adjacent to it. By a long series of ex-
periments reported in many papers (see Wardlaw, 1952a, 1952/7, and
Cutter, 1958) Wardlaw and his colleagues have made important con-
tributions to a knowledge of this differentiation. Much of the work was
done on the apical meristems of ferns. In Dryopteris, Wardlaw (1949&)
determined the region where the next leaf primordium would arise

Meristems 71

(through its place in the phyllotactic series) and then isolated it from
the apical cell by a deep tangential cut. Under these conditions a bud
rather than a leaf primordium developed. Evidently some influence com-
ing from the apex determines whether a new lateral outgrowth will form
the dorsiventral primordium of a leaf or the radially symmetrical, po-
tentially indeterminate one of a bud, a discovery of much importance
not only morphogenetically but morphologically. Cutter (1956) has
found that the three youngest primordia respond in the same way but
that older ones do not. These same young primordial areas (in Osmunda)
if excised and grown in culture will form buds and finally mature
plants, whereas the older areas, if cultured, will grow into typical leaves
(Steeves and Sussex, 1957). There is evidently a point before which the
lateral structure has the potentiality to form either a bud or a leaf, but
after a certain early stage has been reached its fate is determined.

Wardlaw has extended these studies further (1956a, b). When in-
cisions between apex and primordium were so shallow that the pre-
vascular strands were not cut, a leaf primordium still developed, sug-
gesting that this incipient vascular tissue is a pathway for morphogenetic
stimuli. When deep cuts were made on the radial and obaxial sides of a
primordium site, thus without isolating it from the apex, a leaf grew from
it, but this usually showed abnormally rapid growth.

In flowering plants results like these were not obtained, for isolated
primordia do not develop into buds but into dorsiventral leaves or
radially symmetrical leaf-like structures (Sussex, 1955). However, Cutter
(1958) found that in Nymphaea and Nuphar (favorable material be-
cause of their large meristems), although tangential cuts separating a
primordium from the apex did not change it to a bud, buds under these
conditions were formed more often and very close to the primordium.
The critical time for the determination of the fate of a primordium thus
seems to be earlier in flowering plants than in ferns.

The problem of phyllotaxy is closely related to conditions at the meri-
stem, for the arrangement of the leaves is presumably determined by
the distribution of their primordia. This subject will be discussed more
fully in the chapter on Symmetry, but it should be mentioned here that
the experimental work of the Snows and of Wardlaw on the factors that
determine where a given primordium shall arise has yielded much in-
formation. It is evident that the apex has an important influence on the
differentiation of primordia, but whether the exact determination of the
position of these structures results from chemical, mechanical, or geomet-
rical factors is still not clear. Experimental manipulation of the meristem
is a hopeful way of approaching this problem directly.

The differentiation of vascular tissue seems to depend on a stimulus,
probably a growth substance, passing basipetally from the apex. The

72 Growth

influence of buds on the production of vascular tissue below them is
well known. When growth of an adventitious bud is induced in the epi-
dermis, for example, a vascular strand usually differentiates in the paren-
chymatous tissue below it which establishes connection with the vascular
tissue of the leaf or stem (p. 245). More direct experimental evidence on
this problem is available from other sources. When Camus (1944, 1949)
grafted a bud of endive into root callus in culture, provascular strands
were formed below it. Camus attributes this to the effect of auxin (and
possibly other substances) produced by the bud. Wetmore and Sorokin
(1955) and Wetmore (1956) have shown much the same effects from
lilac buds grafted into lilac callus in culture. Here the amount of
provascular tissue induced in the callus below was much increased if
auxin was also added.

Wardlaw ( 1952c ) has called attention to the important effects on stelar
structure which are related to the strength of the meristematic stimulus
in the development of vascular structures. When leaf primordia in ferns
are removed, gaps in the vascular ring below are much reduced. In this
way it was possible to transform the axis of the normally dictyostelic
Dryopteris into a solenostelic form with a continuous ring. By further
reducing the size of the meristem through isolating it on a small piece of
tissue, even a protostelic condition was produced. The basis for such im-
portant morphological differences thus seems to be in the degree of de-
velopment of the meristem.

In recent years the physiology of these tiny shoot apices has also begun
to be investigated. Growth substances are evidently synthesized there,
but just what these are and how they act are still not known. Ball ( 1944 )
found that when auxin in paste was applied to the meristem apex of
Tropaeolum no changes were produced in it, presumably because of the
large amount of native auxin present; but below the tip hypertrophied
tissues, multiple leaves, and abnormal development of vascular tissue
appeared. The role of growth substances at the meristem involves many
important problems in plant physiology and morphogenesis (Chap.
18).

By use of the techniques of paper chromatography, information is
being gained as to the biochemistry and particularly the nitrogenous
components of apical meristems. Some of the pioneer work here is de-
scribed by Steward and others (1954, 1955) and by Wetmore (1954).
The meristematic region is well supplied with free amino acids. The
basic ones, arginine and lysine, are more abundant in the tip of the
meristem than in tissues farther back, in the primordia, leaves, and
stem. A substantial beginning has been made toward a knowledge of
the distribution of these substances and similar ones, as well as of DNA
and various enzymes, throughout the meristematic region and at dif-

Meristems 73

ferent stages in its development. Something is thus being learned about
the chemical as well as the histological organization of the shoot apex.

The techniques of tissue culture have also proved to be very useful for
a knowledge of meristem physiology. It has been found (Wetmore,
1954), for example, that the shoot apex of vascular cryptogams, when cul-
tured with only inorganic substances and sucrose, will produce entire
plants but that they will grow better if supplied with auxin and some
nitrogen source other than nitrates. Angiosperm apices (Syringa), how-
ever, will not grow in this simple medium, but if coconut milk and casein
hydrolysate are added, the tips root, and growth is much better. When in
the culture medium the same amino acids and amides are provided, and
in the same proportions, as are found in meristem tissue, growth is still
very slow and far from normal. Evidently something more is necessary.

Wetmore's demonstration (1954) that when apices of sporeling ferns
are cultured with successively higher concentrations of sucrose the leaves
that they produce correspond to those formed in progressive stages of
normal ontogeny (p. 222) shows the important morphogenetic and mor-
phological implications of nutritional factors.

The rates of metabolic processes in the shoot apex have also been in-
vestigated. Ball and Boell (1944), using the Cartesian-diver technique
by which it is possible to measure the rate of respiration in tiny bits of
living tissue, compared this rate in the apical dome of cells, the region
just below this where the first primordia are appearing, and a third region
below this (Fig. 4-15). In Lupinus, respiration was most active at the tip
and progressively less so below. In Tropoeolum, however, there was less
respiration in the extreme tip than in the region below it. The occurrence
of a descending metabolic gradient in the plant apex thus seems not to
be universal.

These various experimental studies on the shoot meristem have directed
attention even more strongly to this embryonic region. Many believe that
it is of primary importance for development and that in it the major
problems of morphogenesis, at least as far as the shoot system of vascular
plants is concerned, come sharply to focus. This conclusion is supported
by the facts that the apex is autonomous, a small portion of the tip of it
being able to produce an entire plant; and that if it is removed, the
development of the tissues below it finally stops. It is recognized, how-
ever, that certain structures, such as leaf primordia beyond a certain
stage, are partially removed from its control since they will develop in-
dependently in culture and are thus self-differentiating.

Ball has compared the shoot apex to an organizer such as has been
postulated in animal embryology. Such, in a sense, it is, but the com-
parison is not very exact since the organizer is a part of the embryo
which controls the development of the rest, wheeras the shoot apex

74

Growth

corresponds to the whole embryo itself and thus to the organism in minia-
ture. Recent work shows more and more clearly that the apex is an
organized system ( Wardlaw, 1953b, 1957a ) with a structure that is not
only histologically but biochemically integrated. Before this structure
can control development it must itself develop. Growth of the meristem

z

o

>-

X

o

HOURS

Fig. 4-15. Lupinus alhus, left, and Tropaeolum majus, right. Below, location of A, B,
and C pieces in the two shoot apices. Above, oxygen consumption of these three
pieces in milliliters of 02, at successive hours in the apparatus. In Lupinus there is a
gradient from A to C but in Tropaeolum the oxygen consumption is greater in B than
in A. ( From Ball and Boell. )

precedes that from the meristem. The initiation of a meristem may take
place in various ways— from the tip of a young embryo, from adventitious
buds by regeneration, or from groups of cells or even single cells— but in
every case from simple and undifferentiated tissue.

A study of the origin of meristematic centers within masses of tissue

Meristems 75

in culture promises to be enlightening. Here Steward and his collabora-
tors (1958) have done some significant work. They were able to grow
in culture dissociated phloem cells from the root of carrot. Some of these
produced multicellular masses. When a mass reached a certain size there
formed in it a sheath of cambium-like cells enclosing a nest of lignified
elements such as often is found in tissue cultures. In this spherical
nodule there developed a root meristem and then a shoot initial opposite
it. Thus an embryo-like structure was formed which was able to grow
into an entire normal carrot plant. Steward emphasizes the fact that the
change from random cell multiplication to organized development and
the formation of meristems comes only after the group of inner cells has
become enclosed by a wall of outer ones which cuts it off from direct
access to the coconut-milk medium outside and subjects these inner cells
to physical and presumably physiological restraints. Before this happens
they multiply irregularly and form simply an unorganized callus-like
mass. Such studies open up an important line of attack on the problem
of the origin of organized meristems. It will not be possible to understand
the role of meristems in development until we learn through experiments
like these how such an organized apical system comes into being.

THE ROOT APEX

The apical meristem of the root differs in several respects from that of
the shoot. It is relatively short, the elongating region of the root rarely
exceeding a millimeter in length. No lateral organs have their origin at
the apex, and thus there are no rhythmic changes here as in the shoot.
The lateral roots arise farther back, in the pericycle, and push out
through the cortex. The apical meristem produces not only the structures
of the root itself but, from its outer surface, the root cap, or calyptra.
Root meristems received much attention in the early work of Eriksson
(1878), Flahault (1878), Holle (1876), Janczewski (1874), and van
Tieghem and Douliot (1888).

In those lower vascular plants where shoot growth is centered in an
apical cell, the root grows in the same way (Fig. 4-2). In the higher
plants, however, although there is a meristem which is in many respects
like that of the shoot, there is less uniformity in its organization. In
most roots there are seen well-marked layers and to these some workers
have applied Hanstein's terminology. The direct origin of particular tis-
sues from particular layers is not uniform, and the same objections to
regarding the layers as histogenetic ones may be made as for the shoot.
The presence of the root cap prevents smooth and continuous layering
over the root apex, and this is probably the reason why periclinal chi-
meras are not found in roots.

76

Growth

In many forms growth seems to be centered in a small group of cells.
Brumfield (1943) produced specific chromosomal changes in root-tip
cells of Crepis and Vicia by X radiation which could be recognized in
the descendants of these cells farther back along the root. They were
found to form wedge-shaped sectors of the entire root, including parts
of the root cap, epidermis, cortex, and vascular cylinder (p. 268). Such a
sector usually occupied about a third of the area of the root cross section,
and Brumfield concluded that there were about three cells at the tip from

Fig. 4-16. Longitudinal diagram of root development as observed by Williams. The
tissues all arise from a small group of cells at the very tip. 1, epidermis; 2, hypo-
dermis; 3, endodermis; 4, pericycle; 5, mitotic figure; 6, young cortical cells; 7, stelar
initials; 8, dermatogen; 9, metaxylem initial. B, C, D, transverse diagrams showing
origin of cortical cells from a single cell of the endodermis. ( From B. C. Williams. )

which all the tissues of the root were derived, though these cells could
not be recognized in sections of the root apex. Von Guttenberg ( 1947 )
later presented evidence from a considerable variety of dicotyledonous
plants that there is a single apical cell that gives rise to the whole root
and which thus is comparable to the apical cell of lower vascular plants,
but this has received little confirmation.

Popham ( 1955a ) found in Pisum sativum a transverse row of meri-
stematic initials across the root apex that gives rise to all the tissues of
the root and the cap, and Clowes (1954) observed a somewhat similar

Meristems

77

condition in Zea. Both these workers believe that Brumfield's results can
better be explained on the assumption of such a small meristematic cen-
ter than of a group of apical cells, thus far unobserved. Clowes ( 1950 )
found meristematic layers in the root tip of Fagus that seemed discrete
enough to be called histogens.

Williams (1947) observed in many roots of vascular plants a rather
simple pattern of development. The epidermis, hypodermis, and endo-
dermis could all be traced back to a small group of cells at the very tip of
the plerome. The endodermal row, coming from this, gives rise by re-

Fig. 4-17. Phleum root tip. Graph showing rate of root elongation (A), average
length of epidermal cells (B), and new transverse cell walls (C), at various distances
from the root tip. ( From Goodwin and Stepka. )

peated tangential divisions to the cortex. This accounts for the fact that
the cortex, particularly in its inner layers, is often made up of radial rows
of cells (Fig. 4-16). A second small group of cells, just below the plerome
tip, produces all the stelar tissues. The progress of cell division, par-
ticularly in the surface layer and the cortex, was followed by Wagner
( 1937 ) by means of tracing cell groups, or "complexes," each of which
had descended from a single meristematic cell. Sinnott and Bloch (1939)
studied cell division in living root tips of small-seeded grasses by camera-
lucida drawings. Brumfield (1942) continued this work by the use of

78 Growth

photography, and the situation was analyzed more fully by Goodwin and
Stepka (1945; Fig. 4-17) and Goodwin and Avers (1956). Erickson and
Goddard (1951) used still more refined photographic methods. The lo-
cation and rate of cell division in the root offer problems of considerable
complexity.

There are a number of developmental patterns in the root apices of
seed plants. They have been classified into various "types" by Janczewski
(1874), Kroll (1912), and Schuepp (1926). These are well described
in Esau ( 1953&, p. 116). In the structure of the root apex there is ob-
viously less uniformity than in that of the shoot.

The development of the apical meristems in both root and shoot from
their first appearance in the early embryo has been studied by a number
of workers. A typical example is described in Pseudotsuga by G. S. Allen
(1947).

Root tips, with the regions just behind them, were among the first
materials to be used for plant-tissue culture (p. 296) and much has been
learned through this technique as to the physiology of the root. In many
plants, for example, the root cannot synthesize thiamin but depends for
this vitamin on a supply produced in the shoot.

Mention has already been made (p. 41 ) of the work on the physiology
of the root meristem by Brown and his colleagues, who determined the
changes that take place in the activity of the apical cells in various re-
gions, particularly as to growth rate, respiration rate, and protein syn-
thesis. In a general discussion of this work, Brown, Reith, and Robinson
(1952) show that there is a considerable difference in the composition
of the proteins at different distances from the apex. Jensen (1955) has
also made a biochemical analysis of the cells near the root tip in Vicia
faba.

Clowes (1956, 1958) discovered between the active meristematic re-
gion and the root cap a cup-shaped group of cells, the quiescent center
(Fig 4-18), which from their appearance divide rarely. He reports that
these cells synthesize DNA more slowly than do the surrounding ones.
They presumably have some specific metabolic function. Jensen and
Kavaljian ( 1958 ) have made a census or cell divisions in the root tip of
Allium cepa. They found a definite apical initial region where there are
few divisions and agree with Clowes that these have a low DNA content.
Cell division is slower to start in the axial than in the peripheral region of
the tip. They report a very definite daily periodicity in division, with a
maximum about noon.

The growth-substance relations of growing roots have received much
attention (p. 391). Auxin and various synthetic substances stimulate the
initiation of root primordia but usually check the later growth of the
root. Auxin tends to be basipetal in its flow, a fact that helps to account

Meristems

79

Fig. 4-18. Median section of root tip of Zea, showing the quiescent center (stippled).
Its cells are physiologically different from the surrounding ones and seem rarely to
divide or grow. ( From Clowes. )

for the normal preponderance of roots at the base of the plant axis. A
high carbon-nitrogen ratio (p. 366) also favors root growth. Torrey ( 1950)
presents evidence that a growth substance, not auxin, is produced in the
root and moves toward the apex, stimulating the formation of lateral
roots.

Intercalary Meristems. Growth of an axis in length may sometimes take
place at other points than its tip, by the activity of an intercalary meristem.
Thus in many monocotyledons cell division persists in the base of an
internode when it has ceased elsewhere, and the stem elongates all along
its course, somewhat like an extending telescope (Prat, 1935). The gyno-
phore of the peanut, which carries the young fruit down and into the
ground, grows in a somewhat similar way, as has been described by
Jacobs (1947). Such material is excellent for a study of the relations of
cell division and cell elongation to growth.

LATERAL MERISTEMS

The Vascular Cambium. Apical meristems govern growth in length and
produce those tissues commonly called primary. Their cells tend to be
arranged in longitudinal rows, each row being the descendants of a single

80 Growth

meristematic cell. In woody plants, the root and stem axes continue to
grow not only in length but in diameter. This is accomplished chiefly by
the activity of another meristem, quite different in character, the vascu-
lar cambium. The tissues that such meristems produce are termed

secondary.

The vascular cambium is a sheath of embryonic cells extending from
the beginning of secondary growth in the shoot tip to a corresponding
position in the root. It arises between the xylem and the phloem of the
primary vascular bundles and forms xylem on its inner face and phloem
on its outer one. Each cambium cell produces a radial row of daughter
cells on either side. The tissues thus formed can usually be recognized
by this cell pattern, though it may sometimes be altered by the marked
increase in diameter of certain cells, notably the vessels and sieve tubes.
Cells of the apical meristem are relatively uniform, varied though their
products may be. Cambium cells, on the other hand, from the beginning
are differentiated into two quite dissimilar types of cells, corresponding
to the longitudinal and transverse cellular systems in vascular tissue.
Those cambium cells that produce tracheids, fibers, sieve cells, and other
elements of the longitudinal system are termed fusiform initials and are
usually much elongated in the dimension parallel to the axis. The ray
initials are much smaller and essentially isodiametric and produce the
rays in wood and phloem.

The fusiform initials, especially those destined to form tracheids and
fibers, may be from 50 to 100 times as long as wide. Often they do not
differ greatly in length from the mature cells that they produce, though
in some cases the fibers of the summer wood may become much
longer than their initials (Bosshatd, 1951). Most of the divisions of these
initials must be longitudinal and tangential since only in this way can
additions be made to the width of the axis. The division of such an
elongate cell violates Hofmeister's law. It is a remarkable process and
was first clearly described by I. W. Bailey (1920a and b; Fig. 4-19).
The nucleus, usually in the center of the cell, divides mitotically. Be-
tween the two daughter nuclei the cell plate is then laid down by the
phragmoplast, an extension of the system of fibers at telophase. This ap-
pears in longitudinal section as two sets of fibers (sometimes called
kinoplasmosomes) connected by the cell plate, one moving upward and
one downward until the basis of the new division wall has been com-
pleted. An account of division in cambial cells was also given by
Kleinmann ( 1923 ) in a paper written during the war and without a
knowledge of Bailey's work.

Since the circumference of the axis continually increases, it is necessary,
if the cambium cells are not to enlarge in tangential diameter, that they
increase in number by occasional radial divisions. In storied cambia,

Meristems

81

where the initials are in tiers, this is done by radial divisions much like
the tangential ones. More commonly, however, the initial cell divides by
an obliquely radial (pseudotransverse) wall, and the daughter cells move
past one another until the two initials reach normal length and lie side
by side tangentially. The number of such divisions is usually more than
enough to make the number of initials conform to the enlarging circum-
ference of the cambium (Bannan, 1953). In many cases the daughter
cells fail to maintain themselves, and the rows of cells coming from
them are pinched out and gradually disappear (Bannan and Bayly,
1956). This process is so regulated, however, that the normal tangential
diameter of the mature cells is essentially maintained. The length of the
vascular elements originating from the cambium is also regulated to an
approximately constant size.

Fig. 4-19. Early stages in the division of a cam-
bial cell, near the middle of a long initial. The
nucleus has divided, and the cell plate is being
formed by the fibers of the kinoplasmosome
(fc). (From I. W. Bailey.)

The change in relative position of these enlarging cambial daughter
cells involves a problem in cellular readjustments that is of importance
morphogenetically. In 1886 Krabbe published a monograph on what he
termed "sliding growth," presenting evidence that during the differentia-
tion of tissues there was a good deal of change in intercellular position
brought about by the slipping or gliding of one cell past another. This
is common in animal embryology, where cells are more plastic and
often migrate for some distance, and is responsible for many of the
changes that take place in the development of these organisms. Its oc-
currence in plants might therefore be expected and was generally ac-
cepted as true for some time. Krabbe was supported in his position by
some other botanists, notably Neeff ( 1914 ) and Grossenbacher ( 1914 ) .

Priestley ( 1930 ) criticized Krabbe's conclusion and believed that all
intercellular changes were brought about by what he termed "sym-

82

Growth

plastic" growth, a rather vague concept that there is a readjustment
of all the cell walls operating in one "common framework" and with
no slipping between adjacent ones. Sinnott and Bloch ( 1939, 1941 ) studied
living and growing tissues of young roots where the gliding of one
cell past another would be recognized, if it occurred, by alterations in
relative wall positions and found no evidence for it. They suggested

Xylem

o

Cambium

330u

3IOii

365ii

Fig. 4-20. Origin of ray initials in gym-
nosperms. Radial sections from Thuja,
showing progressive subdivisions of fusi-
form initials and the consequent origin
of several ray initials. (From Barman.)

that changes in intercellular relationships come about by intrusive growth
limited to a particular region (such as the tips of cambial cells), so
that the cell may grow in between its neighbors without requiring that
it slide past them. Bannan and Whalley (1950) have shown how this
is accomplished in elongating fusiform initials. Schoch-Bodner and Huber
( 1951 ) present evidence that the phloem fibers of flax, which become very

Meristems

83

long, grow not only by cell stretching as the internode elongates but
also by localized growth at both tips, as a result of which the fibers push
in between adjacent ones. In the readjustments thus made necessary
it is essential that where pits are present the pit fields in adjacent cells
develop opposite each other, since there must be a corresponding opening
in each wall. This evidently takes place after the relative position of the
walls has become fixed. The problem of "sliding growth" has been dis-
cussed at length bv Meeuse (1942).

The increasing circumference of the axis also requires that the number
of rays be continually increased if the proportion between rays and verti-

¥

Fig. 4-21. Radial section of wood of Chamaecyparis, showing transitional cell types
associated with the origin of a ray from a fusiform cell. ( From Bannan. )

cal elements is to be maintained. The origin of new rays has been de-
scribed for gymnosperms by Bannan ( 1934 and Figs. 4-20 and 4-21 ) and
by Barghoorn (1940a and Fig. 4-22) and for certain angiosperms by
Barghoorn (1940b and Fig. 4-23). A new ray arises from a short cell cut
out of the radial face of a fusiform initial, the nucleus first migrating to
the particular place where the new daughter cell is to be produced. The
height of the ray is then increased by transverse divisions of this cell and
its products, and its width by radial divisions. High rays may break up
into shorter ones. The rays as seen in tangential section maintain an al-
most constant distance from one another. How this is accomplished is
described by Bannan (1951).

84

Growth

The cambial region is obviously a much more active and plastic one
than early workers regarded it. New initials are being produced and
others are disappearing. Rays are being formed, fusing and dividing.
Changes and rearrangements are continually taking place among the
initials. The two sides of the cambium are forming quite different types
of cells, and further differentiation within the xylem and the phloem is
beginning. All these changes, however, are so well coordinated and regu-
lated that a specific pattern of structure, constant enough for taxonomic
purposes, is produced and maintained. There are few places in the plant
where histological differentiation can be so well studied as in the prod-
ucts of the vascular cambium.

ii i

I

Fig. 4-22. Radial sections of wood of Ginkgo (A) and Amentotaxus (B and C),- show-
ing relation of young ray to ends of wood cells. ( From Barghoorn. )

The cambium proper consists of a single row of cells, though on the
xylem side there are usually several rows of mother cells, developed from
it, which by their division produce the xylem. Relative activity in xylem
and phloem production differs considerably in different forms. In Thuja,
Bannan (1955) found that phloem began to develop later than xylem but
then continued at a steady rate. In larch, however, Knudson ( 1913 ) had
reported that phloem development preceded that of xylem, though the
most rapid growth of each took place at the same time. In Acer, Cocker-
ham (1930) and Elliott (1935) observed that the first cambial divisions
formed the spring type of sieve tubes. This was followed by xylem
growth, during which no new phloem was formed. As xylem production
ceased, a second phase of phloem development occurred in which the

Meristems

85

smaller summer sieve tubes were formed. The various steps in the develop-
ment of xylem from cambium to heartwood, with particular reference to
changes in the cell wall, have been described by Bailey (1952). Lade-
f oged ( 1952 ) has published a detailed study of cambial activity and wood
formation in six conifers and 13 hardwoods in Denmark, based on obser-
vations from March to November.

The character of cambial products, particularly on the xylem side, as
to the number and size of the cells and the thickness of their walls, is
influenced by various factors though the precise effect of these has had

Fig. 4-23. Origin of ray initial in an angiosperm. Serial tangential sections of wood of
Trochodendron, showing origin of ray initial (stippled) from the end of a fusiform
initial. (From Barghoorn.)

little experimental study. In temperate climates, during the cold weather
of much of the year cambial activity ceases. The contrast between the last
formed wood of one season and the first of the next makes it possible to
identify boundaries of the annual rings formed in each season. These are
absent in regions where growth is continuous. The relations between
climatic factors, particularly annual rainfall, and the width of these rings
has been studied ( Glock, 1955, and others ) . Lines of denser wood within
an annual ring may be related to rainfall differences in a single season
(Dobbs, 1953). Injuries from frost, fire, and insect attack can also be
recognized by their effects on the growth ring. These changes in the

86 Growth

products of the cambium, through the permanent record they leave in the
tree, are of importance in the study of past climatic changes and in
the dating of ancient timbers, and have been actively studied especially
by Schulman ( 1956) and others in the Laboratory of Tree Ring Research.
The course of cambial activity differs among various plants. In herba-
ceous ones it is associated with vegetative growth and generally ceases at
flowering (Wilton and Roberts, 1936). In most woody plants, growth of
the new shoots in length is complete or nearly so before there is much
cambial activity. The age of the tree may make a difference in woody
plants, for Messeri (1948) observed that in old trees cambial divisions
began a month earlier in the twigs than in the main stem whereas in
young ones they started simultaneously throughout. In most conifers and
in ring-porous angiosperms, cambial growth begins at about the same time
throughout the stem (Wareing, 1951). In diffuse-porous angiosperms,
however, division starts just below the buds at about the time they open
and proceeds downward into the branches and then the trunk (Cocker-
ham, 1930; Priestley, Scott, and Malins, 1933). This is apparently related
to the production of auxin in the buds, for there is a close relation be-
tween the appearance of auxin there and the onset of cambial activity
(Avery and others, 1937b).

The relation of auxin to cambial growth has also been studied by Brown
and Cormack (1937), Soding (1940), Kiinning (1950), and others.
Chowdhury and Tandan (1950), working with both evergreen and de-
ciduous trees in India, report that buds burst in February or March and
that growth in length continues until May. Not until the new leaves are
fully expanded and length growth has ceased does cambial activity begin.
It starts at the tip of the last year's shoot and proceeds down the tree and
up into the new shoot. Growth in length begins again in the summer
and is accompanied by cambial activity until both cease in the fall. The
authors suggest that there are two types of substances operating here,
one concerned with apical growth and one with cambial. Aspects of cam-
bium physiology were discussed by Priestley in a series of papers ( 1930
and others).

A continuous cambium, laying down a solid ring of vascular tissue, is
found in all woody gymnosperms and angiosperms and in many herba-
ceous forms. In other herbaceous stems the cambium ring is discontinu-
ous and produces distinct vascular bundles. These may be separated by
undifferentiated fundamental tissue. Across these gaps and connecting the
cambium of one bundle with that of the next there is often an inter-
fascicular cambium, probably a vestigial structure persisting from the
time when the cylinder was continuous and the stem was woody. In many
cases it consists of a row of cells with only a few tangential divisions.
Under suitable conditions, as in the base of a stout herbaceous stem, the

Meristems 87

interfascicular cambium may become active and produce typical xylem
and phloem. Its development offers some interesting morphogenetic

problems.

The distribution of cambial activity over the axis in woody plants also
deserves further investigation. The amount of wood produced by the two
branches at a given fork of a stem, for example, bears a rather close ratio
to the amount in the main axis below them, but this ratio will depend on
the relative size of the two branches, the angle between them, and the
orientation of the main axis itself ( p. 108 ) .

Another relatively unexplored field but one which may become of much
interest for morphogenesis is that of anomalous secondary growth. In
certain families the normal situation of a continuous cambial sheath is
altered (Mullenders, 1947). An additional cambium may arise outside the
phloem and start another vascular cylinder or series of bundles. There
may be more than one of these. Such anomalous bundles may also appear
in the pith. In other cases the surface of the cambium, instead of being
circular in cross section, may be irregular so that radial lobes of secondary
tissue are formed. In more extreme cases the cambium may become quite
atypical and patches of secondary xylem and phloem may be intermingled
in the vascular cylinder. Anomalous growth is often found in stems such
as those of lianas or rhizomes which have other functions than support
or conduction. It is frequently present in fleshy roots. One sometimes has
difficulty in drawing a line between anomalous growth of this sort,
which is really normal for a particular plant, and truly abnormal, or tera-
tological, structures (Chap. 11).

The vascular cambium has been little explored from a morphogenetic
viewpoint. Although it is much more difficult to study directly than are
the apical meristems, its products, especially wood, are so firm and meas-
urable that they offer attractive material for a quantitative study of many
problems in growth relationships.

The Cork Cambium. The vascular cambium and the root and shoot
apices are not the only localized embryonic regions in the plant. Increas-
ing diameter of the axis necessarily results in the rupture of its outer
layers, notably the cortex and the outer phloem. Infection and water loss
would take place through these breaks in the tissue were it not for the
formation of layers of suberized cells, the cork, or phellem. This is sec-
ondary tissue formed by a cork cambium, or phellogen. It has its origin in
a row of cells, tangentially adjacent to each other, which divide peri-
clinally and link up into a meristematic layer that produces a series of
daughter cells on its outer side. There may be from one or two to many
of these and their walls become suberized and impervious to water. On
the inside are formed one or a few layers of daughter cells, the phello-
derm, presumably vestigial in character.

88 Growth

The first phellogen usually arises just under the epidermis, but as axis
diameter increases and outer tissues are ruptured, new phellogens appear
in the deeper layers. Sometimes these form a single continuous layer of
cork which may be peeled off. In other cases the phellogen arises as a
localized, often slightly concave sheet which isolates a scale-like patch of
tissue. In older stems these phellogens appear in the earlier and more or
less crushed and functionless phloem. The phellogen cells obviously are
alive and must originate in still living cells of this outer tissue. In many
cases, corky cells arise beneath wounds in various regions. In the abscis-
sion of leaves and fruits a layer of cork is formed at the region of separa-
tion. In both these cases, growth substances (wound hormones or auxin)
have been shown to be related to the origin of the cork cambium. Corky
layers often show an unusual histological trait in having the new division
walls in tangentially neighboring cells laid down directly opposite each
other instead of being staggered, thus forming a characteristic stratified
structure unlike that of most plant tissues (p. 195).

From a morphogenetic point of view the most interesting thing about
cork-forming cambia is the way in which a continuous layer of such cells
may suddenly arise in a mass of old and partially collapsed tissue. A host
of dormant cells become embryonic again, link themselves up with neigh-
boring cells, and form a cambial layer. In the typical rhytidome form of
bark, this may be somewhat irregular in outline and often is not closely
parallel to the surface of the organ or to the vascular cambium below.
Where cork forms under a wound or just below the epidermis, its position
may be explained by its location at a particular point in a physiological
gradient, but in these more complex cases such an explanation is less
satisfactory. Their origin resembles the way in which a pattern of wall
thickenings or a net of fibers (p. 197), which transcends cellular bound-
aries, may become differentiated in a mass of tissue. The origin of such
phellogen layers is a problem in differentiation which deserves more
attention.

MERISTEMS IN DETERMINATE GROWTH

Potentially, the plant axis can grow indefinitely in length through the
activity of its apical meristems and in width through the activity of the
vascular cambium. Actually, of course, growth finally ceases for various
reasons, but these axial meristems are essentially indeterminate in their
activity.

The organs of the plant other than stem and root, however— the leaves,
floral parts, and fruits— are structures of limited, or determinate, growth.
They finally reach maturity and cease to enlarge. In this respect, one of
them is much like an animal individual with a definite life cycle of its

Meristems 89

own. Such organs provide an opportunity for a study of plant develop-
ment which has been somewhat neglected in favor of the more sharply
limited meristems in apex and cambium. Because of the more diffuse
character of their growth, a study of these determinate organs will prob-
ably throw more light on the development of form than can be gained
from those of indeterminate growth.

How, we may ask, does a determinate organ grow? Is it through the
activity of localized groups of dividing cells, as in the axes, or by un-
realized, interstitial growth, as in most animals? The fact is that both
methods are usually employed.

The determinate organ which has been most extensively studied is the
leaf. The first step in its development is the appearance of a small swell-
ing just below the dome of the shoot meristem. This grows into a leaf
primordium and finally, through a series of developmental steps, into a
mature leaf (p. 187). As to just how much of the meristematic tissue
actually takes part in forming a leaf primordium, there seems to be con-
siderable variability among different groups of plants. Rosier (1928)
reports that in wheat only the outermost layer (dermatogen) is con-
cerned. This pushes out and then pulls together from all sides to meet in
the center, like a collapsing glove finger, so that the whole leaf grows
from this one layer. Schwarz (1927), on the contrary, found that in
Plectranthus and Ligustrum the first two layers produced the entire leaf,
and this part of the meristem he termed the phyllogen. Most other
workers ( see Foster, 1936 ) have found that tissue below the second layer
also contributes often to the formation of the young leaf, particularly the
veins. Whether this is simply tunica or both tunica and corpus depends
on the extent of layering and seems not to be important.

Critical evidence in this problem is provided by a study of leaf pri-
mordia formed by periclinal chimeras (p. 268). Here one or two of the
outer layers come from one of the graft partners and the rest from the
other. In chimeras between nightshade and tomato the tissues from each
can be distinguished by the fact that in nightshade the cells are much
larger. Here Lange ( 1927 ) was able to show that although a leaf primor-
dium in this chimera was formed chiefly from the two outer layers the
third layer also contributed to it. In periclinal chimeras between forms of
Datura stramonium differing in number of chromosome sets (and thus in
cell size) Satina, Blakeslee, and Avery (1940) observed the same thing,
as did Dermen ( 1947« ) in cranberry. In all these cases the third layer
gave rise to the vascular tissue of the leaf.

The way in which the primordium develops into the leaf also differs
considerably in different forms. In fern leaves, growth of the lamina is
largely determined by an apical cell resembling that in the shoot and
root (p. 58). In many higher plants the early growth of the primordium

90

Growth

in length is chiefly apical and seems to be governed by a group of cells
at the tip, just under the epidermis-essentially a meristem. This produces
the central tissues of the young primordial axis, or midrib, and growth of
the epidermis keeps step with it. Such apical growth soon ceases, how-
ever, and later growth is diffuse.

The development of the tobacco leaf studied by Avery ( 1933 ) may be
taken as a typical example of the growth of a determinate organ (Fig.
4-24 ) . After the axis is about 1 mm. long and while still it is very narrow,
growth of the lamina begins on both sides of this axis, pushing out like a
wave of developing tissue. It increases faster in the middle than at either

d2^>

A,

^b=^4=^s

Fig. 4-24. Early developmental stages of a tobacco leaf, from a young primordium
(upper left) to later ones where lamina and veins are being formed. (From G. S.
Avery. )

end, and this produces the characteristic leaf shape. The rate of growth,
as a result both of the division of the cells and of their increase in size,
is greater in certain dimensions than in others. Avery contrasts the growth
differences resulting from such polarized growth, primarily due to differ-
ences in plane of cell division, with localized differences in rate of divi-
sion. Differences in cell shape due to differential cell expansion have little
share in over-all shape changes in the organ as a whole. In most leaves,
growth in the various dimensions of the blade, whatever its cellular basis,
is unequal, so that blade form changes somewhat during development.
These changes are under morphogenetic control, however, and show close

Meristems 91

allometric relationships ( p. 105 ) . The development of a few similar organs
of determinate growth has been studied, such as the thorn shoots of
Gleditsia (Blaser, 1956).

In leaves which do not show the usual dorsiventral character but vari-
ous, more complex shapes, such as pitcher-like or peltate blades, the
origin of these structures is by a system of localized meristems (Roth,
1957). These have not been studied extensively and present some impor-
tant developmental problems.

The growth of other organs, such as perianth parts, ovaries, and fruits,
resembles that of leaves in showing certain localized differences in rate
and direction of growth, but growth is mainly diffuse and nothing com-
parable to a true localized meristem is operative save in exceptional cases.
Not only are the different dimensions of such an organ clearly correlated
in a progressively changing pattern but different parts of the organ, such
as blade and petiole, and fruit and pedicel although often growing at
different rates, also keep in step with each other. Growth of cer-
tain structures, notably the fruit stalk, involves some cambial activity.

Whatever type of growth a plant organ may show, whether by apical
meristems, cambium, or diffusely distributed embryonic activity, it is
under strict developmental control. The problem of this control is some-
what more complex in a plant, where both diffuse and localized growth
occur, than in an animal, where the latter is generally absent. The pres-
ence in a plant of these two somewhat different methods of growth offers
certain advantages because of the possibility of studying in the same in-
dividual two different types of morphogenetic control. However growth
occurs, its activities are correlated and not isolated events.

PART TWO

The Phenomena of Morphogenesis

CHAPTER 5

Correlation

The most significant fact about organic growth, as described in the pre-
ceding chapters, is that it is a process under definite control and thus leads
to the development of bodies of definite form and size. This control is
shown in the character of the growth cycle itself which, as we have seen,
marches forward in an orderly fashion to the attainment of a specific size.
It is shown even better in the distribution of this growth during develop-
ment. If growth were equal in all parts and directions, organisms would
be spherical. The remarkable variety of forms that living things display
and that constitutes one of their important differences from most lifeless
objects is due to the fact that the amount of growth in one region is dif-
ferent from that in another and that its rate in the various dimensions of
a structure is unequal. These differences are not random ones, for if they
were, a jumble of fantastic forms would result; they arise in an orderly
sequence and progress in a regular fashion until a specific organic struc-
ture is developed. Something evidently guides the growth and differenti-
ation of the organic mechanism. Occasionally this control is seriously
disturbed and in such cases abnormal growths and monstrosities of various
kinds appear (p. 275), but in the great majority of cases orderly develop-
ment and the production of specifically formed structures take place. It is
clear that in some fashion the parts of an organism are so related to each
other that a change in one affects the rest and that the whole is thus inte-
grated into an organized system.

All the phenomena of development which are to be discussed— polarity,
symmetry, differentiation, regeneration, and the rest— are simply different
aspects of this developmental relatedness, and the various factors con-
cerned are those which have been found to affect it in one way or another.
The fundamental causes of this integrated development are yet unknown.
They are often attributed to correlation, a term which, because it is in
most cases merely a name for our ignorance, has with many students of
morphogenesis fallen into disrepute. Nevertheless correlation is a fact,
explain it how we will, and no one can approach a study of the phe-
nomena of morphogenesis without recognizing this. Therefore at the be-

95

96 The Phenomena of Morphogenesis

ginning of a discussion of these problems it will be useful to consider
some typical examples of the ways in which growth of one part or dimen-
sion is related to growth elsewhere or to the plant's various activities.
These will illustrate how plant forms arise and an integrated organism is
produced and will serve as an introduction to the fundamental problem
of morphogenesis, approached from many directions throughout this book
—the problem of biological organization.

There have been many discussions of correlation in the literature of
plant development, and for some of them the reader is referred to the
works of East (1908), Harris (1909-1918), Love and Leighty (1914),
Murneek (1926), Goebel (1928), Thimann (1954b), and others.

Correlations have been classified in many ways, as environmental,
physical, morphological, physiological, genetic, compensatory, or meristic,
depending on the characters and factors involved. For purposes of con-
venience in the present treatment, there will be grouped together, as
physiological, those correlations for which a physiological mechanism-
metabolic, hormonal, or other— seems to be operative and as genetic, those
which seem to depend primarily upon the genetic constitution of the
individual and its formative relationships and are thus produced by
mechanisms more deeply seated and obscure than the ordinary physio-
logical ones.

PHYSIOLOGICAL CORRELATIONS

Physiological relationships are of particular morphogenetic interest
since through an analysis of them the mechanisms for other types of cor-
relation may be discovered. The various factors concerned will be treated
in later chapters. The particularly important role of growth substances in
plant correlation has been discussed by Thimann ( 1954fo ) .

It will be useful here to mention a few typical examples of physiological
correlation and to formulate some of the problems that they present.

Nutritional Correlations. The simplest type of correlation is one which
depends on nutrition. A region that does not produce or contain food must
depend for its growth on one that does. Correlation of this sort between
root and shoot must obviously occur. The root-shoot ratio is a favorable
one in which to study correlation and the factors that modify it, and con-
siderable attention has been given to the problem. Kny (1894) cut off
part of the roots from growing seedlings and part of the shoot from others.
When a considerable amount of reserve food was still available in the
seed, loss of one part did not greatly affect the growth of the other.
Pearsall (1923), Keeble, Nelson, and Snow (1930), and others found
that removal of the seedling shoot sometimes actually stimulated growth
of the root, presumably because of reduced competition for food stored

Correlation 97

in the seed. More commonly, however, in older plants and in cuttings, a
rather close balance becomes established between root and shoot and is
restored if altered experimentally.

This ratio is subject to change during development, for in most plants
the shoot grows consistently faster than the root. Other factors also affect
it. In poorly nourished plants the root is relatively large and in etiolated
ones, relatively small. Crist and Stout (1929) found that in some plants
it was affected by soil acidity, soil fertility, and day-length. Roberts and
Struckmeyer (1946) observed that temperature and photoperiod modified
the ratio but not in the same way in all plants. The top-root ratio was
studied by Shank (1945) in maize inbreds with low and with high ratios,
and in their hybrids, under different amounts of phosphorus, nitrogen, and
water in the soil. Increase in each of these substances tended to increase
this ratio. Richardson ( 1953 ) measured root growth microscopically in
small maple seedlings growing in glass tubes under controlled conditions.
Any change in the environment of the shoot which modified photosyn-
thetic activity had a commensurate effect on rate of root growth. Correla-
tions depending on nutrition are evidently rather susceptible to change
by environmental factors.

The influence of shoot on root is not always nutritional but may result
from the action of auxin, vitamins, or other growth-regulating substances.
The nutritional influence of root on shoot is well shown by the horticul-
tural practice of producing dwarf trees by grafting scions from normal-
sized varieties on roots of genetically dwarf types in which the root system
is too small to supply the growth requirements of a large tree.

Among other correlations which have their basis in nutritional factors
are those between the size of a fruit and the amount of leaf area avail-
able for the support of its growth (Haller and Magness, 1925). There is
also a close relation between the amount of foliage on a tree (the size
of its crown ) and the amount of stem growth. Young and Kramer ( 1952 )
and Labyak and Schumacher (1954) have studied this problem by re-
ducing experimentally the size of the crown in pine through pruning and
observing the effect on trunk growth. In apples, Murneek (1954) found a
relationship between fruit size and leaf area (presumably nutritive) and
also between fruit size and seed number per fruit (presumably stimu-
latory ) .

Because of its practical importance, many studies have been made of
the relation between the size of seed planted and the size of the plant
growing from it. If a positive correlation existed between these characters
it would pay to use only large seeds in many agricultural operations.
Agronomists have sought all such characters in fruit and seed that might
be correlated with high yield but have had little success. Where such a
relation has been found, in most cases it is simply between seed size and

98 The Phenomena of Morphogenesis

early plant size. Passmore (1934), working with reciprocal hybrids be-
tween large-seeded and small-seeded cucurbits, and Oexemann (1942),
with several vegetables, observed that plants from large seeds have an
initial advantage in size because of the larger amount of food stored in
the seed but that this usually disappears after a time.

Similarly, in vegetative propagation the size of a "seed" piece in pota-
toes, though it may influence early sprout growth, has no effect on yield
(Wakanker, 1944), though if the bigger pieces have more buds on them,
sprout number will be larger and yield somewhat increased.

A positive correlation between the size of a fruit and of the seeds in it
has often been found, as by Schander (1952) in apple and pear and by
Simak ( 1953 ) for seed size and cone size in pine. In fruits and cones of
the same size, however, seed size was inversely proportional to seed num-
ber. Both nutritional and compensatory correlations are probably in-
volved here.

Ashby (1930) suggested that the larger plant size resulting from
heterosis was due to greater size of the embryos that produce the heterotic
plants, thus giving them an initial advantage which was maintained
throughout growth. Present evidence, however, does not support this idea.

Compensatory Correlations. The nutritional factor in the relation be-
tween two parts of a plant may be evident in other ways than by transfer
of food from one to another. Each growing part or organ constitutes what
Goebel called an "attraction center" which under normal conditions draws
to itself a specific amount of building material. This may be small or large,
depending on its genetic constitution. In one of the higher plants,
which has many similar growing parts such as leaves, flowers, and fruits,
the number of these parts may be reduced by accident or experiment. In
such cases there is often a compensatory increase in the growth of the
remaining structures, so that a negative correlation results between the
size and the number of parts (Lilleland and Brown, 1939). Thinning of
fruits by mechanical or chemical means is sometimes practiced so that
the remaining fruits will grow larger. In the same way, the removal of all
buds but one in a certain type of chrysanthemum results in the develop-
ment of this single flower head, through compensatory growth, to a size
very much larger than normal.

The reverse of this relationship also may occur, for if many fruit are
set, they will be small. In such cases, some may drop off. Thus in apples
there usually occurs a "June drop" in which many of the young fruit,
unable to attract to themselves a sufficient supply of food or auxin, stop
growing and are cut off by abscission layers. In a somewhat similar way,
the more seed developing in a tomato fruit and the more fruits in a
cluster, the smaller will be the weight of each seed (Luckwill, 1939;
Schander, 1952; and Simak, 1953).

Correlation 99

Where flowering and fruiting are continuous, as in squashes, if a certain
number of fruit are set, related to the food-producing capacity of the
plant, the development of more flowers ceases and will not be resumed
unless the growing fruits are removed. There is thus a continuous compen-
satory balance between the development of multiple plant organs and
the amount of material or hormone available for their growth.

A balance also occurs between the vegetative and the reproductive
phases of a plant ( Murneek, 1926 ) . Tomatoes in which fruits are allowed
to form abundantly will soon cease vegetative growth, but if flowers and
young fruits are continually removed, the plants will grow to a much
greater size. A potato plant in which tuber formation is prevented will
often bear a large crop of fruits, structures which normally fail to develop
presumably because of the diversion of food to the tubers. Mirskaja
( 1926 ) removed all flower buds from plants of a number of species and
found that this stimulated formation of lateral shoots and increased the
size of leaf blades, tubers, and pith cells and the amount of lignified
tissue.

Removing the axillary buds from Coleus plants was found by Jacobs
and Bullwinkel (1953) to induce longer stems, larger leaves, and more
rapid growth of the main shoot ( Fig. 5-1 ) . The ancient art of topiary is
simply a manipulation of these compensatory correlations. The removal
of certain buds stimulates the growth of others which would have re-
mained dormant, and by this means the form of the plant can be
altered.

Such correlations may perhaps be called competitive rather than com-
pensatory. In certain hybrid cherries, for example, the embryos start their
development but when partly grown they shrivel and die. Tukey (1933)
and others were able to bring such embryos to normal maturity by re-
moving them from the seed and growing them in culture. In normal plants
the embryo may be thought of as competing successfully with maternal
tissues for food during development, but in these unusual cases most of
the food is drawn instead to maternal tissues, and the embryo dies. Re-
lease from such maternal competition allows it to grow.

Compensatory correlations are also to be observed in the development
of individual organs. MacDougal (1903k), who has reviewed the early
literature, described many examples of this, as did Goebel and others. In
some plants, for example, if the blade is removed from the young and
growing leaf, the stipules will become much enlarged. The building ma-
terial available to the leaf is employed in its growth but the distribution
of this material is not the usual one.

A good instance of compensation is reported by Johnston ( 1937 ) be-
tween the coleoptile and the first internode of Avena. Light stimulates
the growth of the former but depresses the latter. Regardless of light, the

100 The Phenomena of Morphogenesis

total growth is much the same, reduction in one structure being compen-
sated by increase in the other.

Stimulatory Correlations. Many correlations, however, do not depend
upon the distribution of building materials but upon the operation of
other factors which affect development, particularly the stimulatory and
inhibitory action of auxin and other growth substances.

The stimulatory effect is well shown in the control of root growth.
Van der Lek (1925) and others have found that in many cases cuttings

160 -

140 -

E
E

00

c

01

TO

A I 2

Leaf Position

Fig. 5-1. Compensatory correlation in Coleus. Increase in leaf length in 27 days after
removal of axillary buds and branches, as compared with controls. Leaves at left of
vertical line had not unfolded from apical bud. ( From Jacobs and Bullwinkel. )

on which buds are present will root much better than those without buds.
This evidently is due to a root-stimulating substance produced by buds
which passes down to the base of the cutting. The character of the buds
may also be important, for O'Rourke (1942) has shown that blueberry
cuttings root better if the buds on them are leaf buds than if they are
flower buds.

The relation between a leaf and the development of a bud in its axil
is a complex one. Felber (1948) observed that in apple the size of a

Correlation 101

vegetative bud at maturity is proportional to the size of its subtending
leaf, suggesting a nutritional relation. Champagnat (1955 and other
papers) presents evidence that there are several distinct stimulating or
inhibiting influences that the leaf exerts on its bud. Snow and Snow
(1942), on the basis of experiments at the meristem, believe that an axil-
lary bud is determined by the primordium of the leaf that subtends it,
particularly the basal part. If the primordium is partially isolated from
the stem apex, its bud grows larger than it otherwise would.

Related structures often affect each other. The cotton boll and its seeds
will not reach normal size if the involucre of the flower is removed
(Kearney, 1929). Knapp (1930) reports that the perianth of a liverwort
grows only if the archegonium that it covers is fertilized. The ovary in
most plants will not grow into a fruit unless at least a number of ovules
are forming seeds. These developing parts produce substances, appar-
ently, that stimulate the ovary wall to grow. This stimulation can be
imitated by the use of certain synthetic growth substances to produce
parthenocarpic fruits (p. 378). In case of metaxenia (p. 407), where the
male parent has a direct effect on the character of the fruits, this pre-
sumably results from something introduced through the pollen tube.

Inhibitory Correlations. There are many developmental relationships
which are just the reverse of stimulatory and in which one part inhibits
the growth of another by some other means than competition for food.
These relations, like those of stimulation, commonly involve the action
of auxin and related substances.

The best known case of such inhibition is the dominance by a terminal
bud which prevents the growth of lateral buds below it (p. 386). Simi-
larly, the epicotyl and its bud, in seedlings like those of beans, inhibit the
growth of buds in the axils of the cotyledons. Often a leaf can be shown
to inhibit the growth of the bud that it subtends, for if the inhibiting
organ is removed, the bud will then grow. Sometimes physiological iso-
lation has the same effect as removal. Child ( 1919, 1921 ) chilled a portion
of a bean epicotyl and found that the cotyledonary buds then began to
grow. Shading a leaf sometimes results in removing its inhibiting in-
fluence.

Preventing the growth of the apical bud by encasing it in plaster some-
times has the same effect as removing it. Many of the early studies in
growth correlation involved this plaster technique (see Hering, 1896).
For example, if the portion of pea epicotyl between the terminal bud and
the cotyledons is so encased that it cannot grow in width, growth in
length is much reduced as compared with the control.

Nutritional factors may have something to do with the inhibition of
cotyledonary buds, for Moreland ( 1934 ) observed that in bean seedlings
the growing foliage leaves have a greater inhibiting effect on these buds

102 The Phenomena of Morphogenesis

than does the epicotyledonary bud itself and believes that this is owing
to the removal by these leaves of some food material necessary for bud

growth.

Other structures may be inhibited. If root nodules and root tips are re-
moved from roots of red clover inoculated with an effective strain of
nodule bacteria, the number of nodules subsequently formed will be in-
creased (Nutman, 1952). This is thought to be owing to the removal of
inhibitory activity centered in the meristems of nodules and root.

Inhibition by terminal buds has various practical implications. Reed
( 1921 ) found that heavily pruned young pear trees have a greater growth
of new shoots than do unpruned or lightly pruned ones and suggests that
this results from the removal from them of much growth-inhibiting sub-
stance present in the buds near the tips of the branches.

Correlations of Position. Many parts of the plant can be shown to have
the capacity for much more extensive growth than they normally display.
If a leaf is removed and treated as a cutting, it will frequently grow to a
greater size and live much longer than if it had remained a part of the
plant (Mer, 1886; Riehm, 1905; Winkler, 1907; and others). Single cells,
under suitable conditions of isolation and stimulation, will sometimes de-
velop into whole plants. All parts of the plant tend thus to be totipotent.
Why these potentialities are not realized when the part is a member of
an organic whole is a problem. Not only is each part of this whole limited
in its growth, but the particular way in which it develops depends on
where it is. Driesch's famous dictum emphasizes the fact that an or-
ganism is an organic pattern in which every part develops in a specific
relation to the rest. The correlations that these parts display with one an-
other are simply manifestations of the control that this pattern exercises
in development.

Experimental change of the position of a part in this pattern often
effects marked alteration. Ward and Wetmore (1954) partially released
young fern embryos from their contact with the prothallus and found
their growth to be slower and somewhat abnormal. Wetmore asks the sig-
nificant question as to why a spore and an egg should grow so differently.
Each is a haploid cell and they presumably are identical genetically, but
the surroundings under which they develop are very different. He sug-
gests that perhaps the difference between sporophyte and gametophyte
in ferns may be the result of this positional correlation.

Mason (1922) reports that the terminal bud from a cotton shoot that
has stopped growing will grow vigorously if it is budded on a young plant.
A flower bud inserted on a vegetative shoot where it would not normally
occur often changes in its development and may produce a flower cluster
which is gigantic or otherwise abnormal.

The operation of such a constantly regulated balance among activities

Correlation 103

is well shown in the formation of reaction wood (p. 356). This wood (in
conifers) elongates faster than normal wood and thus tends to bend a
branch away from the side on which it occurs. The branches have a spe-
cific angle of orientation to the main axis, or to gravity, which is main-
tained by the development of reaction wood on one side of the branch.
If this normal orientation is experimentally altered, reaction wood will
appear at the precise place and in the precise amount elsewhere which
will tend to restore the normal branch pattern. The origin and character
of this pattern are the essential problem. What happens to any com-
ponent of it depends on the place that this occupies.

There are many other examples of the operation of such developmental
patterns in the plant body. Among these are the studies of Dormer ( 1950)
on the development of xylem in different internodes of the young plant of
Vicia; of Friesner and Jones ( 1952 ) on the relation of primary and sec-
ondary branches in length growth; and of various workers on the struc-
ture of leaves borne at different levels on the stalk. Ashby and his
colleagues (1948) have emphasized the structural and physiological dif-
ferences among successive leaves along the axis and have related this to
the problem of aging. Instances of positional differences shown in topo-
physis (p. 212) are particularly clear and may become irreversible.

The control that the organized whole exercises over its parts is some-
times termed "correlative inhibition." This term explains nothing but it
emphasizes the fact that inhibitory action is certainly involved. In the
physiology of development both inhibition and stimulation are important.
A number of workers, among them Libbert (1954, 1955), have discussed
the various interactions between substances which promote and those
which check the growth of buds. Thimann (1956) has called attention to
the fact that in most physiological processes there is a balance between
reactions tending to promote the process and others tending to inhibit it.
No single factor is solely responsible, but physiological activities, includ-
ing those of development, are often under multiple control. Furthermore,
certain factors such as auxin may stimulate under certain conditions and
inhibit under others.

Some students of development are therefore inclined to look on the
growing organism as the seat of constant competition between different
and distinct processes, a state of equilibrium between opposing forces.
This resembles the concept of the organism as a balance between distinct
cellular individuals each with specific tendencies of its own. It also calls
to mind the older idea of the "battle between the parts" as the basic fact
in development. Analysis of the structures and the activities that go to
make up an organism gives some support to this interpretation of devel-
opment. The close correlations that are everywhere present in develop-
ment, however, and particularly the persistent tendency toward regula-

104 The Phenomena of Morphogenesis

tory action by which a specific norm or pattern of form and function is
restored if disturbed, are difficult to explain on the basis of independent
action by many variables. The organism more closely resembles an or-
ganized army under disciplined control than it does a mob where each
individual acts competitively for himself.

The balance between stimulation and inhibition, however, is worth
careful study by students of morphogenesis. In a few cases it has been
investigated in the lower plants. In the coenocytic alga Caulerpa, for ex-
ample, the "assimilators" (leaves) produce strong growth inhibition but
the rhizoids have the opposite tendency (Dostal, 1945). The balance
between the influences of these two sets of organs has an important effect
on the character of the plant as a whole.

More favorable material for a study of this aspect of correlation is
found in the over-all form of the plant body, especially in such higher
plants as trees. A tree is a rather loose aggregation of axes which usually
does not show as precise a form as does an individual organ such as a
leaf or a flower but which, nevertheless, is characteristic and recognizable.
This has been found to result from an interaction of factors in the ter-
minal buds and in the growing tips of the branches. Some of these factors
tend to push the branches down, in relation to the main axis, and others
tend to lift them up. The relative length of branches and main axis is also
similarly controlled, evidently by domination of the terminal bud over
those of the lateral branches. Munch (1938) has discussed the diverse
tendencies that govern such tree form in conifers and interprets these in
terms of hormonal action, but he emphasizes the harmony and balance
that exist among them. Others (Snow, 1945) have considered the problem.
It is a basic one for morphogenesis since the form of the plant body as a
whole, although relatively variable, is nevertheless a true organic one.
Presumably the factors that govern it resemble those that bring about the
much more constant and specific forms of the separate organs. The body
is an aggregation of these parts, less tightly organized than are its indi-
vidual organs, but clearly showing organization. The beginnings of organ-
ization and of the emergence of those correlations that determine form
may profitably be studied in these plant bodies, which in a sense are in-
termediate between colonies of semi-independent parts and true organic
individuals.

GENETIC CORRELATIONS

Organized bodily patterns, with their localized differences and specific
characters, are examples of physiological correlation though the mecha-
nisms involved are obscure. They doubtless have some genetic basis. Many
other growth correlations, including those concerned in the form of plant

Correlation 105

parts, are more precise but are even further from a satisfactory biological
explanation. They are inherited, but the genetic mechanisms involved
have hardly begun to be explored. At present we can simply describe and
classify these correlations.

The various structures in a growing organic system tend to increase
together and thus to be correlated in size. In a given organ its dimensions
are likewise correlated. Since growth usually is not uniform, as develop-
ment proceeds, the relations between the parts of the system or between
the dimensions of the organ may change progressively and thus produce
differences in form. Growth is usually exponential in character, and there-
fore the relationship between the sizes of two structures growing at dif-
ferent rates may best be found by plotting the logarithms of their sizes
against each other. If the rates are different but the relation between the
two is constant, these values will fall along a straight line the slope of
which measures the growth of one structure relative to that of the other.
It is noteworthy that in most cases where two parts of the same growing
system, or two dimensions of a growing organ, are compared, their
relative rates are found to be constant, however different their absolute
rates may be.

This relationship can be described simply by an equation. If y is the
size of one variable, .t that of the other, b the value of y when x is of some
arbitrary size, and k the ratio of the growth rate of y to that of x, then

y = bxk
or

log y — log b + k log x

This phenomenon of constant relative growth (heterauxesis) has been
observed by many biologists but was first widely emphasized by Julian
Huxley (1932). He termed this type of growth heterogony, a term now
replaced in much of the literature by allometry. The constant b measures
differences in level, or at the beginning of growth, between two variables.
The constant k provides a measure of relative growth rate and may some-
times offer a clue to the mechanisms involved. It may be used to express
differences when these are based on genetic, environmental, embryologi-
cal, biochemical, or even evolutionary factors. This method of analysis
has proved useful in the study of many kinds of growth correlations.

Correlations of Part and Whole. Among the familiar growth correla-
tions are those between an organ and the rest of the body or between
members of a series of multiple parts and the structure that they con-
stitute. In animals, large individuals typically have their organs cor-
respondingly larger than those of small ones. In plants, however, with
their lower level of organization, their often indeterminate growth, and
their multiple organs, this relationship is not so simple. In beans, for

106 The Phenomena of Morphogenesis

example, Sinnott (1921) has shown that there is a positive correlation
between size of leaf and size of entire plant up to a certain plant size.
Beyond this the size of additional leaves is no greater even if leaf
number and plant size may increase considerably ( Fig. 5-2 ) . Size of pod
and of seed show a similar relationship to plant size. These facts suggest
that organ size may depend on the size of the embryonic mass or the
shoot meristem and that this may increase up to a certain point only,
beyond which increase in total plant size involves only the addition of
more units (internodes, leaves, and others).

In cucurbits and many other types, although organs on the same plant
tend to be correlated in size (forms with large fruits also having large
leaves, thick stems, and long internodes), there is a certain amount of
flexibility in these relationships, depending on genetic constitution. Thus

.95

10

30 50

Dry weight of shoot (g )

70

90

Fig. 5-2. Relation of size of leaf to size of shoot in progressively larger bean plants.
For a while, leaf and shoot increase together, but after a certain point, shoot size
increases without further increase of individual leaves. {From Sinnott.)

if a pumpkin type, which has all its parts large, is crossed with an egg
gourd, where they are all small, the Fo generation contains plants that
show some differences in the relative size of their parts, but there are
none that have the large fruit size of the pumpkin and the small vine
type of the egg gourd. The general physiological correlation of parts
within the same plant makes it impossible for sizes of individual organs
to segregate independently in inheritance.

The size of the meristematic region bears some relation to that of
plant and organ size. Crane and Finch ( 1930 ) have shown that the size
of buds has an effect in determining the size of shoots that grow from
them. In a comparative study of large-fruited and small-fruited races in
Cucurbita pepo, von Maltzahn (1957) found that, although the dome-
like undifferentiated meristem is essentially the same size in all types,

Correlation 107

the region just back of this and the primordia of flowers and leaves that
originate there are considerably larger in the large-fruited type.

In this general category of correlations are many of those described
by J. Arthur Harris. In Nothoscordum and Allium (1909), for example,
he found that flower clusters with relatively large numbers of flowers are
borne on relatively long peduncles. Size changes are not always propor-
tional, however, for in Ficaria (1918) he found that flowers with a large
number of sporophylls have relatively more pistils than stamens.

The relation between cell size and body size belongs to the part-to-
whole category. This has been discussed in a previous chapter (p. 32)
and is the basis of a very considerable literature. In a single organ
there are often marked differences among the various tissues in the
strength of the correlation between cell size and tissue size (Sinnott,
1930). In general, it is clear that body size usually does not depend on
cell size but on cell number. In many cases, however, it has been shown
that in organs of limited growth, such as fruits, large cell size is associated
with large organ size, though the range of the former is much less than
that of the latter.

Correlations between Different Parts. There are many genetic correla-
tions which do not involve part-to-whole relationship but one between
different parts and are thus less obvious as to origin. Sometimes these
parts grow at the same rate but more frequently they do not.

One of the most conspicuous of such growth relationships in higher
plants is that between the two main organ systems of the body, the root
and the shoot. Its nutritional aspect has already been discussed. The rela-
tion is often so precise, however, as to suggest that it has a basis in the
genetic constitution of the plant. Its value differs in different plants, at
different stages of development, and under different environments. In
most cases the root is relatively large in the seedling but grows less
rapidly than the shoot. One increases at a rate which maintains a con-
stant proportion to that of the other. Pearsall (1927) plotted the dry
weight of the root against that of the shoot, both logarithmically, in a
series of growing plants in various species. In most cases the allometric
constant k was greater than 1, though its value differed in different
species. In other words, the shoot grew more rapidly than the root. In
etiolated plants, however, it was much greater than 1, and in those with
storage roots, it was much less.

Tammes ( 1903 ) made a study of the growth relationships between an
internode and the leaf above it. She found that removal of a leaf would
shorten the length to which the internode below would grow but would
not reduce the number of its cells. This relationship does not hold in
climbing plants, where internode length is usually attained before the
leaf above becomes very large. In Ipomoea the excision of leaves on the

108 The Phenomena of Morphogenesis

main shoot has a variety of effects on the shape of leaves produced later
by the terminal bud and on the size and number of their cells (Njoku,

1956b).

The various parts of the shoot system also show growth correlations,
and these are responsible for the form of the shoot. They are readily
observable in coniferous trees where the growth of the terminal shoot,
which will form the trunk, is usually greater than that of the branches.
This leads to the spire-like form of many of these trees. There are also
definite relationships between the members of a branch system. The new

o

Hi

Log. Lamina diam.

Fig. 5-3. Allometric relation between lamina and petiole in Tropaeolum. I, a series of
growing leaves. II, mature leaves in shade. ( From Pearsall. )

material added each year is distributed unequally but in regular fashion
throughout the tree.

A somewhat different type of correlation is that between the volume
of the shoot system or any part of it and the cross-sectional area of the
stem that supports it. Murray ( 1927 ) analyzed this relationship in a
number of trees and finds that it is constant and predictable and that as
the tree grows larger the cross-sectional area of its trunk becomes rela-
tively smaller. It has been shown that where a trunk branches the cross-
sectional area of the two branches is larger than that of the united trunk

Correlation

109

below them but that the degree of this difference depends on the rela-
tive size of the two branches and on the angle between them. It is an
expression of the polar tendency of the trunk.

There are also correlations between the parts of an organ. In leaves,
for example, although the length of the petiole is much more variable

2
2

cc
tu

Ui

2
<

o

2.0-

FRUIT /^

y

CF

1.5-

y< STALK

1.0-

i i I j i

l J r 1 1 1 1 1 1 1 1

2
2

a.

ID

i-

UJ

2
<

6

o
o

FRUIT

_i i i i_

Time in Days

Fig. 5-4. Diameter of stalk plotted against diameter of fruit in a large-fruited race of
Cucurbita (above) and a small one (below). Rate of growth is less for stalk than
for fruit but at flowering the logarithmic distance between the two is approximately
the same in both races. ( From Sinnott. )

than the dimensions of the lamina, there is a relation between them. In
Tropaeolum, Pearsall ( 1927 ) found that this was allometric, with lamina
width growing faster than petiole length (Fig. 5-3). In Acer the volume
of the leaf blade is much more closely correlated with the cross-sectional
area of the petiole than with its length. In the runner bean the area of

110

The Phenomena of Morphogenesis

the lamina and the cross-sectional area of the petiolar xylem are related
allometrically, but the xylem grows only about 0.6 as fast as the lamina
(D. J. B. White, 1954). Alexandrov, Alexandrova, and Timofeev (1927)
observed that in Bryonia the number of vessels in any given part of the
stem is correlated with the dimensions of the leaves in that region. These
various facts suggest that physiological factors are here involved and
that the amount of water transpired from the blade is important in de-
termining the conducting capacity of the petiole. This hypothesis will
be discussed later (p. 332). In the light of other evidence, it is doubtful
whether such a "functional stimulus" is actually operative.

Fig. 5-5. Relation of pith diameter to diameter of shoot in young stems of Pinus
strobus of different sizes, showing greater relative size of pith in larger stems. ( From
Sinnott. )

Somewhat similarly, the diameter of a growing cucurbit fruit and of
the stalk that bears it are closely correlated in early growth, the fruit
increasing more rapidly. Stalk growth ceases earlier than fruit growth,
however (Sinnott, 1955; Fig. 5-4).

Some correlations between parts are due to the similar effect of a
gene or group of genes on a series of morphologically related organs. An-
derson and de Winton ( 1935 ) studied the effect of a number of mutant
genes, in Primula sinensis, on the morphology - of the leaf, bract, sepal,
and petal. In several cases they had a very similar influence on develop-
ment (producing lobing) in all four categories of organs. Such correla-
tions are examples of what is sometimes called homeosis..

Many examples of growth correlation are found in internal structures.
Thus Buchholz (1938) in Sequoia has shown that in stems of different
sizes the vascular cylinder occupies a relatively larger portion, as meas-
ured in cross section, in large stems than it does in small ones. In pine

Correlation

111

stems of different size the pith is relatively larger in the large stems and
the cortex relatively smaller (Sinnott, 1936rt; Fig. 5-5).

Sometimes these size relationships are found to extend below the level
of the organ. The relation of cell size to nuclear size has already been
discussed (p. 27). Klieneberger (1918) measured this relationship in
a large number of plants, and the subject has been reviewed by Trom-
betta (1942). Both Budde (1923) and Schratz (1927) found a rather
close correlation between the total surface area of the plastids and the
volume of the cell.

These relationships between structures have important evolutionary
implications which cannot be discussed here. The increasing size of the
leaf during the development of the pteropsid stock seems to have been
correlated with the change from a protostelic to a siphonostelic stem
structure (Wetmore, 1943). The association of the trilacunar leaf trace

Fig. 5-6. Diagram of a trilacunar node,
showing relation between stipules and lat-
eral leaf traces. ( From Sinnott and Bailey. )

with the presence of stipules (Sinnott and Bailey, 1914; Fig. 5-6) is
another instance. This has been emphasized by the observation of
Sensarma (1957) that when only one lateral trace branches only the
stipule on that side develops. Another case is the relation of absolute
size of the axis to its vascular development (p. 359). Among animals there
are many examples of evolutionary allometry where increasing size of
the organism results in a proportionally greater increase of certain organs.
Correlations between Dimensions. Correlations between part and
whole or part and part evidently involve coordinating mechanisms that
bind these parts into an integrated organism. The same sort of control
is shown, though in a somewhat different manner, in the correlation be-
tween the various dimensions of an organ or other determinate structure.
Here one is concerned with the very essence of form itself, with the way
in which growth is distributed in one direction relative to that in an-
other. This relative growth, like that between parts, is under definite con-

112 The Phenomena of Morphogenesis

trol and proceeds in a regular and orderly fashion (Fig. 5-7). Since
most plant organs are determinate structures, their forms are more con-
stant and precise than are those of the whole plant body.

The origin of specific form in a plant or its organs may be studied in
embryological development but more readily in the growth of organs that
originate at the meristem, especially leaves, flowers, and fruits. In some
cases the mature form or a close approximation to it is established very
early, and from an examination of a tiny primordium, when its size may
be only a fraction of a cubic millimeter, the final shape of the organ can
be seen. The critical period in form determination here is evidently near
the beginning of development. More frequently, however, the early
primordium is simple, often nearly isodiametric, and the final form de-
velops by differential growth.

too

i
i-
o

z

Id

-f a *
22 .

z> *
JN

x *
<

2

6
o

10'

10

I I I I

I I I Mill
100

LOG MAXIMUM WIDTH

x 2 x 10V

Fig. 5-7. Relative growth of length to width in developing fern prothallium. (From
Albaum. )

Plant embryology in its widest sense is the record of such differential
growth by which the complexity of organic form is attained. Most of
our knowledge of the process is from verbal or pictorial descriptions,
but in some cases it has been analyzed more precisely. The techniques
of measuring allometric growth are as applicable in such cases as they
are in the more frequently studied ones of part-to-part analysis. Richards
and Kavanagh ( 1943 ) have extended the method further and show how
it may be applied to three-dimensional growth. If this proves generally
feasible, analysis of form development will become much more precise.
Schuepp ( 1945, 1946 ) has used the methods of allometry to supplement
others in a rather complex analysis of the development of leaf shape and
of the origin of the leaf primordium at the meristem.

Sinnott (1936fr) applied these methods to the study of form develop-
ment in fruits of various races of cucurbits where form difference is due

Correlation

113

to differential growth rates in various dimensions ( Fig. 5-8 ) . In the long,
narrow types, such as the "club" gourd, length increases faster than
width but at a constant relative rate, the value of k being approximately
1.2. In other races, such as the "bottle" gourds, width increases faster than
length, k being about 0.8. In the latter race, which has an upper sterile
lobe and a lower fertile one with a constricted isthmus between, the
ratios of the diameters of these to each other and to the polar diameter
of the ovary are specific, so that, as the fruit grows, not only the ratio of
length to width changes but the form of the organ as a whole undergoes

lOOOt

I to

Width (mm)

Fig. 5-8. Relative growth of length to width (plotted logarithmically) of developing
fruits of several types of cucurbits. ( From Sinnott. )

precise development (Fig. 5-9). An organic pattern results not from one
or a few correlations between dimensions but from a complex of such
correlations. In crosses between the two gourd types mentioned, the value
of k has been found to segregate after crossing and at least in one
case in a simple fashion, suggesting that this is what is under direct
gene control (p. 423). Evidently the form of the mature fruit in such
cases depends not only upon the relative rate of its dimensional growth
but upon the total growth attained, so that the problem of the inheri-
tance of form involves not only the genetic basis of relative growth but
also that of size.

Dimensional relationships are not constant throughout the plant. Dif-

114 The Phenomena of Morphogenesis

ferences in shape are often found between early and later fruits, or be-
tween leaves on different parts of the axis. Meijknecht (1955) has
analyzed some of these differences and concludes that this variation is
least when the structure occupies the position on the plant in which it
shows its "ideal" development, the expression of its typical specific charac-
ter. This calls to mind a concept of the early "idealistic" morphology.

so

40
3C-

20

-, /0

So

u

- 8

5 '

s

Miniature'

■1*

x*.»

'Giant'

6 T 8 9 /o
Width (cm)

40 SO

Fig. 5-9. Relative growth of length to width in bottle gourds. Width increases faster
than length, but the relative rate is the same in "miniature" (dots) and "giant"
(crosses), so that although the shape of the two races at maturity is different, their
genotype for shape is the same. The inherited difference between them is in size.
(From Sinnott. )

The mechanism by which the control of relative growth is exercised
and growth correlation established is not known, but evidently cell
polarities are involved. Where growth is more rapid in one dimension
than in another, it has been shown (p. 51) that cell divisions are more
frequent in that direction. Whether the axis of the spindle or the cyto-
plasmic polarity by which this seems in certain cases to be preceded is
what is immediately involved in relative growth, or whether this is second-

Correlation 115

ary to some more general form-determining mechanism, is a basic prob-
lem.

In this chapter there have been presented only a few of the great
number of developmental, physiological, and genetic correlations that
may be found throughout botanical literature, but these are representa-
tive of the rest and emphasize an important fact in plant development. A
plant is typically a rather loosely organized system but every part of it is
nevertheless affected to some degree by its relations with other parts.
These correlations are not random ones but are simple expressions of
that general organized interrelatedness that is the distinguishing charac-
ter of an organism. What happens to the whole affects the parts and what
happens to a part affects the whole. An organ removed from this cor-
relative inhibition may have a very different fate from its normal one. A
single cell, on isolation, will often regenerate an entire plant. That it
did not do so in its original position is owing to this inhibition. The term
"correlation" is simply a description of the facts and explains nothing.
It is of value, however, in emphasizing that the results of any experi-
ment with a portion of the plant body must be interpreted not as an
isolated event but as taking place against the background of the whole
organism. How each portion of this organism behaves under given con-
ditions and what its developmental fate will be depend upon its position
in the organized system of which it forms a part. The nature of this or-
ganized system is the fundamental problem that continually faces the
student of morphogenesis in whatever part of the science he may be at
work.

CHAPTER 6

Polarity

In plant development, growth does not proceed at random to the produc-
tion of a formless mass of living stuff but is an orderly process that gives
rise to specific three-dimensional forms of organ or body. The various cor-
relations described in the preceding chapter are manifestations of this
formative control, which knits the developing organism together so that
growth in one region or dimension is related to growth in the others and
the plant thus becomes an integrated individual. A notable feature of
these bodily forms of plants ( and animals ) is the presence in them of an
axis which establishes a longitudinal dimension for organ or organism.
Along this axis, and symmetrically with reference to it, the lateral struc-
tures develop. The two ends or poles of the axis are usually different
both as to structure and physiological activity. Thus a typical vascular
plant has a major axis with the root at one end and the shoot at the
other and with lateral appendages— leaves, branches, or lateral roots-
disposed symmetrically around it. Growth is usually more rapid parallel
to the axis than at right angles to it, so that an elongate form results,
though this is by no means always the case. Single organs such as leaves,
flowers, and fruits also show axiate patterns, as do the bodies of lower
plants. These patterns appear very early in development as the result
of differences in growth or in planes of cell division. This characteristic
orientation of organisms, which is typically bipolar and axiate, is termed
polarity.

Polarity may manifest itself in many ways. The structures at the two
ends of an axis are unlike, as in the case of root and shoot, "stem end"
and "blossom end" of fruits, and petiole and blade of leaves. In re-
generation, the organs formed at one end are usually different from those
formed at the other. Cells and tissues may show polar behavior in graft-
ing experiments. The transportation of certain substances may take place
in one direction along the axis but not in the other, thus manifesting
polarity in physiological activity. Both in structure and in function there
are gradients of all sorts. Individual cells show polar behavior in plane
of division and in the different character of their two daughter cells.

116

Polarity 117

It is important at the beginning to understand exactly what is meant
by the term polarity. Sometimes this is regarded as an innate quality of
an organism which makes its parts line up in a given direction, like iron
filings in a magnetic field or opposite electrical charges at the two poles
of an electrophoretic system. How far such polarizing factors operate in
organisms we do not know. The term polarity as used most commonly,
and certainly in the present discussion, implies much less than this and
involves no assumption as to its causes. Polarity is simply the specific
orientation of activity in space. It refers to the fact that a given biological
event, such as the transfer of material through an organ or the plane in
which a cell divides, is not a random process but tends to be oriented in
a given direction. If this were not so, an organism would grow into a
spherical mass of cells, like tissue in a shaken culture. This differential
directiveness is responsible for organic form. What is the cause of it we
do not know, but one often invokes it, although as an expression of igno-
rance, in attempting to account for a morphogenetic fact. Polar behavior
is no more and no less mysterious than organic formativeness but is merely
the simplest manifestation of this, the tendency to develop a major axis
with lateral ones subordinate to it.

It is essential to realize, however, that polarity is not a trait that is
originally and invariably present. There is good evidence that entirely
undifferentiated cells, such as eggs in their early stages and other very
simple ones, manifest no polarity at all. Within them, doubtless, there are
polar molecules but these are arranged at random, like iron filings that
are not in a magnetic field. Sooner or later a gradient is established in the
cell which lines up these molecules in a specific orientation. This orien-
tation originates in asymmetric factors in the outer environment, such
as gravity, light, or the influence of adjacent cells, or perhaps within the
cell from gene action. As a result, the various phenomena of polarity make
their appearance, but not until a gradient has first been set up. Once a
cell or a group of cells have thus become polarized, they will usually
proceed to develop into an axiate system which then produces an or-
ganic form without necessity for further environmental induction.

The tendency toward polar orientation, which may be strong or weak or
reversible and is differentially susceptible to outer influences, is the funda-
mental fact of polarity. It must be distinguished from the various factors
of induction that call forth and make manifest this polar tendency. To say
that light induces polarity in the egg of Fucus is to describe a morpho-
genetic fact, but a different problem is to explain the character of the
cell that makes it capable of a specific polarization. An explanation of
polarity in physical and chemical terms is difficult but a beginning at this
task has already been made. In most biological discussions today, how-
ever, the term polarity is primarily a descriptive one.

118 The Phenomena of Morphogenesis

Polarity is involved in many morphogenetic phenomena, and it will
necessarily be referred to repeatedly in other chapters. Thus symmetry
is the orderly distribution of structures in relation to a polar axis. Polar
differences are the simplest aspect of differentiation. Regeneration is in
most cases a polar process. Form results from a pattern of polarities set
up in the developing plant. Polarity may be regarded as the framework,
so to speak, on which organic form is built.

The polar behavior of plants has long attracted the attention of
morphologists and physiologists, from whose work a great body of knowl-
edge has accumulated. Theophrastus and other ancient writers described
the abnormal behavior of plants grown in an inverted position. There are
a number of other early observations, especially those on regeneration
following the girdling of trees, by Agricola, Hales, and Duhamel du
Monceau. The term polarity was used by Allman in 1864 in connection
with phenomena of animal regeneration and is now generally employed
by students of morphogenesis in both botany and zoology. Vochting made
extensive studies of polarity in plants in its relation to problems of re-
generation, growth, and differentiation (1878, 1908, 1918). Important
botanical work was also done by Goebel (1908), Janse (1906), Loeb
(1924), and others. The theoretical aspects of polarity have been ex-
tensively discussed not only by Vochting but by Sachs (1882), Pfeffer
(1900-1906), Klebs (1903, 1904, 1913), Winkler (1900, 1933), Went and
Thimann (1937), Lund (1947), Bunning (1952b), and others. Polarity in
animals has been studied by many workers, notably Driesch, Roux,
Morgan, and Harrison. Reviews of the field of plant polarity or parts
of it have been written by Bloch (1943a), Gautheret (1944), and
Bunning ( 1958 ) . Polarity is important not only for theoretical problems
of plant development but for many practices of horticulture and vege-
tative propagation (Priestley and Swingle, 1929).

The establishment of a morphological axis in which the two ends are
different and along which there is a gradation from one pole to the
other may be looked upon as the first step in the process of differentia-
tion, an important aspect of morphogenesis. The expression of polarity
differs considerably in different plants and under different environmental
conditions and is thus open to a wide range of experimental investigation.
This most conspicuous aspect of organic form will probably not be fully
understood until the mechanism of orderly and correlated growth control
is discovered. As a relatively simple manifestation of form, however, it
provides a useful point of attack on morphogenetic problems.

Polar behavior in plants presents many problems. How far is it an in-
herited character, potentially present from the beginning of development,
and how far induced by the action of various environmental factors or by

Polarity 119

intercellular correlation? Once established, can it be reversed? Are the
physiological manifestations of polarity the cause or the results of mor-
phological polarity? Is polarity an aspect of the whole organism or do
individual cells possess it?

To present the various phenomena of polar behavior and the problems
that they pose, it will be helpful to discuss the subject from several points
of view and to describe its manifestations in external structure, internal
structure, isolated cells and coenocytes, physiological activity, and the
development of organic pattern.

POLARITY AS EXPRESSED IN EXTERNAL STRUCTURE

The most conspicuous expression of polarity is in external morphology.
In higher plants the differences between root end and shoot end are de-
termined very early, perhaps at the first division of the fertilized egg. This
differentiation is not irreversible, however, for roots often appear on stems
under favorable conditions and, less commonly, buds and shoots appear
on roots. Polar behavior occurs in thallophytes and bryophytes, even in
some very simple forms like those of many filamentous algae, though
in such cases it is less sharply marked and more easily reversed than in
vascular plants. Organisms without morphological polarity are rare. A
few amoeboid forms have no axes in the vegetative stage but form
polarized fruiting bodies. Algae like Pleurococcus are spherical and
apparentlv apolar but may be induced to produce filaments, an expres-
sion of axiation. Forms like Spirogyra, desmids, and diatoms have an axis
of symmetry but its two poles seem to be alike. In most filamentous types,
however, a rhizoidal pole and a thallus pole can be distinguished.

Experimentally, polarity can best be demonstrated through its ex-
pression in regeneration, and it is here that most of our information about
it has been gathered. Polar regeneration has long been known and
manipulated in the horticultural practices of vegetative reproduction.

Vochting ( 1878 ) cut twigs of willow and kept them under moist con-
ditions. Some he left in their normal, upright orientation and others were
inverted. Regardless of orientation, however, roots tended to be re-
generated more vigorously from the morphologically basal end and shoots
from buds at the original apical end. This is the classical example of
polarity (Fig. 6-1). If such a shoot were cut into two or more parts
transversely, each part regenerated roots and shoots in the same polar
fashion. Even very short pieces of stem showed this polar character.
Vochting removed a ring of bark in the middle of a shoot and confirmed
earlier observations that roots were formed above the ring and shoots
below, just as if the stem had been cut in two. From these and similar

120 The Phenomena of Morphogenesis

experiments he concluded that polarity was a fixed and irreversible char-
acteristic of the plant axis and that probably the individual cells of which
the axis was formed themselves possessed a polar character.

Experiments like these have been carried out on many plants. A wide
variety of results, often conflicting, have been reported and several

Fig. 6-1. Polarity in willow shoots. Left, portion of a stem suspended in moist air in
its normal position and producing roots and shoots. Right, a stem similarly grown
except in an inverted position. ( After Pfeffer. )

theories to explain polarity proposed. Klebs (1903), for example, found
that roots would grow at the apical end of an inverted shoot, that water
stimulated root formation at any point on the twig, and that removal of
the bark could reverse polarity. He believed that environmental conditions
rather than innate polarity determined the place where buds and roots
develop on a stem. Vochting (1906) replied to these criticisms of the

Polarity 121

theory of polarity. The problem, however, is evidently not quite as simple
as Vochting at first thought.

Polar regeneration is also evident in the lower groups of the plant
kingdom. If fern prothallia are sliced transversely, regeneration from
their cut surfaces is polar (Albaum, 1938fr; Fig. 6-2) and is related to
physiological gradients, especially of osmotic concentration (Gratzy-
Wardengg, 1929 ) . In isolated primary leaves of ferns, polarity is evident,
but both the character and the polar distribution of regenerated structures
are somewhat diverse (Beyerle, 1932).

Fig. 6-2. Polar character of regeneration in fern prothallia from which pieces have
been removed by transverse cuts. An apical portion restores a single heart-shaped
structure, but from a basal one a group of small prothallia is formed. (From Albaum.)

In the regeneration of hepatics and mosses, polar behavior varies. The
gemmae of Marchantia and Lunularia form rhizoids from either surface
while they are young but only from one when they grow older ( Haber-
landt, 1914), indicating that embryonic tissue, as it proves to be in many
other cases, is relatively unpolarized. Polarity here can be reversed by
gravity, light, and other environmental factors ( Fitting, 1938 ) . Vochting
found relatively little polarity in the regeneration of the thallus of
Marchantia. In the mosses, cuttings formed rhizoids at the lower end and
protonemata at the upper one. This behavior could be reversed by in-
version of the cuttings ( Westerdijk, 1907), but regenerating structures
were always more vigorous at the morphologically basal pole.

Polarity is evident in the sporophores of the higher fungi but here,
also, it is not firmly fixed, for a segment of the pileus may be successfully
grafted back to the same pileus in an inverted position ( Lohwag, 1939 ) .

In most algae there is a sharp distinction between the rhizoidal, or
hold-fast, pole and the thallus, or shoot, pole. Especially in the simple
forms and in early stages of the more complex ones, this polarity may be
reversed by changed relations to gravity, light, or other factors (Wulff,
1910; Zimmermann, 1923). Studies on the egg of Fucus and on coenocytic
algae are illuminating here (p. 135).

Manifestations of polar behavior in higher plants are much more uni-

122 The Phenomena of Morphogenesis

form and fixed, presumably because of the higher level of organization
and differentiation among them. It must have its origin verv early in
embryonic development. Vochting's conclusion, however, that every

Fig. 6-3. Transverse polarity in Dioscorea.
Half slice of a tuber with regenerating
shoots next the core and roots on the
periphery. ( From Goebel. )

cell is polarized has been challenged by those who point out that many
cells theoretically may become completely embryonic again and ulti-
mately produce an entire plant and thus can have no fixed polar charac-

Polarity 123

ter. Pfeffer and Klebs have emphasized the probability that the cells of
the terminal growing points have no original polarity of their own, any
more than does an egg cell. In older parts a more stable polarization re-
sults from the influence of conditions in the environment. Vochting's idea
of the irreversibility of polarity in these higher plants has also been dis-
puted. Many investigations concerned with these problems cannot be
judged critically because of insufficient evidence, particularly as to

anatomical facts.

Polarity may be manifest in the transverse axis as well as in the
longitudinal one. This is evident structurally in the transversely polar
gradient often associated with regeneration. Thus Goebel (1908) found
that in half slices of the root of Dioscorea sinuata shoots grew out from
the central part of the axis and roots from the margin directly opposite
to this (Fig. 6-3). Transverse polarity is also manifest in the flow of
auxin in various tropisms (p. 384). The subject has been discussed in
detail by Borgstrom ( 1939 ) .

Stem Cuttings. In stem cuttings, polar regeneration of shoots and roots
is clearly obvious in most higher plants, but there are considerable dif-
ferences between species. Polar behavior may be obscured in various
ways, as by the tendency of monocotyledons to form roots at nodes and
by the influence in many cases of the age of the cutting upon the forma-
tion of root primordia. The specific polar reactivity of tissues from which
buds and roots originate must be taken into account, as well as the fact
that a different complex of conditions may control each of the successive
processes in the development of these structures, such as the formation
of primordia, their growth, their final differentiation into roots and shoots,
or the formation of callus which may give rise to either roots or shoots.

Various modifications of polar behavior in regeneration from stem
cuttings have been reported. Roots, for example, tend more character-
istically to be limited to one pole in their growth than do shoots.
Doposcheg-Uhlar (1911) observed this in Begonia, and Massart (1917)
studied 30 species of plants, some of which showed strongly polar re-
generation of both roots and shoots, some weakly polar regeneration, some
only root polarity, and some only shoot polarity. Root polarity was re-
lated to the growth habit of the plant, for species with pendant branches
rooted readily at their apical ends.

Polar tendency is also expressed in the manner of callus formation
in cuttings, since in most cases callus tends to develop more vigorously
at the basal pole than at the apical. From the basal callus, roots are
usually formed, and shoots from the apical one. Simon (1908) noted
certain anatomical differences between apical and basal calluses and
made the observation that calluses from opposite poles may be made to
fuse but not calluses from the same pole.

124 The Phenomena of Morphogenesis

Various investigators (Klebs, 1903; Kiister, 1904; Freund, 1910; and
Ursprung, 1912) found that local differences in water or oxygen may
affect root production and thus obscure the inherent polar tendency.
Only Plett (1921), who studied phenomena of internode polarity in
410 species, has attempted to explain the variability in distribution of
roots and shoots on the basis of the anatomy of the plant from which the
cutting was taken. He found that shoots from axillary buds regenerate in
a polar fashion, as do adventitious roots that arise endogenously. Ad-
ventitious buds growing from callus or superficial regions of the cortex,
however, are generally distributed rather irregularly, a fact which sug-
gests that the inner layers of the stem have stronger polar tendencies
than do cortex and callus tissues.

Root Cuttings. Cuttings of roots behave in polar fashion. Dandelion,
chicory, and sea kale have been studied most frequently in this regard.
Shoots are commonly regenerated at the basal or proximal pole (the end
next the shoot) and roots from the apical (distal) pole. This polarity
is maintained even when the root cutting is grown in an inverted posi-
tion (Fig. 6-4). Wiesner (1892c) made the observation, often confirmed
since, that, in relatively short pieces of root, shoots regenerate at both
ends. This was also seen by Neilson-Jones (1925) and, in stem cuttings,
by Fischnich (1939). If the growing roots were continually trimmed off
from the apical end, shoots finally appeared there. Czaja ( 1935) produced
roots at both ends by trimming off tissue from the basal end. Centrifuga-
tion toward the shoot pole results in bud formation at the root pole, as
does enclosing the base in sealing wax (Goebel, 1908). These results
are now interpreted as due to the effect of auxin (p. 392), which tends to
move toward the root apex. A high concentration of it tends to produce
roots and a low one, shoots. This has been shown clearly by Warmke
and Warmke (1950). Callus develops more vigorously at the proximal
pole. As early as 1847 Trecul reported that, in root cuttings of Madura,
buds and roots showed polar distribution and were formed endogenously
but that in Ailanthus, where the buds arose in the cortex, polarity was
much less evident. This agrees with Plett's findings in stem cuttings and
emphasizes the more intense polar behavior of the inner tissues.

Leaf Cuttings. Leaves when treated as cuttings behave quite dif-
ferently from stems and roots and show a somewhat different type of polar
behavior, evidently related to the fact that they are organs of determinate
growth. In most cases, regeneration of both roots and shoots occurs at the
leaf base near the cut end of the petiole. Hagemann ( 1931 ) performed
inversion experiments on various species. In certain cases he found that
wound stimulus or water affects regeneration. In Achimenes, shoots were
thus obtained from the apical cut surface and roots from the base under
certain conditions, but Hagemann concluded that, in general, polarity as

Polarity 125

expressed in the location of regenerating structures in leaves is determined
by anatomical structure. Behre (1929) reports that regeneration in the
leaves of Drosera is apolar.

There has been much discussion as to whether, in the higher plants,
polarity once established can be reversed. It has been the common ex-
perience of botanists and horticulturalists that cuttings in which the apical
end is put into the soil will not do as well as those with normal orienta-
tion. Some inverted cuttings are found to take root, however, and may

^ Proximo I

Ditto I

INTACT ROOT

ROOT SEGMENTS REGENERATION

Fig. 6-4. Polarity of regeneration in root of Taraxacum. A root segment produces shoots
at the proximal end ( next the base of the plant ) and roots at the distal end, whether
the segment is normally oriented, horizontal, or inverted. Compare with Fig. 18-17.
( From Warmke and Warmke. )

live thus for some time. Kny ( 1889 ) successfully grew cuttings of Hedera
and Ampelopsis inverted for several years, and Graham, Hawkins, and
Stewart ( 1934 ) did so with willow cuttings, which were still nourishing
after 11 years. The tips of weeping willows will often root at the apex
if they are dipping into water (Pont, 1934). Such inverted structures, how-
ever, often show external malformation and anatomical distortion. Growth
may become normal again if the cutting is restored to its upright orienta-
tion and can form roots at the morphologically basal end. Lundegardh

126

The Phenomena of Morphogenesis

Fig. 6-5. "Inversion of polarity." Etiolated pea seed-
ling with epicotyl decapitated, inverted, and placed in
water. Roots now grow out from the epicotyl and a
shoot from a cotyledonary bud. (After Castan.)

( 1915 ) found that apparent reversal of polar behavior in Coleus was only
temporary.

Reversal seems to be easier to accomplish in seedlings than in older
plants. Castan ( 1940 ) cut off the epicotyl and the primary root from
etiolated pea seedlings and inverted them. Roots then grew out from the
originally apical end and shoots from the basal one (Fig. 6-5). Rath-
felder ( 1955 ) confirmed this observation and believes that it is a real
reversal.

Reversal of polarity is much easier to accomplish in the lower plants
(p. 138).

POLARITY AS EXPRESSED IN INTERNAL STRUCTURE

Polar phenomena are manifest not only in external form but in in-
ternal structure. This is evident in many ways.

Embryonic Development. In vascular plants the first manifestation of
polar behavior is in the division of the fertilized egg. This in most cases
seems to be related to the polar character of the gametophyte. Wetter
( 1952), confirming earlier work of others, finds that in ferns the planes of
division in the young embryo are related to the axis of the prothallium
and that the segment that will form the first leaf is always directed
toward the growing point (notch), a fact also evident later in the orien-
tation of the young leaf itself. This relationship persists regardless of
the direction of the incident light. In Isoetes, the first division of the
fertilized egg is at right angles to the axis of the archegonium, and
early embryo development is not affected by external factors (La Motte,
1937; Fig. 6-6).

Polarity 127

In seed plants the embryo has a definite orientation in the ovule, the
tip of the young radicle always being directed toward the micropyle
and the plumular end toward the chalaza. This has its origin in the polar
relation between embryo sac and ovule, since the archegonium, or egg
apparatus, lies at the micropylar end of the sac. Even the group of four
megaspores is polarized, and it is the one at the micropylar end that
germinates into the female gametophyte. The planes of division of the
proembryo are related to the axis of the ovule. In the young embryo as
it develops at the end of the suspensors, the distinction between root
and shoot begins very early, with the first transverse divisions. The direc-
tion of the polar axis is evidently impressed upon the embryo, as upon
the egg, by the axial organization of the embryo sac and ovule, and
once established this polar behavior persists and is apparently irreversible.

Fig. 6-6. Young embryos in the female gametophyte of Isoetes which have developed
in the positions indicated. Early orientation is with reference to the polar axis of the
archegonium, but when the leaf begins to push out it becomes negatively geotropic.
Z, direction of zenith; R, root; F, foot; L, leaf. (From La Motte.)

Embryonic polarity, however, may arise in other ways than through
this simple relationship to the ovulary axis. In cleavage polyembryony
several embryos may arise from a single egg (p. 206), each showing typical
polar character. Adventitious embryos are sometimes formed by growth
of nucellar cells and not from fertilized eggs, and these grow into normal
plants. Structures essentially like embryos sometimes occur elsewhere in
the plant ("foliar embryos" of Kalanchoe, p. 254) and these show typical
polar behavior. The first manifestation of differentiation in any embryo,
whatever its origin, is the appearance of a polar axis.

A number of cases have been reported (Swamy, 1946) in which the
polar character of the angiosperm embryo sac is reversed, an egg ap-
paratus appearing at both ends, or even the antipodal cells at the
micropylar end and the egg at the opposite one.

Tissue Reorganization. Various histological changes occur in cuttings
grown in an inverted position, as described by Vochting ( 1918 ) and
others. Such plants are evidently abnormal in a number of respects.
There is often a tendency in them to form swellings and tumors, par-
ticularly near the insertion of branches, which now tend to grow upward.

128 The Phenomena of Morphogenesis

The cause of these swellings may lie in the fact that the original tissues
cannot function properly under the changed orientation and that con-
siderable cellular rearrangement must be brought about in the new tissue
formed after inversion. These tumors resemble anatomically the "whorls"
commonly found in wound wood and consist of parenchymatous,
sclerenchymatous, and tracheidal elements. Vochting here has de-
scribed the structure of such tumors in Salix fragilis and other species
and believes them to be due to the innate polar tendency of individual
cells. On such an interpretation, the tissues are thought to twist about
(Fig. 6-7) until finally those of the root and of the new shoot are con-
nected by cells of the same polar orientation ( Kiister, 1925 ) .

There has been considerable controversy as to this hypothesis. Maule
(1896) uses it to explain the behavior of cambium cells in wound wood.

Fig. 6-7. Vessel polarity after budding. I, longitudinal anastomoses between vessels
in normally oriented bud and stock. II, twisting of vessels when bud has been inserted
upside down. At right, single vessel from the latter. (From Vochting.)

Neeff (1922) made an extensive series of studies of the changing orienta-
tion of cambial cells in decapitated stems, finding that these tend to turn
until they become parallel to the newly regenerating axis instead of to
the old one (Figs. 6-8, 6-9), and he explains this in terms of the inherent
polar behavior of the cells, which tends to conform to that of the func-
tional axis. Both Jaccard (1910) and Kiister, on the other hand, disagree
with Vochting's explanation and attribute the changing orientation of
the cells mainly to mechanical factors. Twisting whorls may also appear
in normal callus where mechanical factors can hardly be operative. More
intensive studies are needed of the conditions that cause change in direc-
tion of cell growth. Altered direction of sap flow, for example, might
affect the direction of cambial cell growth in Neeff's experiments. Similar
changes in cellular orientation have been reported by MacDaniels and
Curtis ( 1930 ) in spiral ringing wounds in apple, by Janse ( 1914 ) in
bark strips left across a ringing wound in Acalypha, and by Tupper-

Polarity 129

Carey (1930) in tissue bridges in Acer and Laburnum. Pressure, nutrient
movements, and basipetal cambial activity have been suggested as causes.
The results of Went (p. 384) with inverted cuttings of Tagetes indicate
that the direction of auxin flow in them is ultimately reversed. It is clear
that in some way histological changes are related to the new conditions
under which an inverted cutting has to grow.

Fig. 6-8. Left, diagram showing direction of cambium cells (and their derivatives)
in a normal shoot of Tilia, with a lateral root and lateral shoot growing from it. The
cells are parallel to the particular axis of which they form a part. Right, change of
direction of these cells when the main axis has been decapitated at both ends and the
lateral axes are becoming the main ones. The direction of the cells in the original
main axis has now turned to become parallel with the new ones. ( From Neeff. )

The results of grafting provide a direct way of testing polar differences
in tissues. Vochting ( 1918 ) used the swollen stem of kohlrabi for a series
of such experiments. If the top of a stem is sliced off transversely and a
V-shaped cut made in its upper surface and if the lower portion of
another stem is sharpened to fit this cut and inserted firmly into it, the
tissues of the two stems will knit together. If, however, a piece is sliced
off from the lower part of a kohlrabi stem and it is then inverted, and the
surface now uppermost cut as before, and if a sharpened upper piece
is inserted into this cut, the tissues will not knit. Furthermore, rootlets
will begin to grow out from the upper piece into the lower one, as if

130 The Phenomena of Morphogenesis

growing in a foreign substratum. Thus a root pole will fuse with a shoot
pole but two similar poles, when brought together, will not fuse. Vochting
also found that a square bit of tissue cut out from a beet root and put
directly back will knit in its former place but will not do so if turned
through 180° before being replaced there. These facts can be explained
by assuming that the tissues of the plant, even such relatively undif-
ferentiated parenchymatous ones, have definitely polar behavior. Bloch
(1952), however, observed that tissues of the fruits of Lagenaria do not
behave in this way but that plugs, cut out and replaced, will knit in any

Fig. 6-9. Tangential sections through tissue of an axis like those in Fig. 6-8. Left, nor-
mal wood. Right, after decapitation, direction of cells changing to conform to the axis
of the lateral root, now the main one. ( From NeejJ. )

orientation. Microscopic examination after a few days showed normal
cellular fusion.

In horticultural practice it has long been recognized that buds must
be placed in normal orientation on the stock if they are to knit well.
Colquhoun ( 1929 ) removed buds and pieces of bark in Casuarina and re-
applied them in an inverted position. Observation of the anatomical struc-
ture showed that the cells of the cambium joined freely and continued to
grow regardless of orientation. Wood fibers and vessels, however, show
the characteristic turns and twists reported by Vochting. This suggests
that the cambial cells are unpolarized or in a condition of unstable polar-

Polarity 131

ity and that, as wood elements differentiate, polarity is gradually im-
pressed upon them. Cells inversely oriented are now unable to unite,
and the translocation of materials in them, tending in each to follow the
original direction of flow, is seriously disturbed. This gradual assumption
of polarity is perhaps related to changes at the cell surface as the wall is
formed or in the structure of the wall itself.

Another manifestation of polar activity in histological characters, per-
haps related to the basipetal tendency in the renewal of cambial activity
or to the polar flow of auxin (p. 384), may be observed in the reconstitu-
tion of severed vascular strands across the ground parenchyma of pith
or cortex in herbaceous dicotyledons (Simon, 1908; Sinnott and Bloch,
1945; Jacobs, 1954). This always begins at the basal end of a severed
strand and proceeds downward toward the apical end of the cut bundle
or to uninjured ones.

Cell Polarity. To test Vochting's contention that polar behavior of a
tissue is the result of the polarity of its individual cells is not easy. The
fact that very small tissue pieces retain their original polarity and that
inversely grafted tissues do. not fuse supports Vochting. Many other facts
can also be cited. The two daughter cells following a division are often
unlike (p. 133). In these cases, each of the two types is found invariably
on the same side, toward or away from the tip of the axis. Thus in many
young roots the last division of the surface cells is unequal, the smaller
daughter cell becoming a trichoblast and producing a root hair (p. 190).
This cell is always on the side toward the tip of the root. Before division,
the apical end of the mother cell is also more densely protoplasmic. In
some cases (Phleum) the division is markedly unequal and polar. In
others (Sporobolus) the two cells are more nearly equal and a root hair
is not always formed (Fig. 6-10). Here the polar behavior is much less
marked. In the leaf epidermis of monocotyledons some cells divide
unequally, and the one toward the leaf tip becomes a stomatal mother
cell. These facts suggest that the cells themselves have a polar orienta-
tion.

The tendency of cells to divide in specific directions is at the bottom of
all form determination, since it is concerned with the plane of division
and thus the direction of growth. In the growth of elongate gourd fruits,
for example, divisions are predominantly at right angles to the axis of
the fruit, but in isodiametric ones they are at all angles (p. 51). Whether
polarity is a quality of the whole developing organ or simply of its
component cells is still uncertain and is a problem involving the deeper
one of the relation between cell and organism. Various examples of
polarity in unequal cell divisions have been discussed and figured by
Bunning (1957; Fig. 6-11).

Even when the cell does not divide, the difference between its two

132 The Phenomena of Morphogenesis

ends is often evident. That the cytoplasm is the seat of this polar differ-
ence is shown by the fact that, when vacuolate cells divide, the first
indication of the plane of division, and thus of the polar axis, is the ap-
pearance of a cytoplasmic diaphragm in the position where the future
partition wall will be formed (p. 25). In such cells the direction of the
axis may be related to gradients in hormone concentration, oxygen, or
other factors. This polar difference may be visible in the contents of the
cell, for in Enteromorpha ( Muller-Stoll, 1952), in Isoetes (Stewart, 1948),
and other plants the chromatophore is almost always on the side of the
cell away from the base of the thallus, or plant body. The distribution of
chloroplasts in higher plants is also sometimes polar.

ED EI

B

X

PHLEUM

mmMmsm

B

1

w SPOROBOLUS

Fig. 6-10. Polarity in root-hair development. A, B, and C, successive stages, with root
apex toward left. In Phleum, the last division is unequal, and the cell toward the apex
forms a root hair. In Sporobolus, the division is essentially equal, and the cell toward
the apex does not always form a root hair. ( From Sinnott and Bloch. )

The wall itself may show polar behavior, a fact which is of particular
importance in producing differences in cell shape. Most cells are nearly
isodiametric at the beginning, and if one at maturity is much longer than
wide, this is the result of more rapid growth in length. Such differential
growth, in turn, presumably comes from differences in the fine struc-
ture of the wall, which itself is ultimately dependent on factors in the
cytoplasm. Wilson (1955) has shown that in the wall of the large cells
of the alga Valonia there are two systems of orientation of cellulose
fibrils which converge to two poles at the ends of the cell. The complex
and remarkable shapes of many cells, both in simple organisms and
within the tissues of larger ones, are probably due to a complex pattern

Polarity 133

of wall polarities that determine growth in a number of directions. How
this is brought about is a morphogenetic problem at a different level
from most of those here discussed, and its solution may provide sugges-
tions for an approach to other problems of form.

It is sometimes possible to demonstrate the polarity of single cells ex-
perimentally even though their contents are homogeneous and both ends

Fig. 6-11. Various types of unequal and
polar cell divisions: I, in pollen grain;
II, in differentiation of root hairs in cer-
tain monocotyledons; III, in differentia-
tion of stomata in monocotyledons;
TV, in leaf cells of SpJiagnum; V, in for-
mation of sclereids in Monstera. (From
Biinning. )

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appear to be alike. This can be done by isolating cells and observing the
structures that regenerate from them. Miehe (1905) accomplished this
in the filamentous alga Cladophora. Here polar organization is present
but not conspicuous. At the basal end is a rhizoid which attaches to the
substratum, and the rest of the filament or the thallus, a single row of
cells, is undifferentiated. Miehe plasmolyzed the cells of a filament just

134 The Phenomena of Morphogenesis

enough to pull them away from the walls and break whatever connec-
tions there may have been with other cells, but without killing them.
The plant was then deplasmolyzed. Each cell, now as effectively isolated
as though it had actually been removed, began to enlarge, broke out of
its wall, and proceeded to regenerate a new filament. The significant
fact is that from the basal end of each cell a new rhizoid was formed
and from the apical end, a new thallus. The polar character of the cells,
otherwise impossible to demonstrate, could thus be established. These
experiments were repeated and extended by Czaja (1930; Fig. 6-12).
Borowikow (1914) succeeded in reversing the polarity of Cladophora

Fig. 6-12. Polarity in a single cell.
A cell isolated from a filament of
Cladophora, regenerating a thallus
from its apical end and a, rhizoid
from its basal one. (From Czaja.)

cells by centrifugation, showing again the close relation between the
distribution of material in the cytoplasm and the polarity of the cell.

In some filamentous algae, the plant's organization may disintegrate
under certain circumstances and the individual cells thus become freed
from their correlative inhibition. In Griffithsia, for example, Tobler
( 1904 ) observed such cells in culture and found that, when they began
to regenerate, rhizoids grew from the basal end (distinguishable by its
shape) and shoots from the apical one. Schechter (1935) centrifuged
similar ones and found that their polaritv could be altered by this means
and that shoots always appeared at the centrifugal pole.

The rather loosely organized tissues of these simple algae provide ex-
cellent material for studies in cellular polarity even though their cells

Polarity 135

are not isolated. In bits of tissue cut from Enteromorpha, for example,
Miiller-Stoll (1952) found that the cells near the apical portion of the
piece regenerate papilla-like structures but that the cells at the base
form rhizoids.

To prove the existence of polar behavior in the cells of one of the
higher plants is more difficult. Here it is sometimes possible to re-
generate a new plant from a single cell or small group of cells, especially
in the epidermis, but it is not easy to relate the polarity of the newly
produced structure to that of the cell from which it grows.

POLARITY IN ISOLATED CELLS

In many cases, polarity may be studied in cells that are isolated in
nature and not through experiment. The most notable example of this
is the egg of the rockweed, Fucus, which is discharged into the water and
there is fertilized and grows into a new plant. The Fucus egg is com-
parable to the eggs of certain animals that develop in water and that
have proved such a rich source of knowledge of early embryology. More
work has been done on this egg than on any other naturally isolated plant
cell.

The unfertilized egg is naked, and its nucleus is at the center of the
cell. It shows at the beginning no polarity whatever nor is there any
visible differentiation in its cytoplasm. After fertilization, the egg falls
to the bottom and in about 12 to 24 hours, under normal conditions, a
protuberance appears on its lower surface. This develops into a rhizoid by
which the young plant becomes anchored to the bottom. Soon the egg
divides in a plane at right angles to the axis of the protuberance. The
two cells that result are very different in shape and in their future de-
velopment. The upper, rounded cell gives rise to the main portion of the
thallus. The lower one forms little besides the rhizoid. The growth of
the rhizoid and the first division of the egg establish a permanent polar
axis in a system which at first is quite without one. Here is evidently one
of the simplest expressions of polarity among plants.

Among earlier investigators of the Fucus egg were Kniep ( 1907 ) ,
Nienburg (1922a and b), Lund (1923), and others. The more recent
experiments of Whitaker and his colleagues have provided a large body
of detailed information. Only the main facts will be presented here. This
work has been reviewed by Whitaker ( 1940 ) and Bloch ( 1943 ) .

Gravity seems not to be an important factor in the induction of the
polar axis for, if the eggs are kept in the dark, the rhizoid develops in
any direction. There is evidence that in eggs of the related Cystosira
barbato, if reared in darkness, the rhizoid is formed at the point of en-
trance of the sperm ( Knapp, 1931 ) . Light is clearly a very important

136 The Phenomena of Morphogenesis

factor in Fucus (Hurd, 1920). In eggs lighted from one side by white
light of a certain intensity (or light of particular wave lengths), the
rhizoid always forms on the side opposite the source of light, and the
first wall is laid down at right angles to this direction. Nienburg ( 1922a,
b) showed more specifically that it is not the direction of light but the
intensity gradient that is the determining factor.

Lund ( 1923 ) was able to prove that the first division wall in the Fucus
egg was at right angles to the flow of an electric current and that the
rhizoid grew toward the positive pole. Here the polar axis can evidently
be determined electrically.

A peculiar phenomenon first noted by Rosenwinge ( 1889 ) but studied
particularly by Whitaker is the so-called "group effect." If an egg of
Fucus lies near a group of other eggs, its rhizoid will develop toward this
group ( Fig. 6-13 ) . Whitaker observed that this occurs even when the eggs
belong to different species. These results have been attributed to the

&-^-:>.:.*':''i7 Fig. 6-13. The "group effect" in Fucus eggs. Where
there is a cluster of these, the rhizoidal pole is typically
on the side toward the other eggs. ( After Whitaker. )

establishment, in the medium near the egg, of a concentration gradient
of metabolic products from the other eggs, but Jaffe (1955) finds evi-
dence that such a gradient, if it exists, does not involve H ion, COo, or
02. Jaffe also found (1956) by exposing eggs to polarized light that the
rhizoids tended to develop in the plane of polarization.

Whitaker ( 1937 ) subjected Fucus eggs to centrifugal force and showed
that in such cases the rhizoid grows from the centrifugal pole. Polarity
here seems to be dependent on the rearrangement of materials in the egg.
Other factors, such as pH, temperature, auxin, and even the shape of the
egg have also been shown by Whitaker to modify egg polarity.

Not many other cases of the induction of a polar axis in isolated algal
cells are known, although in certain green algae the polarity of the young
plants developing from swarm spores is determined by the way in which
these spores become attached to the substratum ( Kostrum, 1944 ) .

The remarkable umbrella-shaped alga Acetabularia is really a single
cell though it may be several centimeters tall. During its development it

Polarity 137

has only one large nucleus, situated usually at the base of the stalk.
Here the rhizoids develop. At the summit of the stalk is the disk. If a
nucleus is introduced into a plant or plant segment which lacks one, a
new rhizoid system will arise wherever the new nucleus is placed and
polar behavior of the plant may thus be modified or reversed ( Hammer-
ling, 1955).

In the germination of a moss spore, the young protonema pushes out on
the side of the spore toward the light, and the rhizoid forms at the op-
posite end, indicating that here, as in the Fucus egg, its polarity is de-
termined by light. In several moss species, Fitting (1949) was able to re-
verse this polarity by reversing the direction of the light. In this way the
young protonema becomes converted into a rhizoid.

Heitz ( 1940 ) prevented polar germination of Funaria spores by appli-
cation of auxin. Cell division was also inhibited by this means and
"giant" cells thus produced. D. von Wettstein (1953) confirmed this and
found that vitamin Bi and chloral hydrate destroyed polarity without
preventing cell division. Such apolar growth continued for 50 cell genera-
tions, producing an undifferentiated, tumor-like body. Such a result
emphasizes the importance of polar behavior for orderly development
and the production of form.

How the polar axis is determined in the spores of vascular plants has
been demonstrated in a few cases. In Equisetwn, the spore of which
shows no external or internal polarity, germination is followed by di-
vision into two cells. The division wall, as in Fucus, is laid down at right
angles to the gradient of light absorption (Stahl, 1885). The more strongly
illuminated daughter cell becomes the primary prothallial cell and the
one on the darker side, the rhizoidal cell. Nienburg (1924) showed that
this alignment of the mitotic figure parallel to the direction of the inci-
dence of light does not occur until a redistribution of cytoplasmic ma-
terial has taken place, especially an aggregation of chloroplasts on the
illuminated side (Fig. 6-14).

In germinating fern spores, light modifies the polar behavior but this
effect is different in different wave lengths (Mohr, 1956). Naf (1953),
also working with ferns, found evidence that the spore of Onoclea has an
inherent polarity but that this can be modified by light. He carried the
study of polarity reversal much further by growing the young prothallia
in a liquid culture which was constantly shaken. The prothallia thus
developed in an environment where there were no environmental
gradients and where the plant was exposed on all sides to equal stimu-
lation by gravity, light, and other factors. The result was a spherical,
tumor-like mass of tissue. Grown on agar and without movement, this
tissue again formed structures much like the normal prothallia. The
genetic basis for a normal prothallium, specific in character, is in the

138 The Phenomena of Morphogenesis

spore but such a prothallium will develop only where there is an en-
vironmental gradient by which its polar axis is established. Such results
emphasize the fact that neither genetic constitution nor environment
alone controls the development of organic form, but an interaction be-
tween them.

Polarity is also to be found in the microspores and pollen grains of
higher plants, though here it is not easily open to experimental analysis.
The spore axis, as indicated by the orientation of the division of the
spore nucleus, has a constant relation to the planes of division of the
pollen mother cell.

Fig. 6-14. Origin of polarity in a single cell. I, unpolarized spore of Equisetum. II,
beginning of polarization as shown by changed positions of plastids (chl) and nucleus
(k). Ill, first nuclear division. (After Nienburg.)

POLARITY IN PLASMODIA AND COENOCYTES

In larger and multinucleate protoplasmic units, notably coenocytic
forms, polarity finds a somewhat different expression than in uninucleate
protoplasts. Thus in the plasmodium of Plasmodiophora brassicae, as re-
ported by Terby (1933), the axes of the many nuclear division figures lie
parallel to one another, indicating that the whole mass of protoplasm has
a uniform anisotropic orientation, though here without a polar axis. This
parallelity is also found in the first sporogenic division but disappears at
the second one. In most plasmodia, however, this simple sort of polar
behavior seems not to be present.

True coenocytes show some remarkable examples of organized systems
where there is pronounced differentiation of parts but no cellular parti-
tions in the cytoplasmic body. Conspicuous among these are the algae
Bryopsis and Caulerpo.

Bryopsis has an axis from which "leaves" come off in a pinnate arrange-
ment above and rhizoids below. This polar organization can be com-
pletely reversed if the plant is held in an inverted position. The leaves
then produce rhizoids and the rhizoids, leaves ( Noll, 1888; Winkler, 1900;
and others ) . It now seems probable that a different relation to light rather

Polarity 139

than to gravity is responsible for this reversal. Steinecke (1925) has
shown that in these inverted plants there is a movement of the cyto-
plasm that was originally in the upper portion into the base, and vice
versa. The easy reversal in such plants seems to be related to the fact
that the cytoplasm can move readily throughout the whole body. The
cellular organization of higher plants may contribute to the more fixed
polarity that they display as well as to their higher degree of differen-
tiation.

Caulerpa has a more complex structure than Bryopsis, for it possesses
a horizontal "rhizome" from which "leaves" grow out above and rhizoids
below. The leaves are negatively geotropic, the rhizoids positively so,
and the rhizome is diageotropic. Regeneration in this plant has been
studied by many workers (Wakker, 1886; Janse, 1906 and 1910; Dostal,
1926 and 1929; Zimmermann, 1929; and others ) . Its polar phenomena are
rather complex. Zimmermann found that gravity determines the dorsi-
ventrality of the rhizome and that this can be reversed. He also observed
that in each portion of a cut leaf new rhizoids are formed below new
leaves. An inverted leaf with its tip buried will produce leaves at its
original base and rhizoids at its original apex, as in Bryopsis. Janse has
shown, however, that rhizoids normally appear chiefly at the apical por-
tions of cut leaves, and Dostal finds that, although regeneration is polar
in young leaves, the new organs may be distributed over the entire sur-
face of older ones. Polarity in Caulerpa is less stable than in higher plants
and this, again, is probably because of the ease with which cytoplasmic
movement may take place.

PHYSIOLOGICAL MANIFESTATIONS OF POLARITY

Differences in the external or internal structure of the plant body are
almost invariably accompanied by physiological differences, though the
latter are usually more difficult to demonstrate. Among these are the uni-
directional flow commonly shown by auxin and often by other substances;
the differences in bioelectric potential which can be demonstrated be-
tween different parts of the plant; and the many examples of physiological
gradients in the plant body— in pH, rate of respiration, osmotic concentra-
tion, auxin concentration, and others. These are doubtless related to
visible morphological polarities but the character of the relationship is
obscure. Whether such physiological polarities control the morphological
ones or whether both are determined by more deeply seated morpho-
genetic factors in the living material, which are physiological only in the
broadest sense, is not known.

Electrical polarities are found in many organs and in the plant body as
a whole. Unfortunately, any discussion of the significance of electrical

140 The Phenomena of Morphogenesis

potentials in relation to morphological polarity and polar regeneration
must remain for the present rather hypothetical because of the uncertain-
ties which still exist as to the nature and origin of the potential differences
themselves ( p. 361 ) . The phenomena of organic polarities have so many
similarities to electrical ones that it is tempting to explain the former
entirely in terms of the latter, but there is insufficient evidence as yet for
such a simple solution of the problem.

Physiological gradients of various kinds, particularly metabolic ones,
and their significance have been extensively discussed by Child ( 1941 ) .
Such gradients are along the major axes of the organism, and indeed
their existence is thought by some to establish these axes and to be a
major factor in the origin of polarity. Child believed that they arise early
in development as the result of some unilateral difference in the environ-
ment and that, once established, they persist. He points out that they
often can be obliterated or redirected by external differentials and infers
that they are of great importance in determining patterns of development.
The inherent properties of protoplasm, unable alone to control develop-
ment, produce their morphogenetic effects through specific reactions to
such axial gradients. Prat ( 1948, 1951 ) has reviewed the relations be-
tween physiological and histological gradients.

Gradients in respiratory activity such as have so often been described
in animal axes are found in plants ( Wanner, 1944 ) . Ball and Boell ( 1944 ) ,
however, have shown that in some plants the rate of respiration at the
meristematic tip is less rapid than in the zone immediatelv behind this
(p. 73). Hurd-Karrer (1926) found that in corn stalks the minimal con-
centration of solutes is in the basal internodes and increases upward, a
gradient reported by others for leaves at different levels in a tree. In plant
exudates there is a concentration gradient with the highest values near
the apex (Tingley, 1944). The proportion of ash to dry weight in herba-
ceous plants was shown by Edgecombe ( 1939 ) to increase toward the tip
of the plant. Many other examples might be cited.

These gradients are often related to translocation of solutes and food
and thus to localized and differential growth. Hicks (1928a, b) found
that nitrogen tends to move toward the morphological tip of a stem and
carbohydrates toward the base, even in inverted shoots, so that a gradient
in C/N ratio results in the stem. She believes that this may be respon-
sible for the phenomena of polarity, but this may be a parallelism rather
than a causal relation.

The unidirectional flow of nutrients to particular "centers of attraction"
in shoots, roots, leaves, and other structures has been emphasized by
Goebel as of particular importance in regeneration and other phenomena
of development. What causes the establishment of such centers and thus
directs the location of growth is a question closely related to that of

Polarity 141

polarity. Simon (1920) has suggested that the polar character of regen-
eration in leaves is related to the basipetal movement of carbohydrates.

How much the direction of flow in the phloem is due to polar behavior
in the strict sense and how much to other factors is not clear, but Schu-
macher (1933, 1936) has shown a polar flow of fluorescein there, basipetal
in the petiole and in various directions in the stem. It seems clear that in
most vegetative stems the flow of nutrients in the phloem is predomi-
nantly basal. Sax (1956 and earlier papers) removed a ring of bark in a
young tree and then replaced it in an inverted position. Under these con-
ditions phloem transport is markedly checked and the tree is much re-
duced in growth. This effect is not permanent, however, because the new
bark regenerated at the seam permits phloem transport upward.

The clearest case of physiological polarity and the one most thoroughly
studied is that of the flow of auxin (p. 384). In the Avena coleoptile it has
been shown that auxin normally is produced at the tip and moves toward
its base. If the coleoptile is cut off, decapitated, and auxin applied at
the morphological apex it will move toward the other end, whether the
coleoptile is normally oriented or inverted. If auxin is applied to the
morphologically basal end, however, it will not move toward the tip even
if the coleoptile is inverted and the auxin is placed at the end now upper-
most. Auxin flow here is therefore strictly polar. The cause of this
polarity is not clear, for there is no histological difference with which
it is correlated. It seems to be characteristic of auxin transport gen-
erally, for this substance, commonly produced in buds, moves down-
ward from them but not upward. Jacobs and others (p. 384), however,
report that auxin may sometimes move acropetally, especially in weak
concentrations.

Went ( 1941 ) has shown that the auxin flow continues to be morpho-
logically basipetal in inverted cuttings of marigold but that after a time,
presumably following the production of new and reoriented vascular
bundles, the flow is reversed and auxin now moves downward toward the
new root system. He suggested that auxin polarity is electrical in char-
acter, but this idea has encountered some difficulties ( p. 360 ) .

The significance of auxin polarity for many problems of plant develop-
ment is great since this substance is so intimately related to both stimula-
tion and inhibition of growth and to so many specific growth reactions,
such as the initiation of shoots and roots (p. 390).

It is tempting to explain all structural polarity in the plant as due to this
polar flow of auxin, but here again it may be that both are the result of
some more deeply seated factor. No satisfactory solution of the problem
has yet been found. It is surely a remarkable fact that a simple, relatively
undifferentiated parenchyma cell of the oat coleoptile will allow auxin to
pass through it in only one direction. An understanding of the mechanisms

142 The Phenomena of Morphogenesis

involved in this polar flow would doubtless contribute to the solution of
many problems in physiology and development.

POLARITY AND DEVELOPMENTAL PATTERN

The chief significance of polarity for students of morphogenesis lies in
the fact that it is the simplest expression of the general phenomenon of
organic pattern. These patterns, which are exhibited in such profusion in
the bodies of animals and plants, are each built around a polar axis
which provides, so to speak, the theme or foundation upon which the
whole develops. This, of course, is by no means the only expression of
polarity in the plant. In a tree, for example, not only the main trunk but
the many branches growing out from it may each have a polar axis of its
own. The frequency and size of these branches and the angles which
they make with the trunk produce the characteristic pattern of the tree's
crown, one which is almost as specific as the pattern of its leaf. The char-
acter of this crown is due to the dominance of certain buds or branches
over others and thus to a controlled localization of growth and a balance
between the various axes of the tree. This, in turn, seems to be governed
by a specific polar pattern of auxin distribution. It seems probable that
the form and development of a leaf, which involve a pattern of major and
minor vein polarities, have a similar basis. In such cases as these, organic
form appears to be the expression of a series of interrelated polar axes.

Such a condition probably occurs also in forms in which the organic
pattern is related to the polarity of individual cells. This is well shown
in the development of shoots that grow by a large apical cell. Here the
growth and differentiation of the axis are clearly associated with a precise
series of divisions in various planes, both of the apical cell and of those
cut off from it (p. 58). This pattern of diverse cell polarities is less easy to
trace in other meristematic regions but is evidently operating there as
well. In such a structure as the growing primordium of a young ovary,
cell divisions are very abundant but occur in every direction, as though
the planes of division were at random. That such divisions are all part of
a definite organic pattern, however, is shown by the fact that the structure
in which they occur shows a regular and progressive development toward
its specific form. Each plane of division, presumably determined by the
orientation of the cytoplasm, is related to the complex pattern of diverse
polarities of which it forms a part (Sinnott, 1944).

The polar phenomena of coenocytes and other evidence support the
contention that the basic fact in polarity is the orientation and polar be-
havior of the cytoplasm. Where this is confined within cell walls, more
complex and stable patterns may be produced, but the fundamental prob-
lem everywhere seems to be the development of polar patterns in the

Polarity 143

whole cytoplasmic body of the organism, whether this is cut up into cells
or not.

Polar patterns are not confined to organisms that have developed in the
ordinary way by growth from a reproductive unit such as a spore or egg
but are found in what are essentially organic communities. Thus in cer-
tain slime molds such as Dictyostelium (p. 223) the vegetative individual
is a tiny myxamoeba. At the end of vegetative growth some thousands of

Fig. 6-15. Polarity in Dictyostelium. If an apical piece of a pseudoplasmodium is placed
in close contact with the apical end of another, coalescence takes place. If it is placed
next the basal end, either of the same plasmodium or of another, there is no coa-
lescence, and the terminal piece moves off independently. (From K. B. Raper.)

these become aggregated into a pseudoplasmodium where each retains its
individuality. This colonial structure shows a polar organization, for the
terminal portion of it can be grafted to the decapitated apex of another
pseudoplasmodium, though not to the base (Fig. 6-15). The tip is evi-
dently the dominant region, for if grafted to the side of a pseudoplas-
modium it will withdraw from it a group of individuals and start out as a
new unit. The sorocarp that ultimately develops has a vertical polar axis
and, in some species, lateral axes as well. Polarity in organisms like these

144 The Phenomena of Morphogenesis

appears to be a property not of the individual cells but of the aggregate
that they form.

Three Aspects of Polarity. Polarity is evidently a complex phenomenon
which is intimately related to the whole process of development. It may
be broken down, for purposes of more detailed examination, into several
different aspects or elements which may possibly involve different physio-
logical or developmental processes.

First, one may recognize the oriented behavior of living substance, as
distinct from axiation or bipolarity. This is evident in the differential
growth of cells and tissues, where one dimension increases more rapidly
than the others; in the controlled plane of cell division, in which the
cytoplasm, as evident especially in vacuolate cells, sets up a pattern
oriented in a definite direction; and in coenocytes and plasmodia where
growth, movement, or direction of nuclear spindles is similarly oriented.
The fundamental basis of this behavior is not known. There may be in-
volved the orientation of micelles or other submicroscopic units, the
paracrystalline properties of cytoplasm, the orientation of molecules at
cell surfaces or interfaces, or the nature of the fine structure of the cell
wall. It is reasonable to suggest that some sort of cytoplasmic anisotropy
is concerned in this oriented behavior. Here is evidently a major problem
for the student of the ultimate structure of protoplasm, a problem inti-
mately related to the whole question of directed growth and thus of or-
ganic form. Whatever the basis of oriented behavior may be, in some
cases it can evidently be changed in direction readily by environmental
factors, but in others, when once established, it becomes firmly fixed.

A second aspect or element of polarity is axiation. The oriented be-
havior of living material most commonly, though not invariably, is ex-
pressed in cellular systems which develop symmetrically in relation to an
axis or plane of symmetry parallel to the direction of orientation. Most
cells and most multicellular structures possess an axis. Such structures as
the cells and filaments of unattached filamentous algae may show no evi-
dent difference between the two ends of the axis, either in cell or filament,
but they are clearly axiate. The problem of the symmetrical growth of a
living system about this axis, so characteristic of almost all organic de-
velopment, is an essential part of the general problem of pattern. Experi-
mental attack upon this phenomenon of symmetry is promising, for its
character can often be changed by modifying the environment.

The third aspect of polarity is polar difference, the appearance of dis-
similarity between the two ends of the axis. This is regarded by many as
the essential characteristic of all polarity and is present in the great ma-
jority of organic axes. In not a few cases, as we have seen, cytoplasm may
show oriented behavior, or an axis of symmetry may develop, without any
demonstrable evidence of difference between the two ends of the system.

Polarity 145

Only where polar differences occur, however, with the resulting morpho-
logical and physiological gradients from one end of the axis to the other,
can there develop the complex patterns characteristic of most living
organisms.

The relation between these three aspects of polarity involves the prob-
lem of the origin of polarity itself. If they can be shown to form a pro-
gressive series, in phylogeny or ontogeny, this would indicate that polarity
may increase in complexity. In free-floating algal filaments (as in Spiro-
gyra) there is no evidence that the two poles are unlike. In filamentous
forms like Cladophora, however, where one end is attached to the sub-
stratum, each individual cell displays a polar character in its regeneration.
Here, and in many other cases where environmental factors are different
at the two ends of the axis (as in the Fucus egg), it appears that this
difference sets up an axial gradient in a system originally unpolarized,
which results in the polar difference. Child and his school regard all
polarity as having its origin in such environmentally induced gradients,
which determine both the direction of the axis and the difference be-
tween its poles. On the other hand, since instances of similar poles are
rare, it may be held that the two ends of every axis are fundamentally
unlike and that in cases where they seem alike the difference is merely
masked and difficult to demonstrate. If this view is correct, polarity may
be due to something quite different from a gradient and may be compa-
rable to, and perhaps result from, an inherent polar tendency, presumably
electrical in character.

Whatever its origin, the direction of this bipolar axis is often continu-
ally changing but under definite control, and upon this fact depends the
orderly development of organic patterns. Thus in a three-faced apical cell
the polar axis must shift 120° between successive divisions. In more com-
plex meristems the planes of cell division are equally orderly, though less
evidently so. How such a system of changing polarities is controlled so
that growth in one direction is precisely related to that in another is a
part of the same problem of orderly development which the student of
morphogenesis so often meets.

The ease with which polarity may be reversed in the simplest plants
suggests that even in more complex ones it is not irrevocably fixed by
genetic factors. Like any trait with a genetic basis, polarity is not a specific
characteristic but a specific reaction to a specific environment. The en-
vironmental factor may be external, such as the direction of light, or
internal, like the correlation between the axis of the young embryo and
that of the archegonium, but unless there is an environment to which the
organism can orient itself, the phenomena of polarity will rarely appear.
Sometimes this environmental reaction is determined early and is later
irreversible, as in cases where polarity becomes firmly fixed in the ferti-

146 The Phenomena of Morphogenesis

lized egg. In other instances polar behavior is subject to induction through
environmental factors at all stages. Many cases of polarity are like this.
Sometimes this polar plasticity persists indefinitely, as in Caulerpa. In
other cases, like the egg of Fucus, it lasts only till the polar axis is deter-
mined and then remains unchanged, regardless of the environment. What
is present in all living stuff seems to be a persistent tendency for the
establishment of polar behavior. This, indeed, is an essential preliminary
for the development of a formed and organized system.

The study of polarity has thus far raised more problems than it has
solved. Most of these, however, are of a sort more amenable to analysis
and experimental attack than are many-others in organic development.
Especially through subjecting each of the various aspects of polarity
separately to experiment, aspects which may perhaps involve distinct
developmental processes, is there hope of progress.

CHAPTER 7

Symmetry

The presence of an axis, so generally characteristic of the form of body or
organ in animals and plants, is manifest not so much as an actual material
structure but as an axis of symmetry, a geometrical core or plane around
which or on the two sides of which the structures are symmetrically dis-
posed. One of the most obvious manifestations of organic pattern in
living things is this symmetrical arrangement of their parts.

Symmetry is evident in both external form and internal structure. Lat-
eral roots arise from a primary root in two, three, four, or more equally
spaced rows. Leaves are symmetrically disposed around the stem in a
phyllotactic spiral. Floral diagrams, both transverse and longitudinal, also
provide good examples of axial symmetry, though here the axis is usually
much shortened.

Symmetry is equally conspicuous in internal structure. The cross sec-
tion of almost any vertical plant axis shows symmetrical arrangement of
its tissues, both primary and secondary. Even single cells, especially when
they possess a considerable internal diversity like those of Spirogyra, are
symmetrical.

In horizontal organs the simple radial type of symmetry characteristic
of vertical axes is replaced by a dorsiventral one where the two halves on
either side of a vertical plane of symmetry are alike. Many prostrate stems
and most leaves are examples of such dorsiventrality. Sometimes one type
of symmetry may be changed to the other by modifying the orientation
of the structure to light or gravity. In other cases the pattern of symmetry
is inherited and cannot be influenced by environmental factors.

Many structures are in themselves asymmetric. In leaves of Begonia
and elm, for example, the portions on either side of the midrib are usually
quite unlike; and there are marked internal asymmetries, as when two
daughter cells are dissimilar. In most cases of this sort, however, the
asymmetry proves to be part of a larger and more complex pattern which
is symmetrical.

Symmetry is often more conspicuous in embryonic structures or meri-
stematic regions than at maturity, and some of its most remarkable ex-

147

148 The Phenomena of Morphogenesis

pressions are in soft and watery structures which seem to be a direct
expression of protoplasmic configuration. Even though protoplasm is seem-
ingly an amorphous and semiliquid material, these structures that it builds
are far from formless, and the beautiful symmetries that they display
seem clearly to be manifestations of the fundamentally symmetrical char-
acter of living stuff itself. Organic symmetry presents a basic problem for
students of morphogenesis.

INORGANIC AND ORGANIC SYMMETRIES

There are many examples of symmetry among inorganic objects. These
often resemble the symmetries of living things, but there are certain
fundamental differences between them. What the relation between these
two types may be and whether organic symmetries have their origin in
those of the inorganic world are problems that have long been discussed
but are still far from solution.

The arrangement of iron filings around the two poles of a magnet is a
familiar example of symmetry, as are the lines of force in an electrostatic
field. The least-surface configurations shown by liquids and especially by
liquid film systems provide beautiful examples of symmetry. The resem-
blance of such systems to multicellular structures in plants and animals,
particularly the more minute ones, has been observed by many biologists
and is discussed at length by D'Arcy Thompson ( 1942), who has analyzed
the various forms possible in a film system. The molecular forces that
operate here, however, are probably not important in determining the
symmetry of large organic bodies.

Much is now known, from X-ray studies and other sources, of the actual
structure of molecules, and these are found to display symmetries, often
very complex and specific ones. Whether such molecular forms have any
relation to the bodily forms of plants and animals is a problem which has
aroused much speculation but on which little evidence is available. Harri-
son ( 1945 ) has discussed some of the possibilities here.

Crystals provide the most familiar and remarkable examples of sym-
metry in the inorganic world. Their very specific forms are the reflection
of the forms and relationships of the molecules that compose them. The
study of crystal symmetry is a complex science in itself and has intimate
relationship to geometry, chemistry, and mineralogy. Crystals possess
axes and planes of symmetry, as do organic structures, but crystalline sym-
metry is a much more formalized and rigid phenomenon than organic.
Many biologists have endeavored to find a relation between crystals and
organisms in their form and symmetry, but this search, in general, has
been a rather fruitless one. Organic symmetries can be described in the
same geometrical language that we use for crystals, but whether there is

Symmetry 149

any fundamental similarity between the two is uncertain. For a discussion
of this problem the reader is referred to the work of Haeckel (1866) and
others.

Although many symmetries in cells and minute multicellular structures
resemble those in inorganic systems under the control of surface forces,
organic symmetries are conspicuous in much larger bodies where these
forces are not operative. Organic bodies are semiliquid systems which are
subject to continual loss and replacement of material, as is shown by
tagged isotopes and in other ways, and in this respect are unlike crystal-
line structures, which are usually fixed and static. This semiliquid char-
acter is also reflected in the almost universal presence of curved lines and
surfaces in organic bodies as compared with the systems of straight lines
and planes which distinguish molecular and crystalline forms. This is
what makes possible the infinite number of similar planes of symmetry
around an organic axis instead of the limited number of two, three, four,
and six found in crystals.

Aside from these differences from the inorganic, the symmetries shown
by living plant structures also possess two distinctive features of their
own which provide the key to an understanding of their nature.

First, they are often expressed in multiple parts. A typical plant body
consists of an indeterminate series of repeated, essentially similar parts,
laterally dispersed along a continuous axis. These are leaves, branches,
and lateral roots in higher plants and analogous repetitive structures in
lower ones. The most conspicuous examples of organic symmetry are
found in the relations of these repeated structures to the axis from which
they arise. This is a type of symmetrv unlike that found in most inorganic
systems.

Second, many plant axes, particularly those of the aerial portions of the
plant, have either a spiral twist or a spiral arrangement of their parts.
This complicates the expression of symmetry and, in the case of phyllo-
taxy, has given rise to a great deal of speculation. Spirality seems to be a
characteristic feature of protoplasmic behavior in many cases. The course
of streaming is often spiral in a cell and thus may be reflected in the
structure of the cell itself, as in the familiar cases of Chara and Nitella.
Cell growth may be spiral, as has been shown by Castle ( 1936 ) in the
hyphae of Phycomyces, and there are many other examples.

These two traits— multiple parts and spirality— make the symmetry of
plant parts radically different, at least in external expression, from the
symmetries of the inorganic world.

A few single-celled forms and some colonies like those of Volvox may
be spherical and completely symmetrical around a point. This seems to
be primarily an expression of surface forces, however, rather than of in-
herent symmetry. Most single-celled plants, however, like the desmids,

150 The Phenomena of Morphogenesis

and most protozoa, show axial symmetry, often complex in character; and
all typical examples of symmetry in higher plants are those manifest
around an axis or a longitudinal plane. Three general types of such sym-
metries are recognized: radial, bilateral, and dorsiventral. All the com-
mon patterns for the structure of plants and their organs are based on
these symmetries.

RADIAL SYMMETRY

In this type there is an axis of rotation around which symmetry is uni-
form. There may be one or two evenly spaced longitudinal planes of
symmetry, as in stems with distichous and with opposite-leaf arrange-
ments, or these may be almost infinite in number in stems with spiral
symmetry. Radial symmetry is present in vertically elongated axes such
as those of the main stem and primary root and in many flowers and fruits.
It is therefore much commoner in plants than in animals, since most of
the latter show dorsiventrality, and it is regarded by many as the most
primitive type of symmetry, at least in vascular plants, since their first
axes were presumably vertical.

In Lower Plants. Individual cells often show radial symmetry regard-
less of their orientation, as in Spirogyra and Chara. Many plant bodies in
the thallophytes have this type of symmetry, a familiar example of which
is the "mushroom" form of sporophore in the fleshy fungi. Many red algae
have radial thalli, as do some brown algae. Most true mosses also are
radial.

In Roots. Almost all roots are radially symmetrical. This symmetry is
shown in the straight and evenly spaced rows of lateral roots and in the
characteristically radial primary vascular structures, in which arms of
xylem typically alternate with bundles of phloem in a star-shaped pattern,
with lateral roots arising opposite the xylem arms.

In two respects the expression of symmetry in the root is different from
that in the stem. Roots, even horizontally growing ones, are usually
strictly radial and (save for a few cases such as air roots of orchids)
show no dorsiventrality, regardless of their orientation, whereas horizon-
tal stems commonly do show this. Roots also have very little twisting or
spirality in their internal or external structures, such as most stems dis-
play. These two differences emphasize again the fundamental diversity in
developmental behavior of root and stem which is evident in many other
respects. Whether these differences are inherent or are due to the radical
differences in the environment in which roots and stems usually develop
is an interesting morphogenetic problem.

In Shoots. The symmetry of shoots, and particularly that shown by the
arrangement of leaves (phyllotaxy), has attracted more attention than

Symmetry 151

any other aspect of the problem of organic symmetry. The external sym-
metry of an upright stem is typically radial and often very regularly so. In
the simplest cases, as in certain mosses such as Fontinalis, this is related to
the activity of a three-sided apical cell, the segments cut off from its three
sides giving rise to three rows of leaves. In higher plants, however, leaf
arrangement is not related to meristematic structure.

In stems with opposite leaves, at successive nodes the leaf pairs rotate
through 90°. This decussate phyllotaxy thus shows four rows of leaves
along the stem. More frequently, phyllotaxy shows a spiral character.
Sometimes this is manifest, even in opposite-leaved types, by a twisting of
the whole axis so that members of successive pairs are a little more than
90° apart. Spirality more commonly expresses itself, however, in the ar-
rangement of so-called "alternate" leaves. These are rarely exactly alter-
nate but are so dispersed that a line connecting the points of attachment
of successive ones follows a regular spiral course around the stem. The
fact of this spiral and the various types in which it is manifest have for
many years attracted the interest of botanists and mathematicians. Many
of the discussions and speculations that have centered about the phyllo-
tactic spiral are of no great significance for morphogenesis. Some are
highly theoretical or even almost mystical. The developmental origin of
the various types of phyllotaxy, however, is an important morphogenetic
problem, and a knowledge of the factors involved may contribute to an
understanding of the origin of organic form.

Goethe was greatly attracted by the spirality of leaf arrangement and
made it the basis of one of his theories. Charles Bonnet ( 1754 ) in the
middle of the eighteenth century discussed the spiral structure of the pine
cone. It was the work of Schimper (1836) and Braun (1831), however,
that established the study of phyllotaxy on its modern basis. Various ex-
planations of the origin and significance of spiral leaf arrangement have
been proposed, and the literature of the subject is extensive. No compre-
hensive review of it is available, though the earlier literature has been
surveyed by C. de Candolle ( 1881 ) . For the more important ideas the
reader is also referred to the works of the brothers Bravais (1837), Hof-
meister (1868), Wright (1873), Schwendener (1878), Schoute (1913,
1914), Church (1920), Hirmer (1922), Crow (1928), Goebel (1928),
Snow and Snow (1934), D'Arcy Thompson (1942), Plantefol (1948),
Wardlaw (1949a), and Richards (1950).

Spiral phyllotaxy is not an example of symmetry in the strict sense since
planes of symmetry, in the crystallographic meaning of the term, are
absent. The leaves do have regular positions along the axis, however, with
reference to each other, and these, under proper analysis, can be ex-
pressed in terms of geometrical symmetry. The spiral formed by the
points of attachment of successive leaves— the genetic or developmental

152 The Phenomena of Morphogenesis

spiral— represents the order in which the leaf primordia are formed in the
bud. Their positions in the spiral are not indefinite but commonly fall into
a few precise categories, the relations of which have long excited the
interest of morphologists. Simplest of all is the distichous, or truly alter-
nate, arrangement, with successive leaves 180° apart around the stem. To
pass from a leaf to one directly above it involves one circuit of the axis
and two leaves, a condition which may be expressed by the fraction Vo. In
other types this spiral passes once around the axis but every third leaf is
over one below it, a condition that may be represented by the fraction %.
Commoner than either of these is a spiral where in passing from a leaf to
one above it two circuits of the axis are made and the fifth leaf is reached,

Fig. 7-1. Diagram showing % phyllotaxy.

the % type. Frequently observed in stems is a % phyllotaxy (Fig. 7-1)
and less commonly that of %3. In cones and other compact axes more
complex phyllotaxies of %t, x%4, and 2%5 may be found. The series is
thus V2, Vs, %, %, %8, %lt 13/34, 2%5, 3%9, and so on. Each obviously
represents the fraction of the circumference of the axis, or the angle,
traversed by the spiral in passing from one leaf to the next. The number
in both numerator and denominator of each fraction is the sum of those
in the two preceding fractions. This particular series is known as the
Fibonacci series. The higher fractions become more and more uniform
and approach as a limit the decimal fraction 0.38197, or the angle
137°30'28", the so-called "ideal" angle. It has been shown by Wright
( 1873 ) that if successive leaves were formed at just this angular distance

Symmetry 153

around the stem from each other no leaf would ever be directly over any
below it. The advantage sometimes suggested for this arrangement, that it
would distribute the leaves most evenly to the light and thus be most
efficient in preventing shading, is open to many objections.

The fraction 0.38197 is of interest in another connection, for it desig-
nates the "golden mean," or sectio aurea, the distance from the end of a
line at which, if the line is cut there, the smaller fraction of the line is to
the larger as the larger is to the whole. Thus 0.38197 : 0.61803 = 0.61803 :
1.0. The golden mean has long been known and has received much atten-
tion from artists and mathematicians, and its significance in the geometry
of symmetry may be considerable, but its biological importance seems
negligible. One should also remember that there are other series of frac-
tions which converge to the same limit.

This analysis of the genetic spiral assumes that, as it twists around the
stem, a given leaf position on it is directly over one below, after passing
3, 5, 8, 13, etc., leaves on the spiral. Thus there should be vertical rows
of leaves, relatively few in the simpler phyllotaxies but more numerous
in the complex ones. These have been called orthostichies and mark the
end points of each successive fraction into which the genetic spiral is
divided. Their presence is essential if the mathematical analysis of this
spiral, going back to the work of Schimper and Braun and elaborated by
so many botanists since then, is to mean very much.

The existence of these orthostichies, however, has been challenged by
more recent students of phyllotaxy, who have approached its problems
not by an analysis of mature structures but by a more truly morphogenetic
investigation of the way in which the leaves originate. The best place to
study leaf arrangement, they maintain, is in the bud or at the apical
meristem. Church (1920), one of the pioneers in this method of attack,
discovered that in the arrangement of primordia as seen in a cross section
of the bud there are no orthostichies at all, for no leaf primordium arises
directly over one below. Thus doubt was cast on all the early conclusions-
based on the assumption that the genetic spiral could be divided into re-
peated portions.

But other relationships are more important than this. A study of leaf
primordia packed into the bud, or of other cases such as pine cones and
sunflower heads where there are a great many structures spirally arranged
but crowded together, shows the existence of another series of spirals,
resembling the genetic one in certain respects but reached in a different
fashion. If one looks at the cross section of a bud, or the face view of a
sunflower head in fruit, or the base of a pine cone, he will notice that the
units are not packed uniformly together like the pores of a honeycomb.
Instead, the various structures— leaves, primordia, fruits, or scales— form
two sets of spiral curves, starting in the center and moving to the circum-

154 The Phenomena of Morphogenesis

ference, one going to the right (clockwise) and the other to the left
(counterclockwise). The effect is something like that of a spinning pin-
wheel, or rather of two spinning in opposite directions. The inner mem-
bers of each spiral are progressively smaller since they were formed later.
We are looking down, in effect, on the top of a growing system, even
though growth may have stopped. These spirals are logarithmic ones,
since the radial distance to each successive unit on them increases geo-
metrically and not arithmetically. The spirals are termed parastichies,
or sometimes contact parastichies since each unit is usually somewhat
flattened against its inner and outer neighbors in the spiral, a fact which

Fig. 7-2. A pine cone seen from below. The scales are in two sets of parastichies, 8
counterclockwise and 13 clockwise.

makes the spiral easy to trace ( Fig. 7-2 ) . The spirals intersect each other
at an angle which is near to 90°.

In a bud or meristematic tip that will give rise to a shoot with a rela-
tively low phyllotactic fraction ( % or % ) , the units are fewer than in
large structures like a cone. In a cross section of such a bud (Fig. 7-3) it
is possible to distinguish by the relative sizes of the leaf primordia the
order in which they were produced. The genetic spiral can thus be traced,
compact and almost two-dimensional here although later it will be pulled
out like a telescope when the shoot elongates. In a bud like this one can
confirm the observation of Church, that orthostichies do not exist. Were
they here, they would appear as radial rows made by every fifth, or

Symmetry 155

eighth, or thirteenth primordium. These are not to be seen. Furthermore,
if one carefully studies the angular divergence between successive pri-
mordia he finds (in the great majority of cases) that it is close to the
"ideal" Fibonacci angle of 137.5° which the series of phyllotactic fractions
approaches as a limit.

The number of clockwise and of counterclockwise parastichies in a
given axis is not the same. In different types, however, their relative num-
bers are fixed and specific. These also fall into a characteristic series. Thus
in the bud section shown in Fig. 7-3 one can count five parastichies turn-

Fig. 7-3. Cross section of apical bud of Pinus pinea showing absence of orthostichies.
The primordia, numbered in succession, are separated by the Fibonacci angle. Five
counterclockwise parastichies and eight clockwise ones are evident. (From R. Snow,
courtesy of Endeavour. )

ing to the left and eight to the right. In simpler forms there may be three
in one direction and five in the other. In more complex cases, such as
many pine cones, there are 8 of one and 13 of the other, or 13 of one and
21 of the other. Some systems have 21 and 34. Most sunflower heads show
34 spirals in one direction and 55 in the other. Arranging these pairs of
numbers in the form of fractions, as was done with the genetic spiral, one
obtains the series %, %, %, 8/13, 13/2i, 21/34, 3%5, 5%9, and so on, though
the higher fractions are rare. The numbers in numerators and denomi-
nators form a series, as in the genetic spiral, but here the denominator of
one fraction forms the numerator of the next one instead of the next but

156 The Phenomena of Morphogenesis

one. The fraction which this series approaches as a limit is 0.61803, the
larger one of the two which are separated by the golden mean. This frac-
tion is thus the difference between 1.0 and 0.38197, the limit approached
by the other series. The two spiral systems are evidently related but just
how they are is a nice mathematical problem. It is no wonder, as D'Arcy
Thompson says, that these various relationships have long appealed to
mystics and to those who seek to square the circle or penetrate the secrets
of the Great Pyramid!

Parastichies are present in shoots around which leaves are borne in a
phyllotactic spiral, but because they are pulled out so far lengthwise
they are much less conspicuous than when many structures are packed
together. In elongate shoots orthostichies, though absent in buds, can
usually be demonstrated. The tensions resulting from elongation ap-
parently operate to straighten out the spirals and in many cases to bring
the insertion of a leaf almost directly over one that is three or five or
eight leaves below. Not much of a twist is needed to accomplish this and
to produce an orthostichy. One should recognize, however, that such are
secondary rather than primary phenomena of symmetry.

The problems of phyllotaxy were already involved enough when a
French botanist, Lucien Plantefol (1948), added a further complexity.
His theory has been extensively developed by others, particularly in his
own country. It is based on a study of the insertion of the leaf traces on
the stem. Plantefol does not regard the genetic spiral as significant. He
traces two (sometimes more) foliar helices connecting the leaf bases in
parallel spirals that wind up the stem, and he usually represents these
helices as projected on a plane where their relationships can more easily
be seen (Fig. 7-4). They originate in the traces of the two cotyledons,
and the series remain distinct as they pass up into the bud. Here they
terminate in a generative center of embryonic tissue just below the tip
of the meristem ( Fig. 7-5 ) . In this the new primordia are differentiated.
The position of each is determined, he believes, by stimulation from the
foliar helices below, the relations being harmonized by an "organizer."
Lance (1952) found in a number of cases a zone of abundant mitoses
somewhat below the apex of the meristematic dome but few at the very
tip. Crockett (1957) finds some evidence of the same thing in Nicotiaha.
Loiseau ( 1954 ) cut off the tip of the meristem in Impatiens and observed
that in many instances this resulted in changing the number of helices.
This he believes was due to a disturbance of the generative center.
Popham (1958), on the other hand, in a census of mitoses at the apex
of Chrysanthemum, found no evidence of a generative center nor of its
necessary corollary, a region of few mitoses at the very tip. Newman
(p. 60) made the same observation in living material. The problem has
been discussed by Wardlaw (1957b), who concludes that, although there

Symmetry 157

are various complexities in the shoot meristem, there is little good evi-
dence from this source in support of Plantefol's theory.

Although this theory has received strong support from a number of
French botanists, objections have been raised against it in other quarters.
What are chosen as foliar helices are evidently one of the parastichies or
spiral rows of leaf traces to be seen along the axis, but which of these is
the true helix in any instance seems difficult to determine. The leaves
on a helix must have some vascular connection with each other, accord-
ing to the theory, but in most stems at least two different parastichies
could be chosen which would fulfill this requirement. A figure in one

Fig. 7-4. Two foliar helices, the members of one connected
by dots and of the other by dashes, seen as though
the surface of the stem were removed and spread out.
(From Plantefol.)

en
i

Fig. 7-5. Diagram of shoot apex according to Plantefol's
hypothesis, showing the generative center and the ab-
sence of divisions at the very tip. Dots indicate mitoses.
( From Plantefol. )

of Dr. Esau's papers (1943, Fig. 1), though it was not drawn to clarify
the problems of phyllotaxy, makes these relationships evident (Fig.
7-6). This is a diagram of the primary vascular system of Linum. The
genetic spiral is shown, with the leaves numbered along it. In the series
25-33-41, the bundle is continuous with a branch that passes laterally to
the next in the series, and there are eight of these helices around the
stem. In the series 28-33-38, the right-hand lateral of one is continu-
ous with the left-hand lateral of the next, and there are five helices.
Members of the series 30-33-36 have no direct vascular connection with
one another but are in a definite row. Which of these spirals should be
chosen as the foliar helix? One might determine the true one, perhaps,

•^~-L.

~£9

• 37

Fig. 7-6. Diagram of the primary vascular strands in
the stem of Linum perenne. The numbers from 21
(above) to 49 (below) mark the positions of leaves in
the generative spiral, indicated by a thin line. The
bundles are shown by heavy lines for those on the
nearer surface and by dotted ones for those behind.
Various helices, in Plantefol's terminology, may be dis-
tinguished, such as 30-33-36, 28-33-38, and 25-33-41.
There seems no certain way to determine which are
the "true" ones. ( From Esau. )

—I

kffi

f"e\

X»-i-

mi.i

158

Symmetry 159

by tracing the system back to the cotyledonary node. Camefort (1956)
has presented a full account of Plantefol's theory and has endeavored to
reconcile it with the classical concepts of phyllotaxy and modern experi-
mental studies.

The solution of these problems of leaf arrangement is evidently to be
sought near the apical growing point where the leaf primordia actually
originate, for their relations here will determine those between mature
leaves on the elongated stem. This emphasis on the study of primordia
is a return to the point of view of Schwendener ( 1878 ) , who believed
that mechanical contact and pressure exerted by the primordia on one
another accounted for their distribution, and especially of Hofmeister
(1868), who proposed the general rule that a new primordium arises
in the largest space available to it. This conclusion is generally accepted,
but the developmental basis for it is not clear. The essential morpho-
genetic problem beneath all this is what determines the origin of a par-
ticular primordium at a particular place and time.

An early idea was that a leaf-forming stimulus passes along the genetic
spiral, but the significance of the spiral itself now seems rather slight.
Church (1920), concerning himself chiefly with parastichies, believed
that the point of intersection of the two major ones determined the point
of origin of a primordium. This leaves undetermined the reason for the
course of the parastichies themselves. Some workers are inclined to think
that stimuli from previously formed leaves or primordia determine the
position of new ones. Plantefol assumes that a foliar helix extends up-
ward into the meristem to the generative center where the primordia are
formed. Sterling ( 1945 ) finds that in Sequoia the procambial strands are
always continuous with the older ones below and differentiate acropetally,
pushing up into the apical meristem before the emergence of the pri-
mordia into which they will pass, and suggests that these procambial
strands may influence the position of the primordia. Gunckel and Wet-
more ( 1946 ) reach the same conclusion for Ginkgo. Opposed to this
idea is some experimental evidence, chiefly derived from isolating part
of the meristem from regions below it by incisions without disrupting
normal phyllotactic arrangement, a result which suggests that the stimu-
lus for the development of a primordium does not come from below.
Perhaps in such cases as this it is incorrect to assume that a given devel-
opment is the cause of another which succeeds it in time. A series of re-
lated structures and processes are part of the same organized whole and
should be thought of as developing together rather than each step as
inducing the one that follows it.

The problem of what determines the phyllotactic series is open to
experimental attack, and much work has been done on it by various
people, among them Wardlaw, Ball, and especially the Snows. They have

160 The Phenomena of Morphogenesis

been able to modify phyllotaxy operatively in a number of ways. Thus
in Epilobium hirsutum, a species in which the leaf arrangement is
decussate (opposite), the Snows (1935) split the apex diagonally and
found that the two regenerating shoots had spiral phyllotaxy. They were
also able ( 1937 ) to change the phyllotaxy in the same way by applying
auxin to the shoot apex. There may be a rather delicate balance between
decussate and spiral phyllotaxy in this plant, for in the group to which
it belongs (and even in a single plant of this species) both types may
occur. In other plants the direction of the phyllotactic spiral may be
reversed in regenerating shoots after splitting the apex.

What determines the location of a given primordium is the basic prob-
lem here, and as to this there are two major hypotheses. One, first pro-
posed by Schoute (1913), assumes that the presence of a primordium
tends to inhibit the development of another one near it, presumably by
the sort of inhibition by which one bud checks the growth of another
through the agency of auxin. This is the same problem studied more
recently by Biinning (p. 199), who has evidence that each stoma produces
a substance that prevents the development of another stoma close to it,
thus accounting for the regular spacing of these structures. Such a hy-
pothesis is in harmony with physiological theory, but some experimental
results seem to be opposed to it. For example, the Snows (1952) re-
moved the youngest actual primordium in an apex of Lupinus and after
14 days determined the positions of the next three successive primordia
that had appeared since this was done. In every case these later ones
occupied the places in which they normally would have appeared, in-
dicating that their positions in the series had not been affected by removal
of a primordium and any inhibitory influence from it.

That the primordia develop independently of either stimulatory or in-
hibitory influences from neighboring ones is also shown by an experi-
ment of Wardlaw's in which he isolated by radial cuts the areas pre-
sumably to be occupied by the next primordia in the series, thus effec-
tively isolating them from physiological contact with primordia already
formed. He found that these areas developed primordia normally.

Other factors than chemical ones may here be involved. Wardlaw
( 1948 ) finds that each primordium tends to produce a region of tangential
tensile stress around it but that this is absent in the area where new
primordia are to arise. He suggests that a primordium will develop where
tensile stress is at a minimum.

The second hypothesis assumes that a primordium will not develop
unless there is sufficient available free space for it. This is related to the
ideas of Schwendener and Hofmeister and really comes down to the
problem of the most efficient filling of the space on the surface of the
meristem. It has been supported, in essence, by van Iterson (1907), and

Symmetry 161

in recent years the Snows have brought forward evidence in its favor.
Among other experiments ( 1952 ) they isolated by two radial cuts the
larger part, but not the whole, of the area presumptively to be occupied
by the next-but-one leaf primordium. In such a case none develops be-
tween the cuts, although this region grows and continues otherwise to
be normal. They explain this result as due to the fact that the area now
available was too small for a primordium to be formed.

These two hypotheses, though stressing different factors, are not dia-
metrically opposed to each other. What is to be explained is the even
distribution of primordia, equidistant from each other (in origin) and
regularly arranged. This is the same problem posed by the distribution
of multiple structures. Something regulates the differentiation of each of
these structures in such a way that each occupies an area of its own and
that these individual areas are of about the same size. In the case of
leaf primordia the situation is complicated by the fact that these arise
on a curved surface and in a progressive series in time. Although me-
chanical and chemical factors are doubtless involved in the distribution
of primordia, as in all morphogenetic processes, it is perhaps too
simple an explanation to regard the determination of each as due to
crowding by its neighbors, to the presence of the "first available space,"
or to inhibition by other primordia. It seems more logical to regard the
problem of the distribution of primordia at the growing point as another
instance of a self-regulating biological pattern which may have its roots
in genetic factors, the fine structure of protoplasm, or whatever else may
be responsible for organic form.

On either hypothesis mentioned above, if primordia are to arise in a
spiral around the axis each should be as far as possible from its immediate
neighbors, those coming just before and just after it in origin. In op-
posite leaves each is placed as far away as possible, 180°. In spiral
phyllotaxy this cannot be done. If primordium B, let us say, originates
at an angle from A of 137.5° (the golden-mean fraction of the circum-
ference), and if the next one, C, is placed at the same distance farther
on (thus incidentally dividing the remainder of the circumference by
the same ideal proportion), B is equidistant from A and C, and this is
the maximum possible distance at which successive members can be
placed from each other. If the distance A-B and B-C is less or greater
than this ideal angle, C will not arise in the middle of the largest space
available, as Hofmeister's postulate requires. What this means is that
only if successive primordia are separated by this ideal angle will they fill
the available space evenly and with the greatest economy. This is the
property of golden-mean spacing that makes it significant in problems
of this sort.

Richards (1948, 1950) has worked out some of the implications of

162 The Phenomena of Morphogenesis

this fact and has returned to methods of mathematical analysis in ap-
proaching the problem of the development of the primordia at the meri-
stem. He emphasizes the importance of the plastochron ratio, the ratio of
the radial distances from the center of the meristem to two consecutive
primordia. Where this distance increases considerably in each plasto-

Fig. 7-7. Diagram showing a spiral succession of points, each separated from the next
by the Fibonacci angle, or about 137.5°. Parastichies can be recognized by intersec-
tions of approximately 90° between them. At the center there are five counterclock-
wise ones and eight clockwise. The counterclockwise series soon shift from 5 to 13,
and later the clockwise ones from 8 to 21. (From F. J. Richards.)

chron, both the genetic spiral and the spirals of the parastichies will open
out rapidly. The meristem itself under these conditions will tend to be
relatively steep, the primordia few and the parastichy numbers low. On
the contrary, when the radial distance increases but little from one
primordium to the next, the primordia are packed closely, the meristem

Symmetry 163

is likely to be flatter (as in a cone or flat head), the primordia will be
more numerous, and the parastichy fractions will have higher numbers.

Richards calls attention to the fact that the parastichies at a growing
point are not limited to the two conspicuous "contact" ones emphasized
by Church but that there may be a series of others though these are
not obvious since they do not intersect each other at right angles. An
advantage of this concept is that it makes clear how the parastichies shift
from one pair of numbers to another, a problem that has troubled stu-
dents of phyllotaxy. Richards (1948; Fig. 7-7) has constructed a diagram
of a rather large meristem, something like a sunflower head, showing a
series of primordial positions numbered along the genetic spiral in
which each diverges from the last by the Fibonacci angle of 137.5°. In
such a system one can readily trace parastichies. Near the center there
are five counterclockwise ones crossing eight clockwise, the % arrange-
ment, which intersect at approximately right angles. To trace this series
very far out becomes difficult since the angles of intersection diverge in-
creasingly from 90°. As one moves out, therefore, the system seems to
change and the five counterclockwise spirals shift to thirteen, giving the
%3 arrangements of spirals that now have more nearly right-angled
intersections. Still farther out the eight clockwise spirals are less easy
to trace, and 21 others become more conspicuous, now making the 1%i
arrangement and restoring the steeper intersections. Thus in the more
complex systems with large, flat meristems and little difference in radial
distance between successive primordia, the parastichies, at least those
that are conspicuous and easy to trace, may be seen to shift to pro-
gressively higher numbers. This does not happen in ordinary shoots
where the meristem is steeper and the primordia are fewer and larger
and increase rapidly in size at each plastochron but it may sometimes be
seen even in such cases (Fig. 7-8). These changes involve no biological
mystery, as Church was inclined to believe they do, but are simply the
result of the unique properties of the Fibonacci angle.

Barthelmess ( 1954 ) has pointed out that the scheme proposed by
Richards is essentially a two-dimensional one, whereas the meristematic
region has three dimensions, a fact that must be taken into account.
There are various other complications presented by an analysis of
phyllotactic patterns. Bilhuber (1933) and others, for example, find
that the situation in many of the cacti is often different from that in
most families. These plants are essentially leafless and have angled
stems so that in the apical regions one actually finds what look like
orthostichies, which are related to the development of the angled pat-
tern. Bijugate spirals (Hirmer, 1931; Snow, 1950) occur in some groups,
where a % pair of parastichies, for example, becomes split into a %0.
Here primordia occur in opposite pairs but the plane of each pair is not

164 The Phenomena of Morphogenesis

at right angles to the previous one. This produces two parallel spirals.
For a discussion of other recondite aspects of spiral phyllotaxy the reader
is referred to the work of Church, Hirmer, Richards, the Snows, and
others who have gone deeply into these problems.

Of some morphogenetic interest is the direction of the genetic spiral
itself. Observers generally agree that leaf positions around the stem are
as likely to be in a clockwise as in a counterclockwise spiral. Beal ( 1873 ) ,
studying cones of Norway spruce, found 224 cases of the former and
243 of the latter. Allard ( 1946 ) examined 23,507 tobacco plants and found
that the two types were almost exactly equal. Direction of spirality was
not inherited. How the direction is determined for a given plant is not
known, but it is probably in some critical early cell division. This neutral-
ity of the phyllotactic spiral is unlike the behavior of climbing plants,

Fig. 7-8. Diagram of distribution of pri-
mordia at the shoot apex, each diverging
from its predecessor by the Fibonacci
angle. As the primordia increase in size,
the recognizable contact parastichies shift
from 5 + 8 near the center to 8 + 13
farther out. ( From Barthelmess. )

in almost all of which a given species climbs in either a clockwise or a
counterclockwise manner exclusively.

The difference in direction of the phyllotactic spiral, however, some-
times alters from one part of the plant to another in conformity to a
general pattern of symmetry, much as in the case of floral structures
(p. 167). In shoot growth of Citrus, for example, Schroeder (1953a) re-
ports that there are successive "flushes" with a dormant period between
them and that a regular alternation occurs between right and left
spirality in successive shoots. Secondary shoots have spirality opposite
from their parent one. Thorns develop to the left of the petiole in left-
handed shoots and to the right in right-handed ones. The direction of
spirality in axillary shoots of View also takes place in a precise and
alternating order which depends on their position (Dormer, 1954).

Spirality. Spiral phyllotaxy involves a number of problems as to the
spacing and relative position of leaves which are not present in decus-

Symmetry 165

sate (opposite-leaved) phyllotaxy. In the latter type the two primordia
at a node are as far apart as they can be, and the position of each suc-
cessive pair is at right angles to the pairs above and below. This more
nearly fulfills the requirements for efficient spacing and maximum
divergence than does the spiral arrangement. One therefore wonders
why the latter is so much more common, particularly since the cotyledons
and sometimes the first foliage leaves are opposite. The transformation
of an opposite to a spiral phyllotaxy involves a radical rearrangement of
the meristematic region. This seems to be an expression of an inherent
tendency toward spirality which is evident in so many places in the
structure and activity of plants and their parts. This inherent spirality,
imposed on systems of different sizes and forms may, from the mere
geometrical necessities of the case, result in the various systems of
spiral phyllotaxy that we have been discussing. Physiological factors
doubtless have an important role here— auxin, mechanical pressure,
genetic determination of growth, and others— but the underlying spirality
seems to be a phenomenon fundamental to all organisms. This may
appear to be an oversimplification of a problem that has involved more
diverse hypotheses than almost any other in plant morphology. If it proves
possible, however, thus to get at the heart of this mass of facts and
pick out one that underlies them all, we shall have come closer to an
understanding of one aspect, at least, of the phenomenon of organic
symmetry.

Spirality seems to be deeply seated in living stuff. It is evident in the
spiral movements (nutations) seen in the growth of roots and shoots,
particularly when this is speeded up by time-lapse photography. Tendrils
coil spirally. Protoplasm streams in a spiral course. Molecules of DNA
are spiral. Spiral threads (cytonemata) occur in cytoplasm (Strugger,
1957). Spiral grain has been found almost invariably in tree trunks
(Northcott, 1957). In protoxylem the wall markings are in spirals, save
in the earliest cells, and there are spiral markings in many other xylem
cells. Whether these are all due to the same basic cause may perhaps be
doubted, but one can find spirality almost everywhere in the plant
body.

The simplest place to study it is in the cell itself and especially in
the ceil wall. Much now is known about the submicroscopic structure of
this wall and of the system of microfibrils that compose it (Preston,
1952; Frey-Wyssling, 1953). The sporangiophore of the fungus Phycomy-
ces is favorable material for this sort of work since, as it elongates, it
twists spirally, as can be shown by following the course of marks placed
on the cell surface (Castle, 1942). Spirality here seems to have its basis
in the minute structure of the wall. Heyn (1939) believes that it is due
to the fact that the chitin molecules which form the framework of the

166 The Phenomena of Morphogenesis

cell take up positions at angles of 13.5 or 27° from the long axis of the
organ, these angles resulting from the character of the chitin molecule.
Denham (1922) observed that in the cotton hair, at least, the spiral
markings and striations on the wall coincide with the spiral path of the
streaming nucleus and cytoplasm. Preston ( 1948 ) compares the growth of
this cell to the pulling out of a flat, spiral spring which rotates as it ex-
tends, and he has suggested an explanation for this in mechanical terms;
but Castle ( 1936 ) thinks that this does not determine the structure of the
growing wall, though it may produce a spiral layering where the wall is
not elongating. He points out that not only the structure of the wall but
its elastic properties must be taken into account and believes (1953)
that, although the growth of the wall is helical, its course is not absolutely
fixed by its structure, since the angle of spiral growth can be reversed by
a change of temperature. Frey-Wyssling ( 1954 ) calls attention to the fact
that in certain polypeptid chains the divergence angles between the
amino acid residues show the same regularities as are found in the
Schimper-Braun phyllotactic spiral and suggests that the same geometric
cause— the necessity for most efficient packing— may underlie both.

Green ( 1954 ) studied the growth of the long cells of Nitella which had
been marked and found that these marks, as well as the two natural
striations in the cell, showed a uniform dextral twist. Its regularity is
maintained by growth processes evenly distributed through the whole
cell and presumably resulting from changes in the fine structure of the
cell wall.

The spiral grain found in the wood of many trees is another manifesta-
tion of spirality. This may be very conspicuous in some cases and seems
to be most common in trees growing in exposed situations or under
unfavorable conditions. The spiral may be right-handed or left-handed.
This subject has been reviewed by Champion ( 1925 ) . Preston ( 1949 ) ,
using the data of Misra (1939), attempted to relate spiral grain to the
spiral growth of single cambium initials and assumes that these twist or
roll spirally. This would involve some slipping of cells past each other.
From what is known of intercellular relationships, it is rather unlikely
that such a change occurs. The essential fact in most cases of spiral grain
is that vertical files of cells become tilted slightly to the right or to the
left and that this results in a spiral course for the cells of the wood. Some
slipping of the cells may be involved, but this might be accomplished
by localized intrusive growth (p. 82) such as has been shown to take place
at the tips of the cambial initials. The tilt seems to be related to a change
in cell polarity. Neeff (p. 128) found that when a new polar axis was
established the cambial cells gradually changed their direction until this
became parallel to the new axis. That there may be a spiral polarity in
the trunk itself is suggested by the work of Misra (1943), who reports

Symmetry 167

that where there is eccentricity in the woody axis the position of maxi-
mum thickness in any eccentric ring follows a spiral course along the
length of the axis. There is also a relation between this eccentricity and
spiral grain, for the degree of both decreases upward in the trunk,
and the direction of the spiral eccentricity (left or right) is the same as
that of the spiral grain in any given axis.

Priestley (1945) distinguishes between true spiral grain, characteristic
of hardwoods and resulting from a twist in the primary cambium cylin-
der, and tilted grain, characteristic of softwoods where the grain is al-
ways straight in the wood of the first year.

In Flowers and Inflorescences. Angiosperm flowers are apparently to
be regarded, in an evolutionary sense, as shortened axes; and their parts,
particularly the calyx and corolla, often show evidence of the same sort
of spiral symmetry that exists between leaves. This can rarely be shown
by the actual insertion of the parts, since they are at essentially the same
level and might be regarded as a whorl, but is evident in the relation of
their expanded portions to one another, particularly as visible in the bud.
In flowers of dicotyledons there are usually in each circle five parts or a
multiple of five. A very common relationship here (in the calyx, for ex-
ample) is that two of the sepals have both edges outside the others, two
have both edges inside, and one has one edge outside and one inside.
This quincuncial arrangement can be interpreted through developmental
evidence as a % spiral, since the parts appear in the same order as
leaves in % phyllotaxy. Various modifications of this are found, but the
typical dicotyledonous flower may be regarded in its symmetry as rep-
resenting a % spiral. The flower of monocotyledons, on the other hand,
has its parts typically in threes and may be regarded as a % spiral in
symmetry. The problem of flower symmetry, particularly as expressed
in transverse diagrams, has been the object of long study by floral
morphologists and forms the basis of an extensive early literature (Eich-
ler, 1875).

For students of morphogenesis the symmetry displayed by inflo-
rescences provides a notable example of the orderly control of growth
relationships. Matzke (1929) has described a particularly fine example
of such symmetry in Stelloria aquatica (Fig. 7-9). Here the inflorescence
is a cyme, and the first flower terminates the main axis. Just below this
flower arise two buds in the axils of opposite bracts, and from these buds
shoots arise, each of which is likewise terminated by a flower. Below
each of these flowers, in turn, two shoots again arise, and so on. The
flower in this species shows quincuncial arrangement of the sepals. These
sepals may show a clockwise spiral or a counterclockwise one. As an
observer looks down on a diagram of such an inflorescence, it is evident
that, of the two flowers below the first, one is clockwise and the other

2,

bO £ 'O

S^

Q a

^E^

Symmetry 169

counterclockwise and that this holds for each succeeding pair. This rela-
tionship is not a random one, for the two types show a regular order as
one progresses to successively later pairs so that the symmetry of each
flower is predictable. Furthermore, the relative position in each flower
of the "odd" sepal also changes with complete regularity. In one member
of a given pair of flowers it has rotated 72° in a clockwise direction from
the single flower next them, and in the other, 72° counterclockwise. The
particular edge of the sepal which is inside also has a definite and pre-
dictable position. The whole inflorescence is thus a complex pattern of
symmetries, each successive floral meristem fitting precisely into its place
in this pattern. The factors that determine the symmetry of each flower
are therefore not purely local ones but operate as members of a much
larger system. Such a system, with its parts so widely separated and so
easy of observation, offers a particularly good opportunity for the ex-
perimental study of symmetry.

BILATERAL SYMMETRY

This is a relatively rare type in which there are two planes of sym-
metry, so that front and back, and right and left sides, are similar. A
bilaterally symmetrical organ resembles a radial one that has been com-
pressed equally on two opposite sides.

This type occurs chiefly in vertically oriented structures in which, from
one cause or another, one of the dimensions is smaller. Thus the stems
of certain cacti such as Opuntia are bilaterally symmetrical, as are the
still further flattened phylloclads of Muehlenbeckia and Phyllocladus.
These have doubtless arisen from radial types. The leaves of Iris and
similar plants are essentially bilateral but have probably come from
dorsiventral structures. All plants, such as the grasses and some other
monocotyledons, which are truly distichous (the leaves arising only on
two opposite sides of the stem) may be regarded as bilaterally sym-
metrical. So may the flowers of the mustard family, Cruciferae, since two
of the six stamens, directly opposite each other, are short and the other
four long. A few of the simpler bryophytes have distichous leaves or
leaf-like structures, as in Schizostegia, and are thus bilateral, as is the
pinnate plant body of the coenocytic alga Bryopsis. The thallus of some
of the larger algae, notably forms like Fucus and Laminaria, is flattened
and shows this type of symmetry.

In a few cases, as in some of the algae, a transition from radial to
bilateral symmetry may be seen, and in Schizostegia the apex is radial.
Doubtless in many instances one type could be induced from the other
experimentally. Certain abnormal structures, such as many fasciated
stems, are bilaterally symmetrical.

170 The Phenomena of Morphogenesis

DORSIVENTRAL SYMMETRY

In this type there is only one plane of symmetry, which extends
vertically through one dimension of the structure. The two sides are
alike but the front and back (or top and bottom) are not, thus distin-
guishing it from bilateral symmetry. It is characteristic of structures grow-
ing under an environment which is asymmetrical, as in the case of hori-
zontal ones, of those exposed to light on one side only, and of those
growing attached to some substratum. Among plants, creeping stems,
rhizomes, most leaves, many thalli, a wide variety of flowers, and, in
general, those structures which are not vertically oriented often show
dorsiventral symmetry.

Dorsiventrality in plants is manifest in external form, in internal struc-
ture, and in physiological behavior. Single cells and coenocytes may
show such symmetry. Dorsiventrality may be genetically determined and
thus appear under various environments, or it may be directly induced
by environmental factors. Thus a dorsiventral structure may sometimes
become radial, and vice versa. In some cases the plant body may actu-
ally alternate between radial and dorsiventral symmetry, as in Mnium
undulatum and Cladonia verticillaris.

Cases of dorsiventrality which are most obvious and easy to study are
those in structures that are typically horizontal, either because they are
weak and rest on the ground or because they are plagiotropic and tend
to grow in a horizontal position.

In Thalli. Among lower plants many thalli are dorsiventral. The
coenocytic plant body of the alga Caulerpa is typically horizontal and
on its lower surface bears "rootlets" and on. its upper surface, "leaves."
The familiar heart-shaped prothallus of a fern is similarly dorsiventral,
bearing sex organs and rhizoids on its lower surface only. This type of
symmetry is characteristic of the plant body of many liverworts, both of
the thalloid and the leafy types ( Halbsguth, 1953 ) . The factors which in-
duce it in such plants have been studied by various workers (Fitting,
1935, 1950; Pfeffer, 1871; Bussmann, 1939; and others, p. 355). Fitting
studied especially the gemmae of liverworts. These are roundish, notched
plates of cells the dorsiventral orientation of which is determined by the
balance between light, gravity, and stimuli from the substrate, acting on
preformed meristems in the notch. Fern prothallia exposed to an en-
vironment without gradients ( shaken or on a turntable, p. 137 ) lose their
symmetry as well as their polarity.

In Roots. Dorsiventrality is much less evident in roots than in stems.
Indeed, horizontally growing subterranean roots show little or no
change from radial symmetry either externally or internally. A few forms,

Symmetry 171

such as Isoetes, have roots that are not radial. In a number of orchids,
the air roots are dorsiventral in symmetry ( Janczewski, 1885; Goebel,
1915). This is especially conspicuous where the root is in contact with
a substrate (Bloch, 1935a).

In Shoots. Horizontally growing stems and branches are often con-
spicuously dorsiventral. Notable examples of this are found among the
conifers where the lateral shoots tend to branch in a single plane and
thus form flat sprays (amphitrophy). This form may become so firmly
fixed that it persists even in cuttings (p. 189). In some species of Ly co-
podium and especially Selaginella, these flattened branch systems look
almost like much dissected compound leaves. Indeed, there is evidence
that the large pinnately compound leaves of ferns may have evolved
from such branch systems. In many horizontal shoots the leaves are
usually horizontal in orientation and confined to the two sides. This may
result from a torsion of the petioles which are actually inserted on the
stem in a spiral or decussate fashion or, more rarely, from an actual
modification of the phyllotaxy.

Aside from this tendency to form flattened systems of leaves and
branches, the dorsiventral character of shoots is also conspicuous in the
dissimilarity of the leaves borne on the two sides. Such differences, to
which Wiesner gave the term anisophylly (1895), are common in
many plants and have been much discussed (Figdor, 1909; Goebel,
1928).

Anisophylly is often induced by external factors, notably gravity and
light. It is particularly conspicuous in woody plants with opposite, decus-
sate leaves. In horizontal shoots of maple, for example, the upper mem-
ber of a vertically oriented pair is much smaller than the lower; and in
a horizontally oriented pair the upper half is smaller than the lower
(Fig. 7-10). Experiment shows that in many cases if shoots which would
normally be vertical are held in a horizontal position as they grow
from winter buds they become anisophyllous. In horizontal branches
twisted through 180° before their buds open, the new shoots show
reversed anisophylly, the lower leaves (originally on the upper side)
now becoming the larger.

Anisophylly of this sort is present in certain species of Lycopodium
(such as the common ground pine, L. complanatum), where the creep-
ing rootstock is radially symmetrical but the ultimate branches flattened
and dorsiventral (though they are radial if grown in darkness, Fig. 7-11).
These branches have four rows of leaves, one on the upper side, one
much smaller on the lower, and two lateral ones, the lateral leaves being
the largest. Transitions from radial to dorsiventral symmetry are com-
mon, and the differences between the two are clearly due to environ-
mental factors. In conifers such as Thuja the ultimate branches are

172 The Phenomena of Morphogenesis

dorsiventral and anisophyllous and much resemble those of Lycopodium
(all tending to grow horizontally).

There are other plants in which the occurrence of anisophylly seems
much less directly dependent upon environmental factors and occurs
throughout the plant. This "habitual" anisophylly, as Goebel calls it, is
probably to be interpreted as a genetic tendency to develop in this way

vu

Fig. 7-10. Diagram of a horizontally grown branch of maple, showing anisophylly.
The vertically oriented pair of leaves (VU, VL) differ greatly in size but are sym-
metrical. In the horizontally oriented pair (HL, HR), the lower half of each leaf is
larger than the upper. ( From Sinnott. )

under such a wide range of environments that it has become essentially
an inherited trait. In many foliose liverworts, for example, the axis has
three rows of leaves, two of them lateral and the third, the much
reduced amphigastria, borne on the under side. Most species of Sela-
ginella have four rows of leaves: two lateral and relatively large and the
other two on the upper surface between these and somewhat smaller.

Symmetry 173

Among some families of angiosperms this same genetic or habitual
anisophylly occurs. Thus in Pellionia ( Urticaceae ) , in Centradenia
( Melastomaceae, Fig. 7-12), and in Columnea ( Gesneriaceae ) one mem-
ber of each pair is a large typical foliage leaf but the other, directly
opposite it, is a small bract-like structure. These differences are ap-
parently unrelated to environmental conditions. It is noteworthy, how-

Fig. 7-11. Dorsiventral (flat) shoot of
LycQpodium. At right is a branch grown
in the dark, which is radially symmetri-
cal. ( From Goebel. )

Fig. 7-12. Anisophylly in CeftfrL'denia.
Leaves are opposite but one member of
each pair is much larger than the other.
Only the larger ones have axillary shoots.
( From Goebel. )

ever, that this anisophylly is most extreme in horizontal shoots of such
plants and is much reduced in those which grow more nearly vertically.
On flattened plagiotropic shoot systems there are often changes in the
pattern of symmetry that are more complex than anisophylly. In such
shoots, for example, many leaves are asymmetric, but in a regular and
predictable fashion (Fig. 7-13). Thus in horizontal branches of elm and
linden, the inner half of the leaf, directed toward the apex of the shoot,

174 The Phenomena of Morphogenesis

is larger than the outer, and its blade often reaches farther down the
midrib. In the beech, on the other hand, it is the outer part of the leaf
which is the larger. Many cases of leaf asymmetry, notably the conspicu-
ous examples in species of Begonia, are related to the position of the
leaf on the stem, although here the stem is often short and inconspicuous.
Somewhat similar expressions of apparent asymmetry are evident in
the branch pattern of plagiotropic shoots. In some cases, the branches
which arise on lateral shoots are larger on the inside, toward the apex
of the shoot, as in flat stems of Thuja. More commonly those on the out-
side, away from the axis, are larger, a phenomenon which Wiesner
(1892a, 1895) has called exotrophy and which he explains as due to nu-
tritional causes. Leaves on the outside of lateral shoots are often larger
than those on the inside, a special type of anisophylly.

Fig. 7-13. Anisophylly in Goldfussia. Diagram, of shoot from above. The leaves are
opposite but the pairs are somewhat displaced. One member of each pair is larger
than the other, and one side 'of each leaf is larger than the other side. In the axillary
shoot, position with reference to the symmetry of the whole determines leaf size.
( From Goebel. )

All such structures, which in a strict sense are asymmetric, are really
complex patterns of symmetry induced when a fundamentally radial
system becomes dorsiventral. What the factors are— whether nutritional,
hormonal, or other— which determine these differences is not known. This
is evidently the point where the relatively simple phenomenon of sym-
metry merges into the more complex one of organic pattern in general.
In flat, dorsiventral shoots, which are essentially structures in two di-
mensions only, there is an excellent opportunity to analyze the problem
of pattern in one of its simplest expressions.

The external dorsiventrality of stems is often accompanied by dorsi-
ventrality of internal structure. Where the stem is flattened, the vascular
cylinder is likely to be so as well. Sometimes the symmetry changes do

Symmetry 175

not involve the whole cylinder. In the horizontal rhizome of Pteridium,
for example, the outer ring of bundles is essentially circular in section,
but the group of medullary bundles tend to be flattened dorsiventrally.
In Selaginella the few bundles which form the vascular system also tend
to be flattened in the same way. This flattening may even persist in those
orthotropous shoots which have become radially symmetrical externally.

Examples of internal asymmetry in the stems of seed plants are found
in the horizontally growing branches of woody plants. Here the branch
itself is not flattened but its internal structure is excentric, the pith oc-
cupying a position some distance above the geometrical center of the
branch in gymnosperms and below it in angiosperms. The nearer the
branch approaches a vertical orientation, the less this excentricity is. There
has been much discussion of the factors responsible for this internal
dorsiventrality (p. 356). The problem is far from a simple one and seems
to be involved with the specific pattern of branching characteristic of
the plant.

In Leaves. All leaves are typically dorsiventral structures, but those
of pteridophytes and seed plants are most characteristically so. A leaf,
to perform its usual functions satisfactorily, must be relatively broad and
thin and oriented with its major surface at right angles to incident light.

Dorsiventrality of leaves is especially evident in their histological
structure. The stomata and spongy tissue tend to be confined to the lower
part of the leaf, with the palisade layer and a continuous epidermis on
the upper. Some vertically oriented leaves such as those of Iris are equi-
facial and show no dorsiventrality, either external or internal. Others, such
as those of certain rushes, may actually be tubular and essentially radial
in their symmetry.

The dorsiventrality of leaves in the higher vascular plants, however,
is inherent in something more fundamental than the orientation of the
blade. The vascular supply for each leaf is a segment, or group of seg-
ments, of the primary vascular ring with phloem outside and xylem in-
side. When this passes outward into the leaf as the leaf trace and finally
becomes the vein system, the phloem therefore tends to be on the lower
surface and the xylem on the upper, a characteristic dorsiventral orienta-
tion from the first. Even the leaf primordia become dorsiventral very
early. There is evidence, however, that this is the result of induction
from the meristematic apex, for if a region where a primordium is to
form is isolated from the apex by an incision, the structure that emerges
may be radially symmetrical (Sussex, 1955).

In Flowers. Floral structure provides many examples of dorsiventrality.
The presumably primitive types of flowers are radially symmetrical, or
actinomorphic (regular). In many families, however, such as the papi-
lionaceous legumes, the figworts, the orchids, and others, especially those

176 The Phenomena of Morphogenesis

in which the flowers are borne laterally on an inflorescence, this radial
symmetry has become dorsiventral and the flower is said to be zygomor-
phic (irregular; Fig. 7-14). The pea flower, with its standard, two wings,
and keel is a familiar example, and the median plane of symmetry here
is especially well marked. Flowers of this sort provide many of the
notable adaptations for insect pollination. In most cases zygomorphy is

Fig. 7-14. Dorsiventrally symmetrical ( zygomorphic ) flower of Linaria vulgaris.
( Courtesy of Rutherford Piatt. )

evident from the beginning of development and is unaffected by the rela-
tion of the flower to gravity or other environmental factors. In other
cases (such as Epilobium, Friesia, and Digitalis), if the flower develops
in a vertical orientation or on a clinostat, it becomes radial, indicating
that dorsiventrality here is directly affected by gravity (Fig. 7-15). In
cases of peloria (p. 282) the flower of a species which is normally zygomor-
phic (as in Linaria or Digitalis) may become radially symmetrical. Most

Symmetry 177

zygomorphic flowers are geotropic and will assume a definite position
with relation to gravity.

In some cases certain flowers of an inflorescence are dorsiventral and
others radial. This is true of the ray florets of Compositae and of certain
Umbelliferae, where that part of the corolla directed toward the outside
of the head is much larger than that directed toward its center. In such
cases the entire inflorescence shows a radial symmetry. Here, again, the

Fig. 7-15. Flower of Asphodelus.
Below, under normal conditions.
Above, after developing on a
clinostat. (From Vdchting.)

whole pattern is symmetrical though certain of its elements are by them-
selves asymmetric. The situation may be still more complex. In some
Compositae there are as many as five types of fruits, as to size and shape,
formed on the head but showing symmetrical distribution (Pomplitz,
1956).

Most inflorescences (like that described for Stellaria, p. 167) are radially
symmetrical, but some are definitely dorsiventral. A familiar example of
this is the heliotrope and its allies, where the flower cluster is one-sided

178 The Phenomena of Morphogenesis

and constitutes a scorpioid cyme. The vetches and some other legumes
are less extreme cases, and there are many others. The flowers of such
dorsiventral inflorescences may themselves be radially symmetrical.

Physiological Dorsiventrality. Dorsiventrality is manifest in physio-
logical activity as well as in structure, though usually not so obviously.
Plagiotropic roots, shoots, and other organs assume this position presum-
ably because of specific distribution of growth substances in the growing
tip such that the pull of gravity is counteracted and growth maintains
either a horizontal course or one at a given angle to a vertical axis. In
cases where the first division of a cell sets apart two different daughter
cells, as in the first division of the egg of Fucus, there is clearly a physio-
logical difference between the upper and lower halves. Indeed, the dif-
ferentiation of root and shoot in the embryonic axis, with the radical
differences in activity of these two poles, may be looked upon as an
example of physiological (and morphological) dorsiventrality.

In leaves of certain water plants, externally alike on both surfaces,
Arens ( 1933 ) has presented evidence that the physiological activities at
the two surfaces are unlike, materials from the environment entering
through the lower surface and waste products (chiefly carbon dioxide)
being given off from the upper. What the mechanism of such physio-
logical dorsiventrality may be is not known, but bioelectrical differences
(p. 361 ) are perhaps involved.

DEVELOPMENT OF SYMMETRY

The causes of organic symmetry are not well known, but in endeavoring
to find them it is first necessary to determine how these relations actually
arise in the process of development.

The Origin of Symmetry in Coenocytic and Colonial Systems. Sym-
metry is by no means confined to cellular structures. From the Plas-
modium of myxomycetes, formless and unsymmetrical, there arise spe-
cifically formed and radially symmetrical fruiting bodies of great variety.
Here the morphogenetic process may be seen in one of its simplest ex-
pressions, as the sporangium is molded from the plasmodial mass.

Even more remarkable are those slime molds belonging to the
Acrasiaceae (Dictijostelium and its allies, p. 223) where the vegetative
body is a single myxamoeba. At the end of the vegetative period thou-
sands of these come together into a pseudoplasmodium but do not fuse.
This colony, after some migration, settles down and develops into a
radially symmetrical stalked sorocarp.

More closely resembling the bodies of the higher plants but still with-
out cellular boundaries are the coenocytic members of the algae and
similar groups. Here there is no formless mass of protoplasm but, from

Symmetry 179

the beginning, an organized system which grows at the tips of these
branches that constitute the "rhizome," "leaves," and "roots." These sys-
tems are symmetrical, either radially as in Bryopsis, or dorsiventrally as in
Caulerpa. In all these cases the origin of symmetry obviously is not re-
lated to planes of cell division or to other aspects of a multicellular sys-
tem but is dependent upon the behavior of the entire protoplasmic sys-
tem.

Origin of Symmetry in Cellular Systems. In cellular plants, the origin
of symmetry can be traced more readily because it is expressed in the
division, growth, and relationships of cells at meristematic regions.

In simple colonial forms like Pediastrum there is a regular sequence
of cell divisions from which a symmetrical plate of cells arises. In manv
algae with an indeterminate thallus, growth is controlled bv a large
apical cell. The origin of branches and the whole pattern of symmetry
are determined here. In simple two-dimensional thalli, the apical ceil
cuts off a daughter cell, first on the right-hand side and then on the
left, to form the so-called pendular symmetry. In most leafy liverworts
and mosses there is a pyramidal apical cell with three faces, and from
each of these, in regular succession, a daughter cell is cut off. The origin
of leaves is related to these faces, and in the simplest cases there are three
rows of leaves produced directly by this apical cell.

In ferns and Equisetum, however, which also grow by a three-sided
apical cell, there is usually no relation whatever between the phyllotaxy
of the shoot and the configuration of this cell. In the seed plants there is
no single apical cell and no evident relation between the spiral pattern
of symmetry and any visible structures in the meristem. It seems clear that,
in all except the simplest plants, the origin of spiral symmetry is not re-
lated to cellular configuration at the meristematic region but must have
its basis in the entire embryonic mass.

Dorsiventral symmetry in most cases is not established at the meristem
itself but has its origin in changes which arise later. Almost all meristems
or terminal embryonic regions are radially symmetrical. Dorsiventrality
may arise from these in the process of normal development. This is some-
times due to the influence of external factors such as light or gravity. It
is sometimes the result of position in the general plant body, as when a
branch becomes dorsiventral in symmetry. It is sometimes associated with
particular stages in the life cycle. In plants that are dorsiventral through-
out the mature plant body the seedlings are usually radial. In Hedera, the
vegetative stage of the life cycle is dorsiventral but the flowering shoots
are radially symmetrical (p. 213). Such changes are evidently due to
alterations in the internal environment.

Such modifications of symmetry, particularly the change from the
radial to the dorsiventral type, involve not local regions but the entire

180 The Phenomena of Morphogenesis

pattern, which may be deformed much in the fashion that D'Arcy Thomp-
son has demonstrated (p. 424). This can be seen by comparing the dorsi-
ventral maple shoot in Fig. 7-10 with one growing vertically.

SYMMETRY AND FORM

An analysis like this emphasizes the close relationship that exists be-
tween symmetry and organic form in general. Such form results from the
symmetrical distribution of material around an axis in a specific pattern.
An important part of this pattern lies in its symmetry. As we have seen,
certain portions of the pattern (as the lateral leaves of the maple shoot
in Fig. 7-10) appear by themselves to be asymmetrical, but they never-
theless constitute a part of a larger pattern of symmetry which may be
modified in various ways. A second part of the pattern is polar axiation,
affecting the lengthenings or shortenings of the axis and the steepness of
gradients along it. A third is the tendency toward spirality already em-
phasized. Organic form results from the genetic and environmental
modification of these three developmental tendencies.

CHAPTER 8

Differentiation

At the beginning of its development the young plant, as it grows from a
fertilized egg or from some larger embryonic mass, is relatively simple
and homogeneous. A characteristic feature of the developmental process,
however, is the origin of differences in the amount, character, and loca-
tion of growth which lead to differences between the various parts of an
individual. Such structural or functional differentiation and its origin in
development constitute one of the chief problems of morphogenesis.

Differentiation is the manifestation of that "division of labor" which is
so conspicuous a characteristic of living things. Organs are differenti-
ated. Tissues in their development become unlike each other. Cells grow
very diverse in character. Even the contents of a single cell are divided
into nucleus and cytoplasm, and each of these possesses a considerable
diversity of its own. There is evidence that even the clearest cytoplasm
possesses submicroscopic differentiation. Strictly speaking, there is
probably no really undifferentiated structure in a plant. Protoplasm is
an organized system, not a homogeneous material, and this implies a
degree of physical and chemical diversity. Furthermore, because of the
dynamic quality of protoplasm, differentiation in living cells can never
be entirely stable but is subject to change under changing conditions.

Differentiation occurs wherever a true development is taking place and
may be expressed in many ways. At a terminal meristem like that of a typi-
cal shoot, the primordia of leaves, buds, and flowers early become dis-
tinguishable. From cambium cells, uniform in character, there differen-
tiate sieve tubes, fibers, tracheids, vessels, and other cell types. In the
primordium of a fruit, where growth is diffuse and determinate, internal
differences of many sorts begin to manifest themselves throughout the
mass. In regenerative development a single cell or group of cells may
dedifferentiate (p. 232) and become meristematic, and from this embryonic
center a new series of structures then differentiates. Many differences have
no visible expression in structure but involve physical, chemical, or
physiological distinctions only. During ontogeny the course of dif-

181

182 The Phenomena of Morphogenesis

ferentiation often changes, not only as to the structure of the parts de-
veloped but as to their reactivity and developmental potency.

An important aspect of the process of differentiation is that it seems
not to involve genetic diversity. The regeneration of an entire normal
plant is sometimes possible from a single cell, which may come from
almost any of the parts of the plant body, and from various tissues (p.
253), a fact which suggests that every cell of the plant is totipotent and
identical genetically with all the rest. This conclusion is supported by
the common observation that the number and character of the chromo-
somes, and thus presumably of the genes, are the same in all cells, save
for the occurrence of somatic polyploidy. Although the process of dif-
ferentiation is doubtless under genetic control, this cannot operate, as
Weismann and others once suggested, by a parceling out of genetic "de-
terminers" during development. The conclusion seems obvious that in
these processes that part of the cell must be involved which is not
identical everywhere in the body, namely, the cytoplasm. The origin of
structural diversity in the midst of genetic identity is the chief problem
that faces students of differentiation.

GROWTH AND DIFFERENTIATION

Although growth and differentiation usually proceed together, they
seem to be distinct processes, each more or less independent of the other.
Growth may occur without differentiation by a simple multiplicative
process, as in large parenchymatous masses such as the endosperm of a
seed, in the tissue of an amorphous gall, or in tissue culture. In the early
stages of many embryos, on the other hand, in the development of the
female gametophyte in certain lower vascular plants, and in similar cases
there is differentiation without growth. A notable example of this is fur-
nished by the Acrasiaceae, a family of slime molds (p. 223). Here the en-
tire vegetative growth occurs while the individuals are myxamoebae, and
the elaborate differentiation of the colonial sorocarp does not begin
until this vegetative phase is over. Animal embryology, particularly
in the early cleavage stages from large eggs, provides many similar
cases.

The independence of these two major developmental processes is
further emphasized by the fact that conditions which favor one tend to
be different from those which favor the other. In general, abundance of
water and available nitrogen tend to induce growth, whereas abundance
of accumulated carbohydrates, with less nitrogen and water, promotes
differentiation (Loomis, 1932). Red rays of the spectrum tend to pro-
mote growth and blue rays differentiation (p. 313). Under one photo-
period a given species will produce nothing but vegetative growth

Differentiation 183

whereas another photoperiod will stimulate the differentiation of re-
productive structures ( p. 315 ) .

When the cycle of differentiation is complete, growth usually ceases.
Thus, after the formation of reproductive organs in one of the higher
plants has begun, growth of the plant as a whole is reduced and finally
stops. When a fruit is fully differentiated, its growth in volume ceases,
though dry weight may continue to increase for some time. The two
processes of growth and differentiation may go on at different rates, and
therefore their relative rates are important in determining differences in
size. Where growth is relatively rapid, a large size will be attained before
the completion of the cycle of differentiation stops; where it is slow, the
cycle will be complete before much growth has occurred and the struc-
ture will be much smaller. This is well illustrated by the analyses of
inherited size differences in gourd fruits (p. 20). The balance between
these two major processes in development— the addition of new material
and its differential distribution— is of much significance.

The process of differentiation and the problems it presents may be ex-
amined from several different points of view.

1. Differentiation may be studied in plant structure, for it is here that
differences can most readily be seen. For purposes of convenience we
may distinguish between external differentiation, which involves the out-
ward structure and configuration of the plant, and internal differentiation,
which involves the cells and tissue systems of which the plant body is
composed.

2. Differentiation may be considered in its ontogenetic aspects. It is not
a static process, evident in mature structures alone, but often changes its
expression during development. Differentiation in a young plant is unlike
that in a mature one, and these changes proceed in an orderly cycle
of development both of the plant as a whole and of each of its com-
ponents. Such differences are not in structure alone but in the reactivity
and developmental potency of its parts.

3. What course differentiation will take is determined not only by the
genetic constitution of the plant but by the particular environment in
which development takes place. External factors of many sorts affect the
character of the structures which arise in the process of differentiation.

4. The ultimate basis of differentiation must be in physiological
changes in the living material itself. Most of these express themselves
sooner or later in visible structural diversity, but there are many cases in
which cells, structurally alike, can be shown to differ physically, chemi-
cally, or in physiological activity.

Examples of these four aspects of the process of differentiation, and the
problems they involve, will be considered in the present chapter.

184 The Phenomena of Morphogenesis

DIFFERENTIATION AS EXPRESSED IN STRUCTURE

External Differentiation

One of the most obvious examples of differentiation is that which
arises between the ends of a polar axis (p. 116). In all but the simplest
axes the structures that are developed at the two ends are quite unlike.
The most familiar instance is the differentiation of the shoot and root in
higher plants. These two systems are set apart very early, almost at the
beginning of embryonic development, and are fundamentally unlike in
structure, function, and method of growth. Roots frequently develop
from shoots but shoots less commonly from roots. Berger and Witkus
(1954) have reported that in Xanthisma texanum the cells of the root
always have four pairs of chromosomes but in those of the shoot, some
plants have four pairs and some have five. The two types of plants are
morphologically indistinguishable. How this difference in chromosome
number arises in development is not known, but it is present in young
seedlings.

Another conspicuous instance of differentiation in structure is that be-
tween the vegetative and reproductive phases of the life cycle. In its
early stages, the plant is becoming established. Its roots and leaves are
formed or its vegetative thallus developed, and its career as a food-pro-
ducing or food-acquiring organism is begun. Few plants, however, are
permanently vegetative. When a certain stage is reached, growth no
longer produces exclusively vegetative structures. Flower buds appear
at the meristem, or in lower plants reproductive organs of various sorts
begin to develop. These usually are formed as the result of internal
metabolic changes in the plant, such as the accumulation of carbohy-
drates or the production of specific substances. The onset of the reproduc-
tive phase, however, is often closely related, as to time and extent, with
certain environmental factors, notably light (p. 315). Short-day plants will
flower only when the daily period of illumination is relatively short, and
long-day ones only when it is longer. Some plants may never flower, and
others may do so when they have hardly begun to develop. The balance
between vegetation and reproduction may be tipped in various ways but
the potency for reproduction is always present in the genetic constitution.
This may not always be for sexual reproduction. In species which repro-
duce chiefly by vegetative means flowers may be present but fail to
function (as in the potato), may be much reduced (as in the banana),
or may even be quite absent. Reproduction of some sort obviously is
necessary, and the alternation of vegetative and reproductive phases,
each essential in the life of the plant, is an important manifestation of
differentiation.

Differentiation 185

The difference between these two types of structure begins at the
meristem and may often be recognized there by the presence of a large
number of axillary buds which are destined to be flower buds. The de-
velopment of the floral apex has been studied by many workers (p. 67).
A single flower is a modified axis, and its parts arise from primordia
which, although limited in number, are distributed in a precise pattern.
The differentiation between them takes place early and produces sepals,
petals, stamens, and carpels. The origin of these parts from particular
layers of the meristem has been worked out, through the aid of chimeras,
by Satina and Blakeslee ( p. 272 ) . In abnormal growth some floral organs
may be so modified that they resemble others, as in the conversion, partial
or complete, of petals to stamens or sepals to leaves (p. 277).

In many trees the differentiation of flower buds begins very early,
usually in the season before the flowers are borne. This is an important
matter for horticulturalists and has been extensively studied (Zeller,
1954, and others), since environmental conditions favoring flower pro-
duction must be provided early. Whether a tree will flower (and
fruit) well in a given season is often determined in June of the year
before.

Implicit in the process of reproduction is the differentiation between
the sexes. In plants with perfect flowers this is evident only in the dif-
ference between stamens and pistils. In monoecious plants, there are two
kinds of flowers on the same plant and in dioecious ones these are on dif-
ferent plants. The significance of such differences lies in the various
mechanisms that tend to accomplish pollination, in many cases cross-
pollination. A genetic basis has been found for some of these and is
doubtless present in others. Environmental factors of various sorts are
also operative here, notably nutrition and light. It is sometimes possible,
for example, to change a staminate into a pistillate plant by altering the
photoperiod (p. 317). The existence of sexual reproduction itself, in con-
trast with the much less precarious method of vegetative reproduction, is
based on the presumptive advantage of the higher variability that results
from the recombination of genetic potencies following svngamy and
meiosis.

Other traits are sometimes associated with the fundamental difference
between the sexes, as observed in Mercurialis annua (Basarman, 1946),
Valeriana dioica (Moewus, 1947), Urtica dioica, and Rumex acetosa
(Umrath, 1953; Fig. 8-1). In general, the female plants are larger and
are also different from the males in the size and shape of their leaves.

A conspicuous example of external differentiation, since it involves an
entire plant body, is that between the gametophyte and the sporophyte.
In many of the simpler plants the two generations are very much alike,
but they are markedly different in bryophytes and vascular plants. The

186 The Phenomena of Morphogenesis

advantage of this differentiation into sexual and nonsexual plants may
lie in the possibility of the extensive multiplication of the products of a
single sexual union. Among flowering plants, where mechanisms for
effecting fertilization are more efficient than in many lower ones, the
differentiation into two generations has almost disappeared.

A gametophyte, coming from a spore produced by meiosis, typically
has the haploid number of chromosomes, and the sporophyte has the
diploid number. Many haploid plants are now known, however, which
are undoubtedly sporophytes, and diploid gametophytes may readily
be produced. Chromosome number is evidently not the cause of the
difference between the two generations, but it is difficult to see why a
haploid spore and a haploid egg (or diploids in each case) should pro-

Fig. 8-1. Bryonia alba. Left, leaf from a shoot bearing male flowers; right, one from
a shoot bearing female flowers. ( From Umrath. )

duce two structures as unlike as the prothallus and the sporophyte of
a fern. The difference is probably attributable to the very different en-
vironments in which these two cells develop.

Origin of Differences. In most cases the origin of an organ or part is
first evident as a group of meristematic cells which, by growing more
rapidly in certain dimensions than in others, produces a definite form.
For an analysis of such specific differentiation, however, it is necessary
to determine how such a developing organ originates and the successive
steps by which it becomes distinct from others. Sometimes this is
relatively easy. In leptosporangiate ferns, for example, the sporangium
can be shown to arise from a single cell of the epidermis. In eusporangiate
forms, like some of the ferns and all higher plants, the sporangium

Differentiation 187

initial can be traced to a cell of the subepidermal layer. Analysis of
differentiation in terms of cell lineage can often be carried further.

The development of larger organs involves more than a single cell
lineage. It may be studied in the differentiation of lateral organs in the
apical regions of both root and shoot. From the root there grow only
lateral roots, which arise in the pericycle and push out through the cortex.
The shoot meristem, however, is more complex ( p. 89 ) . At the base of the
terminal dome of cells arises a series of minute protuberances, the early
leaf primordia, arranged in a precise order.

The cause of the differentiation of these primordia from the rest of the
apical meristem is not known. Schiiepp ( 1952 ) suggested that, since cell
division in the outer layer of the meristem is always anticlinal but in the
tissue below may be in various directions, this surface layer will expand
more rapidly than the surface of the underlying tissues and will thus
tend to buckle or pucker, starting the formation of primordia. This would
not explain the very regular pattern in which these arise, however, and
it can also be shown that the initial bulge results from division in a group
of cells just beneath the surface layer. Snow and Snow (1947) have sub-
mitted this theory to experimental test by making shallow incisions at
the surface of the meristem. Instead of closing up, as they would do if
the outer layers were under pressure, these gaps open, indicating that this
region is actually under tension.

The fate of a small lateral primordium may not always be to grow into
a leaf. Wardlaw and his students (p. 71) have performed various experi-
ments on the meristems of ferns in which, by deep cuts, they were able to
isolate from the apex a young primordium or a region that was about to
develop into a primordium. In most cases this structure, instead of form-
ing a dorsiventral leaf, developed into a radially symmetrical bud-like or-
gan which, in culture, was capable of growing into a whole plant. Factors
in the surrounding meristematic tissue evidently help determine into what
sort of structure a given primordium will differentiate.

The growth of the leaf primordium into a mature leaf has been studied
by many workers (p. 90, and Foster, 1936). In general, the upper and
lower epidermis is continuous with the outer layer of the meristem, and
what will later form the palisade and spongy layers is continuous with
the subepidermal layer. The veins usually arise from a layer just below
this. The differentiation of the leaf of tobacco has been described by
Avery (1933) and of Linum by Girolami (1954; Fig. 8-2). Foster (1952)
has reviewed the development of foliar venation. The mode of develop-
ment and differentiation in certain leaves of unusual shape, as in
Podophyllum and Sarracenia, is described by Roth ( 1957 ) . The growth
of a fern frond, at least for some time, takes place by the activity of an
apical cell (Steeves and Briggs, and Briggs and Steeves, 1958).

188 The Phenomena of Morphogenesis

An important morphogenetic problem here is how far the development
of such a lateral structure depends on factors in the meristem from
which it grew and how far it is independent. Steeves and Sussex ( 1957 )
removed primordia of several sizes and ages from the meristem of
Osmunda and other ferns and grew them in sterile culture. These de-
veloped normally into mature leaves just as they would have done if at-
tached to the plant, except for being smaller. Evidently after a certain
stage is reached the control of development is within the leaf itself. This

Fig. 8-2. Early stages in development of the leaf of Linum. SI, subapical initial; x,
procambial elements. ( From Girolami. )

self-differentiation has been found in other cases and shows that the
organization of the plant is not as tight as it is in animals but that there
is some degree of independent control of differentiation in individual
organs.

A branch or secondary axis differentiates by the activity of a bud aris-
ing in the axil of a leaf primordium (Garrison, 1955). In herbaceous
plants such a bud develops directly but in woody ones it has a dormant
period and is covered by bud scales, or cataphylls. Bud development in
pine has been studied by Sacher (1955) and in angiosperms by Foster

Differentiation 189

(1931). In inflorescences the leaves may be reduced to bracts. Foliage
leaves, bracts, and cataphylls are presumably equivalent morphologically,
and the development of a primordium into one or the other depends on
its function. Primordia at a meristem are thus multipotent (Foster),
since they may form several kinds of structures.

How a given structure differentiates is closely related to the position
that it occupies in the developmental pattern. Not all morphologically
equivalent organs develop alike. In Ginkgo the axis is differentiated
into short shoots and long shoots (Gunckel and Wetmore, 1949). All
buds form short shoots but some of these will grow into long ones. The
ratio of the two affects the form of the tree. A somewhat similar situation
occurs in Cercidiphyllum (Titman and Wetmore, 1955).

The vertical axis of a tree and the lateral axes ( branches ) that it bears
also may differ markedly, the former being radially symmetrical and
orthotropic, the latter more or less dorsiventral and plagiotropic. Conifer-
ous trees offer familiar examples, where the lateral branches are much
flattened and branches of the second order occur in two lateral ranks. In
Abies and Picea this is evidently related to gravity, for if the terminal
bud or branch is removed, a lateral branch will bend upward and replace
it. In Araucaria excelsa, however, this difference is so deeply seated that
if cuttings are made from the lateral branches, the flattened character
now persists in the new plant even if the cutting is oriented vertically.
Not only structure but physiological behavior may be permanently
altered, for such lateral branches will grow horizontally in whatever posi-
tion they may now be placed. Carvalho, Krug, and Mendes (1950)
report a similar behavior in Coffea. There are many other examples of
such topophysis (p. 212).

The differentiation of particular organs— root, stem, leaf, flower—
during development is markedly influenced by growth substances of
various sorts (Chap. 18).

Internal Differentiation

Visible differentiation involving external diversity in organs and their
parts is accompanied in most plant structures by a high degree of internal
diversity. This involves differentiation among various types of cells and
tissues.

Histological differentiation presents two chief problems : ( 1 ) How do
cells become different from one another and (2) what is the origin
of the various tissue patterns found in the internal structure of plant
organs?

Origin of Cellular Differences. Cells differ from each other in many
ways. Frequently it is possible to determine the exact cell division at
which such a difference becomes evident. In young roots of certain grasses

190 The Phenomena of Morphogenesis

(p. 131), for example, the last division of many (sometimes of all) of
the surface cells results in a small daughter cell at the apical end and a
larger one at the basal end. This initial difference is intensified during
the later development of these cells, for the smaller cell (a trichoblast)
sends out from its surface an elongate sac which becomes a root hair.
Such a structure is lacking in the larger cell (Cormack, 1949). The
beginning of this difference may be seen even before the last division,
for the cytoplasm at the apical end of the mother cell becomes much
more dense than that at the basal end. Differentiation between the two
daughter cells is thus related to the strongly polar character of the mother

Fig. 8-3. Section through developing liverwort sporangium showing differentiation of
alternating spores and elater cells. ( From Goebel. )

cell. In Phalaris the epidermal cells contain a natural red pigment which
is deeper in color in the prospective root-hair cells, and they can be
distinguished early for this reason (Bloch, 1943b). In many plants the
surface cells of the root are all potentially alike, and the differentiation
of some cells into root hairs and others into hairless cells is not de-
termined at a differential cell division but by environmental factors. The
difference between these two types of root-hair determination may be
related to anatomical characters (Cormack, 1947). A close relation exists
between the distribution of cellulose-forming enzymes and the location
of the root hair on a surface cell ( Boysen-Jensen, 1950 ) .

There are many somewhat similar cases of cellular differentiation. In

Differentiation 191

Ricinus the secretory cells are formed, in the young meristem or in later
development, by differential cell division (Bloch, 1948), though conform-
ing to no sharp pattern. Once formed, these cells continue to divide, pro-
ducing rows of similar cells in a cell lineage. This may even persist in
tissue culture.

The differentiation between chlorophyll-bearing and colorless cells in
the leaf of Sphagnum results from a differential division, preceded by a
polar movement of the cytoplasm (Zepf, 1952). The origin of elaters in

Fig. 8-4. Trochodendron. Section of leaf with a large branching sclereid. (From
Foster. )

the capsule of liverworts is similar, a cell of the archesporial tissue divid-
ing into a spore mother cell and an elater cell ( Fig. 8-3 ) .

Certain trichosclereids develop in much the same manner. These cells,
which in Monstera become very long and thick-walled, are set apart at
the last division of certain cells of the meristematic cortex. The smaller
daughter cell (this time at the basal end), possessing a relatively larger
nucleus, develops into the sclereid and the other into a typical parenchyma
cell. Although the sclereid begins in this case as the smaller daughter cell,
it soon sends out one or more processes which grow longitudinally be-

192 The Phenomena of Morphogenesis

tween neighboring cells and often become very long (Bloch, 1946). A
study of the origin of such idioblasts ( cells distinctly different from their
neighbors) (Fig. 8-4) may throw light on problems of cellular dif-
ferentiation ( Foster, 1956, and others ) .

Stomatal initials are set apart by differential cell divisions ( Bunning and
Biegert, 1953 ) . A smaller, more densely cytoplasmic cell and a larger one
are formed by a late division of a surface cell. The former divides again,
this time equally and longitudinally, to form the guard cells, the contents
of which soon become markedly different from those of the other epidermal
cells. In monocotyledonous plants like this, where the cells are in regular
longitudinal rows, the stomatal initials are cut off at the ends of elongate
cells. In most dicotyledons, where the cells of the developing epidermis
are more nearly isodiametric, the initial is cut out of a corner of the cell
and divides again to form the guard cells.

A number of cases have been reported where the differentiation of one
type of cell evidently induces changes in the character of adjacent ones.
Thus in Sedum there are groups of cells that form tannin, and in these
regions stomata do not differentiate (Sagromsky, 1949). In Potamogeton
roots those cells of the exodermis that are just under the already dif-
ferentiated trichocytes divide several times, unlike the other cells in this
layer, and so form groups of small cells, one below each trichocyte
( Tschermak-Woess and Hasitschka, 1953b ) . In a species of Begonia where
there are silver spots on the leaf surface, there is a hair formed in each
spot save the very small ones, and the larger the spot, the longer the hair
(Neel, 1940).

Cell Size (p. 29). Some of the most conspicuous differences between
cells are in their size. Meristematic cells in most cases are small, and after
the final division the daughter cells increase considerably in size. The
extent of this increase is determined by the time in development when
division ceases in that particular cell lineage and by the position of the
cell in the general histological pattern. Pith cells are usually large be-
cause they have had a long period of enlargement since their last division,
and epidermal cells relatively small since division there lasted longest.
Many size differences, however, such as those between the large vessels
of ring-porous woods and the small elements around them, are due to
local differential factors, since the cambial initials are alike.

One type of cellular differentiation is unlike all others in that it in-
volves fundamental alteration of the cell itself. Many instances are now
known in which mature cells, aroused to division by various agents, are
found to have twice as many chromosomes (or more) as they did at
their last preceding mitosis. During the differentiation of such a cell
from meristematic condition to maturity a doubling of the chromosome
complement must have taken place. Such a change, though not directly

Differentiation 193

observable in the cell, is usually reflected in increased cell size and may
be a factor in other changes which occur during differentiation. How
important this factor is in cellular differentiation is not known. It may
account for some of the diversity in cell size but probably has little to do
with other aspects of differentiation ( p. 441 ) .

The Cell Wall. Some of the most distinctive ways in which cells differ
are concerned with the cell wall. The wall is of much greater variety and
significance in plant cells than in animal cells, and the key to cellular
differentiation in plants is often to be found in it. Walls may differ greatly
in thickness, chemical composition, and structure, depending upon the
function of the cells of which they are parts. In certain tissues the cells
die early, and only the thickened walls which they formed remain. The
size and shape of the cell and the manner of its growth seem often to
be dependent primarily upon the character of the wall. Studies of the
chemistry and fine structure of the wall show how complex its consti-
tution may be and make clear that any detailed analysis of cellular dif-
ferentiation must pay attention to changes not only in the living material
of the cell— the true protoplast— but in the wall that is the result of its
activity (Bailey and Kerr, 1935; Frey-Wyssling, 1955).

In a few cases the origin of differentiation in the wall may be observed,
especially where sculpturing occurs, as in the ringed, spiral, and retic-
ulate cells of the xylem and in other tissues with similarly unequal
wall thickening. Criiger (1855) and Dippel (1867) many years ago
showed that the first indication of where such thickenings were to occur
in developing cells was the accumulation of cytoplasm, more densely
granular than the rest, in a definite pattern. The thickenings of the
wall (rings, reticulations, or others) were laid down in close relation to
this cytoplasmic pattern (Barkley, 1927). Strasburger (1882) observed
streaming of cytoplasm along these strands. Large and vacuolate paren-
chyma cells that are being redifferentiated as reticulate xylem cells in re-
generation are particularly good material in which to observe the
cytoplasmic network upon which the wall reticulum is being built ( Sin-
nott and Bloch, 1945; Fig. 8-5). Kiister ( 1931) called attention to the simi-
larity between such cytoplasmic configurations and Liesegang rings.
Denham (p. 166) reports that in many cells the directions of cytoplasmic
streaming has a definite relation to the micellar configuration of the wall.

Differentiation and Position. In all the cases of cellular differentiation
here described, the position of the cell in the developing system is evi-
dently closely concerned with the type of differentiation that it under-
goes. A notable example is the formation of reaction wood, which dif-
ferentiates in the precise position where it will tend to bring a terminal
or lateral axis into a specific orientation in the pattern of the whole
(p. 356).

194 The Phenomena of Morphogenesis

We may distinguish position with reference to the external environ-
ment (light, oxygen, chemical stimuli, and many others), with refer-
ence to various factors in the internal environment (surfaces, air spaces,
conducting strands, and cells previously differentiated), and with refer-
ence to the autogenously unfolding and genetically controlled pattern of
development. To distinguish these aspects of position is often diffi-
cult or impossible. The important fact is that in the organized system
specific parts are markedly unlike each other and that these differences,
which in the aggregate distinguish the system, may arise from various
causes.

Fig. 8-5. Portion of a regenerating xylem strand in Coleus, showing pattern of wall
thickenings laid down along bands of granular cytoplasm. Earlier stage at right.
( From Sinnott and Bloch. )

Intracellular Differentiation. The parts of a single cell often show a
high degree of diversity. The distinction between nucleus and cytoplasm
is present even in embryonic cells, but as the differentiation of the
cell takes place, the protoplast may exhibit a wide range of structures.
Conspicuous among these are the plastids. In the algae (as Spirogyra),
these may be represented by large and often complex chromatophores.
Much more minute bodies, the mitochondria, occur and multiply (Soro-
kin, 1955; Hackett, 1955). Bodies similar to the Golgi apparatus of
animal cells have been reported (Weier, 1932), but their general oc-
currence is doubtful.

Differentiation 195

The proportions of these intracellular structures often change during
differentiation. Thus in moss protonemata the nucleus increases in size
from the tip of the caulonema backward but the nucleolus decreases for
the first few cells. The nucleus also gradually changes from a spherical to
a spindle shape, and other changes are evident (Bopp, 1955). Intra-
cellular diversity is particularly conspicuous in the differentiation of large
coenocvtic bodies, as in certain algae.

Differentiation of Histological Patterns. Differentiated cells rarely occur
separately but are grouped into tissues. Endodermis, vascular tissues,
and many others are familiar examples. These tissue patterns begin
to appear in the embryo (Miller and Wetmore, 1945; Fig. 8-6; Spurr,
1949; Esau, 1954), grow more diverse in the seedling, and reach their
maximum differentiation in the mature plant. Nowhere else are the com-
plexities of differentiation so evident as in the development of these

O.OMM

Fig. 8-6. Beginnings of differentiation in early embryo of Phlox. Successive stages,
showing origin of central procambial core. (From Miller and Wetmore.)

histological patterns. Specialized as these may be, each constitutes an
element in an integrated whole.

Wall Relationships. One of the basic elements in histological pattern
is the relationship of cells to each other. This is determined primarily by
the position of new walls in dividing cells relative to walls in adjacent
cells. In most tissues a new wall is so placed that it does not come op-
posite a neighboring cell partition, and the cells are thus "staggered"
in position, like bricks in a building (p. 47). In a few cases, however,
walls in adjacent cells are exactly opposite, so that they extend in con-
tinuous lines across the tissue (Fig. 8-7). This is particularly evident in
cork and in regenerating tissue at wounds. This arrangement lends itself
well to the development of aerenchyma, since when such cells pull
apart at their corners a larger volume of intercellular space results than if
the walls were staggered. The two types of pattern may well be seen

196

The Phenomena of Morphogenesis

Fig. 8-7. Partition walls opposite adjacent ones. At left, dividing cells in tissue of
wounded petiole of Bryophyllum, the walls being laid down directly opposite those
in adjacent cells. At right, similar divisions in more mature tissue below wound
surface. ( From Sinnott and Block. )

in the transverse section of certain roots, where the inner cortex is radially
concentric, with opposite walls, but the outer cortex shows the alter-
nating arrangement typical of ordinary parenchyma ( Fig. 8-8 ) .

Endodermis. One of the simplest of these tissue patterns is shown by
the endodermis. This is a single layer of cells differentiated in a specific
way, as by special thickenings in the walls or the presence of a Casparian
strip. It separates the vascular cylinder from the cortex. The position
it occupies is usually a very definite one, and in such plants as Equisetum
its particular pattern with reference to the bundles is specific enough to
be valuable for taxonomic purposes.

Fig. 8-8. Transverse sections of two roots. Left, Sporobolus, in which there are three
layers of radially concentric cells in the cortex, the walls having been laid down
directly opposite those in adjacent cells. Air spaces later appear at intersections. Right,
Agrostis, in which the cell walls in the cortex always avoid adjacent ones. (From
Sinnott and Bloch. )

Differentiation

197

The exact localization of the endodermis makes it of particular interest
morphogenetically. Light is important in its development, for it is well
differentiated in roots and etiolated stems and much more poorly de-
veloped in the light (Bond, 1935). Venning (1953), however, finds that
factors other than light are responsible for the formation of a typical
endodermis. Van Fleet in a series of papers has studied differentiation
histochemically ( 1954a and b ) , with particular reference to the position
of the endodermis on an oxidation-reduction gradient as well as to the
distribution of various enzymes. He has stressed the importance of histo-
chemical determination of enzyme distribution (1952) as a means of dis-
covering chemical differentiation before it is evident in structure (Fig.
8-9).

Fig. 8-9. Chemical differentiation of the endodermis. Its cells stain differently from
those of adjacent tissues. ( From Van Fleet. )

Fiber Patterns. An example of the differentiation of a somewhat more
complex pattern but one consisting of a single type of cells is provided
by the development of a system of fiber strands such as that found in the
pericarp of the cucurbit fruit, and especially well developed in the
"dishcloth" gourd, Luff a (Sinnott and Bloch, 1943). Here the pericarp
tissue in the early ovary primordium consists of longitudinal rows of
squarish parenchyma cells with most of the divisions at right angles to
the axis of the young ovary or parallel to it. Here and there begin to
occur divisions not in these two orientations but obliquely at various
angles (Fig. 8-10). Parallel to each such division is a series of others so
that in a given cell or its neighbors several elongate and parallel cells
are cut out. This group becomes connected with other groups in a con-
tinuous series, though successive members of this series may arise at
somewhat different angles. The result is that strands of cells are formed,
twisting about through the original rectangular cellular system and

198 The Phenomena of Morphogenesis

connected in an interwoven pattern. These small elongate cells expand
with the growth of their parenchymatous neighbors and develop into
long sclerenchymatous cells aggregated into strands a fraction of a milli-
meter wide which are organized into the complex fibrous "sponge." This
sponge is not a random mass of fibers but has an organization of its own,
for the outer members of it are arranged in rows transverse to the axis
of the fruit and most of the inner ones extend lengthwise. They are
united into a continuous system. This system seems to be the expression
of a histological pattern superposed upon the fundamentally different
system of regularly arranged parenchyma cells of the early ovary. How
the course of its interconnected but continuous strands is established is
a baffling problem. In somewhat the same way as these sclerenchym-
atous strands develop, the young bundle initials of the veins arise in

Fig. 8-10. Young ovary of Luff a. Successive early stages in the origin of a fiber strand
differentiating in ground parenchyma. ( From Sinnott and Bloch. )

the mesophyll of a developing leaf blade, as described by Meeuse ( 1938;
Fig. 8-11).

Cambium. A familiar example of a complex pattern of differential de-
velopment is that of the vascular cambium and its products (p. 84). The
typical cambium consists of a continuous tangential layer of elongate
initials in which most of the divisions are in the tangential plane. The
cells cut off on the inside develop into tracheids, fibers, vessels, paren-
chyma, and ray cells of the xylem, and those on the outside into sieve
tubes, companion cells, fibers, and other phloem cells. There are pro-
found differences between a huge vessel element in oak wood and a
small parenchyma cell beside it but both come from similar cambium
cells.

There are a number of morphogenetic problems presented by a study
of this development of secondary vascular tissues.

Differentiation 199

1. What determines the relative frequency of divisions on the inside of
the cambial initials to those on the outside, the relative amount of
xylem and phloem?

2. What determines how cambium derivatives differentiate into the
widely diverse sorts of cells found in the mature tissues?

3. What maintains so perfectly the anatomical pattern of the xylem
and phloem?

Bannan and others (p. 81 ) have shown that many radial files of cells are
begun at the cambium and then die out and that many rays are initiated
only to disappear, the net result being a very precise distribution of rays
and vertical elements with reference to each other. The files of tracheids
remain at a constant width, and the rays are evenly spaced with reference
to each other, as can be seen in a tangential section of wood. These rela-

Fig. 8-11. Portion of transverse section of leaf of Sanseviera. Bundle of fibers be-
ginning to differentiate in the midst of fundamental tissue. Compare with Fig. 8-10.
( From Meeuse. )

tionships are so constant and specific that they are used as taxonomic
characters.

This same problem of a specifically patterned distribution of structures
meets us in many other places, such as in the spacing of bundles in cross
sections of the stems of monocotyledons, of stomata in the leaf epidermis,
of root hairs, or of developing sclereids in the cortex. Biinning has ex-
plored this problem (1948, pp. 173-179). He suggests that a specific
developing structure prevents the differentiation of another like it within
a certain distance of itself and cites some experimental evidence in sup-
port of this idea (Biinning and Sagromsky, 1948). In the cells immediately
around a young stoma initial, the nuclei always lie on the side of the
cell next to the initial, as if in response to a chemotactic stimulus (Fig.
8-12). A few cells farther out, they have normal positions. Biinning be-
lieves that a hormonal substance passes out from the young stomatal cells
which stimulates cell division, as shown by the production of accessory

200 The Phenomena of Morphogenesis

cells and others, and thus inhibits differentiation of stomata (and some-
times of hairs or glands). Near wounds, cell division occurs but stomata
are not differentiated. If auxin paste or juice from crushed tissue, pre-
sumably containing wound hormones (p. 402), is applied to the young

Fig. 8-12. Relation of nuclei to stomata. Nuclei of cells adjacent to stomatal initials,
in young and developing leaves, are pressed closely to these initials as if chemically
attracted to them. ( From Biinning and Sagromsky. )

leaf, cell divisions are plentiful but stomata do not develop (Fig. 8-13).
This suggestion is of much interest in relation to the differentiation of
other evenly spaced structures, but it does not explain how the inhibiting
center itself is initiated in the first place. This is a promising point, how-
ever, at which to attack the problem of organic pattern.

In the histological pattern that originates back of the apical meristem,
Biinning ( 1952# ) believes that the meristem itself inhibits differentiation
within a certain distance. Farther back, each bundle initial, which is in the

Fig. 8-13. Left, epidermis of developing leaf two weeks after treatment with auxin
paste. Stomata are almost absent. Right, epidermis of untreated half of the same
leaf. ( From Biinning and Sagromsky. )

Differentiation 201

process of growth but is not part of the meristem proper and which he
terms a meristemoid, inhibits the development of others near it.

The differentiation of tissues produced by the vascular cambium has
been studied by Linnemann (1953), who observed that in beech the
proportion of rays is greater in the wood of isolated trees than in dense
stands but that it does not vary consistently with age or as between
trunk and branches. Rays tend to increase in width during an annual
ring and to be wider in the narrower rings.

The fact that vessel elements occur in longitudinal series to form a
duct indicates the operation of a continuous stimulus longitudinally
along the axis. Priestley, Scott, and Malins (1935) have shown that a
single duct differentiates almost simultaneously throughout a long extent
of trunk. A leaf trace passing down into a young stem exerts a consider-
able correlative influence upon vessel differentiation below it. Alexandrov
and Abessadze (1934) found that there are fewer vessels in a segment
just below a leaf trace and that they appear earliest next the rays that de-
limit the trace. The vessel-forming stimulus clearly moves downward,
thus suggesting the operation of a hormonal control.

That auxin has a role in the initiation of the ring-porous condition is
suggested by the work of Wareing (1951), and Chowdhury (1953) has
analyzed some of the factors responsible for the transformation of
diffuse-porous to ring-porous structure in Gmelina.

Continuity in differentiation of similar cells is also shown by the cork
cambium, or phellogen (p. 88), in old cortex or phloem. Here it arises
as a series of almost simultaneous divisions which, as seen in transverse
section, somewhat resemble those described for the Luffa strands, since
they are connected to one another in a series and often follow a somewhat
irregular course through the tissue in which they arise. They form a
continuous sheet of meristematic cells, often in localized patches, which
cut off elements from their outer faces. Their cells suberize later, thus
sealing off the outside tissues. The origin of these phellogens is the more
interesting because they have their beginning in tissues where the cells
are mature and intermixed with dead or necrotic ones. Their origin
after wounding is related to the operation of wound hormones.

A notable example of the differentiation of a histological pattern is
furnished by the system of lignified thickenings (the "reseau de soutien"
of van Tieghem, 1888) in the air roots of certain orchids, which is pre-
sumably concerned with providing rigidity for tissue otherwise soft and
easily collapsed. These arise as bands of lignified wall thickenings which
surround individual cells. They may occasionally fork. It is noteworthy
that the band in a given cell is directly contiguous to that in an adjacent
cell, so that a continuous patterned network of thickened strands is
established (Fig. 8-14). This reminds one of the way in which the ringed

202 The Phenomena of Morphogenesis

thickenings in protoxylem and regenerating xylem cells are directly op-
posite those in adjacent ones.

In all these examples of the differentiation of histological pattern it
is evident that the pattern as a whole transcends cellular boundaries and
involves an extensive and correlated series of changes. This poses in most
direct fashion the problem of pattern in general.

More Complex Patterns. In most cases an anatomical pattern consists
of more than one type of tissue and thus is much more complex than
the ones just described. In plants that grow by a large apical cell at
the meristem, differentiation of the various tissues from particular cells
cut off from this apical cell may be traced. Thus in Selaginella (p. 58),

^°

NC s

H

Fig. 8-14. Continuity in the differentiation of various wall thickenings. Left, rings
and spirals in protoxylem of Zea. Center, thickenings in reticulate vessel elements
that have developed from parenchyma cells in bundle regeneration. Right, lignified
bands (reseau de soutien) in cortex of air root of an orchid. In all these cases the
thickenings form a continuous pattern across cell boundaries. {From Sinnott and
Bloch. )

the apical cell, by an unequal division parallel to one of its faces, pro-
duces on its apical side a large cell, the continuing apical initial, and
on its basal one a cell which, seen in section, has parallel anticlinal walls
(Barclay, 1931; Fig. 4-4). This cell divides into two by a wall at right
angles to the first division. Each daughter cell divides again into two
in the same way. Thus a row of four cells is produced. Proceeding down
the shoot axis, in a longitudinal section, one can observe the fate of simi-
lar rows of four cells which had been cut off by previous divisions of the
apical cell. The outermost of the four becomes a cell of the epidermis.
The second (by later divisions) produces the cortex. Descendants of the
third and fourth form the innermost tissues. Thus the progress of dif-
ferentiation can usually be followed in various lineages of cells. Specific

Differentiation 203

types of differentiation seem to be related to specific lineages, almost as
though "determiners" were being parceled out at each division. The same
type of differentiation has been described by Bartoo (1930) in Schizaea.
In these cases differentiation is a true development, the unfolding of an
internally directed pattern, with each division evidently related to the
polarity of the cell. Cell division here seems a dominant factor in the
determination of pattern. It should be noted, however, that there are
often irregularities in this progression and that it is by no means always
so precise.

In many other plants, especially those with large apical cells, differen-
tiation also follows a rather regular course like that just described. Chara,
Fontinalis, and some species of Equisetum (Fig. 4-3) are examples. In
others, however, such precise relationship between a specific type of dif-
ferentiation and cell lineage does not occur, for a particular tissue may
sometimes have one cell ancestry and sometimes another. The origin of
root, stem, leaf, and foot from the quadrants of a young fern embryo, for
example, is not rigidly determined.

In higher vascular plants where an apical cell has been replaced by a
mass of meristematic tissue, in most cases it becomes impossible to trace
the origin of a group of differentiated cells from a single ancestor or to
determine the precise divisions at which a fundamental difference be-
tween two cells (or their descendants) originates. Such divisions may
occur, but in these there is no great difference between daughter cells
nor is regularity of lineage usually observable. It is probably true that in
very many instances differentiation is the result of factors of environment
or position and is not related at all to differential cell division.

There is, however, a good deal of cellular differentiation to be seen in
the apex of shoot and root, either as layers or zones (p. 62 ) and these often
bear a close relation to the structures that develop from them. Thus in
periclinal chimeras ( p. 272 ) it is possible to determine with much accuracy
the derivation of particular tissues from particular layers at the apex.
Nevertheless, in forms without meristematic layering ( as in some gymno-
sperms) differentiation of tissues takes place equally well. The problem
of how the histogens become distinct from each other, in forms which
show them, is one which for its solution must go back to the young
embryo.

In the mass of relatively undifferentiated tissue below the apex arise
the beginnings of vascular tissue. The distinction between the procambial
or provascular cells (those which are to give rise to the primary vascular
tissue) and the cells of the fundamental tissue begins to make its appear-
ance early in development near the tip of the meristem. The first differ-
ence to be observed here often is not a structural one but a difference in
the staining reaction of the cells. The earliest structural difference to be

204 The Phenomena of Morphogenesis

seen, in most cases, is the elongate form of the procambial cells in longi-
tudinal section. This form is due either to fewer transverse divisions in
these cells as compared with their neighbors or to more frequent longi-
tudinal ones. From groups of these elongated provascular cells arise the
vascular bundles of the stem. There is a close relation between the differ-
entiation of these bundles and of the leaf primordia near the apex, for the
young leaf traces that enter the base of each primordium are continuous
with the differentiated vascular tissue below.

There has been some difference of opinion as to just how the pattern
of vascular differentiation originates. It is now rather generally agreed
(Esau, 1953Z? ) that the procambial strands develop acropetally, continu-
ous with the mature vascular tissue below and pushing up into the bases
of the primordia themselves. In a transverse section of the axis, the pro-
cambium forms a ring which may be continuous or consist of a series of
bundles. On the outside of a procambial strand the first phloem differen-
tiates, and on the inside, the first xylem. The developmental history of
these tissues is different, however. The phloem, like the procambium,
develops continuously from the base toward the tip. The xylem, on the
contrary, differentiates first in the base of the enlarging leaf primordium
and then both upward and downward. In its downward course it meets
the upward developing xylem in the axis below (Miller and Wetmore,
1946). Jacobs and Morrow (1957) traced the downward differentiating
xylem strands and found that they did not always make connection with
the normally opposite ones below. In the root, the procambium, phloem,
and xylem all differentiate acropetally and continuously ( Heimsch, 1951;
Popham, 1955k).

The physiological significance of these facts is not clear, but morpho-
genetically they are concerned with the important question as to whether
the course of initiation and development of structures at the apical meri-
stem, notably the position of the leaf primordia and the pattern of internal
differentiation, results from stimuli proceeding up from the mature struc-
tures below or whether in its development the tip is independent of what
has gone before. This problem is discussed elsewhere in the light of some
experimental results (p. 238). Torrey (1955), working with root tips cut
off and grown in culture, presents evidence that the pattern of vascular
differentiation (triarch, diarch, or monarch) just back of the tip is not
induced by the tissue farther back but is related to the dimensions of the
apical meristem at the time the cylinder is differentiated.

Much work has been done on this problem of differentiation at the
apical meristems, and it is well covered by Esau ( 1953b ) . Among other
recent publications are an extensive review by Esau ( 1954 ) and papers
by Rathfelder (1954), Young (1954), Wetmore and Sorokin (1955),
McGahan (1955), and Jacobs and Morrow (1957).

Differentiation 205

DIFFERENTIATION DURING ONTOGENY

Differentiation, like most problems of morphogenesis, must be studied
not only as it is found in the structure of the mature plant but as it arises
during development. The mature plant is obviously very different from
the embryo and the seedling, but an important question, still far from
settlement, is whether the changes that take place here are simply the
result of increased size and the effects of environment or are internal
modifications arising during development and becoming manifest in the
progressive differentiation of the individual as its life cycle unfolds.

It is obvious that environment is of great importance in determining
the differences that arise, and most of the experimental work in morpho-
genesis is concerned with a manipulation of environmental factors. It is
also clear that the specific response to an environment depends on the
innate genetic constitution of the individual. What is not so evident, how-
ever, is whether this response always remains the same or changes as the
organism grows older.

There is a good deal of evidence that changes in the plant, independent
of environmental conditions, do indeed occur as development proceeds.
Juvenile stages are often very different from adult ones. That these are
real and often irreversible differences is proved by the fact that they can
be perpetuated by cuttings. Progressive changes in the shape and char-
acter of organs, especially leaves, at successive points along the stem have
often been observed and by some biologists are attributed to advancing
maturity or physiological aging. The onset of actual senescence has been
reported in some cases. A considerable school of physiologists believe that
the life history of a plant, particularly up to the time of flowering, consists
of a series of successive phases, each the necessary precursor of the next
but independent of the amount of growth attained. This concept has come
in part from the idea of vernalization ( p. 339 ) .

In such phasic development the major change is the onset of the repro-
ductive period after one of purely vegetative development. This appar-
ently begins by a physiological change, the "ripeness to flower," as Klebs
called it. Only after this has begun do the floral primordia appear at the
meristem. They may not be the first visible evidence of the onset of repro-
duction. Roberts and Struckmeyer ( 1948 and other papers ) have shown
that the induction of the flowering phase is very early indicated by a
number of anatomical changes. Root growth is much reduced, cambial
activity almost ceases, and the vascular tissues tend rapidly to complete
their full differentiation. In other words, the plant structures become ma-
ture. Reproduction is a sign of maturity, and these anatomical changes are
evidence of a more general one that is about to take place. Many factors

206 The Phenomena of Morphogenesis

are involved here, either as causes or concomitants. There seems to be a
major physiological change involved in this shift from vegetation to repro-
duction. An important problem in both physiology and morphogenesis is
to find what is involved in this shift. To solve it would throw light on one
of the major formative processes in the plant.

Embryology and Juvenile Stages. The science of embryology in the
higher plants, in the sense in which it has been developed in animals, can
hardly be said to exist. The early embryo is relatively inaccessible and
is simple in structure. The divisions immediately following fertilization
have been studied for many plants by Soueges (1939) and Johansen
( 1950; Fig. 8-15) and show differences in certain groups, but little as pre-
cise as the early stages in animal embryology is to be seen. Toward the
micropylar end of the ovule the young radicle begins to differentiate and
forms an apical meristem at its tip. At the other pole, in gymnosperms and
dicotyledons, arise the cotyledons, with the first bud between them. The
monocotyledons have a somewhat more complex structure here but it
follows the same general course.

Especially important to students of morphogenesis is Wardlaw's book
on Embryogenesis (1955a), which discusses embryogeny throughout the
plant kingdom, with particular emphasis on the factors that determine
development. Maheshwari (1950) has written a general survey of angio-
sperm embryology, including a useful discussion of experimental embryo
culture. The ability to take embryos out of the ovule at a very early stage
and grow them in culture has opened up a wide field of investigation
which should be fruitful for morphogenesis.

Several facts of significance, particularly for regeneration, have come
from a study of plant embryos. In a number of cases the young embryo
may spontaneously divide into several parts each of which apparently has
the capacity to develop into a whole plant. Such cleavage polyembryony
has been studied by Buchholz and others (p. 235). In certain plants,
notably some members of the citrus family, embryos may arise not only
through a sexual process but by budding from the tissues of the nucellus.
Such nucellar embryos are important for genetics as well as for morpho-
genesis.

Of particular interest, however, are those forms in which the early struc-
tures are markedlv different from later ones and in which characteristic
"juvenile" stages can be seen. This type of development has been termed
heteroblastic by Goebel in contrast to the more gradual homoblastic type.
The difference is particularly conspicuous in the character of the leaves,
which in the seedling are often quite unlike those of the mature plant.
The first pair of leaves in the Eucalyptus seedling, for example, are hori-
zontally oriented and dorsiventral in structure though all later foliage is
characteristically pendulous and bifacial. The juvenile leaves of Acacia

Fig. 8-15. Development of the embryo of Capsella bursa-pastoris
from the first division of the fertilized egg to the mature embrvo.
( From Johansen, after Soueges and Schuffner. )

207

208 The Phenomena of Morphogenesis

are pinnately compound but the adult ones are reduced to phyllodes
(Fig. 8-16). In pine, the seedling leaves are not in fascicles but are borne
singly. The young plant of Phyllocladus has needle-like leaves, common
in most other conifers, but the adult plant bears phylloclads only. Seed-
lings of cacti have leaves but these are absent in adult plants. Many more
such examples could be cited (Jackson, 1899).

There are some cases in which the internal structure is markedly dif-
ferent in young plant and adult, usually being simpler in character in the

Fig. 8-16. Juvenile leaves of Acacia seedling (pinnately compound) contrasted with
the flattened phyllodes that constitute the adult foliage. (After Velenovsky.)

former. Thus in ferns which have a complex vascular system in the ma-
ture plant, the young sporeling possesses a relatively simple protostele or
siphonostele. Species with many-bundled leaf traces usually have only
three in the seedling. Secondary tissues are also less complex in young
plants. Schramm ( 1912) finds that juvenile leaves generally resemble adult
shade leaves in structure. There are differences, particularly as to vena-
tion, between the early, deeply pinnatifid leaves of Lacunaria and the
simple mature type ( Foster, 1951 ) . Robbelen ( 1957 ) finds that in chloro-
phyll-defective mutants the juvenile form of leaf is retained later than

Differentiation

209

normally and has a relatively small meristem. Normal leaves are not pro-
duced until the meristem reaches a diameter of 80 to 90 /*.

Schaffalitzky de Muckadell (1954) has reviewed the literature on ju-
venile stages.

Juvenile traits often resemble those of plant types presumably an-
cestral for the stock in question (Sahni, 1925, and others). This seems
evident in many of the examples cited. Most Leguminosae other than
Acacia have leaves and not phyllodes, and most Myrtaceae other than
Eucalyptus have dorsiventral leaves. These facts suggest that the seedling
repeats or recapitulates ancestral traits, much as the animal embryo has

LEAVES AT NODES 1-5

A-8

A-24 A-20

A-9

A-24XA-8
Fi

Fig. 8-17. Changes in leaf shape in cotton at five successive nodes above the cotyle-
dons, in four varieties of cotton and an Fi. ( From Dorothy Hammond. )

been thought to do. There is much doubt in many cases, however, as to
what the course of evolution actually has been and so much variation in
early ontogeny in many plants that it is impossible to establish the doc-
trine of recapitulation as an invariably useful guide to phylogeny.

Progressive Developmental Changes. More common than these con-
spicuous cases of differentiated juvenile stages are those where there is
not a sharp distinction between juvenile and later forms but a gradual
change from the younger part of the plant to older ones. Many examples
of this are reported in the literature. Goebel (1896) described eight suc-
cessive leaf types in the climbing aroid Anadendrum medium which
occurred at different levels and showed an increasing degree of com-

210 The Phenomena of Morphogenesis

plexity. Hammond (1941; Fig. 8-17) and Stephens (1944) have described
similar changes in leaf shape in cotton, and Montfort and Miiller ( 1951 )
in mistletoe. Von Maltzahn (1957; Fig. 8-18) has compared leaf char-
acters throughout plant development in large and small races of Cucur-
bita and the hybrid between them.

Similar alterations have also been found in reproductive structures. In
Chamaecyparis there is a gradient of sexuality in the branches, the tips
being sterile, with female cones below and male ones still farther back
(Courtot and Baillaud, 1955). There is a flower bud in the axil of each
leaf of Cucurbita pepo but the type of flower produced by it tends to vary
with the position of the leaf on the plant, in the following sequence:
underdeveloped male, normal male, normal female, inhibited male, and
parthenocarpic female (Fig. 8-19). The order of these steps in progressive
feminization is constant but the length of each is affected by temperature

Fig. 8-18. Change of leaf size during
plant growth. Lamina length of succes-
sive leaves in cucurbit plants of small-
fruited and large-fruited types and the Fi
between them. ( From von Maltzahn. )

I 3 5 7 9 I I 13 15 I 7 19 21

and day-length, high temperatures and long days extending the male
phase and delaying the female one ( Nitsch, Kurtz, Liverman, and Went,
1952).

Leaves are especially good material in which to study such changes,
and Ashby ( 1948/?, 1950a, and Ashby and Wangermann, 1950) has made a
thorough investigation of the changing character of the leaves in Ipomoea,
describing the progressive differences in their size and shape and in the
size and number of their cells from lower nodes to upper ones (Fig.
8-20). He presents evidence that these changes are not primarily due to
environmental factors (although such are operative) but to alteration of
inner conditions. In his 1948 papers Ashby reviews this field and discusses
at some length Krenke's theory (1940) that such changes are due to the
physiological age of the plant, as contrasted to its age in time. Krenke
regards aging as progress toward maturity, particularly reproductive ma-
turity, which is sometimes followed by further changes, in a cycle. At
points along this progression rejuvenescence may occur, as on shoots
grown from lateral buds. Successive nodes are units in a developmental

Differentiation

211

scale, and the form of the leaf is a quantitative criterion of physiological
age. In cotton, maximum lobing of the leaf is reached at flowering, earlier
and later leaves being less lobed. The cyclical change proceeds more
rapidly in early-flowering than in late-flowering types, and conditions that
hasten flowering hasten lobing. Krenke believes that rate of change in
leaf shape is inherited and that early-maturing varieties may thus be dis-
tinguished in the seedling stage.

PARTHENOCAKP1C

FEMALE
FLOWERS

^

GIANT FEMALE
AND INHIBITED
MALE FLOWERS

Fig. 8-19. Cucurbita. Sequence of flower
types on a plant of the acom squash.
( From Nitsch, Kurtz, Liverman, and
Went.)

OJ

NORMAL

MALE 8 FEMALE

FLOWERS

NORMAL
MALE FLOWERS

UNDERDEVELOPED
MALE FLOWERS

Ashby has confirmed some of Krenke's conclusions but finds others very
doubtful. The possibility, however, of relating successive morphological
changes to physiological ones has important implications for the problem
of form determination. One may question Krenke's assertion that his
hypothesis is based on dialectical materialism, but the hypothesis itself
should be explored as one hopeful approach to morphogenetic problems.

The bearing of Krenke's ideas on the problem of senescence is of in-

212 The Phenomena of Morphogenesis

terest. Attention has already been called (p. 38) to Benedict's work on
progressive reduction in size of structural units (cells and vein islets) in
vegetatively propagated clones as they grow older, presumably the result
of loss of vigor. This conclusion is still open to doubt, however.

Topophysis. The changes so far discussed have been either juvenile ones
or those distributed through most of the life cycle. In many plants, how-
ever, the contrast in differentiation does not come until the onset of repro-
ductive maturity. Diels ( 1906) observed that environmental factors which
promote flowering also hasten the transition from juvenile to adult foliage.

z
o

CO

1X1
LU

NODES NUMBERED FROM BASE

T

~l 1 1 1 1 1 « ■ » TTT1

2 3 4 5 6 7 8 n-8 n-7 n-6 n.

Fig. 8-20. Change in leaf shape at successive internodes from base to tip in Ipomoea
caerulea. (From Ashby.)

The reproductive stage is marked by characteristic changes at the meri-
stem, especially in the shape of its terminal dome. In the vegetative phase
this is typically low and rounded, but when flower buds are to be differ-
entiated it assumes a much steeper and more elongate form. The produc-
tion of reproductive organs marks for most plants a radical reorganization
of their developmental processes (p. 184) and is often accompanied by
changes so profound that they are irreversible. This is of especial morpho-
genetic significance.

In most cases these changes have little effect on the character of the
vegetative organs, but such cases are sometimes found. In the conifer

Differentiation 213

Dacrydium ciipressinam, for example, needle-like foliage (resembling
that of seedlings in many species with scaly leaves ) occurs not only in the
seedling but throughout the early life of the tree. Only when it begins to
bear reproductive organs, at the age of 20 years or more, does the foliage
assume the scale-like character which then continues throughout the rest
of its life. This may be interpreted as the persistence of a juvenile con-
dition until the period of reproduction.

A more conspicuous example and one which has been widely studied
is that of the English ivy, Hedera helix ( Fig. 8-21 ) . The vegetative phase
of this plant is a vine with five-lobed leaves climbing by adventitious roots

Fig. 8-21. Hedera helix. Flowering shoot with ovate, entire leaves, and a single leaf
of the vegetative "juvenile" region. (From Goebel.)

and flattened against its support and often is the only form of this species
to be seen. After some time and under conditions favorable for reproduc-
tion, however, flower-bearing shoots arise and will grow for many years.
Their tropistic behavior is changed, for they no longer climb but grow
directly outward toward the light and away from their support. Their
structure is also much altered, for the leaves are now oval rather than
lobed and are spirally arranged. The lobed climbing form may be re-
garded as a persistent juvenile condition.

The reorganization of the pattern of differentiation in the transition
from seedling to adult or from the vegetative to the reproductive phase

214 The Phenomena of Morphogenesis

of the ontogenetic cycle is usually reversible in the sense that cuttings
taken from any part of the shoot system or at any stage of development
will, by regeneration, produce a normal plant. In some cases, however,
changes at the growing point have been so great that the newly developed
structures seem to have undergone irreversible modification. A notable
example of this is the English ivy described in the preceding paragraph,
for in this plant cuttings made from the flowering shoot rarely revert to
the climbing form but instead produce upright, radially symmetrical
plants, the variety arborea of horticulture. These are often used as dwarf,
tree-like ornamentals but usually die after a few years. No genetic change
is involved here, for seeds produce the climbing, lobed form again. There
has been a good deal of debate as to the complete irreversibility of this
change (Bruhn, 1910; Furlani, 1914), but the usual behavior is the one
just described. Kranz (1931), however, finds that the transition from
juvenile to adult foliage is often not a sudden one but that the five-lobed
type gives place to a three-lobed one before the mature, ovate leaves are
formed. Robbins (1957) was able to change the adult form of foliage to
the juvenile one by treatment with gibberellic acid.

A somewhat similar case is the persistence of juvenile structures which
can sometimes be induced by growing cuttings from the seedling stem.
The most notable example of this is found in certain of the cypress-like
conifers, where the seedling leaves are needle-like but are soon followed
by the scale-like foliage characteristic of the species. If cuttings are made
from the lateral branches arising just above the cotyledons in Thuja, for
example, they will produce plants, often growing to small trees, which
bear nothing but the needle-like juvenile foliage, the horticultural variety
"Retinospora" (Beissner, 1930). Such plants do not flower and are rela-
tively short-lived. In some way, severance of the juvenile shoot from its
roots seems to have prevented completion of the normal ontogenetic
cycle. Other cases have been reported in which seedlings used as cuttings
grow very differently from those which are left on their own roots
(M. R. Jacobs, 1939). Beissner's results were challenged by Woycicki
(1954), who grew cuttings from seedlings of Thuja, Chamaecyparis, and
Biota but found that the juvenile foliage did not persist. He believes that
the Retinospora forms arose by spontaneous mutations in seedlings or
young shoots.

Whatever the facts in this case may be, others have been reported in
which it is certain that cuttings taken from various parts of the plant
produce individuals different from the normal type and like the part of
the plant from which they came and in which these differences persist
during the life of the cutting, or at least for a long time, but do not involve
genetic change. This phenomenon Molisch ( 1930 ) termed topophysis. A
familiar example occurs in Araucaria (p. 189), where the flattened, dor-

Differentiation 215

siventral character of the lateral branches persists in cuttings made from
these branches. All these cases of persistent differentiation are of particu-
lar interest in providing material for a study of the cause and character of
differential change.

The origin of differences arising at different times in a repeated cycle,
rather than at a different place on the plant, Seeliger (1924) has termed
cyclophysis.

DIFFERENTIATION IN RELATION TO ENVIRONMENT

Most of the examples of differentiation thus far cited seem to be pri-
marily the expression of a developmental pattern controlled by the genetic
constitution of the individual. Obviously such a constitution cannot op-
erate except in an environment of some sort, for genes control specific
differences in reaction to specific environmental factors. It is therefore to
be expected that differentiation should be greatly influenced by the en-
vironment, both internal and external.

The basis for differentiation itself is provided by the environment, for
the most important contribution that the physical environment makes,
morphogenetically, is to set up a gradient in the organism. This cannot
be done unless the environment itself displays a gradient in direction or
intensity. Fern prothallia, for example, grown in culture on a shaking
machine, and thus exposed equally to gravity on all sides, or on a revolv-
ing table, and thus exposed equally to light on all sides (p. 137), are in a
homogeneous environment which has no gradients, no single direction of
gravity or light. As a consequence the organism produces an amorphous
mass of tissue for it is without a polar axis, the basis for its differentiation.
Such an axis must be induced, at least at the very start, by an asym-
metrical environment.

Environment and External Differentiation. The most obvious relation
between environment and differentiation is in the effect that external
factors have on the form and character of plant organs. Most of the final
part of this book will be concerned with the morphogenetic effects of such
factors. Light influences the differentiation of reproductive and other
structures by its intensity, its wave length, and the duration of its photo-
period. The amount of available water is important in the induction of
xeromorphic structures. Temperature, particularly in early development,
seems to affect the rate of certain processes that are precursors to flower-
ing. Chemical agents, notably growth substances, have a marked influence
on differentiation of all sorts. The discussion of these problems must wait
until later pages. There are a few conspicuous instances, however, where
differentiation obviously is dependent on environmental factors which can
best be described here.

216 The Phenomena of Morphogenesis

One is the general phenomenon of heterophylly, where two or more
widely different types of leaves, usually without intermediate forms, may
occur on the same plant. This difference is most commonly, though not
always, associated with the plant's ability to live either submersed in
water or rooted in the ground with its shoots in the air ( Gliick, 1924, and
p. 330 ) . This may be interpreted as a case of heteroblastic development in
which the manifestations are reversible. It is related to the problems of
juvenile stages and progressive development discussed in the preceding
section.

In many species of the pondweeds (Potamogeton) the floating leaves,
which rest on the surface of the water, are relatively broad and have an
internal structure not unlike ordinary herbaceous foliage, whereas the
leaves borne under water are long, narrow, and membranous, thus being
adapted to live as submerged organs. Somewhat similar differences may
be seen in various "amphibious" plants (p. 332), such as the water butter-
cup (Ranunculus aquatilis) and the mermaid weed (Proserpinaca palus-
tris ) . These species live in environments where part of their foliage grows
in air and part is submersed under water. Under the former condition,
the leaves are relatively broad and well provided with stomata and inter-
cellular air chambers. In the latter they are much dissected and thinner.
These effects of the environment on water buttercup were observed by
Lamarck and played an important part in the development of his theory
of evolution. The relation of differences between the "water" and "land"
forms in such plants to those between juvenile and adult stages has been
discussed by various workers. Burns (1904) believes that the "water"
form of Proserpinaca is the juvenile stage, associated with unfavorable
conditions, and the "land" form the adult type and associated with flower-
ing. He found that only the broad, entire leaves were formed in the
flowering season and only the dissected ones in the winter. Whether all
such cases of heterophylly may thus be interpreted is a question. Vischer
( 1915 ) has called attention to the close relation between certain environ-
mental factors (such as removal of leaves, weak light, damp air, deple-
tion of carbohydrate reserves, and increased soil fertility ) and the produc-
tion of juvenile foliage (see also p. 206). Factors which favor reproduction
tend to produce adult foliage. Under certain conditions a return to the
juvenile condition may be induced (Woltereck, 1928). There is no evi-
dence that the ribbon-like submersed leaves of Potamogeton are juvenile
in type, however. Arber (1919) points out that in Sagittaria (another
"amphibious" plant) the first leaves are thin and ribbon-like even when
the plant is growing out of the water and that they appear at maturity
whenever the plant grows weakly. She believes that an aquatic environ-
ment is not responsible for heterophylly but that the occurrence of hetero-

Differentiation 217

phylly is a necessary prerequisite for the ability of a plant to live in both
aquatic and terrestrial habitats.

Pearsall and Hanbv (1925) have evidence that leaf variation in Pota-
mogeton is due, at least in part, to chemical differences in the soil, and
Gessner ( 1940 ) and Bauer ( 1952 ) relate it to rate of metabolism in the
buds. McCallum (1902) thought that in Proserpinaca the water type of
leaf arose primarily because of reduction in transpiration. H. Jones ( 1955)
has made extensive studies of the differences in development of the pri-
mordia that produce the linear and the ovate leaves of Callitriche and
the conditions under which these are formed.

There are many instances where, instead of the permanent induction
of structures at certain ontogenetic levels, there may be reversion to earlier
stages under certain environmental conditions. This is especially frequent
in those cases where juvenile stages are adapted to different environments
than are the adult ones. A commonly cited example is that of Campanula
rotundifolia, which has rounded juvenile leaves adapted to weak light,
although the mature leaves are linear. A mature plant grown in low
illumination will often revert to the juvenile type of foliage. Seedlings,
even in strong light, however, bear nothing but juvenile foliage. Often
wounding will bring about such reversion, as in shoots growing from in-
jured regions of certain pines, which for a time bear foliage like that of
the seedling. With many perennials there is a partial return to the juvenile
stage at the beginning of each growing season.

Frank and Renner (1956) found that in Hedera helix chemical treat-
ments of various sorts did not induce reversion to the juvenile state but
that cold shocks and X irradiation did so. De Zeeuw and Leopold ( 1956 )
were able to induce flowering by auxin treatment in juvenile plants that
otherwise would not have flowered. They suggest that the completion of
the juvenile phase may be due to the accumulation of a sufficient auxin
level. Robbins ( 1957 ) has shown the effectiveness of gibberellin in ju-
venile reversion. Allsopp ( 1955 ) attributes heteroblastic differentiation
in general to changes, chiefly of size, in the shoot apex following alter-
ation of the water balance ( p. 332) .

Environment and Internal Differentiation. Internal differentiation, also,
may be greatly affected by environmental factors. It is important to recog-
nize that changes that take place in this process are part of an underlying
pattern of relationships among the cells and between them and the en-
vironment.

This fact is made clear whenever such relationships are disturbed. If
tissue like the cortex, for example, is exposed to the outside air by re-
moval of the outer cell layers, structures tend to differentiate at the new
surface which are characteristic for such a position. Thus when Vochting

218 The Phenomena of Morphogenesis

( 1908 ) sliced off a portion of a kohlrabi tuber, the living cells at the new
surface differentiated into a rather typical epidermis in which even
stomata were formed. In roots of the Araceae and air roots of orchids,
where there is no cell division after an injury, parenchyma cells near a
newly exposed surface redifferentiate into thick-walled ones essentially
like those of a normal hypodermis.

Even more complex patterns may be reconstituted under the influence
of a different environment. In the roots of Philodendron Glaziovii there is
a row of brachysclereids a few cell layers below the surface. After the
experimental removal of the outer tissues, a similar row of thick-walled
cells differentiates at about the same distance below the new surface
( Bloch, 1926 ) . In the air root of Monstera, the cells of the cortex normally
remain undifferentiated for a considerable distance back from the tip.

Fig. 8-22. Air root of Philodendron. Below arrow,
normal hypodermal tissue pattern, with layer of
brachysclereids. Above, regeneration of similar
layer below wound. (From Bloch.)

At this point, however, the four or five cell rows next the outside often
form thick, lignified walls and develop into brachysclereids. The differ-
ence between these cells and their unlignified neighbors is not evident at
the last cell division nor can it be traced through any cell lineage. It arises
as these two types of cells become mature. The occurrence of lignification
is apparently related to the position of cells with reference to the surface
of the root and thus probably to such an environmental factor as an
oxygen or water gradient. When a root of Monstera is wounded in such a
manner that the parenchyma cells of the inner cortex are now exposed to
a new, artificially produced surface, they become thick-walled brachy-
sclereids (Bloch, 1944; Fig. 8-22). When Wardlaw isolated the central
core of the shoot meristem by vertical incisions, he observed that the
cylinder of vascular tissue regenerating inside the core developed at a
constant distance from the new surface made by the cuts ( p. 238 ) .
In a few instances where the normal ontogeny may be completed under

Differentiation 219

a given environment, exceptionally favorable conditions will enable the
plant to realize developmental potencies which it never would display
otherwise. Thus Bloch (1935/?) has shown that in Tradescantia flumi-
nensis, which typically has bundle sheaths with only thin-walled cells,
wounding may so stimulate differentiation that thick-walled sheath cells,
similar to those in related species of Tradescantia, may be formed. Here
the ontogenetic cycle has been extended beyond its normal course, either
in reversion to a former evolutionary level or toward the realization of
developmental potencies not yet normally expressed by this species,
though common in related ones.

Often the whole histological pattern may be affected. In air roots of
orchids growing freely, adventitious roots are produced on all sides; but
if the root is in contact with a support, these lateral roots are formed only
next the support, presumably because of differences in moisture or other
factors on the two sides (Bloch, 1935«). Anatomical differences are also
evident in these two root sectors.

In differentiation, the role of specific substances, particularly growth
substances, is important (p. 390). Root-forming substances, shoot-forming
substances, flower-forming substances, and others have been postulated.
That a substance by itself has a specific organ-forming character is prob-
ably too naive a conception, but certainly auxin and various other hor-
mones and growth substances are effective as stimuli which call forth
specific morphogenetic responses in the plant. Auxin influences the growth
of cambium, the development of vessels, and other histological processes.
It also inhibits certain activities. Beneath epidermal cells that regenerate
new shoots (p. 245) vascular tissue often differentiates, presumably because
of a substance coming from the young bud, which thus is able to estab-
lish a connection with the main vascular system. Camus has shown that
buds grafted to pieces of fleshy root in tissue culture induce the differen-
tiation of vascular tissue in parenchyma cells beneath them, and Wetmore
found that auxin alone does the same thing ( p. 405 ) .

In general, environmental factors seem chiefly to affect the later stages
in cellular differentiation and especially the character of the cell wall. The
fundamental pattern of a structure is less affected than are its quantitative
expression and the size and character of the cells that compose it.

What a cell or tissue will do depends in part upon its innate genetic
potentialities and in part upon the environment in which it happens to be.
Cells possess different degrees of reactivity to environmental differences.
In some, this is small, and the fate of the cell is therefore rather fixed and
limited, regardless of its environment. In others its developmental reper-
toire is much wider, and it may be greatly influenced by the conditions
which surround it. It should be remembered that the degree of a cell's
reactivity is not constant but that it may vary with the position that the

220 The Phenomena of Morphogenesis

cell occupies in the whole developmental pattern and in the ontogeny
of the individual and especially that it depends upon the point that the
cell has reached in its own cycle of maturity. The developmental expres-
sion of the genetic constitution of a plant and of its various parts is there-
fore not fixed and constant but is continually changing.

PHYSIOLOGICAL DIFFERENTIATION

All differentiation, of course, has its basis in the physiological activities
of living substance, but it can usually be recognized most readily when
these activities result in the production of visible differences in structure.
It is such differences that have chiefly been considered in the preceding
pages. Physiological differentiation itself, however, can often be demon-
strated, and experiments in this field offer hope for the solution of many
developmental problems. A few typical examples will be discussed briefly
here and others in later pages.

The diversities in structure between root and shoot are doubtless the
expressions of fundamental physiological differences. One of the most con-
spicuous of these is in vitamin synthesis. By culture methods it is possible
to grow roots indefinitely from a bit of root tip. Such root cultures must
be provided with the necessary mineral salts and also with a source of
carbohydrates (usually sucrose). These alone prove to be not enough to
secure indefinite growth, and they must be supplemented by small
amounts of certain vitamins, in most cases thiamin. It is clear, therefore,
that such roots are unable to synthesize this vitamin. Since thiamin is
known to be present in the shoots of plants, this is evidently the region
in which it is produced. In nature, roots must obtain their supply from
the shoots. Just when this physiological differentiation first occurs is not
known, but it is probably at the time when root and shoot are set apart
in early embryology.

It has been shown that root and shoot also differ in their ability to
synthesize certain alkaloids. Tobacco shoots can be grafted onto tomato
roots, and leaves and stems of such shoots are free from nicotine (Daw-
son, 1942). If tomato shoots are grafted on tobacco roots, however, the
tomato tissues contain large quantities of this alkaloid. It is therefore
obvious that in such cases the capacity to synthesize nicotine is confined
to the tobacco root and is not possessed by its leaves, as has commonly
been assumed. Certain other alkaloids (as quinine) can be shown by such
experiments to be synthesized in both roots and shoots. The fact that a
substance occurs in a certain part of the plant is evidently no proof that
it is formed there. This technique of reciprocal grafting provides a useful
tool for the demonstration of physiological differentiation of this sort.

Differentiation 221

Studies of geotropic reaction of typical roots and stems show that they
are also different in their response to auxin, the growth of roots being
inhibited by concentrations which stimulate growth of stems, a fact which
explains the geotropic reactions characteristic of these two organs. They
differ physiologically in other respects, for Collander ( 1941 ) has shown
that certain cations may be differentially distributed between root and
shoot, sodium and manganese being more abundant in the former and
calcium, strontium, and lithium in the latter.

Differences between vegetative and reproductive phases of the life
cycle are sometimes physiological as well as structural. Many early workers
(Sachs, 1880, 1882) noticed the difference between "blind" and "flower-
ing" stems, the former when used as cuttings producing vegetative growth
only and the latter, flowering shoots. This difference has now been shown
to be related to the presence of some substance or substances which
induce flowering (p. 397). Torrey (1953) reports that three synthetic
substances which inhibit root elongation have specific effects on the ac-
celeration or retardation of the differentiation of xylem and of phloem.

Physiological differentiation must evidently be important in sex deter-
mination, and chemical differences between the sexes have been found
by several workers. By the Manoilov reaction, for example, staminate
and pistillate plants of poplar can be distinguished, as well as "plus" and
"minus" strains of Mucor ( Satina and Blakeslee, 1926 ) . Stanfield ( 1944 )
has described chemical differences between staminate and pistillate
plants of Lychnis dioica. Aitchison (1953) found that in several genera
the sexes were unlike in oxidase activity, this being greater in some cases
in males and in others in females. Hoxmeier (1953), working with Canna-
bis and Spinacia, reports that the tissue fluids of staminate plants are more
acid than those of pistillate ones. In Cannabis, Cheuvart (1954) observed
differences between the sexes in chlorophyll content, especially in the rate
at which this is reduced at the time of flowering. Reinders-Gouwentak
and van der Veen ( 1953 ) found that in poplar the female catkins tended
to stimulate wood formation on the stem below them whereas males did
not, suggesting a difference between the sexes here in the production of
a growth substance.

Regular changes in the physiological activity of the series of successive
leaves on a plant, related to both position and age, have been observed
by various workers. Dormer ( 1951 ) determined the dry weight per unit
of length in successive internodes of Vicia from the apex downward and
found that during the unfolding of the ninth leaf there was a sudden
change in the distribution of the dry-weight increment. The nutritional
history of an internode thus seems to be a function of its position in the
stem. The developing seedling has also been shown to change in its physi-

222 The Phenomena of Morphogenesis

ological character. Rietsma, Satina, and Blakeslee (1953a), by growing
Datura embrvos in tissue culture, have shown that the minimal sucrose
requirement falls steadily from the earliest stages to the mature em-
bryo.

A notable example of physiological ontogeny has been reported by Wet-
more (1954). In the developing fern sporeling the first leaves are two-
lobed. These are followed by three-lobed ones and finally by pinnate
leaves in which an apical cell has appeared. Shoot apices from small fern
sporelings, cultured in mineral nutrients and various concentrations of
sucrose, grew into whole plants. Where the concentration was low, only
two-lobed leaves were formed. Higher concentrations produced three-
lobed ones and still higher, pinnate ones. The normal ontogenetic progres-
sion here thus seems to be related to an increasing supply of sucrose.

Metabolic gradients are marked by various physiological differences,
especially as to the rates of reactions. Prevot ( 1940) observed that respira-
tion in the apical region of the root of several genera was greater than
in the more distal regions. This is not always the case, however, in shoot
meristems (p. 73).

Wardlaw (1952c) has found that the nutritional status of the apical
region in ferns has an important effect on the size and character of the
leaves and stelar structure. Apices that normally produce large and com-
plex leaves and an elaborate vascular system, if reduced in size by poor
nutrition, will form "juvenile" leaves and simpler stelar patterns.

Biochemical differences of many sorts, presumably indicating physi-
ological diversity, can be shown in cells and tissues. Differential staining
reactions are familiar examples of this. Differences in hydrogen-ion con-
centration between cells visibly alike can be shown by the use of indi-
cators. Blakeslee (1921) demonstrated the presence of two chemically
different areas of cells in the petals of certain races of Rudbeckia with
solid petal color by dipping the petals into phenolphthalein. Sometimes
differentiation is shown by the occurrence of natural pigments, as in the
root tips of Phalaris arundinacea where the trichoblasts are pigmented
but the cells that are not to produce root hairs are colorless. Van Fleet's
work on the histochemical differentiation of the developing endodermis
has been mentioned (p. 197). Microchemical tests of various sorts being
out differences between many kinds of cells, even in early development,
such as tannin cells, crystal cells, and latex ducts. Spectrometric demon-
stration of differences in distribution of the nucleic acids are among
notable recent examples of this sort of analysis.

Less work has been done in demonstrating physical differences be-
tween cells. In fern prothallia Akdik (1938) and Gratzy-Wardengg (p.
121 ) found a definite pattern of differences in osmotic concentration over
the surface of the prothallus, and this seems to be related to differences in

Differentiation 223

behavior of these regions in regeneration. In iris leaves Weber ( 1941 )
showed that the first indication of differentiation of stomatal mother cells
is a difference in osmotic concentration.

Much cellular differentiation is due to changes in the cell wall. Boysen-
Jensen ( 1957 ) in a series of papers has demonstrated various wall changes
in the differentiation of root hairs with particular references to the action
of enzymes.

These and many other observations show that morphological differen-
tiation has its physiological concomitants. To explain how these arise dur-
ing development is a major task of the student of differentiation.

DIFFERENTIATION WITHOUT GROWTH

There are a number of instances among the fungi where development
of the fruiting structures does not take place until the vegetative phase
of the life cycle has ended and no more food is absorbed from the en-
vironment. Growth, in the broader sense of the term, is therefore com-
pleted before differentiation begins, and the latter process can be studied
without the complications that are usually involved when growth accom-
panies it. One of the .most notable examples of this is furnished by the
Acrasiaceae, a family of the slime molds.

The vegetative individual in these plants is a single amoeboid cell, or
7ni/xamoeba. These multiply profusely by simple division and live chiefly
on several species of bacteria. They can readily be grown in culture. After
vegetative life has gone on for some time and when external conditions
are favorable, a large number of these myxamoebae, in a group of from
several thousand to about 150,000, begin to move toward a center of
aggregation, streaming in from all sides and piling up into a mass of cells,
the pseud oplasmodium (Fig. 8-23). This is a millimeter or two in length,
is elongate in form, and somewhat resembles a small grub. It is sur-
rounded by a thin sheet of slime. By the time that this aggregation begins,
all vegetative growth has ceased, so that in the life cycle of these plants
growth (in the sense of increase by assimilation) and differentiation are
separate from each other in time.

The process of aggregation seems to be controlled by the production
of a chemotactically active substance, acrasin. The timing and mechanism
of this process have been discussed by Shaffer ( 1957 ) . As to what deter-
mines the origin of these centers of aggregation, however, there is some
difference of opinion. Sussman (1952) believes that a few initiator cells
appear in the population and attract their neighbors into a many-celled
aggregate.

Wilson (1952) presents evidence that aggregation has its origin in a
sexual process, two myxamoebae fusing early in aggregation and estab-

224 The Phenomena of Morphogenesis

lishing a center. Other fusions occur later and are followed by meiosis.
The zygotes can be distinguished by their greater size.

In the pseudoplasmodium the myxamoebae do not fuse but each cir-
culates freely among its neighbors, and the whole mass moves over the
surface of the substratum by means that are not yet clearly understood.
This body of separate cells, however, is not without some degree of differ-
entiation. It is elongated in the direction of its movement, which is toward
the light. The apical end is slightly pointed and lifted above the rest and
is richer in acrasin than the other regions. It is the part of the mass that is

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Fig. 8-23. Dictyostelium. Stages in aggregation of myxamoebae into a pseudoplas-
modium. ( From J. T. Bonner. )

sensitive to the stimulation of light and seems to serve as a directive
center for the whole. A pseudoplasmodium from which the apex has been
removed will stop its motion and settle down at once to form a fruiting
body.

Two groups of cells may be distinguished in the pseudoplasmodium.
Those near the apex and destined to form the stalk of the sorocarp are
somewhat larger than the ones in the posterior region, which will later
form spores. The proportion between these two types is maintained by
a regulatory process irrespective of the size of the whole mass. Some cell
division continues in the pseudoplasmodium but the rate is different in its

Differentiation 225

two regions. If the apical and the basal halves of the pseudoplasmodium
are experimentally separated, each will form a sorocarp, but the one from
the apical half produces the larger spores. Despite these evidences of
the beginning of differentiation, cells in one group can be changed to
resemble those of the other, and every cell apparently is totipotent. If a
few cells are removed from the mass they are no longer subject to its
organizing control, and if food is present, they will become vegetative
cells again and proceed to multiply.

That the pseudoplasmodial axis is polarized is shown not only by the
difference in structure of its two ends but by their behavior. K. Raper
(1940Z?) performed a series of grafting experiments between plasmodia
that could be distinguished by their color, one group having fed on red
bacteria. The apex, if cut off and placed at the rear of another plasmo-

DICTYOSTELIUM DISCOIDtUM

Fig. 8-24. Migration of the pseudoplasmodium and formation of the sorus in Dictyo-
stelium discoideum. (From ]. T. Bonner.)

dium, will not fuse with this one but will start off by itself. It fuses
with the apical end of a decapitated plasmodium (Fig. 6-15). If an
apex is cut off and placed next the side of an intact plasmodial mass it
will attach itself there and finally draw off a considerable mass of cells
and establish a separate plasmodium. The tip of the mass sometimes
splits, and in this case two are formed. If two happen to come together,
they may fuse into a single one of double size.

Morphogenetically the most significant part of the life history is the
formation of the stalked fruiting body, or sorocarp. After a few hours of
migration, or when a pseudoplasmodium reaches drier surroundings, it
stops moving and attaches itself firmly to the substratum by a disk of dif-
ferentiated cells (Fig. 8-24). The cells of the apical region, from which
the stalk is to be formed, become large and vacuolate and each is en-
closed in a cellulose sheath. As this is happening, they are pushed down
into the pseudoplasmodium by other prestalk cells climbing up around

226 The Phenomena of Morphogenesis

them which in turn become stalk cells (Fig. 8-25). As Bonner describes
it, "The process is the reverse of a fountain; the cells pour up the outside
to become trapped and solidified in the central core which is the stalk.
In so doing the whole structure rises into the air until all the prestalk
cells have been used up." This description applies to the species most
commonly studied, Dictyostelium discoideum. In D. mucoroides and D.
purpureum, however, the stalk begins to be formed during the brief
migration of the pseudoplasmodium.

About 10 per cent of the myxamoebae take part in the formation of
disk and stalk. The others, still moving freely over one another, follow
the growing tip of the stalk upward in a body and (in Dictyostelium)

O Undrfferer*oled
© Supportive
Spores

n

Fig. 8-25. Dictyostelium discoideum. Diagram of sorocarp formation. A, B, migrating
pseudoplasmodium. ( From J. T. Bonner. )

form a spherical mass of cells, the sorus, at its summit. Here each myxa-
moeba rounds up to make a dry spore, and these spores are later carried
away by air currents, each now capable of developing into a myxamoeba.
Wilson presents evidence that some mitotic division occurs before spore
formation.

In the genus Polysphondylium there is not only an apical sorus but
several whorls of lateral stalks along the main one, each terminating in
a smaller sorus, so that the sorocarp becomes a structure of considerable
complexity.

These plants, though so unlike higher ones, have constant generic and
specific differences ( Fig. 8-26 ) . If myxamoebae belonging to two species
grow intermingled in the same culture or if pseudoplasmodia of two
species are crushed and experimentally mixed, the cells in time sort them-

Differentiation

227

Polysphon dylium
violaceum

P. pallidum

D. purpureum
Dictyostelium
mucoroides

Fig. 8-26. Sorocarps of various members of the Acrasiaceae. (From K. B. Raper.)

selves out and form sorocarps typical of each species. The specific char-
acter of the sorocarp can be shown to be carried by its spores.

Sussman ( 1955 ) has found a number of mutants of Dictyostelium dis-
coideum in which the aggregating groups, and consequently the size of
the sorocarps they form, is much smaller than normal. In some of these
the fruiting body consists of as few as 12 cells but it still retains the form,

228 The Phenomena of Morphogenesis

proportions, and cellular structure of the larger ones, surely a remarkable
example of the inherent formativeness of these cells. Here form deter-
mination finds one of its simplest expressions. The behavior of the myxa-
moebae in the Acrasiaceae reminds one of the well-known instance among
the sponges where the entire body may be separated into its constituent
cells and these later will come together and re-form the body of the
sponge. The mechanism by which such morphogenetic movements occur
in the slime molds and sponges presents some of the most baffling prob-
lems in biology.

The Acrasiaceae have been studied intensively in recent years. For more
detailed accounts of experimental work on them the reader is referred to
the publications of Bonner, Raper, Shaffer, Sussman, and Wilson, some
of which are listed in the bibliography. The field has been reviewed by
J. T. Bonner (1959).

A somewhat similar example of the differentiation of a formed struc-
ture by a mass of undifferentiated cells is shown by a specialized family
of bacteria, the Myxobacteriaceae. This is a group in which the individual
is a rod-like cell which divides by transverse fission, it lives on other
bacteria. In the vegetative period these cells may be distributed through-
out a colonial mass or may occur in radiating strands or ridges. Myxo-
bacteria do not possess flagella, but their gliding or creeping movements
are in some way associated with the abundant slime that they secrete. In
the fruiting phase the individuals aggregate into masses, probably under
the chemotactic influence of an acrasin-like substance, but no true pseudo-
plasmodium is formed. In simple types the aggregates are merely rounded
mounds, but in forms like Chondromyces crocatus complex stalked and
branching systems are formed. Here, as the rods move upward, piling on
top of one another, the mass is constricted at the base and the layer of
slime secreted by the advancing rods hardens into a stalk. The apical
mass of cells continues to move upward and divides to form branches
which culminate in multicellular cysts. In the production of these com-
plex fruiting structures by the migration of individual cells, and in the
specific character which these structures display, the Myxobacteriaceae
resemble the Acrasiaceae, though the groups are not closely related. The
same morphogenetic problem as to how a specifically formed structure is
produced by independent and undifferentiated cells is presented by both
groups of plants.

A general account of the Myxobacteriaceae has been written by Quin-
lan and Raper for Volume XV of the "Encyclopedia of Plant Physiology."

Another case resembling these but involving much larger size and a
higher level of organization is to be found in the development of the fruit-
ing body in the fleshy fungi, such as the common mushroom, Agaricus
campestris. The vegetative body here is a much branched mycelium which

Differentiation 229

absorbs food from the organic matter in the soil. When it has a good
supply of this, and other conditions are also favorable, the mycelial mate-
rial is mobilized into a rounded mass just below the surface of the ground.
This develops into a "button" and then into the familiar mushroom fructi-
fication, with its high degree of differentiation. This is composed not of
a mass of cells that are attached in a firm tissue, as in the higher plants,
but of a body of tangled hyphae, free to slide past each other. As the
stalk increases in length, these hyphae tend to be oriented parallel to
its axis, though at the base and in the pileus ("umbrella") they remain
much tangled. Growth takes place primarily by elongation of the cells of
the hyphae and is entirely at the expense of food already available in the
mycelium. How, from such an apparent chaos of snarled threads, the
very precisely formed fruiting body of the fungus grows and differen-
tiates poses the same difficult problem as does the development of the
sorocarp in the Acrasiaceae, and one lying at the heart of the morpho-
genetic process. Bonner, Kane, and Levey (1956) have reexamined the
development of Agaricus and confirmed and extended the results of the
classic studies of de Bary, Atkinson, and Magnus, but the problem has
attracted relatively little attention in recent years. The development of
these fungus fruiting bodies, however, offers to the student of the prob-
lems of differentiation and form determination some of the most promising
material available for his work.

CHAPTER 9

Regeneration

In the preceding chapters there have been considered those morpho-
genetic phenomena which manifest themselves in normal development.
Polarity, symmetry, differentiation, and the wide variety of correlative
manifestations evident as the plant and its parts progress from embryo to
maturity are all indications of the orderly control of growth processes
which is the visible aspect of biological organization. But the progress of
development is not always unimpeded. Accident and injuries of various
sorts may happen to the growing plant which remove a part of its tissues
or divide it into two or more incomplete portions. In nature this may
result from the attacks of fungi, insects, or higher animals; from mechani-
cal injuries of many sorts; or from unfavorable conditions which impede
the functions of its organs. The changes that follow such injuries, losses,
or functional disturbances often throw much light on morphogenetic
activities, and one of the most fruitful methods of studying developmental
processes has been to observe the consequences which follow their ex-
perimental disturbance. Indeed, this is the only way at present by which
many of these processes can be investigated at all.

This field of morphogenetic research is not as active today as it was in
earlier years, and many of the most important papers in it go back to
some decades ago. For a review of the earlier literature the student is
referred to McCallum (1905), Kupfer (1907), and Goebel (1908). Ban-
ning ( 1955 ) has discussed some of the recent work.

An important fact which such studies reveal is that the organism shows
a tendency to restore or replace parts that have been removed and thus
to produce again a complete individual. To this general process, which
includes a wide range of developmental phenomena, the term regenera-
tion is commonly applied. Regenerative activities are much more common
in plants, with their less highly organized bodies, than in animals and can
often be subjected to a more complete developmental analysis.

Regeneration can be brought about not only by the removal of a part
but by isolating it physiologically from the rest of the plant. In a young

230

Regeneration 231

bean plant, for example, if the epicotyl is decapitated the buds in the
axils of the cotyledons will grow into shoots, thus replacing the leafy
shoot that would have grown from the epicotyl; but these buds may also
be induced to grow by chilling a portion of the epicotyledonary stem and
thus preventing the interchange of stimuli or substances between it and
the tissues below ( Child and Bellamy, 1919 ) .

In general, the more simple and undifferentiated a plant is, the more
completely will it restore missing parts; and the more specialized and
differentiated it is, the less regenerative capacity it will show. Early devel-
opmental stages are thus more likely to regenerate readily than later ones,
and groups lower in the phylogenetic scale than those of higher position.
Ability to regenerate is often completely lost.

The origin of regenerative powers in plants and animals is sometimes
explained as the result of natural selection, much as in the case of other
traits. That a long process of competition and selection conferred the ability
to repair almost every type of injury seems unlikely. However this may
be, the developmental activities in regeneration are not essentially dif-
ferent in their origin and control from those which occur in normal de-
velopment. In both, the production of a single, complete individual is the
final result. The factors involved in regeneration seem neither more nor
less difficult to understand than those in normal ontogeny, nor do they
require a fundamentally different explanation. Both are manifestations of
general developmental control, a fundamental self-regulation in the indi-
vidual. Both seem to be the result of the same formative process.

Begeneration is a term that has been variously defined. The author pro-
poses to use it here in the broadest sense, as the tendency shown by a
developing organism to restore any part of it which has been removed or
physiologically isolated and thus to produce a complete whole. This
covers processes from wound-healing to the reproduction of adventive
structures and vegetative multiplication, in which many different activ-
ities are involved.

In general, the method of restoration of lost parts is different in plants
and in animals. Animal tissues are composed of thin-walled cells, usually
able to divide and often to migrate. Most plant cells at maturity are
relatively thick-walled and ordinarily do not divide or grow further,
though it has been shown that many retain the power to do so. Begenera-
tion in animals, therefore, consists largely in a reorganization of the re-
maining portion of the organ or body. In plants, on the contrary, this type
of regeneration is limited to meristematic or rapidly growing regions or
to the relatively rare cases where cells become embryonic again. Much
more commonly, at least in the higher types, replacement of lost parts
results from the growth of dormant buds or primordia or the development
of new ones. Such primordia arise from cells in the plant body which

232 The Phenomena of Morphogenesis

remain alive and are potentially meristematic. These primordia, often very
numerous, remain dormant under ordinary conditions.

This fact raises the question of what it is, if these primordia are
capable of growing and forming new organs, that prevents them from
doing so. The concept of the organism as a balance between stimulatory
and inhibitory factors suggests itself here, but the problem remains as to
what localizes and correlates the activitv of these factors so that a specific
organic system is established, maintained, and restored, and what stops
the regenerative process when this has been accomplished.

It should be remembered that, in spite of modifications acquired during
the process of differentiation, all the cells are probably identical geneti-
cally, save for occasional polyploidy. The potentially meristematic cells
thus serve, so to speak, as a "germ plasm" or genetic reserve which can
direct the processes of regeneration and further development. Each cell,
at least in theory, is capable of producing an entire individual.

In regeneration, mature or nearly mature cells may sometimes become
embryonic again and then undergo changes that restore a disturbed tissue
pattern. How this is accomplished is of much interest for morphogenesis.
In it the first visible step is usually a marked increase in the amount of
cytoplasm and in the size of the nucleus and an acceleration of metabolic
activity. The wall also tends to become thinner. This process, commonly
termed dedifferentiation, has been described and the literature reviewed
by Buvat ( 1944, 1945, 1950 ) . Dedifferentiated cells assume the character
of meristematic ones and can divide and grow. The tissue thus formed
may then differentiate again in conformity with its new function or
position in the regenerated structure.

REGENERATION IN THE LOWER PLANTS

Among the thallophytes and bryophytes, with their simpler bodies and
lower level of organization, regeneration is relatively common. It will be
discussed briefly in these groups before taking up the more complex
aspects of it that vascular plants display.

In most of the lower plants single cells or groups of cells have the
ability to develop readily into a whole plant, and in many instances they
do so regularly as a means of vegetative reproduction. Extreme instances
of this are the conversion of vegetative cells into specialized nonsexual
reproductive cells such as zoospores and others.

Even when not thus differentiated for reproduction, the cells of many
algae are readily separable from the loosely organized thallus and grow
into new plants, as in Callithamnion (Weide, 1938) and Cladophora
(Schoser, 1956). In the last genus the cells may be separated from one

Regeneration 233

another by plasmolysis, and each then grows into a new plant. Among
simpler fungi almost any adult cell on isolation will give rise to a new
mycelium. Kerl (1937) found that single cells from the surface of
Pi/ronema confluens would do this. Such instances could be multiplied
almost indefinitely.

Individual cells, if injured, will often restore themselves, especially large
ones like those of Vaucheria ( Weissenbock, 1939 ) , Dasijcladus ( Figdor,
1910), and Acetabutoria (Hammerling, 1936) or the coenocytes of Bryop-
sis and Caulerpa ( Janse, 1910; Winkler, 1900; Dostal, 1926). In such algae
as S-phacelaria, which grow by an apical cell, this cell may be replaced,
if injured, by the cell next below it, which first undergoes considerable
reorganization (Zimmermann, 1923). Other cases have been described.
Hofler (1934) observed in the filamentous alga Griffithsia that, if a cell
dies, the one above it will send a tube either through it or around it
which makes connection with the cell below and thus restores the con-
tinuity of the living filament.

In the early development of certain animal embryos, if one of the first
two blastomeres is killed, the other develops into an entire organism. A
somewhat similar instance in plants occurs in Fucus. Here, after the fer-
tilized egg has formed two cells, an apical and a basal (rhizoidal) one,
the apical cell will produce a new rhizoid at the basal pole if the first is
destroyed (Kniep, 1907). Setchell (1905) in his studies of the kelps de-
scribes the way in which a stipe, if the blade is cut off from its tip, will
regenerate a new one from the cut surface. This commonly happens in
nature where these plants are buffeted by the waves, for there has devel-
oped an intercalary meristem near the leaf base which becomes active
when the blade is removed. Killian ( 1911 ) describes the way in which an
injured stem is reconstituted in Laminaria digitata.

Some of the most remarkable cases of regeneration occur in the fruiting
bodies of the fleshy fungi— toadstools, mushrooms, bracket fungi, and
similar types. These are formed from masses of tangled hyphae which do
not adhere to their neighbors as do cells in higher plants but are merely
packed together in a weft of tangled threads. Even so, they tend, if in-
jured, to restore the missing portions and produce a normal sporophore.
This has been observed in Stereum by Goebel (1908), in Agaricus by
Magnus (1906), and in other fleshy fungi. Under favorable conditions
almost any part of one of these fruiting bodies will restore portions of its
tissues that are removed. Such structures provide promising material for
studies in regeneration. Brefeld and Weir maintain that every cell of
C&prinus has the potentiality of producing an entire sporophore.

Among bryophytes, the hepatics regenerate with particular readiness.
Early work with these plants has been reviewed by Correns ( 1899 ) . The

234 The Pnenomena of Morphogenesis

process here is a common means of reproduction. In Sphoerocarpos,
Rickett (1920) found that regeneration occurs from single cells (or some-
times groups of adjacent cells) from almost anywhere on the thallus. At
first the mass of cells is globular, cylindrical, or ribbon-like but it soon
develops into a typical thallus much as does a germinating spore.

In a study of vegetative reproduction in Metzgeria, Evans (1910) ob-
served that certain cells on the thallus dedifferentiate and that each then
grows into a gemma from which a new plant arises. The distribution of
these regenerative cells is not a random one, however. A robust thallus
produces no gemmae, and they are fewer in plants that bear sex organs.
If the apical region is very active, there are no gemmae near it. If a piece
of thallus is isolated, however, gemmae arise in it abundantly. Evidently
there are factors in this plant that tend to inhibit regeneration by its cells.

Plantlets are frequently produced from single cells in the leaves of
Jungermanniales, and here they often, though not always, develop much
as spores do. It is sometimes difficult to tell whether they come from ordi-
nary vegetative cells or from ones that are predisposed to produce them.
Fulford ( 1944, 1954 ) has described many cases of reproductive regen-
eration in these plants.

Many mosses also regenerate readily. The early work here has been
reviewed by Heald (1898). Protonemata and, from these, new plants arise
on the stem of some mosses but rarelv from the leaves unless the latter

J

are detached (Gemmell, 1953). Here they grow chiefly from the surface
cells of the midrib.

Morphogenetically, the most significant aspect of moss regeneration is
that under appropriate conditions protonemata develop not only from
the gametophyte but from sporophyte tissue, both seta and capsule, and
thus are diploid. From these diploid gametophytes, tetraploid sporophytes
can be produced. This possibility was first discovered by the Marchal
brothers (1907-1911) and opened up a wide field for exploration. Its
genetic and physiological aspects have been explored by F. von Wettstein
(1924) and his students (p. 437). In several cases (as by Springer, 1935,
with Phascwn ) sporogonia have been observed to develop directly and
apogamously from diploid gametophytes without a sexual process. Still
more remarkable, Bauer (1956) observed that diploid protonemata of
another moss, Georgia pellucida, under certain conditions form buds
which do not develop into leafy gametophytes, as ordinarily happens in
such cases, but produce sporogonia directly. Spores in these develop
rarely, but when they do they germinate into normal haploid protonemata.

Regeneration of diploid gametophytes from sporophytes of Anthoceros
was accomplished by Rink (1935) through cutting away portions of the
sporophyte. Here the diploid thalli are smaller and more irregular in
shape than the haploid ones.

Regeneration 235

REGENERATION IN THE HIGHER PLANTS

Among vascular plants there is a much higher degree of differentiation
than in lower forms and as a consequence the processes of regeneration
are more complex. In these plants we may recognize, for convenience,
three rather different types of regenerative activities. Reconstitution, or
regeneration proper, includes those cases in which, as in animal regener-
ation, there is a reorganization of the embryonic tissue by which its orig-
inal structure is re-formed. This is usually limited to truly embryonic
regions, such as growing points and young embryos, and to structures
where there is a reorganization of the tissue pattern by dedifferentiation
and subsequent redifferentiation. Restoration describes the wide range
of cases where missing tissues or organs are replaced through meri-
stematic activity arising in adjacent regions. This may result from the
activation of dormant buds or primordia already present or in the forma-
tion of new ones such as occurs in the origin of new roots and shoots in
the familiar processes of vegetative propagation. Reproductive regener-
ation, or vegetative reproduction, involves the separation, by natural
means, of a part of the vegetative body from the rest and its establishment
as a new plant, a process which often occurs in the lower groups. Similar
cases are those where plantlets develop on the leaves and drop off to form
new individuals. These are all specialized instances of the ability of the
plant, under favorable conditions, to produce a new whole from a part
of its body, an ability that comes from the totipotency of its various
members.

Reconstitution

This process, the reorganization of living material by which the normal
structure is restored when disturbed by outer circumstances, is relatively
uncommon in plants, since truly embryonic conditions persist in them for
only a relatively short time before changing into a mature state where
reorganization is difficult. Such reconstitution as does occur is of two
sorts. In one, truly embryonic or meristematic tissues may be reshaped
into a new whole. In the other, tissue already well along toward maturity
may undergo a certain degree of dedifferentiation and redifferentiation
so that its structure is reorganized and the original pattern, at least in
part, reconstituted.

Meristematic Reconstitution. Among the simplest cases, and one which
not infrequently occurs in nature, is cleavage polyembryony. In many
conifers (Buchholz, 1926), though less commonly in angiosperms, the
early embryo rudiment, carried down into the endosperm at the tip of
the suspensors and still consisting of only a few cells, divides and de-

236 The Phenomena of Morphogenesis

velops into two or more parts (Fig. 9-1). These all grow for a time but
usually only one survives and develops into the embryo of the seed. A
portion of the original embryo thus reconstitutes a complete whole. This
recalls the not infrequent cases among animals where one fertilized egg
produces two or more individuals (as in identical twins) or where a
single blastomere, experimentally isolated, will form a whole.

Fig. 9-1. Cleavage polyembryony
in Torreya. This group of young
embryos have all come from a sin-
gle fertilized egg by cleavage.
(From Buchholz.)

It is with the terminal meristems of the older plant axis, however, that
most of the experimental work on regeneration has been carried on. In
roots it is generally agreed by observers that if only the extreme tip is
removed, about y2 to % mm., a new growing point will regenerate di-
rectly at the wound surface from the underlying tissue of the plerome. If
a little more is cut off, regeneration is only partial and chiefly by the for-
mation of new growing centers in the outer portion of the root. If still
more is removed, true reconstitution ceases and a callus is formed with

Regeneration 237

adventitious roots growing out from it. The early papers of Prantl (1874)
and Simon ( 1904 ) on angiosperms and of Stingl ( 1905 ) on gymnosperms
present the basic facts, which have been reviewed by Nemec ( 1905 ) .

More recently Torrey ( 1957Z? ) has studied the regeneration of decapi-
tated roots grown in culture media and as affected by auxin. If an abun-
dance of auxin was present, the vascular cylinder of the new roots was
hexarch instead of the normal triarch. Such a root reverted to triarch
again if returned to the usual medium. Torrey interprets these changes
as due to the direct effect of auxin on the size of the meristematic tip,
the structure of which evidently is not determined by the mature tissue
farther back.

If the young root is split lengthwise, scar tissue forms on the inner
portion of the cut surface but each tip will become reorganized into a
new and complete meristem and will finally reconstitute a normal root
(Lopriore, 1892). This argues against the idea that there is a single apical
cell in the root. Ball ( 1956 ) split the hypocotyl tip of a Ginkgo embryo
and found that the effect of this was evident for some distance upward
in the epicotyl in the differentiation there of a divided vascular cylinder.

In the shoot meristem the situation is complicated by the presence of
leaf primordia. Only the terminal dome, about 80 /x back of the actual tip,
will be regenerated if it is removed. The earlier workers believed that a
new apex was formed here, as in the root, by direct growth from the cut
surface, and more recently Mirskaja ( 1929 ) has reported that this occurs
in Tradescantia. Most observers, however, have found that scar tissue
forms over the wound and that one or more new meristems arise at the
edges of this.

Several plants have marked powers of meristematic reconstitution. In
the much reduced aquatic Podostemon ceratophyllum, if the tip of the
shoot is cut off a new one arises from a group of cells just back of the
cut surface in or around a vascular bundle. A decapitated root is recon-
stituted in much the same way (Hammond, 1936). In Zamio, a new shoot
will often grow out directly from the stump of an old one, usuallv from
the region of the central cylinder (Coulter and Chrysler, 1904). Such
simple and direct regeneration in plants is rare.

Karzel ( 1924 ) and others split growing shoot tips and found that each
half regenerated more or less completely, depending on the species.
Pilkington (1929) split simply the terminal meristem itself and observed
the same result. From the tissue of dodder which remains within the host
plant after the external portion of the parasite has been experimentally
removed, Truscott (1958) observed the regeneration of a shoot meristem
which pushed out through the surface and developed into a normal
dodder shoot.

Much experimental work on the regeneration of the shoot apex has

238 The Phenomena of Morphogenesis

been done by Ball in Lupinus and Tropaeolum and by Wardlaw in
Primula and several ferns. Ball ( 1948, 1952« ) went still further than
Pilkington and was able to split the meristematic apex into four, and later
even into six, strips ( each still connected basally with the axis ) and found
that each was able to reconstitute a whole shoot unless its tip had been
reduced below a minimal size. Vascular tissue tended to be poorly devel-
oped in it until leaves were formed by the new shoot.

Both Ball ( 1952/? ) and Wardlaw ( 1950 ) isolated the central core of the
shoot meristem from the rest of the axis by three or four longitudinal in-
cisions (Fig. 4-14), thus leaving the meristematic dome (or the apical
cell and its neighbors) connected with the vascular tissues below only
by a plug of pith tissue. Both investigators found that this isolated tip
continued to grow and in time produced procambial tissue independent
of that in the axis below. In the flowering plants studied this differen-
tiated basipetally and finally joined the vascular system of the main axis.
In the ferns, however, it did not do so. At the apex of the isolated core
new primordia were formed and (except in ferns) if this core was not
below a minimal size, it finally developed into a normal leafv shoot.
Wardlaw observed that the phyllotaxy of the new shoot in Primula was
continuous with that of the original axis but in Ball's material it was inde-
pendent and often showed reversal of the earlier spiral. Wardlaw ob-
served that the vascular tissue developing in the central core followed the
outline of the cut piece and differentiated at a rather constant distance
from the cut surface, suggesting that its position was dependent on a
gradient of some sort (Fig. 9-2).

These experiments are of morphogenetic interest since they show that
the apical meristem is a self-determining region which can produce a nor-
mal shoot without any connection, other than through undifferentiated
pith cells, with the tissues below. Furthermore, Ball (1946) and others
have shown that small meristem tips, growing in tissue culture, will pro-
duce entire plants. All this is not surprising, however, since many cases
are known where a single cell (p. 253), without any vascular connection
with other tissues at first, develops into a fully differentiated plant. It is
to be expected that an active terminal meristem would do the same. Al-
though the differentiated tissues below the meristem may not be necessary
for its growth, they contribute to the character of its development, for
through them come water, nutrients, and various morphogenetically im-
portant substances. The terminal meristem seems neither to be completely
self-determining nor completely under the control of the rest of the plant,
but the two act together as an integrated system.

Reconstitution of parts other than the meristems of the axis has often
been reported. In a number of ferns such as Gleichenia, the leaf grows
at the tip by a terminal meristem, thus perhaps harking back to the time

Regeneration 239

when the leaf was a lateral branch of indeterminate growth. In most fern
leaves, unlike those of angiosperms, growth continues longest at the tip
and in some species the leaves root readily there. It is thus to be expected
that fern leaves should sometimes reconstitute new tips if the old ones
are injured or removed. Goebel (1908) with Polypodium and Figdor
( 1906) with Scolopendrium cut away a small bit of tissue from the grow-
ing leaf tip and found that this meristematic region was reconstituted
but that a double or forked lamina was produced.

Fig. 9-2. Diagram of transverse section of apex of Primula in which a central plug of
pith was isolated by four vertical incisions ( broken lines ) . In this plug a new vascular
cylinder has been regenerated at a constant distance from the surface. (From Ward-
law.)

Among higher plants, leaves of some of the Gesneriaceae are easily re-
generated. In Saintpaulia and some species of Streptocarpus, Figdor
( 1907 ) split a young leaf nearly to the base along the midrib and found
that a considerable amount of new lamina was regenerated from the
basal part of the cut surface, which is the latest to mature. If the blade is
removed from a young primary leaf of Cyclamen, two new blades re-
generate by reconstitution of the meristematic region at the sides of the
petiole apex (Winkler, 1902). Figdor also reported (1926) that if the

240 The Phenomena of Morphogenesis

terminal leaflet of the pinnately compound leaf of Bryophyllum (Kalan-
choe ) was cut off when the leaf was very small, it was partially regener-
ated. Other cases of such regeneration have been reported, but the leaf,
doubtless because of its generally determinate growth, shows meri-
stematic reconstitution much less readily than does root or stem.

Gametophytes sometimes display this type of regeneration. Albaum
(1938rt), confirming earlier workers, found that if the ordinary prothal-
lium of certain ferns is cut transversely the anterior portion, near the
meristematic notch, will re-form the typical heart-shaped structure again.
In the posterior region this does not happen, but new adventive pro-
thallia are produced from the cut surfaces (p. 121). Meyer ( 1953) reports
that the meristematic region in the notch of the prothallus, and particularly
its apical cell, seems to inhibit the formation of other apical cells; for if
the prothallus is divided lengthwise into three parts, the central one,
which includes the apical cell, will regenerate its lost portions whereas
the two lateral pieces will each first produce a new apical cell and then
proceed to develop into typical prothallia. True reconstitution of a meri-
stematic region thus seems to be limited to very early developmental
stages. In later ones, even though the tissue may still be meristematic, it
has lost some of its morphogenetic potencies and injury will result either
in simply a wound reaction or in the production of new adventitious
growing points rather than in a remolding of the old one.

Reconstitution of Tissue Patterns. A somewhat different type of recon-
stitution occurs where the structure that is removed is not a meristem but
a part already differentiated, at least to some degree. To restore the dis-
turbed tissue pattern involves a more complex process and is rarely as
complete as the reconstitution that occurs in a meristem. Where mature
or nearly mature cells are part of this pattern, some of these cells must
evidently become embryonic again and assume a new function in the
reorganized system. There are some remarkable examples of this which
provide particularly interesting morphogenetic problems.

The first step in such a reconstitution is healing of the wound itself.
Wound reactions differ with the type of plant and the conditions. Cells
near the wound surface generally become more active and soon, under
the influence of wound hormones, cell division is initiated parallel to the
surface. A phellogen here develops which forms a layer of protective cork
over the wound. In many cases this is all that happens. Sometimes a callus
is formed here and from it primordia of roots and shoots may develop.
The phenomena of wound reactions have been reviewed by Bloch ( 1941,
1952). Fourcroy (1938) has discussed the same subject and particularly
emphasizes the accelerating influence of wounding on differentiation and
its effects on vascular anatomy.

In many plants, however, the tissues under the wound may be reorgan-

Regeneration 241

ized to some degree. This is especially true of the epidermis. In kohlrabi
Vochting (1908) observed that when the layer of wound cork was
sloughed off an epidermis had developed under it which was essentially
identical with that of the normal tuber and in which typical stomata
were present. Cells destined to be cortical in character had been radically
altered to form a tissue appropriate for their new position in the system.

Fig. 9-3. Vascular strands a and b regenerating in parenchymatous tissue to connect
strand G with others; c, an earlier stage in this process, where procambial strands are
being differentiated. (From S. Simon.)

Such reconstitution has been reported by others. The cuticle of epidermal
cells may also be regenerated if it has been sliced off ( Fritz, 1935 ) .

More deeply seated tissues may be regenerated by the ^differentiation
of others, as is the exodermis in air roots of orchids ( Kiister, 1899; Bloch,
1926, 1935b) and hypodermal sclerenchyma (p. 218) in air roots of palms
and Araceae (Bloch, 1937, 1944). In every case these newly developed

242 The Phenomena of Morphogenesis

tissues are appropriate in character for the place where they now are and
are much like those normally present in such regions.

Somewhat more complex is the redifferentiation of vascular bundles
in places where these have been severed. Simon (1908; Fig. 9-3), Nemec
(1905), Sinnott and Bloch (1945), and Jacobs (1952) have studied this
in various herbaceous stems. If a bundle or group of bundles is severed
by a lateral incision and the region examined in longitudinal section after
a week or two, a new vascular strand can be seen developing behind the
incision and connecting the severed upper and lower ends of the bundle
( p. 193 ) . This strand is formed by the conversion of large, squarish paren-
chyma cells of the pith into xylem cells with reticulate lignified thicken-

Fig. 9-4. Left, regeneration of connection between severed vascular bundles in stem
of Coleus. Right, differentiation of parenchyma cells into reticulate xylem cells in the
development of this strand. Arrow shows the direction of its development. Note
new walls parallel to it. ( From Sinnott and Bloch. )

ings (p. 194 and Fig. 9-4). Differentiation seems always to be basipetal,
suggesting the downward passage of a morphogenetic substance, pre-
sumably auxin, from the upper bundle toward the lower. The regener-
ated strand is not directly at the cut surface but about the same distance
behind it that the normal bundles are from the uninjured surface. Jost
( 1942) caused the plant to form these vascular bridges in manv ways and
finds that, although their general course is basipetal, they may develop
acropetally for a while in passing around an obstacle. They do not always
take the shortest route. The position of the strand seems to be determined
by a gradient of some sort from the wound surface inward. It is significant
that the conversion of parenchyma to xylem is an "all or none" reaction,
with no cells intermediate in character.

Regeneration 243

A somewhat similar regeneration of vascular strands is to be seen in
leaves where some of the veins have been cut. New strands are differen-
tiated in the mesophyll cells which connect the severed ends. Freundlich
( 1908 ) studied the origin of these xylem strands, and Kaan-Albest ( 1934 )
followed the differentiation of new sieve tubes (Fig. 9-5). The latter do
not arise, as do those of the xylem, by conversion of whole parenchyma
cells, but small cells are cut out of the sides of these larger elements and
join up with one another, end to end, from one cell to the next. These

Fig. 9-5. Impatiens. Sieve-tube connections developing between phloem bundles, one
of which has been severed. ( From Kaan-Albest. )

phloem strands in their development suggest the fiber strands of Luffa
(p. 197).

What are the factors, one may ask, that impel the ^differentiation of
a vascular system when intercommunication among its parts has been
interrupted? Auxin may be diffusing from the end of a cut bundle, but
how this operates to convert a series of parenchyma cells into a vascular
strand is difficult to understand. Here is differentiation in very simple ex-
pression. Doubtless the same general factors are involved as in normal
development but the process takes place here on a greatly enlarged scale
where it can be more readily studied than in the very small-celled tissues

244 The Phenomena of Morphogenesis

near the meristem. Regenerative tissues of this sort are particularly prom-
ising material for a study of cytological differentiation.

These are examples of the relatively simple reconstitution of a tissue
pattern. A much more involved one is that described by Vochting ( 1908 )
in his classic studies of regeneration in kohlrabi. If a young and growing
tuber of this plant was cut transversely at about half way from the tip to
base, care being taken not to injure the leaves on the basal portion, the
cut surface of this portion soon began to swell and by the end of the sea-
son had developed a convex, rounded structure which in some cases
restored the general form of the normal tuber except that no leaves de-
veloped on its surface. Internally, however, the complex system of bundle
connections in the reconstituted half was hardly to be distinguished from
that of the original portion. This provides the most remarkable example
so far described of a structure already well differentiated internally which
proceeded to reorganize itself and reconstitute, in almost its original form,
a large mass of tissue. There was meristematic activity here, following
the dedifferentiation of much of the structure near the cut surface, but it
was diffuse meristematic activity like that of a leaf or fruit rather than
that of a localized growing point. Studies on regeneration in this very
promising material have been largely neglected in the half century since
Vochting's description of his work was published.

Restoration

Most regeneration in plants is not due to the reorganization of em-
bryonic regions but to the onset of meristematic activity in regions ad-
jacent to the place where loss has occurred. This leads to the production
of substitute structures that restore the original whole by indirect means.

These processes are examples of compensatory correlation (p. 98) in
which the balance of the organism is restored after being disturbed. As
redifferentiation after injury often throws light on the problems of differ-
entiation and tissue pattern, a study of the restoration of lost structures
offers a useful means of analysis of developmental potencies and the proc-
esses of correlation.

In many cases, as the result of wounding, a callus is produced (p. 288)
at the cut end of a stem or root. This often originates from the cambium
but may come from other tissues. From such calluses primordia of roots
and shoots commonly arise. This is the most frequent type of regeneration
in the higher plants and underlies the horticultural arts of multiplication
by vegetative propagation, chiefly the rooting of cuttings. This field has
been reviewed from the botanical point of view by Priestley and Swingle
(1929) and Swingle (1940, 1952).

Almost every plant organ has been used as a cutting— stem, root, leaf,
hypocotyl, floral axis, and flowers— and all have been found to have some

Regeneration 245

ability to restore lost parts. The axial organs-stem and root-are the ones
most commonly employed in the practices of propagation and have been
most thoroughly studied.

Stem Cuttings. In stem cuttings of dicotyledons buds develop most fre-
quently at the apical end and roots from the basal one (p. 119) but this
polarity varies considerably. The buds may be the usual axillary ones,
many of which would not normally develop, or they may be accessory
buds. If these are absent, dormant primordia may grow. Carlson (1950)
has described the origin and distribution of dormant root initials on
willow shoots. Primordia may also develop anew, from callus or from
the normal tissues of the stem. Adventitious roots in young stems usually
come from the pericycle but in older ones they may have a deeper origin
in the vascular cambium (Plett, 1921). Mahlstede and Watson (1952)
found that adventitious roots in blueberry originate in cambium or phloem
and push out through vascular tissue, cortex, and epidermis. Priestley
( 1926a ) stated a general rule that, of the two lateral meristematic regions
of the axis, the phellogen is more likely to produce buds and the vascular
cambium to produce roots. Morphogenetic problems here involved con-
cern the causes of the differentiation of dormant or "reserve" primordia
in particular places and especially the factors that first keep them dormant
and then stimulate their development in regeneration.

Bud formation is frequent on hypocotyls and has been studied particu-
larly bv Rauh ( 1937 ) . In a few species these buds normally develop into
shoots. In other cases they may be present but do not develop and in still
others they may be induced only by the stimulus of regeneration, after
the decapitation of the hypocotyl. In Linum usitatissimum, the origin of
these buds has been traced, in decapitated hypocotyls, to single cells of
the epidermis ( Crooks, 1933; Link and Eggers, 1946a ) in which divisions
begin to appear. A group of cells is thus produced which develops into a
bud initial and finally into a shoot. Several buds may begin to grow, only
one of which becomes dominant. In undecapitated hypocotyls a few epi-
dermal cells may divide but they rarely produce buds. Bud development
is induced more readily in young hypocotyls than in older ones. After a
bud begins to grow, vascular strands differentiate which connect it with
the main vascular cylinder (Fig. 9-6). Van Tieghem (1887) described
similar bud development in the hypocotyl of Linaria, as did Bain ( 1940 )
in cranberry. Such hypocotyls offer a good opportunity for the study of
cellular totipotency and the redifferentiation of vascular tissue.

So-called "adventitious leaves" (really reduced shoots, Rauh believes)
are produced abundantly on the decapitated hypocotyl, or seedling tuber,
of Cyclamen (Boodle, 1920; Rauh, 1937) and develop there from sub-
epidermal cells. There are transitions here from simple leaves to fully
developed buds. The great number of these buds normally produced sug-

246 The Phenomena of Morphogenesis

gests that this is a case of reproductive regeneration rather than of
restoration.

The stems of most monocotyledons lack a cambium, and this somewhat
limits the possibilities of regeneration of lost parts in them. Axillary buds
are often present, however, and the nodes and bases of leaves remain
somewhat meristematic. New roots commonly arise in these regions. Meth-
ods of regeneration and of vegetative reproduction are generally very
specialized. Some members of the Juncaceae and Cyperaceae reproduce
vegetatively from tips or nodes of culms, as in Eleocharis rostellata, where
buds grow from the sterile culm tips ( La Rue, 1935 ) .

Fig. 9-6. A young adventitious bud which has grown from epidermal cells on a de-
capitated hypocotyl of flax. Note the cell divisions in the cortex which will give rise to
a vascular connection with the stele. (From Crooks.)

Factors in the rooting of conifer cuttings have been discussed by
Deuber (1940).

The physiological basis of such regenerative processes has been widely
investigated. Gardner ( 1929 ) observed that, in both deciduous and ever-
green trees, cuttings from 1-year-old stems rooted more readily than those
from older ones. The influence of auxin and of various synthetic growth
substances has been much emphasized ( p. 391 ), particularly in root forma-
tion. Van der Lek (1925) found that cuttings rooted better if there were
buds on them, presumably because of the production of root-stimulating
substances by the buds. Discovery of the effectiveness of various organic

Regeneration 247

acids in root formation has made "root hormones" of importance in horti-
culture.

Bud formation, also, is influenced by physiological conditions. Miller
and Skoog ( 1953 ) report that tobacco-stem segments, in sterile culture,
form buds much more readily if adenine is present and that indoleacetic
acid reduces their development. Both results, presumably, are due to
effects on nucleic acid metabolism. Ruge (1952) and a number of earlier
workers observed that a functioning chlorophyll apparatus is necessary
for the successful rooting of most cuttings. Shoots with variegated leaves
or in the dark root poorly. Whether this is owing to the production by
the leaves of food or of a growth substance is not clear, but van Overbeek,
Gordon, and Gregory ( 1946fo ) believe that the main function of leaves in
the rooting of cuttings is simply to supply nutrition.

Hereditary tendencies may also influence the character of regeneration,
as in the conversion of axillary buds into tubers in the potato (Isbell,

1931).

Root Cuttings. Under natural conditions shoots are produced by roots
rather infrequently and chiefly in woody plants. In many cases roots may
be used as cuttings, however. Here the restoration of lost structures by
the production of adventitious roots or shoots occurs much as in the stem,
shoots tending to be restored at the basal (proximal) end and roots at
the apical ( distal ) one. Most growth is from callus. Roots show a greater
tendency to form adventitious buds than do stems. Naylor ( 1941 ) finds
that both structures arise from meristematic tissue produced by paren-
chyma cells in the younger phloem and not from the cambium. The polar
development of regenerating structures on fleshy roots has been studied
by various workers (p. 124).

Way ( 1954 ) investigated regeneration on apple roots of different sizes.
In some varieties the larger ones ( 8 to 12 mm. in diameter ) produced only
shoots and the smaller (3 mm.) only roots. When both were formed, the
zone of shoot production ( at the proximal end ) extended farther distally
in the wider roots, and that of root production (at the distal end) ex-
tended farther proximally in the narrower ones. Way interprets these dif-
ferences as due to auxin gradients, with different concentrations in large
and small roots.

Buds on roots are usually endogenous in origin. In Bryophylhim they
arise from the subepidermal layer (Ossenbeck, 1927), and Rauh finds
them originating at the scars of the delicate branch roots. In Aristolochia
and the Podostemaceae they grow from the cortex. Carlson ( 1938 ) reports
that in the orchid Pogonia an adventitious shoot arises by enlargement
and division of the surface and cortical cells at the tips of lateral roots.
This forms a swelling in which a bud develops.

An important morphogenetic question concerned with regeneration

248 The Phenomena of Morphogenesis

from roots and one which has been rather widely discussed is whether the
early primordia of new organs are "indifferent" in nature and may pro-
duce either buds or roots, or whether they are determined from the first
to form one or the other. A bud is a young shoot and has the rudiments of
leaves, which the root primordium does not have, and it should therefore
presumably be easy to tell one from the other. This seems often to be
difficult, however, in the very early stages, and many instances where
root primordia have been reported to change into shoots, and vice versa,
may be due to erroneous observation. Dore (1955) has studied the origin
of young primordia in the regeneration of horseradish roots and finds that
these are produced as organized meristems in close association with the
scars of lateral roots and that they originate in the phellogen of the main
root. He is certain that at the beginning they are capable of developing
into either roots or shoots. That this is so is suggested by the fact that the
ratio of buds to roots, where they can be definitely distinguished, is not
constant but varies with conditions, as though neutral primordia were
being tipped in one direction or the other. If this should finally prove to
be the case and the existence of truly indifferent primordia be established,
useful material would be provided in which to examine the very early
stages in the differentiation of these two structures which soon become so
dissimilar. This reminds one of the case in Selaginella reported by Wil-
liams (1937). Here an "angle meristem" near the tip will normally pro-
duce a rhizophore, a structure somewhat intermediate between root and
shoot and which finally grows downward and forms typical roots. If the
main axis of the shoot is decapitated, however, the young primordium
which would have produced a rhizophore will now grow upward into a
typical shoot. Mention has been made earlier (p. 71 ) of cases where a
young leaf primordium, if isolated by deep cuts from the meristem tip,
will grow into a bud-like structure.

Cuttings from Other Parts. A variety of phenomena of regeneration has
been described in typical leaves and in cotyledons, scales, and carpels, as
well as in inflorescences, flowers, and fruits. In contrast to the axial portion
of the plant, leaves are organs of determinate growth, and the restoration
of lost parts by them is thus somewhat different from the process in
axial structures. It is especially common in succulent leaves.

The restoration of roots or shoots on leaves detached from the plant
and with petiole placed in soil has often been observed ( Stingl, 1908; and
Yarwood, 1946). In such cases, after adventive roots and buds have been
formed on lamina or petiole, various anatomical changes may be observed,
especially a marked increase in the vascular tissue of the petiole. Further-
more, instead of being disposed in an arc, as in normal petioles, this tissue
often enlarges to form a complete vascular ring. The petiole thus becomes
structurally as well as functionally a stem. Winkler ( 1907o) reviewed cases

Regeneration 249

of such conversion and studied a particularly good example of it in
Torenia asiatica. He believed that increased transpiration is the cause of
the change. Simon (1929) found essentially the same thing in Begonia
and noted that the bundles from the young roots induced new vascular
tissue only in that part of the petiole just below them, suggesting the
polar distribution of a hormone. Similar results were obtained by Doyle
(1915) through grafting buds onto the petioles of rooted leaves.

In leaf cuttings, adventitious structures are formed predominantly at
the leaf base. Hagemann (1931), in an extensive survey of the regener-
ative ability of leaves, investigated 1,204 species of gymnosperms, dicoty-

Fig. 9-7. Petals of Epilobium angustifolium which produced roots when cultured on
nutrient agar. ( From La Rue. )

ledons, and monocotyledons. He found that some of these showed no
restoration, a very few formed shoots or both roots and shoots, and the
largest proportion roots only. Schwarz ( 1933 ) examined many other spe-
cies. The location of the regenerated structures is determined mainly by
the anatomy of the leaf. It is noteworthy that in a number of species, pre-
dominantly though not always succulents, restoration and vegetative
reproduction occur in other parts of the leaf than the base, as in species
of Drosera, Achimenes, Begonia, Torenia, and the Crassulaceae. In Utric-
ularia Goebel (1908) found adventive shoots formed by the leaf tips.

Restoration of organs may also occur from isolated cotyledons. Kiister
( 1903fo ) obtained both roots and shoots from cotyledons of Cucumis and

250 The Phenomena of Morphogenesis

Luffa, Kowalewska ( 1927 ) shoots from Phaseolus and Visum, and Carlson
(1953) only roots from Raphanus and Brassica. La Rue (1933) reviewed
work on this subject and reports his own success in obtaining roots on
excised cotyledons of 19 species and shoots on those of 22 species.

Several investigators have studied regeneration in inflorescences. If this
structure is cut off and treated as a cutting, root formation and subse-
quent vegetative development of the inflorescence often follow. Bor-
mann (1939) reviewed the literature and made extensive investigations
himself, finding that, of 391 species studied in 65 genera and 45 families,
the conversion of an inflorescence into a vegetative shoot by treating it
as a cutting occurred in about 17 per cent of all the species.

Flower cuttings of Cactaceae, where the stem is incorporated into the
fruit, have been found to form roots and develop dormant buds ( Goebel,
1908 ) . The ovary of Jussiaea as well as immature fruits of Lecythis react
in the same way. Carriere (1877) describes the rooting of the capsule of
Lilium speciosum and Kupfer (1907) that of pods of Plwseolus.

La Rue (1942) found that, under favorable cultural conditions that
provide both moisture and food, many flowers or their parts may be
induced to root ( Fig. 9-7 ) , and by this means he obtained roots on flow-
ers of three genera of monocotyledons and 22 genera of dicotyledons. He
went further and was able to induce regeneration even in gametophytes.
Female gametophytes of Zamia in sterile culture not only increased in
size markedly but in a few cases developed small roots and buds. The
latter produced leaves resembling miniature seedling ones. He later
obtained similar results with Ctjcas (1954).

Reproductive Regeneration

The ability of a part of the plant to restore missing structures and
thus regenerate a whole is essentially the ability to reproduce. Regenera-
tion is a reproductive process, and it is understandable that during the
course of evolution many plants should have developed means to use
the totipotency of their individual cells and tissues as means for vege-
tative reproduction. In many cases this has become a normal and spon-
taneous process, as in the formation of foliar embryos on the leaves of
many Crassulaceae or of bulbils in other forms. Isolation or injury may
stimulate the growth of similar structures, and this process thus grades
over into regeneration. In many cases it is difficult to distinguish be-
tween the two.

This type of reproduction has been described most commonly in
leaves and leaf cuttings (Fig. 9-8). Many cases have been studied in
both dicotyledons and monocotyledons. Goebel cites a variety of these
from the earlier literature. In some cases plantlets occur naturally on
leaves and drop off to form new individuals (gemmipary). In others

Regeneration 251

these appear only when the leaf is removed from the plant or its vigor
reduced. Instead of actual plantlets, bulbils or bulblets may be formed,
modified buds which drop from the plant and produce new individuals.
Many plantlets develop from preformed meristematic cells or cell
aggregates and thus are clearly to be regarded as reproductive struc-
tures even though in some cases they are induced only by rather ab-
normal conditions. Others arise from unspecialized cells, usually epi-
dermal or subepidermal ones, much as do the shoots on the hypocotyls
previously described. When these are frequently formed in nature they
are usually to be regarded as reproductive rather than regenerative struc-
tures. Only a few typical examples can be mentioned here.

Fig. 9-8. Leaves of Achimenes, used as cuttings, regenerating roots and bulbils from
the base and producing plantlets where veins have been cut. ( From Goebel. )

A familiar one is that of Tolmiea menziesii (Yarbrough, 1936a), in
which a plantlet regularly is formed at the junction of petiole and blade
from a preformed bud at that point. This readily separates from the
parent plant and forms a new one. In Cardamine pratensis (Goebel, 1908)
adventitious shoots or plantlets grow in the autumn or under special
conditions from the axils of the leaflets by the activity of groups of
meristematic cells. At the junctions of the larger veins occur slight
swellings and these may also develop into plantlets (Fig. 9-9). In such
forms there are evidently many cells that can easily be induced to become
meristematic and form plantlets. How such cells differ physiologically
from others it is important to discover.

252 The Phenomena of Morphogenesis

Some species of Drosera may also readily be induced to form shoots on
their leaves (Behre, 1929). These develop from single epidermal cells
on the morphologically upper side of the lamina, at the base of a tentacle,
on the petiole adjacent to stomata or trichomes, or in young inflorescences
adjacent to glands. In Drosera binata, a species with linear leaves, the
young plants thus produced have roundish blades much like those of our

Fig. 9-9. Cardamine pratensis. After a leaf is removed, plantlets develop on it from
preformed embryonic areas (a). ( From Goebel. )

own common Drosera rotundifolia. It would be interesting to find
whether this fact has any phylogenetic implications.

In Begonia rex and some other varieties of begonia, shoots may be
induced very readily on petiole and blade by removing the growing
points of the shoot. Prevot (1938, 1939) found that these arose from
epidermal cells, but only after they had reached a certain stage of ma-
turity. Hartsema ( 1926 ) has described the changes that such cells undergo

Regeneration 253

at the start of shoot development ( strong protoplasmic streaming, migra-
tion of the nucleus, and increase in cytoplasm). Here and in a good
many other plants, shoots will appear on the blade if one or more of the
veins are cut (Fig. 9-10), thus perhaps preventing the access of in-
hibiting substances. Prevot was able to induce bud formation on begonia
leaves by the application of various substances and by growing the
plants in the absence of oxygen. He also found that strips of epidermis
removed from the leaf would form buds. Not all begonias have high re-
generative ability, and this seems to be an inherited character when
various types are crossed.

Much like these cases is the development of young plants on the leaves
of Saintpaulia ionantha. This species is often reproduced in cultivation
by plantlets formed on leaves that have been cut off and placed in a
humid atmosphere. From individual cells of the upper epidermis shoots

Fig. 9-10. Propagation of rex begonia. If a leaf is removed and placed on moist sand
and certain of its major veins severed, plantlets will regenerate at these cuts. (From
Avery and Johnson.)

develop, and roots originate from parenchymatous cells near the boundary
between xylem and phloem in the veins ( Naylor and Johnson, 1937; Fig.
9-11).

Torenia asiatica behaves in much the same way (Winkler, 1903). In
leaf cuttings, numerous shoot primordia begin to develop over the sur-
face of the blade, each from an epidermal cell above a vein. Only a few
of these primordia grow into shoots, and a single leaf thus shows a
wide range of stages in shoot development. The shoots that form come
to flowering very quickly, sometimes when they have only one well-
developed leaf, and should thus make excellent material for a study of
the factors that induce flowering.

Many members of the family Gesneriaceae, to which these plants be-
long, regenerate readily. Leaf cuttings of Achimenes produce clusters of
bulblets at the base of the petiole and shoots from the blade if the veins
are severed ( Doposcheg-Uhlar, 1911). Streptocarpus (Goebel, 1908) illus-
trates most types of regeneration.

254 The Phenomena of Morphogenesis

The most familiar examples of reproductive regeneration are provided
by members of the Crassulaceae. In Kalanchoe pinnatum ( Bryophyllum
calycinum), plantlets develop from the marginal notches of the fleshy
leaves. This may sometimes take place while the leaf is attached to the
plant but is more common after it has fallen to the ground. In each
notch is a preformed foliar embryo (Fig. 9-12), long ago described by
Berge (1877) and more recently by Yarbrough (1932) and Naylor
( 1932 ) . This is more than a mass of meristematic cells, for it has already
taken the first steps toward organization of a plantlet and shows the
minute beginnings of root, stem, and leaf. In other species the degree

Fig. 9-11. Development of an adventitious bud from cells of the leaf epidermis of
Saintpaulia. ( From Naylor and Johnson. )

of differentiation of the foliar embryos varies (Stoudt, 1938). In K.
daigremontana and K. tubiflora the plantlets attain appreciable size be-
fore the parent leaf has reached maturity. In K. rotundifolia there is a
residual meristem on the axial surface of the petiole which develops a bud,
but root primordia do not become differentiated until after the leaf has
fallen from the plant.

The factors that induce the foliar embryos to develop into plantlets
have been actively discussed. Loeb (1920), who made an extensive study
of regeneration in this genus, believed that a hormonal mechanism in-
hibited their growth as long as the leaf was attached to the plant. Reed
(1923) attributed their behavior to the metabolic condition of the leaf
and showed that they tend to grow if the lamina loses vigor. Ossenbeck

Regeneration 255

( 1927 ) regards the mechanical or physiological conduction between the
leaf and the growing points of stem and root as important factors in
inducing their development. Mehrlich ( 1931 ) exposed plants to a wide
range of environmental factors in an attempt to solve the problem. In the
activity of certain enzymes and in the relative amounts of carbohydrates,
he noticed a difference between leaves in which the foliar embryos grew
out and those where they did not. Varietal differences were also evi-
dent. Gotz (1953) finds that plantlets grow out readily in long days
but that short days tend to inhibit them. They are accelerated if the

Fig. 9-12. Section through a notch on
the leaf of Kalanchoe, showing a pre-
formed "foliar embryo" with two leaf
primordia below and a root primor-
dium above, buried in the tissue.
(From E. E. Naylor.)

vessels between lamina and petiole are cut or if auxin levels are low
(Vardar and Acarer, 1957).

Other Crassulaceae differ in some respects from Kalanchoe. In Byrnesia
weinbergii, Stoudt (1934) found that the foliar meristem from which a
plantlet comes is at the base of the blade, not the margin. It is quite
undifferentiated and will not develop until the leaf is removed from the
plant. In Sedum (Yarbrough, 1936c) there are no preformed meristems
at all, but these arise after the leaf is detached.

In Crassula multicava (McVeigh, 1938) a still different condition oc-
curs and one reminiscent of Begonia and Saintpaulia, for here, after a
leaf has been kept for a time in a moist chamber, plantlets begin to de-
velop. Entire plants— not the shoot alone, as in many other cases— have

256 The Phenomena of Morphogenesis

their origin in single epidermal cells. These cells are not only presumably
but demonstrably totipotent.

In a considerable number of forms the reproductive structures arising
in regeneration are not plantlets, already differentiated and ready to
start growth, but dormant, almost seed-like structures. In Lilium tigrinum,
for example, in the axils of the upper leaves there are, instead of buds,
hard black bulbils which fall off and produce new plants. Detached
scale leaves in a number of the Liliaceae form adventive buds or bulbils
from their bases. On leaves of Hyacinthus, removed from the plant, simi-
lar structures may be formed, but Naylor (1940) has shown that in this
case they do not come from preformed meristematic tissue but develop
from epidermal and subepidermal cells.

In many ferns vegetative cells of the prothallus may produce sporo-
phytes by apogamy. Aposporous gametophytes are also frequently formed,
especially on isolated juvenile leaves. Lawton ( 1932, 1936 ) was able to
induce apospory in 13 species of ferns and obtained from them tetraploid
sporophytes by methods similar to those used in mosses. Aposporous struc-
tures are often strictly gametophytic, but Beyerle (1932) found adventive
structures in 34 fern species to include sporophytic buds, undifferen-
tiated structures, prothallia, and bodies intermediate between sporophytes
and prothallia (reviews by Du Buy and Neurnbergk, 1938, and Steil,
1939, 1951).

Regeneration in the fern sporophyte often results in the production of
new plants. Buds may be formed on leaves and roots, and foliar em-
bryos resembling those of higher plants may be produced, as in Campto-
sorus ( McVeigh, 1934; Yarbrough, 1936£> ) . A review of reproductive re-
generation in ferns, covering 35 genera and 197 species, has been made
by McVeigh (1937).

There should also be mentioned a special kind of reproductive re-
generation that occurs in vegetative tissues of the embryo sac and ovule,
by which embryos develop from synergids, antipodal cells, or cells of
the nucellus and not only from the fertilized egg (Lebeqne, 1952).
Strasburger (1877) called this adventive polyembryony (as opposed to
cleavage polyembryony, p. 235 ) . Examples of this are known in Funkia,
Coelebogyne, Citrus, and others (review by Webber, 1940). The em-
bryos here formed somewhat resemble the foliar embryos of the
Crassulaceae and similar plants. Though sometimes started in their
development by a regenerative stimulus, these are cases of specific repro-
ductive processes made possible by the totipotence of cells in various
vegetative portions of the plant and which in a way are comparable to
asexual propagation by spores.

In recent years experimental work on morphogenetic problems has
been concerned primarily with the effects of environmental factors,

Regeneration 257

particularly light and physiologically active substances. There is still op-
portunity for fruitful investigation through an experimental manipulation
of the developmental process itself, especially by work on problems of
regeneration such as have been discussed in this chapter. The significant
results of earlier botanical workers in this field, now cultivated somewhat
less actively than in the past, could be extended very profitably by sup-
plementing the older methods with the advantages of modern techniques.

CHAPTER 10

Tissue Mixtures

In animal bodies such combinations of genetically unlike tissues as grafts,
mosaics, and chimeras are rare in nature and rather difficult to bring
about experimentally, but in plants these are much commoner and easier
to produce. This is presumably due, in large measure, to the presence of
localized growing points in plants, which knit together readily. The arts
of grafting and budding have long been known to horticulturalists and
provide means for combining two or more varieties of related plants and
especially for vegetative multiplication of types that cannot be propa-
gated by seeds or in which cuttings do not easily root.

In chimeras and in localized genetic changes, tissue mixtures may
be much more intimate than in ordinary grafting and provide oppor-
tunities for a study of organization and tissue relationships which are
not available in homogeneous plant bodies.

STOCK-SCION INTERRELATIONS

In the practice of grafting, a small branch or shoot, the scion, is in-
serted into a larger rooted portion, the stock, by means of a cleft or
other opening in such a way that meristematic regions of the two come
into contact. The same result is achieved in a somewhat simpler fashion
by budding. Here a bud from one type is slipped under a cut in the bark
of another so that the two cambia are in contact, the bud later growing
into a shoot. A third piece, in "double-worked" trees, is sometimes
inserted as an intermediate between stock and scion. In practice, these
methods are used chiefly in woody plants and are the means by which
most horticultural varieties of trees and shrubs are propagated. The prob-
lems in these plants will therefore be discussed first.

A question of much importance both practically and theoretically
concerns the effects produced by the stock on the scion or the scion on
the stock. What substances can, and what cannot, pass from one to the
other across a graft union? Do the two graft partners remain in com-
plete physiological isolation save for the passage of water and solutes

258

Tissue Mixtures 259

from stock to scion, or in a mutual exchange between the two do the
specific qualities of one become transferred, in any measure, to the other?
There has been much disagreement about these matters in the past, and
final answers are not yet available.

There are several means by which the two graft partners may affect
each other. Of most importance, probably, is nutrition. If a root into
which a scion is grafted has less capacity to absorb, store, or utilize nu-
trients than do the roots of the plant from which the scion was taken,
reduction of size and vigor of the shoot system produced by the scion
will result. Many cases have been found where there are such physio-
logical differences between stock and scion clones which modify the
effect of one on the other, particularly of root on scion. Second, there
may be differences between the two partners in the ease with which they
translocate water and nutrients. The wood of dwarf rootstocks usually
has a much smaller proportion of vessels than normal roots. Differences
in phloem transport are probably even more important, as is shown by
the dwarfing effect of inverted rings of bark and in other ways. Finally,
there may be differences between partners in the amount of auxin in
each or in the rate at which it is inactivated. In several herbaceous plants
it has been shown that dwarf types are relatively poor in auxin. This
may be the case in woody forms, for dwarf types of fruit trees are
much branched, an indication that auxin-induced bud inhibition is weak
in them. Other growth substances may pass from one partner to the other.
It is clear that water and salts from the soil pass from stock to scion
and that carbohydrates also pass across a graft union, and in either
direction. Certain nutritional changes are thus produced by one on the
other. A common practice in producing dwarf fruit trees is to graft
scions of standard varieties on stocks which are genetically small and
thus have small roots. This reduces the amount of top growth. Most of
this dwarfing results from the reduced water supply available from the
roots (Colby, 1935), and dwarfing rootstocks also tends to cause earlier
cessation of growth in the fall (Swarbrick, 1928). Dwarfing may be pro-
duced in other ways than by reduction in root size. Tukey and Brase
( 1933 ) found that where a dwarf variety was used either as a rootstock,
intermediate stem piece, or top scion its effect was to dwarf the whole
plant. Some dwarfing may also be attributed to defective graft unions
and the consequent failure to transfer materials readily (Bradford and
Sitton, 1929 ) . Dickson and Samuels ( 1956 ) have studied translocation
across a graft union by means of radioactive tracers and find that there
is a high concentration of the isotope at the junction of stock and scion,
suggesting that the dwarfing effect may be due to a block in the flow
of nutrients to the roots.

But there seem also to be more subtle factors involved. A special kind

260 The Phenomena of Morphogenesis

of dwarfing is that produced in some plants by growth from seeds that
have not been afterripened. A case of this sort in the peach where the
dwarfs retained their dwarf character when grafted on normal plants
was studied by Flemion and Waterbury ( 1945). The roots of such dwarfs
were able to support normal shoot growth, so that the seat of the dwarfing
seems to be in the shoot. There is no evidence of a stimulating substance
produced in the normal plant or of an inhibiting one in the dwarf.

Some varieties are incompatible in grafting and so do not thrive to-
gether even though the graft union between them may be good or a
variety compatible to both is inserted as an interstock ( Sax, 1953, 1954 ) .
Tukey and Brase present evidence that not only the character of stock
and scion and their compatibility are important in determining tree size
but also the effect of environmental factors on each partner and on their
combination.

Aside from purely quantitative effects of stock on scion in horti-
cultural plants, other traits have been reported to be transmitted from
one to the other. McClintock ( 1937) found that leaves of the Grimes apple
grafted on Virginia crab stock have a greater green weight and are
physiologically different in some respects from those of the same va-
riety on other stocks. Blair (1938) grafted Bramley Seedling apple on
French crab but in a number of cases inserted between stock and scion
a 9-in. piece of one of three other varieties, Mailing II, IX, and XIII. Even
though here stock and scion were the same, the effect of these middle
pieces on the tree that grew out of them was markedly different in
each case, as shown in leaf poise, general habit of branching, leaf color,
and time of defoliation. The effect of the various middle pieces on the
root was also evident. Rogers, Beakbane, and Field (1939), however,
found that intermediate pieces from different sources had relatively little
effect on the rootstocks. By grafting apple scions from various sources on
roots, Swarbrick and Roberts (1927) found that the character of the
root tended to be like that of the variety which contributed the piece of
stem just above it, whether this was scion or middle piece. Amos, Hatton,
and Hoblyn ( 1930 ) dispute this conclusion and believe that the effect of
scion on root is simply quantitative.

In citrus fruits Halma ( 1934 ) reports that Eureka lemon scions grafted
on sour-orange roots greatly modify the form and color of the latter.
In the reciprocal graft, only the color of the root was changed. These
changes were observed in grafted but not in budded trees.

Early work on the stock-scion relationship is reviewed by Swarbrick
(1930), and Garner (1949) has presented the subject from a practical
point of view.

The mixture of tissues by grafting and the relation between the graft
partners pose problems of wider interest than for horticulture alone. It

Tissue Mixtures 261

has long been known, for example, that successful grafts are usually
limited to closely related plants, either between those of the same
species or between species close together taxonomically. In exceptional
cases grafts can be made between genera and very rarelv between
families. Simon (1930), for example, has grafted Solarium and Iresine,
belonging to the widely separated families Solanaceae and Amarantha-
ceae. Nickell (1948) grafted white sweet clover on sunflower, and the
plants continued to grow with normal vigor for 5 months. Silberschmidt
(1935) studied 550 grafts between plants of the same species, of related
species, and of unrelated species. Anatomical fusion in some cases oc-
curred in grafts of unrelated species but here union was slower and less
extensive, passage of nitrogen from scion to stock was reduced, and
proteolytic activity of stock juices increased. The last fact is presumably
concerned with the failure of unrelated grafts.

Schroter (1955) reports that Zinnia elegans, one of the Compositae,
can be grafted to tobacco, although not on some plants in the same
family as tobacco. He attributes the successful Zinnia grafts to the pres-
ence of nicotine in this plant. Mothes and Romeike ( 1955 ) grafted scions
of tomato, petunia, belladonna, and tobacco on tobacco stocks of vary-
ing nicotine content and found that the richer the stock was in nicotine,
the poorer was the development of the grafted scion.

The passage of nicotine from tobacco roots to tomato scions has been
described (p. 220). Hieke (1942) found that in grafts between Lyco-
persicon, Nicotiana, Atropa, and Datura the alkaloids found in the scion
were those characteristic of the root to which this was grafted.

Kostoff (1929) presented evidence from grafts between various plant
types that immunity, as tested by the precipitin reaction, can be acquired
by plants much as in animals. Chester and his colleagues, however, in a
series of papers (1932 and others) showed that the precipitates re-
ported are not the result of a true precipitin reaction but are simply
calcium oxalate, a widespread substance in plants.

Monocotyledonous plants have been found more difficult to graft than
dicotyledonous ones, presumably because they lack a cambium. Muzik
and La Rue (1954), however, grafted a number of species of grasses,
including some belonging to different genera.

The closer to the embryonic condition a tissue is, the more readily it
can be grafted. The smallest successful graft of this sort seems to be one
made by Gulline and Walker (1957) in which a shoot tip containing
only about 600 cells and with a volume of less than %ooo cu- mm- was
grafted back on the apex from which it had been cut. Later development
was normal.

As to the reciprocal relations of stock and scion in nonwoody plants,
many conflicting results have been reported. Daniel described various

262 The Phenomena of Morphogenesis

instances of a marked qualitative effect of stock on scion or scion on
stock. The production of tubers, for example, he believed could be trans-
ferred by grafting from the Jerusalem artichoke to the common sun-
flower, which normally bears no tubers. In one of his last papers (1929)
Daniel maintains that these induced changes have sometimes become
transmissible through seed for several generations and regards this as
proof of the inheritance of an acquired character.

This is essentially the position taken by Lysenko and his Russian
colleagues. One of them, Avakian (1941), reported marked reciprocal
effects, on fruit color and other characters, of red-fruited, yellow-fruited,
and white-fruited tomatoes when grafted together in various ways. Simi-
lar experiments were repeated in this country by Wilson and Withner
(1946), who were unable to confirm these results in any respect. Bohme
(1954) also found that no inheritable effects were produced by grafting
between varieties of tomatoes.

There are a number of well-authenticated cases, however, of the trans-
mission, between graft partners, of factors that determine qualitative
and not simply quantitative and nutritional differences. These present
some important problems both for morphogenesis and for physiology.
Conspicuous among them are the numerous instances where a flowering
stimulus, from a plant which has been induced to flower by a particular
photoperiod, can be transferred by grafting to a nonflowering plant and
cause it to flower (p. 396). Evidently some substance is transmitted across
the graft that stimulates flowering.

The effect of this stimulus may be modified in various ways. Haupt
(1954), using a late-bearing variety of peas, grafted terminal shoots of
different ages on stocks of different ages. If scions of young plants are
grafted on older ones, flowering takes place up to six nodes earlier than
in controls grafted to stocks of their own age. Evidently the substance con-
cerned with flower development is not formed in the first stages of
the plant's growth but can be effective then if introduced from older
plants.

The production of flowers after grafting may be due to other factors
than a specific flower-inducing substance. The Jersey type of sweet po-
tato rarely flowers in this country but can be made to do so by grafting
it to another species of Ipomoea that does not form storage roots (Kehr,
Ting, and Miller, 1953). These authors believe that flowering results
from the accumulation of carbohydrates in the shoots after grafting.

The tendency to form tubers in potato may be transmitted by grafting.
If the shoot of a variety that produces tubers under a long day is grafted
to a short-day variety and grown under long days, the short-day variety
will now produce earlier and larger tubers than it would have done by
itself (Howard, 1949). This effect was not transmitted through these

Tissue Mixtures 263

tubers when they were used as seed. Somewhat similar results are re-
ported by Gregory (1956), who also found that the tuber-forming stimu-
lus could be transmitted from all parts of the shoot by grafting.

Some recent experiments on the graft transmission, or lack of trans-
mission, of plant traits are the following:

In English ivy (Hedera helix) Doorenbos (1954) grafted scions from
the juvenile type (with lobed leaves) onto the adult, upright, flowering
form and found that the latter often lost its abilitv to flower and
showed other juvenile traits.

Popesco (1949) reports that when Sophora japonica, a woody peren-
nial leguminous plant, is grafted to the common bean, the bean flowers
15 to 20 days later than it otherwise would and becomes perennial in
habit.

Hybrids between Meliotus alba and M. dentata are deficient in
chlorophyll because of some gene interaction and die in a few days. If
such hybrids are grafted to sweet clover, however, they grow well,
flower, and bear seed (W. K. Smith, 1943).

In spruce (Picea abies), Muller-Stoll (1947a) examined grafts of shoots
from the tops of old trees on young seedlings. After 3 years these
flowered abundantly, far earlier than they would have done otherwise.
Only female cones were produced, presumably because the branches
used as scions were from the top of the tree, which bears chiefly female
cones. This localization the author interprets as an instance of topophysis.

Many cases have been described of the effect of stock on fruit size
in the scion. Bitters and Batchelor ( 1951 ) report such a case in the orange,
where Washington navel oranges were grafted on 32 different root-
stocks and Valencia on 26. Differences were found between stocks in
their effects on fruit size in the scion. These differences are not related
to those in tree size or in number of fruits.

An incompatible graft is reported in cucurbits by Wellensiek (1949).
Grafts of muskmelon on Cucurbita ficifolia grew for a time and then
suddenly wilted and died. Muskmelon as an interstock between cucum-
ber and C. ficifolia has the same effect. If a few leaves are left on the lat-
ter, however, the graft with muskmelon is successful. The reciprocal graft
thrives, so that incompatibility is in only one direction. The author
believes that muskmelon fails to give the stock of C. ficifolia a sub-
stance necessary for its growth and that this is provided if a few leaves
are left on it.

Yampolsky (1957), in the dioecious Mercurialis annua, grafted male
and female plants together in a variety of ways but found no alteration
in the sexual character of either.

Of particular interest for genetics are those cases where there is a
known genetic difference between scion and stock. Hijoscijamus niger,

264 The Phenomena of Morphogenesis

the black henbane, has an annual variety and a biennial one, the annual
forming a flower stalk and flowers in a single season but the biennial re-
maining in the rosette stage for the first year unless experimentally ex-
posed to low temperature for some time. This difference is due to a
single gene, with the biennial character almost completely dominant.
Melchers ( 1937 ) grafted a scion from the annual variety ( and also scions
from Petunia, Nicotiana, and other related annual plants) into the
rosettes of the biennial variety in its first year and by this means induced
the biennial to flower in the same season. Melchers attributes this to the
passage across the graft union of a nonspecific flower-forming substance.
The genetic difference between the annual and the biennial varieties
seemed to be due to the ability of the former to produce a flower-form-
ing hormone without previous exposure to low winter temperature.
Melchers later (1938) found that if a short-day variety of tobacco,
grown under long-day conditions and thus unable to flower, was grafted
into biennial Hyoscyamus in its first season, the latter soon produced
flowers. The gene in Hijoscijamus may thus control the ability to respond
to the flower-inducing substance rather than to form it.

In Petunia nyctaginiflora von Wettstein and Pirschle (1938) found a
gene d which differed from the normal D in producing plants that are
smaller and have fewer branches, smaller and more rounded leaves, and
a marked chlorophyll deficiency. Scions of dd grafted on DD stocks had
slightly larger leaves and stems and more branches but were not much
different from ungrafted dd. Scions of DD on dd showed general reduc-
tion in size and a chlorophyll deficiency, which was greatest next the
graft union and decreased in intensity above this. The authors believed
that a substance was produced in the mutant that passes into normal
scions and there either inhibits chlorophyll formation or causes chloro-
phyll degradation. Pirschle later ( 1939 ) presented evidence that dd lacks
a hormone, present in DD, that stimulates growth in size but does not
affect the shape of leaves or flowers. Objection may be raised that these
are nutritional and not hormonal effects.

When tobacco and tomato are grafted with the dd mutant of Petunia,
their leaves show chlorophyll deficiency when the dd plant is used as a
stock and to a lesser degree where it is used as a scion (Pirschle, 1940).
The gene-produced d substance is clearly not species-specific. The
possibility cannot be disregarded that the supposed d mutant is actually
a virus infection, although its clear genetic segregation from D would sug-
gest that it is not.

The single-gene mutants nana of Antirrhinum siculum and sterilis of
Solanum lycopersicon were produced by radium irradiations and have
been studied by Stein (1939). The former has a single unbranched
main stalk (unlike A. siculum); is flowerless; and has larger, thicker,

Tissue Mixtures 265

and darker leaves. When grafted as a scion on A. siculum stock, the
stem is somewhat . shorter and bears abnormal flowers but is otherwise
unchanged. The tomato mutant is dwarf, has scanty chlorophyll, and
lacks branches and flowers. When grafted as a scion on tomato stock
its chlorophyll remained deficient but its growth became approximately
normal as to height, branching, and flower development. The particular
interest of these cases lies in the fact that the various effects of a gene
here seem to be separated, some of them passing across the graft union
and others not doing so. Such material offers a favorable opportunity
for the study of gene action.

Rick (1952) found a tomato mutant, wilty dwarf (wd), which differed
from normal in having fewer and shorter internodes, smaller leaves, thin-
ner stems, blue-gray leaf color, and a tendency to wilt in summer. This
was grafted in various ways on homozygous normal ( + ) lines differing
from wd in only this one gene. Control grafts of wd on wd and of + on -}-
showed no modification. Reciprocal grafts of -f- on wd and wd on + had
their leaf dimensions and stem lengths shifted markedly toward the
character of the stock. In double graft combinations, wd/ -\- /wd and
-h /wd/ +, the top scion was unaltered but the middle piece was changed
in the direction of the stock. The author concludes that the effect of
stock on scion here is not due to factors in the stem or leaves but in the
root system of the stock.

Kostoff ( 1930Z? ) observed irregular meioses in the pollen cells of tobacco
grafted to other genera, and such scions produced much abortive
pollen. If flowers on them were selfed, various chromosomal aberrants
appeared in the progeny but none in the controls.

In Petunia, Frankel ( 1956 ) grafted fertile scions to stock showing
cytoplasmic male sterility and found sterility in the offspring of such
scions, suggesting that cytoplasmic sterility determinants had passed
from stock to scion. The author recognizes the possibility that nutri-
tional changes induced by grafting may have been responsible for these
effects.

Wagenbreth ( 1956 ) made grafts between a number of species of
legumes and found by inoculation experiments that, although bacteria
specific for the stock would produce nodules in such plants, bacteria
specific for the scion would not.

Common experience has shown that strictly qualitative characters such
as shape are usually gene-controlled and not influenced by grafting,
despite early claims to the contrary. A few pieces of positive evidence,
however, have been reported in recent years. Heinicke (1935) observed
that Mcintosh apples borne on defoliated scions grafted into Northern
Spy, and thus grown from material produced by Northern Spy leaves,
tended to be modified in the direction of the latter variety. Southwick

266 The Phenomena of Morphogenesis

(1937) also found that Mailing stock had some influence on the form
and size of Mcintosh apples grown on it. These cases need confirma-
tion.

In general, from the mass of literature available, one may conclude that
stock can influence scion in producing differences in plant size, size of
leaves and fruits, plant habit, flowering time, life span, content of inor-
ganic and certain organic substances and growth substances, and to some
extent in fertility and resistance to disease. Influence of scion on stock
is much less marked. Most of these effects definitely have a chemical or nu-
tritional basis, and few cases of strictly qualitative changes are known.
It should be recognized, however, that a purely quantitative difference,
as in fruit or leaf size, may influence shape by allometric correlation
(p. 105). Truly morphogenetic effects rarely-perhaps never-pass across
a graft union. The great preponderance of evidence also supports the con-
clusion that no permanent genetic change is induced by one graft part-
ner on the other.

Stock-scion relationships have been reviewed by Rogers and Beak-
bane (1957). Much of the literature on grafting (and many other
things) is summarized in Krenke's (1933) monumental work. The theo-
retical aspects of grafting have been reviewed by Roberts ( 1949 ) .

CHIMERAS

The instances of tissue mixture just described have been by the arti-
ficial union of two genetically different plants. These types remain sharply
separated, each branch or other unit of the plant belonging definitely
to one or to the other. There are tissue mixtures, however, where the fusion
is much more intimate than this and where an organ such as a stem, leaf,
or root is not homogeneous but is made up of two or more tissues that are
genetically unlike. This difference may arise by somatic mutation, the
mutated cells multiplying and forming a part of the whole, or it may be
the result of a mixture of meristematic tissues at a graft union. The im-
portant fact, morphogenetically, is that these diverse groups of cells
do not each form an organism or produce developmental abnormalities
but that they coexist as parts of the same organized system. What is pro-
duced is a normal, whole plant. Here the organizing capacity of living
stuff and the self-regulatory quality of the organism are particularly
conspicuous.

Mixtures of tissues that come from different sources are called chimeras,
a term proposed by Winkler (1907b) from the analogy between such
plants and the chimeras of mythology which were part lion, part goat,
and part dragon. A number of types of chimeras are recognized, depend-
ing on the relationship of their components.

Tissue Mixtures 267

The work on chimeras has been reviewed by Swingle (1927), Weiss
( 1930), Neilsoh-Jones ( 1934, 1937), and Cramer ( 1954).

In the so-called mixed chimeras the two kinds of tissue are mingled
irregularly together. This mixture may persist but it is often a tem-
porary stage and succeeded by one of the more regular types as the
meristem becomes better organized. In mericlinal chimeras, often de-
rived from mixed ones, one type of tissue forms a thin layer over a part
of the surface of the other.

The other types show a more regular relation between their two
components. In sectorial chimeras, a definite sector of a radially sym-
metrical structure such as a root, stem, or fruit is of one type and the

Fig. 10-1. Sectorial chimera in apple. (From Zundel.)

rest is of the other (Fig. 10-1). It is not uncommon to find in fruits
such as apple or orange a sector in which the color or texture of the
skin is different from that of the rest and which sometimes can be traced
into the axis of the fruit. Such a sector may be distinguished in the stem,
also, and the line between the two components sometimes runs out through
the blade of a leaf. The term sectorial chimera may be used more
broadly for a type in which there are large masses of diverse tissue
adjacent to each other, regardless of whether the boundary line has
any relation to the axis of symmetry. Thus an apple in which the terminal
portion is of one type and the basal another, with an irregular boundary
between, has been called a sectorial chimera. Sectorial chimeras are
often found in shoots that arise from the vicinity of a graft union. Some
of them may really be mericlinal ones, with one member covering a

268 The Phenomena of Morphogenesis

sector but only skin deep. Sectorial chimeras may sometimes be dis-
covered by a study of their internal structure (Brumfield, 1943, p. 76,
and Fig. 10-2).

Of most interest to morphogenesis, however, are periclinal chimeras.
In these remarkable plants the outer cell layers are derived from one
graft partner and the entire inner portion of the plant from the
other. "Graft hybrids," which have long been a puzzle to horticultural-
ists, prove to be periclinal chimeras. They arise from grafted plants and
partake of certain of the characters of each, but their own characters
cannot be transmitted through seed. One of the familiar forms is
Crataegomespihis, originating from a graft between two rosaceous
genera: Crataegus, the hawthorn, and Mespilus, the medlar. Another is

Fig. 10-2. Sectors of a root of Vicia after previous exposure to X radiation. Stippled
cells are those in which observed mitoses showed that the chromosomes were un-
changed. Black cells are those where a chromosomal change could be observed.
These cells presumably are descended from a cell at the very tip in which a change
had been induced and which had then given rise to a sector or wedge of similar cells.
( From Brumfield. )

Cytisus-labiirnum, coming from a graft between these two leguminous
genera.

Plants of this sort were first experimentally produced and carefully
studied by Winkler ( 1907fc, and later papers ) . He grafted two closely
related species, the nightshade, Solarium nigrum, and the tomato, Solanum
hjcopersicon. After union, most of the scion was cut off, and from
adventitious buds arising near the point of union plants developed
which sometimes showed mixtures of the two types of tissue. Most of
these were sectorial chimeras. Occasionally, however, Winkler found
a plant that showed no obvious separation into two types of tissue but
was clearly intermediate in character between nightshade and tomato.
Several distinguishably different types of such "graft hybrids" appeared in
these experiments, were maintained by vegetative propagation, and bore

Tissue Mixtures 269

flowers, fruits, and seed. Whether these were really mixtures of tissue,
or, in some cases at least, were actual vegetative hybrids, was not clear
at first. Baur's (1909) analysis of a Pelargonium with white-margined
leaves showed that in this plant both the epidermis and the layer
beneath it lacked chlorophyll. This conception of a continuous layer
of one type of cells covering a core of another type was applied to
Winkler's chimeras, and the latter proved to be periclinal ones. Such
forms apparently arise at a place where there is a thin layer of one
tissue over the other. A growing point, originating in the deeper tissue,
pushes up and carries on its surface one or two cell layers of the other
type. From this layered meristem a new shoot is formed. Mericlinal
chimeras may thus be converted into periclinal ones. Jorgensen and
Crane (1927) repeated Winkler's experiments, using five species of
Solarium, and observed in more detail the origin of chimeras.

In the tomato-nightshade chimeras four different forms were recog-
nized, propagated, and even given Latin names. In one there was a
single layer of tomato over a core of nightshade; in another, two layers;
in a third, one layer of nightshade over tomato; and in a fourth, two
layers of nightshade. The reason that there are rarely more than two
layers of the outer component is presumably because a new growing
point always arises near the surface.

In Winkler's material it was relatively easy to distinguish the two
components of the chimera cytologically, since tomato has 24 chromo-
somes (2n) and nightshade 72. When chromosome counts could not be
made, the size of the cells (much larger in nightshade) was almost as
good a criterion. It was found that the layers could be distinguished
at the apical meristem and that they maintained their specific character
throughout the life of the plant. When the outermost layer at the grow-
ing point was from one partner (tomato, for example) only the epi-
dermis of the plant was of that type. When the second layer of the
meristem, as well, was from tomato, the two outer layers of the plant
were of this type. Occasionally in certain tissues of the mature plant these
layers would become somewhat thicker by periclinal divisions and thus
include more cells, but this was relatively uncommon.

In periclinal chimeras (as in all seed plants) the genetic character of
the plant is determined by the cell layer just beneath the epidermis.
From this layer the sporogenous tissue is formed. The offspring of a
chimera, by seed, is therefore identical with the graft partner that con-
tributes the subepidermal layer of cells.

Winkler maintained that two other types of chimeras that he obtained
from grafts were true burdos, or vegetative hybrids, in which one layer
had arisen by an actual nuclear fusion between cells of the two com-
ponent species. The aberrant chromosome counts (cells with neither 24

270 The Phenomena of Morphogenesis

nor 72 chromosomes) can probably be explained in other ways. Brabec
(1954) repeated Winkler's work and found cells with varying and
irregular chromosome numbers but attributed this fact to the origin of
the new shoot from highly polyploid cells. Pith cells, as has been shown
by various workers, are often polyploid, and when chimeras come from
such tissue the chromosome situation is often complicated. The genetics
and .cytology of the Solarium chimeras have been studied by Gunther
(1957). Present evidence is against the occurrence of vegetative
hybridization and the existence of burdos. In the light of recent knowl-
edge of periclinal chimeras, Bergann (1956) has reinvestigated the
Crataegomespili.

Control 2n, 2n, 2n

8n, 2n, 2n

4n, 2n, 2n

2n, 4n, 2n

Fig. 10-3. Apical meristems of four periclinal chimeras in Datura consisting of 2n, 4n,
and 8n layers. Labels refer to the first two layers and the core. ( From Satina, Blakes-
lee, and Avery. )

In leaf and fruit, the tomato and the nightshade are very different.
Each of the four periclinal chimeras produced by Winkler by grafts
between them shows distinctive combinations of these traits so that it
is possible to determine the effects of one and of two cell layers of each
type when it covers a core of the other. Such chimeras provide an excel-
lent opportunity to study the morphogenetic influence of the various
meristematic layers and the developmental origin of shape differences
and of tissues.

The most complete and thoroughly analyzed series of periclinal chim-
eras are those studied by Satina and Blakeslee in Datura (1941, 1943,
1944, 1945; Fig. 10-3). By soaking seeds of Datura stramonium in col-
chicine solution, polyploidy was induced in certain cells of the shoot

Tissue Mixtures 271

meristem in 68 plants. The first cell layer (L I), the second (L II), and
the third (L III, including everything below the first two) were often
affected independently. L I was changed most often and L II least. These
layers retained their specific chromosome complement throughout the
structure of the plant that developed from this meristem. These plants
are periclinal chimeras, not obtained from graft unions but by chemical
induction. Unlike the tomato-nightshade forms and similar ones, here
there may be three genetically different layers (2n, An, and 8n) instead
of two, and these three were found to occur in almost any order from
without inward. In the first report there were the following distributions
of polyploidy among the layers: 2n, 2n, An; 2n, An, 2n; 2n, An, An; 2n, 8n,
An; An, 2n, 2n; An, 2n, An; An, 8n, An; 8n, 2n, 2n; 8n, An, An. Other combi-
nations were found later.

There is little difficulty here in distinguishing the layers since cell
size is approximately proportional to chromosome number and the 2n,
An, and 8n cells are thus markedly different. Since plants belonging to
the polyploid series differ little except in size, morphological combinations
of characters, as in the tomato-nightshade chimeras and others where the
partners are so unlike, cannot be seen.

An understanding of periclinal chimeras has aided in the solution of
a number of horticultural and morphological problems. Not only have
the classical examples of the "graft hybrids" been given a satisfactory
interpretation but other facts discovered in vegetatively propagated
plants are now explained. Bateson (1921), for example, found that in a
variety of Bouvardia with pinkish-white flowers root cuttings produced
plants with red flowers. Here it is probable that the core of the plant
was of a red-flowered variety and only the outer layers were genetically
pink. Since lateral roots arise from the vascular cylinder ( here genetically
red) and push out through the cortex and epidermis, buds from these
lateral roots would be expected to form red flowers. Asseyeva (1927) ob-
served in the varieties of potatoes arising by bud mutation that if the
buds are removed from the seed tuber the new ones which now arise
from the deeper tissues form plants like those from which the mutant
variety had come. Zimmerman ( 1951a ) reports a similar case in roses.
Such vegetatively propagated plants are probably periclinal chimeras
with only the outer layer or layers of cells belonging to the mutant type.

Other horticultural plants prove on examination to be chimeras. Einset
and his colleagues at the Geneva (N.Y. ) Experiment Station have
found that six large-fruited sports of several apple varieties are really
periclinal chimeras. The core tissues of the meristem are tetraploid, and
these are covered by one, two, or rarely three layers of diploid cells
(Einset, Blaser, and Imhofe, 1947; Blaser and Einset, 1948).

Dermen has worked extensively with polyploid chimeras. In apples he

272 The Phenomena of Morphogenesis

found some types in which (like those examined by Einset) the layers
are 2n, 2n, An. In others, these are 2n, An, 2n, the whole core being
diploid (Dermen, 1951). He has also studied chimeras in the cranberry
(1947a). Einset and Lamb (1951) conclude that most of the so-called
tetraploid grapes are actually diploid-tetraploid periclinal chimeras, as in
apples.

Fig. 10-4. Portion of carpel wall and placenta of Datura in a periclinal chimera that
was 2n, 8n, 2n in constitution. In material like this it is possible to trace the origin
of tissues from specific layers at the meristem. (From Satina and Blakeslee.)

Kerns and Collins (1947) obtained chimeras in pineapple with col-
chicine. Some had a 2n epidermis with all the other tissue An, and these
resembled the completely tetraploid plants. Some had a An epidermis and
the rest In and resembled completely diploid plants. These authors be-
lieve that there are only two "germ layers" in the pineapple.

Periclinal chimeras have made an important contribution both to
morphology and morphogenesis by making it possible to trace the con-
tinuity between the regions of the meristem and the structures of the
mature plant, since when the cells of the components of a chimera are
distinguishable, their descendants can be traced throughout develop-

Tissue Mixtures

273

ment (Fig. 10-4). This is particularly true in the polyploid chimeras.
The work on Datura by Satina and Blakeslee has provided much infor-
mation here, and Dermen (1953) presented similar evidence for the
peach. There seems to be no invariable rule as to just what mature
structures are produced by different layers at the meristem. The particu-
lar tissues contributed by L II and L III are not only different among
species but between large and small individuals of the same species
(Dermen, 1951).

It is significant that in the root, where a root cap is present and con-
tinuous layers of cells do not cover the tip of the meristem, periclinal
chimeras do not occur. Sectorial chimeras, however, have been ob-
served in roots (p. 76).

Fig. 10-5. Somatic mutation. Sectors of cells in corolla of Pharbitis resulting from
mutation from colorless to colored sap. The wider the sector, the earlier was the origin
of the mutation in the development of the flower. ( From Imai and Tobuchi. )

SOMATIC MUTATIONS

Mixtures of various types of tissue may appear not as a result of graft-
ing or experimental treatment but spontaneously. Mutations in vegetative
cells are not uncommon in some plants. Where a mutant cell is dis-
tinguishable, by color or in other ways, its descendants form a spot or
stripe of tissue unlike the rest (Fig. 10-5). The earlier the mutation oc-
curs, the larger the mass of tissue that will be produced. In annual
Delphinium, Demerec (1931) found a gene that mutated frequently in
petal cells, changing their color from rose to purple. An early mutation
altered a large part of the plant but later ones formed only small spots
on the petals. Some cases of variegation, as in maize pericarp (Anderson
and Brink, 1952), are due to mutable genes of this sort though most
color patterns in plants result from differentiation during development
and not from a mixture of genetically different tissues. Some genetically
variegated plants become chimeras, and Dermen ( 1947b ) has been able
to determine the specific meristematic layer (LI, L II, or L III ) in which
the mutation took place.

274 The Phenomena of Morphogenesis

McClintock (1929) reported a case in maize where the microsporocytes
had 19 chromosomes but the root tips 20, suggesting that a chromosome
had been lost during the development of the upper part of the plant.

A number of instances are known in hybrid plants where twin stripes
or spots occur, differing from each other and from the background
color. These have been interpreted as the result of crossing over in so-
matic cells. Thus in Phaseolus the Fj of a cross between plants with violet
and with lilac flowers produced a form with light violet flowers. In one
of these there were two stripes, side by side, one of them violet and one
lilac (Prakken, 1938). A sectorial chimera presumably due to such
vegetative segregation was reported for a pear fruit by Gardner, Crist,
and Gibson ( 1933 ) . Twin spots, also apparently caused by somatic
crossing-over or chromosome translocation, are frequent in maize peri-
carp (Jones, 1938).

Huskins and others (Huskins, 1948; Huskins and Cheng, 1950) re-
ported numerous instances where, as the result of low temperature or of
various chemical treatments, somatic mitoses occur in which the number
of chromosomes is reduced, as it is in meiosis. Wilson and Cheng
(1949) found that in such cases members of homologous pairs separated
much oftener than they would have done by chance, indicating a true
genetic segregation in the body cells of a heterozygous plant.

In all these instances of genetic alteration in a few cells, the difference
between these cells and the normal type is usually not very great, and
there is less to be learned morphogenetically than in grafts and chimeras.
Whenever genetically different tissues from any source are present to-
gether in the same individual, however, their coexistence in a single
whole is evidence of the organizing capacity of living stuff.

CHAPTER 11

Abnormal Growth

The basic problem of morphogenesis, as stated frequently in the preced-
ing chapters, is posed by the fact that every organism is an organized
system that in its development tends to produce forms and structures of
specific character. Within each organism there seems to be a norm toward
which its development conforms. The expression of this norm, however,
may vary greatly as the result of a wide range of environmental factors.
Such variation is familiar and to be expected. There are many cases,
however, where divergence from the norm is so great that we usually
speak of them as "abnormal" or "atypical." Just what do we mean by
these terms?

Every organism, and doubtless every cell, has a far wider range of
development potencies than it generally displays. When conditions are
different from the usual ones, the expression of its norm is also different,
but the norm is just as specific as before and the organism still per-
sistently regulates its development in such a way that the characteristic
form for that environment is produced. Norms of the individuals in a
given species are much the same. The basis of each is the genetic con-
stitution of the organism. It is well understood by geneticists, however,
that what a particular gene determines is not a particular character
but a particular reaction to a particular environment, external or in-
ternal. In many cases it requires very special environmental factors,
such as wounding, irradiation, application of growth substances, or
deposition of an insect egg to bring to expression developmental poten-
cies which would otherwise remain latent.

Under such unusual conditions, or from genotypes which are markedly
different from those of most members of the species, individuals some-
times develop which are so unlike ordinary ones that they are called
"abnormal." This does not mean that they are exceptions to the general
biological determination that controls the growth of all living things.
Neither do they constitute a sharply defined group set apart from all
others, for every gradation between normal and abnormal may be found.
One may be uncertain, for example, as to whether the occasional pro-

275

276 The Phenomena of Morphogenesis

duction of different forms of leaves on the same plant or the growth
of plantlets on the leaf margins or many structures appearing during the
process of regeneration are normal or not. What seems at first to be ab-
normal may prove to be simply an intensified or exaggerated manifesta-
tion of developmental potency. The degree of divergence from the
average is the basis on which we term a structure or an individual ab-
normal, and biologists often disagree as to how divergent an organism
must be to warrant this designation. "Abnormalities" in animals and
plants are recognized largely as a matter of convenience in order not to
complicate still further an already difficult taxonomic and morphological
situation.

Thus there are two concepts of what a norm is and therefore of what
is abnormal. One is a developmental concept: the norm or standard,
based on a specific protoplasmic pattern, to which the organism tends
persistently to conform. The existence of this norm is the basic fact in
biological organization. Its expression may vary greatly as the environ-
ment changes but it always remains as the core of the morphogenetic
process. In this sense, nothing is abnormal. The other concept of the
norm is a purely statistical or taxonomic one. In most species the de-
velopmental norms of its individuals do not vary widely in their expres-
sion since these individuals are genetically very similar and have been
exposed to a relatively narrow range of environmental influences. This
rather constant developmental expression may for convenience be re-
garded as a norm, and everything that differs from it substantially may
be called abnormal. It is in this statistical sense that the term "abnormal
growth" is generally employed.

The student of morphogenesis, however, does not put aside these in-
stances of abnormal growth and development as unimportant for his
purpose. Such may well prove to be more enlightening than most "nor-
mal" individuals. They are exceptions, extreme cases, and from exceptions
like these often come clues to the solution of particularly difficult prob-
lems. Furthermore, in many cases of abnormal growth certain levels of
the very quality that we associate with life— organization— have disap-
peared. Tissue cultures and many tumors and galls are formless, largely
unorganized masses of cells which no longer produce the beautifully
coordinated structures called organisms. Individual cells here must still
retain a basic, vital organization in their living stuff, for otherwise they
would die, but the higher levels of organization have now broken
down. In other types of abnormal growth quite the opposite change
has occurred and entirely new structures, specifically formed and well
organized though on a different plan, are produced, as in many insect
galls.

The subject of abnormal growth is therefore a promising one for stu-

Abnormal Growth 277

dents of plant morphogenesis since by the study of these unusual struc-
tures development may be examined at various levels and degrees of or-
ganization. Relatively little work has been done in this field, however,
and most of the results are descriptive and relate to mature structures.
In the few cases, such as crown gall, where many experimental and
developmental studies have been made, these have proved to be very
rewarding.

There is some confusion between the concepts of "pathological" and
"abnormal" growth. Pathology is concerned with questions about the health
and survival of the organism when it is attacked by parasites or sub-
jected to unfavorable conditions. Abnormal growth is often produced
by this means though here, again, it is difficult to draw the line. One would
hardly call the aecium of wheat rust an abnormal growth, but a crown
gall certainly is one. There are many cases of abnormal growth, on the
other hand, which clearly are not pathological, such as inherited fascia-
tions or the root tubercles of legumes. A student of abnormal growth is
not concerned with the health of the plant, nor does a pathologist ex-
amine primarily the ways in which the plants with which he deals
diverge from the norm. Historically, however, the two fields have been
close together, and Kuster's (1925) classic book on abnormal growth is
entitled "Pathological Plant Anatomy."

There is no very obvious way in which to organize the widely various
phenomena of abnormal growth. It will be most logical, perhaps, to
proceed from cases where divergence from the norm is relatively slight
and move to those where it is more extreme. In the present chapter
there will be discussed (1) the abnormal development of organs be-
longing to the usual categories, (2) the production of new types of or-
ganized structures, and (3) the production of amorphous structures.
The whole field has been briefly reviewed by Bloch ( 1954 ) .

ABNORMAL DEVELOPMENT OF ORGANS

In many cases structures still recognizable as leaves, stems, roots, flow-
ers, or other organs have been modified in many ways, sometimes very
radically. This is the field of teratology, the study of malformations,
freaks, and monstrosities, which has long excited the curiosity of bot-
anists (Moquin-Tandon, 1841; Masters, 1869; Worsdell, 1915; Penzig,
1921; and Heslop-Harrison, 1952). Little but descriptive work has been
done on most of them. For a long time their scientific value was chiefly
to morphologists, who looked to malformations for evidence as to the
morphological nature of certain organs. Thus the "metamorphosis" of
petals and sepals into leaf -like structures (phyllody; Fig. 11-1) suggests
that they are really leaves but have been modified in function during

278 The Phenomena of Morphogenesis

evolution. Heslop-Harrison lists three causes for such phenomena: ab-
normalities in growth, of little morphological significance; abnormalities
in development, owing to failure of hormonal systems or other form-

Fig. 11-1. Sepal phyllody. Sepal
of a rose flower showing abnor-
mal development into a structure
much like a foliage leaf. (From
T. E. T. Bond.)

determining factors; and minor abnormalities arising from genetic or
environmental causes. Some teratological changes may be reversionary
and some progressive.

Fig. 11-2. Left, normal tendril of Cucurbita. Right, abnormal structure intermediate
between a tendril and a foliage leaf. ( From Worsdell. )

There are various categories of these abnormal structures, or tera-
tomata (Figs. 11-2, 11-3), which are only loosely related to each other.
About certain of them a considerable literature has grown up. In many
cases the causal agent is known, but often it is not. Little developmental
work has been done on most of them.

Abnormal Growth

279

Organoid Galls. Under this term Kiister (1910) included many cases of
abnormal development or distribution of organs which are clearly the
result of parasitism, nutritional disturbances, or other known causes and
which often show little constancy of form or structure. Such galls may
appear at some distance from the site of the stimulating agent. With these
are usually included similar types of abnormalities even if their causal
factors are unknown.

In some of these galls it is chiefly the form that is abnormal. In the
leaves of various species of Juncus parasitized by Livia juncorum, for
example, the sheath reaches extraordinary size while the lamina remains
small or atrophied. In Populus tremula small stipules turn into large, leaf-
like structures. Eriophyces also produces floral abnormalities in which

Fig. 11-3. Abnormal flower of
gloxinia, with extra petal-like
structures on the outer surface
of the corolla and an increase
over the normal number of
corolla lobes. ( From Worsdell. )

stamens or carpels become petal-like. Flower buds that have been
grafted in a place where leaf buds would normally be sometimes produce
unusually large and abnormal flowers, evidently because of nutritional
changes.

Some of these changes are comparable to those occurring in regenera-
tion. Thus in vigorously regenerating shoots of Symphoricarpos simple
leaves become pinnately cut, and in regenerating stalks of Sambucus,
stipules may be converted into leaves. The removal of the main shoot
in the seedling of Vicia faba results in the formation of primary leaves
or transitional ones instead of those of mature type. It is well known
that decapitation, defoliation, and similar injuries lead to various
changes. Goebel (1882) thus obtained leaves instead of bud scales in
Prunus padus, and Blaringhem (1908) reported many morphological ab-
normalities due to wounding. The formation of cups or aecidia on

280 The Phenomena of Morphogenesis

leaves seems often to be due to nutritional disturbances. Bond (1945)
found that sepal phyllody in roses is an effect of hormones that control
the vigor of growth and the balance between reproductive and vegeta-
tive tendencies. This and other transformations of one sort of floral
organ into another may be compared to changes in sex expression that
have been found to occur after hormone treatment (Love and Love,
1946 ) or as the result of photoperiodic change.

In other organoid galls, abnormality consists in the formation of struc-
tures in places where they do not ordinarily occur. Thus ovaries may
appear in normally staminate flowers, stamens within an ovary, or
ovules on its surface. In the well-known case of Lychnis vespertina at-
tacked by the smut fungus Ustilago antherorum, stamens are produced
in the female flower ( Strasburger, 1900). Flowers and cones may pro-
liferate into vegetative shoots after attack by mites or for other reasons.
Cecidomyia causes the formation of rootlets on the stalk nodes of Poa
(Beyerinck, 1885) and Eriophyces fraxini small, shortened shoots on
the leaves of Fraxinus. The attack by mites sometimes results in the
growing out (enation) of small leaves on large ones or the formation of
extra perianths.

Familiar examples of abnormal development which may also be classed
as organoid galls are "witches'-brooms" (Fig. 11-4), dense clusters of
small, much-branched shoots, chiefly on woody plants and resulting from
excessive production of buds which grow immediately into shoots. At-
tacks by mites and various fungi, especially Exoascaceae and Uredineae,
are often the causal agents, though in many instances no parasites are
known to be involved. The physiological basis for the development of
such structures has been thought to be the accumulation of nutrients,
though doubtless there are other factors.

A rather extensive literature has grown up about the character and
causation of witches'-brooms, for which the reader is referred to Solereder
( 1905 ) and Liernur ( 1927 ) . Liernur cites 96 instances the causes of which
are known, occurring on 49 species of plants in 19 families, and 51 cases
of unknown origin. They differ in morphology, anatomy, and etiology but
resemble each other in their general character of copious, compact
branching. As compared with normal structures, the tissues of their leaves
and branches tend to be somewhat less highly differentiated, thus ap-
proaching cataplasmatic galls, though mechanical elements are often well
developed.

Fasciations. A special type of abnormalities of a rather distinct kind
and which may be classed with organoid galls are fasciations. These are
cases where a normally cylindrical or radially symmetrical plant part be-
comes flattened and elliptical in cross section to form ribbon-like or some-
times ring-like structures. The origin of fasciation has attracted a good

Abnormal Growth

281

deal of attention among morphologists. Much of the literature is reviewed
in the papers of Schoute (1936), Bausor (1937), and O. E. White (1948).
The term fasciation, like others in the field of abnormal growth, has
been applied to a rather wide variety of phenomena which probably have
different origins even though the final result in all of them is a flattened
structure. Frank (1880) distinguished between fasciations that arise by
a gradual expansion of the growing point in one plane and others that
come from lateral fusion or connation between two or more separate

Fig. 11-4. "Witches'-broom" on a fern leaf. (After Giesenhagen.)

structures, in natural self-grafting. Schoute believes that the term fasci-
ation should be limited to Frank's first category, and this is now the com-
monest practice. The difference between the two concepts can be deter-
mined only by developmental studies. Johansen (1930) has shown that
the genesis of fasciation may be recognized even in early embryogeny.

Fasciation is most conspicuous in the main-shoot axis but occurs also
in roots (Schenck, 1916) and may be found in almost all parts of the
plant. It may vary from one part to another. Many abnormalities resem-
bling fasciation are to be seen in leaves, such as "double" leaves and
others.

282 The Phenomena of Morphogenesis

Certain instances of fasciation have received special study. It has long
been observed that if the epicotyl of a seedling of Phaseolus multiflorus
is cut off and the buds in the axils of the cotyledons are then allowed to
grow they will produce flattened shoots. These later revert to a cylindrical
form and produce normal branches. This is an unstable kind of fasciation,
and the factors responsible for it are not yet clear (Sachs, 1859; Klebs,
1906; Georgescu, 1927; Bausor, 1937).

Fasciations resulting from other types of mutilations and from wounds
are discussed by Blaringhem ( 1908 ) . They frequently follow pruning in
Salix, Populus, Robinia, Tilia, and Corylus.

Various other factors, both external and internal, have been found to
produce fasciation. Growth substances applied in high concentration may
induce such vigorous local growth that ribbon-like structures result
(Bloch, 1938). In strawberry varieties that have a tendency toward fas-
ciation, this is emphasized by short day-lengths ( Darrow and Borthwick,
1954). It has been suggested that fasciation is due to a high level of
nutrition, to insufficient nutrition, to changes in correlation produced
by growth substances, and to various factors that have been shown,
in both normal and regenerative growth, to induce correlative disturb-
ances.

Of especial interest are those instances where fasciation, or a tendency
toward it, is inherited. The best known of these is in the cockscomb,
Celosia cristata, where the inflorescence is often much flattened. Heredi-
tary fasciation has also been found in Nicotiana (O. E. White, 1916),
Pharbitis (Imai and Kanna, 1934), and Phlox drummondii (Kelly, 1927).
The large-fruited varieties of tomato with more than two carpels may be
regarded as examples of genetic fasciation.

Fasciation is found in all groups of vascular plants. Penzig ( 1921 ) has
reported it for Psilotum and Lycopodium; Kienholz (1932) for Pinus, and
Schenck ( 1916 ) for other gymnosperms. It is widespread in angiosperms,
both dicotyledonous and monocotyledonous, and many instances are cited
by Masters. It is particularly frequent in Taraxacum, Antirrhinum, and
Delphinium and has even been found in the giant cactus, Carnegiea
gigantea.

Pelory. Pelory (or peloria) is a type of floral abnormality, quite dif-
ferent from the others that have been mentioned, in which dorsiventrally
symmetrical (bilabiate) flowers become radially symmetrical. It was first
discovered by Linnaeus in Linaria vulgaris, where it may frequently be
found in nature, and has been studied by Sirks ( 1915 ) and others ( Fig.
11-5). In this species peloric flowers, where they occur, are found at the
base of the inflorescence and may show a transition to normal ones at the
top. This is perhaps another instance of phasic development. Peloric
flowers have also been investigated in Linaria spuria, Antirrhinum majus,

Abnormal Growth 283

and Digitalis purpurea. Pelory is frequent in Labiatae, where it usually
occurs at the top of the inflorescence.

As to the cause of pelory, opinion is divided. In cases such as Digitalis
the difference between the bilabiate and the radial condition is clearly
induced by gravity for it can be reversed experimentally. Peyritsch found
that in Labiatae it may be induced by strong illumination. Sachs believed
that physiological factors are operative in causing it. There are many
cases, however, reported by Vrolik, Darwin, de Vries, Baur, Lotsy, and
others, where this type of abnormality, or at least a tendency to produce
it, is inherited.

Fig. 11-5. Peloric flower of Linaria
vulgaris, almost radially symmetrical.
(From Goebel.)

PRODUCTION OF NEW TYPES OF ORGANIZED STRUCTURES

In organoid galls and similar types of abnormalities that have been dis-
cussed, structures recognizable as those found in normal plants are
present, though their size, form, and arrangement may be altered and the
general pattern of organization distorted. In the group now to be consid-
ered the structures produced are entirely novel and cannot be placed in
any such morphological category as leaves or stems. They can hardly be
regarded as organs, but they are much more than tissue abnormalities
for they have a constant and specific form, size, and structure and a very
considerable amount of histological differentiation. They result from the
attack of parasites. In most cases they undergo a definite period of devel-
opment, or life cycle, correlated with that of the parasite and thus are
different from the cataplasmatic abnormalities to be discussed later. In
Kiister's terminology they are prosoplasmatic galls. There is no sharp line
between these and the simpler gall types but their large number and
definite forms set them apart as a rather distinct group. The majority are
zoocecidia (galls formed by animals). The most conspicuous and best
known owe their origin to parasitism by the gall wasps or cynipids, a
family of the Hymenoptera. Others are produced by flies of the gall
midges and simpler ones by mites. A few are the result of fungus parasites.

284 The Phenomena of Morphogenesis

Prosoplasmatic galls are so numerous and so remarkable in many re-
spects that they have received much attention and are the basis of an
extensive literature. They are discussed in many papers and books by
Beyerinck (1883), Molliard (1895), Magnus (1914), Thompson (1915),
Felt (1917), Kostoff and Kendall (1929), Kiister (1930, 1949), Ross
(1932), Carter (1939, 1952), and others. A typical example has been
described in detail by Hough ( 1953 ) .

The small galls produced by some of the rusts or by Synchijtrium pilifi-
cum on the leaves of Potentilla may perhaps be included among proso-
plasmatic galls, as may those formed on the petioles of Populus by
Pemphigus bursarius. Here the gall is simply a mass of expanded epider-
mal and cortical cells which have divided anticlinally.

Fig. 11-6. Insect galls on leaf of rose. (From Wells.)

There is a higher degree of organization in cynipid galls, and they have
received much more attention than any others (Fig. 11-6). In these the
female wasp deposits an egg in the body of the plant, where the larva
develops, and the gall results from the reaction of plant tissues to stimula-
tion from the egg and the developing larva. Such galls possess a concen-
tric type of organization. The histology of these structures is as varied as
their form (Figs. 11-7, 11-8). Some are relatively simple but others con-
sist of three, four, or even five different types of tissue. Some of these
tissues show adaptation to specific functions such as mechanical support,
storage, and aeration. The mechanical tissues are of particular interest be-
cause of their relation to the position of the larva within the gall and the
means of its escape.

The special morphogenetic significance of these galls is that in them a

Abnormal Growth

285

specific modification of the tissue pattern of the host plant is caused by
the presence in it of an egg and larva of the parasite. A given cynipid will
always produce the same kind of gall on a given plant species, and the
galls induced by different wasps on the same plant are quite dissimilar.
On Celtis occidentalis, Carter found 17 different sorts of galls formed by
17 species of wasps. Each type of gall is related to the character of the
larva that develops within it.

Doubtless the formation of these formed galls results from a specific
stimulus coming from the wasp or the growing larva and a specific re-
sponse by the tissues of the host plant, but how such a subtle control of

Remains of the egg membrane

Vein of the 2nd order of branching
Ruptured lower epidermis

Leaf upper epidermis

Vein connecting leaf and gall

Cup of platform cells

Additional sclerenchyma ring

Funnel-shaped sclerenchyma mass

Nutritive tissue cells

Plate-like sclerenchyma mass

Gall cavity containing larva

1 mm.

Large air-spaces region
Gall vascular stand

Stellate hairs
Gall parenchyma
Gall-stalk sclerenchyma
Gall epidermis

Fig. 11-7. Diagram of a longitudinal section through a cynipid gall on the leaf of oak,
showing its specific form and considerable structural differentiation. (From Hough.)

the morphogenetic potencies of the host cells is exerted by the parasite is
unknown. Various theories have been proposed and many experiments
performed to throw light on this problem. It has been suggested that the
gall-inducing stimulus is a mechanical one, but this seems rather unlikely,
and most workers now believe that the stimulus is chemical in nature,
perhaps an enzyme or a specific formative substance.

Many investigators have tried to extract the gall-forming agent from
the insect, inject it into a plant, and thus produce a gall artificially, but
earlier attempts all failed. Recent ones have been more successful. Parr
(1940) and Plumb (1953) injected extracts from the salivary glands of
coccids and an aphid into young needles of Norway spruce and induced
the formation of galls much like those normally produced by these insects.

286 The Phenomena of Morphogenesis

K. M. Smith (1920) had shown that the damage to leaves of apple by
capsid bugs was caused by secretions of the salivary glands, and this sug-
gested the possibility that the glands of the gall-producing larva secrete
an enzyme which calls forth a specific growth reaction in the host tissue.
Parr demonstrated the presence of enzymes in the gland extract but found
that these did not stimulate gall formation when sterilized. Martin

T

Fig. 11-8. Section through portion of an insect gall showing modification of normal
leaf structure (left). The larval chamber is surrounded by mechanical tissue. (From
Kiister. )

(1942), however, produced abnormal growth in sugar cane with steri-
lized extracts.

Substances produced by the growing larva rather than those injected
with the egg are probably most important in gall formation. Little is
known about these substances, however, or the place and manner in which
they are introduced into the tissues of the plant (Kostoff and Kendall,
1929).

A morphological problem of some interest is whether these galls and

Abnormal Growth 287

the tissues that compose them are really to be considered as "new"
structures, morphologically different from the familiar categories. Cer-
tainly they have cells and tissues unlike any normally found in their host
plants. Such are the various hairy projections on the surface of certain galls,
the opening mechanisms, the mechanical tissues, and others concerned
with nutrition and aeration. As to whether these are "new" or not depends
on our definition of that term. A given morphological category, such as
the leaf, presumably has a continuous evolutionary history beginning
with early vascular plants. It is part of the norm of plant structure. In
this sense such galls are certainly new. They have arisen, however, be-
cause of a novel factor in the plant's environment-the gall wasp. It seems
probable that if such wasps had existed in the Paleozoic they would have
induced galls in the vascular plants of that era. Gall-making ability on
the part of the wasp is advantageous to it and doubtless has been devel-
oped by selection, but the gall response by the plant to the parasite is not.
Presumably the capacity for producing these galls has long been among
the developmental potencies of plants. It can be regarded as new histori-
cally but not morphologically.

From the morphogenetic point of view the most important fact about
these prosoplasmatic galls is that they are highly organized and specifi-
cally formed structures induced by an outside stimulus. Here we can see
the process of form determination manifest in a simpler fashion than in
normal development, for here the inducing agent is not a part of the
developmental mechanism but is introduced into the organism. If we
understood exactly how these galls are formed, we should doubtless gain
some important clues as to the morphogenetic process generally. Some-
thing more is involved here than partial loss of organization, the change
that takes place in most other galls. Here is operating a constructive, not
a degenerative, process.

AMORPHOUS STRUCTURES

In the two previously discussed categories of abnormal growth the
original organization was either present in altered form or something
entirely different from the normal was produced. There is a third group
in which organization at its highest level, with the production of specifi-
cally formed structures, is inoperative to a large degree, and only form-
less, or amorphous, structures are developed. Within these structures
there may be some histological differentiation but it is much less than in
normal tissue. The cells remain alive, however, and perform many normal
physiological activities. They must still possess a certain amount of organ-
ization, evident in regulatory action. If this were not so, death would
ensue.

288 The Phenomena of Morphogenesis

There are various sorts of amorphous structures which are not easy to
distinguish from each other, but a number of categories may be recog-
nized, such as intumescences, callus, tumors, and galls. The terms "gall"
and "tumor" have no very precise meanings, but a gall is most commonly
regarded as an anomalous growth due to an attack by a parasite and a
tumor as one which results from other causes, though there are many
exceptions to these definitions.

Intumescences. The simplest sort of amorphous abnormal growth is one
in which a group of cells at the surface of an organ expands into a wart
or pustule. These are termed intumescences (Sorauer, 1899) and result
from various causes (Wallace, 1928). Sometimes, as on the leaf of cab-
bage (Von Schrenk, 1905), they are groups of watery (hyperhydric) cells,
swollen by excessive absorption of water resulting from contact with
spray materials or other substances. In woody plants intumescences
usually are formed by proliferation of cork cells, sometimes from lenticels
and sometimes elsewhere. Such intumescences involve an increase in the
cell number (hyperplasia) as contrasted with an increase in cell size
(hypertrophy) as in the cabbage leaf. They may result from exposure to
ethylene gas and other substances. Intumescences often resemble natu-
rally occurring corky spots on certain plants, especially at lenticels.

Callus. As a result of wounding, a layer of cork cells is usually produced
over the wound surface through the action of wound hormones (p. 402).
This perhaps is not to be called "abnormal" tissue in the ordinary sense,
since it is very common and indeed accompanies bark formation in trees,
where new cork layers cover the breaks resulting from expansion of the
axis. In many cases, however, these do not occur in the intact, uninjured
plant and may best be included among abnormal structures.

In cases of more serious wounds, as where a cutting is removed for root-
ing, something more complex than a few layers of cork cells is formed
at the surface. Here often develops callus, an amorphous mass of rather
large-celled, loosely arranged parenchymatous tissue, produced by cell
division in the ground tissue or more commonly from cambium (Fig.
11-9). Its elements show relatively little differentiation, but there may be
some meristematic growth near the surface. For its nutrition, callus de-
pends on food from the normal tissues beneath it.

A callus may reach considerable size but its mass has no definite form
and there is little morphogenetic control over its growth. In its later
stages, callus may undergo various types of development depending on
the kind of plant, the location of the wound, and the external conditions.
Often some differentiation appears in it, and cells are produced resem-
bling those of normal tissue. Isolated nests of single cells or groups of
cells may develop into tracheid-like elements, usually with reticulate pit-
ting. Sclereids are formed in the same way. These irregular nests have a

Abnormal Growth 289

characteristic appearance, and their presence often indicates the origin
of a meristem in the callus.

The structure and arrangement of the cells in such wound tissue as
callus are often atypical, especially near the wound itself. The cells twist
and turn, and so-called "whorls" thus formed have been described by
Maule (1896), Neeff (1914), and others. Krieg (1908) observed several
concentric circles of cambium in the pith of ringed branches of Vitis
adjacent to a wound. In the outer ring, development was inverted, phloem
being formed toward the inside and xylem toward the outside.

Fig. 11-9. Callus on cut stem of Cleome produced by application of growth substance.
( Courtesy Boyce Thompson Institute. )

Save under particular conditions, a callus does not remain callus
indefinitely but tends to produce normally organized structures again.
This it does by means of new apical meristems, both of shoots and roots,
which frequently appear in it. Such meristems arise in several ways. Cells
abutting on nests of tracheids may produce a meristem in the form of a
hollow sphere. Others may appear elsewhere in the callus or where it is
in contact with the pith, cambium, or cortex. These meristems may form
secondary wood or phloem. Meristems of roots tend to arise well below
the surface and those of shoots either at or just below the surface. From
such meristems typical organs may be regenerated in any region of the
callus, thus showing that there have been no fundamental changes in
the genetic character of the callus cells themselves. Their potencies to
produce typically organized structures have been masked but not lost.

290 The Phenomena of Morphogenesis

Structures much like calluses may be induced by other factors than
wounding, especially by various chemical substances. Among these sub-
stances are ether, chloroform, camphor, ethylene gas, liquid paraffin, and
especially various growth substances (p. 407). Many are nonspecific in
their action, and it is to be assumed that their effect is primarily one of
injury to the tissues, which produces changes in the cells and thus leads
rather indirectly to atypical growth reactions. Others, especially the
growth substances, produce rather specific reactions.

One of the properties of the synthetic growth substances (such as in-
doleacetic, indolebutyric, and naphthaleneacetic acids and paraffin) is
their action in stimulating an increase in the number and the size of cells
to which they are applied. Sizable overgrowths and calluses may thus be
formed on various plant organs if sufficiently high concentrations of these
agents are applied; and if this treatment is repeated, tumor-like masses
are produced (Schilling, 1915; Brown and Gardner, 1936; Kisser, 1939;
Levine, 1940; and others ) . These often resemble the ones associated with
certain bacterial infections.

Callus-like overgrowths are more readily obtained if the paste in which
the inducing substances are carried is applied to the more sensitive
regions such as those near the shoot tips, particularly after decapitation.
Many experiments have been performed, especially on herbaceous dicoty-
ledons, to test the effects of various growth substances on development
(see especially the publications from the Boyce Thompson Institute and
those of E. J. Kraus and his colleagues at the University of Chicago,
p. 405). Differences have been found among the growth substances in the
character and extent of abnormal growth they induce, and their effects
are also related to the kind of plant, its age, and the region treated. His-
tological study of these tumors shows that they resemble other calluses
and wound tissues, especially in the absence of a constant form or size,
the presence of some cellular differentiation as the tumor ages, and the
development on them of root and shoot primordia.

Amorphous Calls Produced by Parasites. Amorphous structures which
in certain respects resemble intumescences, calluses, and chemically in-
duced tumors are caused by various parasites such as nematodes, mites,
insects, fungi, and especially bacteria. Even viruses are now known to be
involved in their production (Black, 1949). There is a great variety of
these, from small, simple structures to large and relatively complex forms.
Some of the huge burls on trees are due to parasites but others apparently
are caused by mechanical or other nonparasitic factors. Many amorphous
galls have a somewhat more highly organized character than others but
they show little constancy in size or form and their histology is less
regular and their differentiation simpler than in normal structures. Kiister
describes and figures many of these (1903a, 1911, 1925). He gave

Abnormal Growth

291

them the name by which they are now commonly known, cataplasmatic

galls.

Crown Gall. Here belongs the gall that has been studied more inten-
sively than any other, crown gall (Fig. 11-10). This is produced on a
wide variety of plants, at least 142 genera in 61 families, by the bacterium

Fig. 11-10. A crown gall on sunflower. (Courtesy Department of Plant Pathology,
University of Wisconsin. )

Agrobacterium tumefaciens. There are reviews of work on such galls by
Levine (1936); Riker, Spoerl, and Gutsche (1946); de Ropp (1951a);
Klein and Link (1955); and Braun and Stonier (1958). Crown gall has
been investigated by Erwin F. Smith and his colleagues ( 1911, 1917, and
many others) and later by various botanists among whom Braun,

292 The Phenomena of Morphogenesis

Gautheret, Levine, Riker, de Ropp, and P. R. White have been especially
active.

The inception of a crown gall seems always to come by means of a
wound. In the early stages of this infection the reactions of the host cells
produced either directly or indirectly by the parasite are much like wound
reactions, but in the young gall the new cell walls soon lose the regular
arrangement found in wound tissues. Reparative wound calluses and those
formed at grafts often resemble the early stages of crown gall, but as the
gall develops, rapid cell division occurs in the outer layers and a large
mass of callus is formed. The great difference between crown gall and
ordinary callus, however, is that the latter is self-limiting and soon be-
comes quiescent whereas gall tissue is capable of indefinite and amor-
phous growth. This is a fact of particular morphogenetic significance.
There is now good evidence that the cells of crown gall have undergone
a permanent change in character. This seems to involve an acquirement
of the capacity for autonomous growth, which may result, Rraun ( 1958 )
believes, from the permanent activation of a series of systems by which
growth substances are synthesized. In normal cells these systems are
precisely regulated and growth ultimately stops. Normal cells in cul-
ture require auxin from an outside source but crown-gall cells do not.
Crown gall thus differs from most other galls, which are self-limiting and
do not grow indefinitely. In some cases the crown gall matures, stops
enlarging, and undergoes some histological differentiation. Nests of vascu-
lar cells, chiefly xylem, appear in it (Fig. 11-11), and the primordia of
roots and shoots may develop. The cytological and histological changes
in the development of a typical crown gall have been described by Ther-
man (1956) and Kupila (1958).

The process of conversion of normal cells into tumor cells is a gradual
one. Its inception depends both on a wound stimulus and on the pres-
ence of an auxin ( Rraun and Stonier, 1958 ) . Tumors differ in appearance,
in the degree of their organization, and in their capacity for growth. These
differences may be the result of their location on the plant, the virulence
of the strain of infecting bacteria, or other factors. Crown-gall tissues
can be grafted into normal ones, and these may be carried through an
indefinite series of graft transfers. There is no good evidence that they
induce adjacent normal tissue to form tumor cells, though temporary
alterations may take place there. Gall tissues can readily be grown
in culture and can then be grafted back to normal ones and form galls.
In all these cases their cells remain unchanged.

In a few plants secondary tumors may develop, often at some distance
from the original gall or primary tumor. In certain cases this results from
an infection near the apical meristem and a subsequent separation of
the secondary from the primary gall by growth. Sometimes, however,

Abnormal Growth

293

secondary galls develop after growth in length is over but always in close
association with the xylem, as though the latter were the pathway of
induction. Secondary tumors behave much like primary ones in grafts
and in culture, and there seems to be no very fundamental difference
between the two.

Remarkably enough, many crown galls, particularly secondary ones,
seem to be free from bacteria. There is evidence, however, that bacteria
must always be present at the very beginning of tumor growth but
that they soon disappear. Braun and White (1943) made Vinca rosea

Fig. 11-11. Section of a young crown gall on Pelargonium, showing a nest of vascular
cells. ( From Noel. )

galls free of bacteria by heat treatment. Such tissues retained their gall-
producing properties when grafted into healthy plants (White, 1945).
Although bacteria are required for the inception of crown gall, once the
change is induced they no longer seem necessary for the growth of gall
tissue.

Crown gall (and presumably other amorphous galls of this general
type) does not result from a single cause but involves a series of factors.
Klein and Link ( 1955 ) discuss this in their extensive account of the
etiology of crown gall (Fig. 11-12). There is first a conditioning phase,
perhaps induced by wounding and involving wound hormones. This
makes the cells susceptible to conversion into tumor cells. It is possible

294 The Phenomena of Morphogenesis

that the activation process in ordinary wound healing and in the incep-
tion of tumors may be the same. This is followed by an induction phase
in which a tumor-inducing substance of some sort enters the host from
the bacterium. A heat-labile product of virulent crown-gall bacteria has
been found to alter conditioned cells into incipient tumor cells. How this
is done is not clear. The substance may itself be the agent of change,
possibly a virus or a macromolecule of DNA or even a gene or a
hereditary agent in the cytoplasm; or it may induce the change by
causing gene mutation or the production of permanent, self-reproduc-
ing bodies, sometimes called plasmoids. Finally, in the promotion phase
the gall grows to completion. Here auxin is involved, in the promotion of
an incipient into a primary tumor cell, in the multiplication and per-

PRIMARY TRANSFORMATION PERIOD

CONDITIONING
PHASE

INDUCTION
PHASE

PROMOTION and COMPLETION
PHASE

CONDITIONED
CELL |

MtltH

Tumor- inducing

principle

INCIPIENT
TUMOR CELL

* t.t
Auxin

Auxin

Tumor-inducing
I principle i |

Mill'1

- $■ *"

AGROBACTERlUM TUMEFACIENS

PROMOTED
CELL

PRIMARY
TUMOR CELL

WOUNDING

N0CULATI0N

Fig. 11-12. Diagram of probable interrelations of various factors in the transformation
of a normal cell into a primary tumor cell. ( From Klein and Link. )

haps the differentiation of tumor cells, and in causing various host effects
which accompany tumor formation. The physiology of crown-gall for-
mation has been further discussed by Klein (1958).

A question often raised is whether crown gall and its derivatives are
really plant cancers, as Smith vigorously maintained they were, or if
something different from true cancer is here involved. This question
has been discussed by Levine (1936), White and Braun (1942), and
others. It should be remembered that such a condition as malignancy
is difficult to define in the same terms in organisms as different in struc-
ture and organization as plants and animals. The unrestrained, invasive
type of growth characteristic of animal cancer, with its metastases and
lethal quality, could hardly be expected in a plant, which has no true
circulatory system and lacks the high degree of organization that makes

Abnormal Growth 295

animals so vulnerable. The animal cancer cell has lost its specificity and
become, so to speak, an independent parasitic entity of unlimited
growth. What this change involves and what causes it are still not
understood. Crown-gall tumor cells are certainly in this same category
for they grow indefinitely and do not depend on the continual presence
of the factors that induced them. The true cell invasions and metastases,
in which bits of cancer tissue are carried away to other parts of the body
and there develop new centers of malignancy, are absent in plants, but
transfer of gall tissue from place to place by grafting is readily ac-
complished. Many students of the problem are inclined to regard crown-
gall tumors as basically no different from animal cancers. It is obvious
that these examples of abnormal growth provide some of the best ma-
terial known for a study of the way in which the higher levels of or-
ganization in the plant are broken down. For students of morpho-
genesis they long have had a particular interest.

Root Nodules. Another type of cataplasmatic galls rather different
in character from the others here described and of much practical im-
portance to man are the nodules formed on the roots of leguminous
plants from the invasion of their cortical tissues by species of Rhizobium.
They are an example of what has been called "controlled parasitism,"
for the relation between this bacterium and the plant may better be
regarded as symbiosis rather than parasitism since the host plant ob-
tains an advantage because of the atmospheric nitrogen fixed by the
bacteria. These nodules have a higher degree of organization and pro-
duce more specialized structures than do most cataplasmatic galls
and perhaps should be included under prosoplasmatic ones (Allen and
Allen, 1953). The particular character of the nodule depends upon the
host plant and the species of bacterium that invades it. As in crown
gall, auxin action mav here be involved.

Abnormal Growth Due to Other Causes. Manv cases have been re-
ported of abnormalities due to other factors than parasitism or chemical
stimulation. X rays may produce them ( Sankewitsch, 1953), as may
ionizing radiations (Gunckel and Sparrow, 1954). Some resulted from
the A-bomb tests in the Pacific (Biddulph and Biddulph, 1953).

In some plants tumors arise from no recognizable cause and are
presumably due to somatic mutations or to a modification of organized
development by other genetic factors. The best known case is that of
the tumors occurring spontaneously in hybrids between Nicotiarui
glauca and N. Langsdorfii (Kostoff, 1930a; Kehr and Smith, 1954). These
are small amorphous structures appearing on stems and branches, and his-
tologically resembling wound callus and crown gall. Kostoff believes that
they are due to a disturbed growth balance, either in nucleus or cyto-
plasm, between these two particular species. These tumors, removed

296 The Phenomena of Morphogenesis

from the plant, are the ones used by P. R. White in his first tissue cul-
tures (1939). He found later that they retained their specific proper-
ties in culture for years and continued to grow as tumors when grafted
into young stems of Nicotiano glauca (1944). Satina, Rappaport, and
Blakeslee (1950) studied the development of somewhat similar tumors
appearing in fertilized ovules from incompatible crosses in Datura.

Changes in cellular character are sometimes associated with abnormal
growth. Prothallia of some ferns, when grown in culture, often produce
various types of proliferations (Partanen, Sussex, and Steeves, 1955).
Some of these remain essentially prothallial in character and show no
fundamental deviation from normal. Their cells are still able to re-
generate normal prothallia again. Certain tumor-like forms, however, are
modified much further, for they have lost this ability. This loss is ac-
companied by a modification in cellular character, visible as an increase
in chromosome number from In to 3n or 4n. Such forms may be com-
parable in a sense to crown gall. White and Millington (1954) have
described a woody, nonbacterial tumor in spruce which begins in a
single cambium cell. This has been altered, physiologically or geneti-
cally, and forms a mass of abnormal tissue. The plant becomes what is
essentially a sectorial chimera.

Various aspects of the problem of plant tumors have been discussed
by P. R. White (1951), de Ropp ( 1951a ), Klein and Link (1955), and
others.

Tissue Cultures. Tissue cultures can hardly be called tumors or galls,
but in them the normal organization of the plant has disappeared to a
greater extent than in any other case here discussed. A book on mor-
phogenesis is not the place to consider this subject in any detail but it
does have some important morphogenetic implications that should be
mentioned. So-called tissue cultures of plant material on sterile media
have been studied actively in recent years, and for an account of them
the reader is referred to the publications of the pioneers in this field,
especially P. R. White, Robbins, Gautheret, and Nobecourt.

Animal tissues have been cultured for half a century but it was much
more recently that this was done successfully with plants. The problems
involved were first clearly stated by Haberlandt, who himself failed to
grow isolated cells from higher plants in artificial media. A necessary
prerequisite for the success later attained was the development of
satisfactory media consisting of pure substances of known chemical
character, including salts, carbohydrates, organic nitrogenous materials,
vitamins, and growth substances. The media developed by the early
plant workers were superior to the sera and other complex and little
understood ones previously used by tissue culturists.

The first plant cultures were not tissue cultures in the strict sense that

Abnormal Growth

297

they consisted of only one kind of cells, as in many animal cultures.
Most were really organ cultures. Those grown from root tips can be
carried through an indefinite number of subcultures and produce large
masses of root tissue. Shoot axes may be cultured in the same way
from apical meristems, and Nitsch (1951) and others have succeeded
in growing fruits from small primordia. Leaves can be grown to maturity
in the same way (Steeves and Sussex, 1957), as also can ovules
(Maheshwari, 1958). These organ cultures have given much informa-
tion on the nutritional requirements of various parts of the plant and have

Fig. 11-13. Culture of stem callus of tobacco on nutrient agar, six weeks after trans-
fer to new medium. (Courtesy Department of Plant Pathology, University of Wis-
consin. )

been of importance for an understanding of their physiology. Wet-
more (p. 222) grew fern plants from shoot apices in culture and found
pronounced morphological effects of differences in the medium, a re-
sult of much morphogenetic significance.

Something closer to a true culture can be attained by growing calluses,
tumors, parenchyma, and bits of tissue from the cambial region (Fig.
11-13). Structures much like amorphous tumors and galls result. In these
the strict morphogenetic control is relaxed and the explanted material
may be grown in unlimited quantities by subculturing. Such cultures
have been made of spontaneous tumors and of secondary crown gall.

298 The Phenomena of Morphogenesis

Gautheret (1945) showed that with ordinary plant material, as in carrot,
endive, and various woody plants, a callus must first be allowed to de-
velop from an excised piece and that this callus could then be cultured.

There are many differences between species and between different
parts of the same plant as to growth and structure of the culture pro-
duced. Pieces of tissue from the cambial region, for example, which
retain some degree of organization for a time, gradually lose it in
successive transfers. Some cultures finally become essentially homo-
geneous masses of parenchyma. In a few cases, however, patches and
whorls of tracheid-like tissue appear in these, as do meristems of roots
and shoots. The conditions under which this differentiation occurs vary,
depending in part on the source of the material and especially on the
character of the nutrient medium and the age of the culture.

It is now possible to produce plant cultures where the cells are not
united into masses but grow and divide as individual cells, much as they
do in certain animal cultures. This may be thought of as representing
the lowest level of plant organization, the loss of all relationships above
the single cell. Among those who have done pioneer work in this
field are Muir, Hildebrandt, and Riker (1954, 1958); de Ropp (1955);
Nickell (1956); Reinert (1956); Torrey (1957a); and Tulecke (1957).

Of particular interest for morphogenesis is the culture work of Steward
and his collaborators (1958 and p. 75). Using a basic liquid culture
medium supplemented by coconut milk and continually rotated, they
grew small explants of carrot tissue taken from the phloem of the
root. Single cells here often became separated and floated freely, dividing
very irregularly and growing into small cell aggregates. When these
reached a certain size, the cells at the middle of the aggregate began to
show differences from the rest, and some developed as tracheid-like struc-
tures, surrounded by a ring or sheath of cambium-like cells. From this
center, one or more root meristems developed. When such an aggregate
is grown on the surface of an agar medium it produces a shoot meristem
and in time a carrot plant. So far, a whole plant has not been produced
directly from a single cell but only by way of a cell aggregate. It is sig-
nificant that although bits of carrot phloem tissue, placed directly in
culture with coconut milk, may form large masses of callus-like tissue,
they much less readily produce roots and shoots, perhaps because of
inhibiting substances still present in them.

Radical though the changes are which plant tissues display when
cultured, there is no evidence that any permanent or genetic effect is
produced in them or any new developmental potencies induced. A con-
siderable degree of morphogenetic control has been relaxed, just as it
has been in amorphous galls.

It is evident that there is an immense amount of information available

Abnormal Growth 299

about abnormal growth but that students of morphogenesis have not as
yet made very much use of it for their purposes. Three facts, however,
which emerge from a study of this subject have already proved to be
of much morphogenetic significance:

1. The actual developmental potencies of most plant cells are far
wider than ever come to expression in normal development.

2. It is possible to break down the organization of the plant body into a
series of successively lower levels and then to restore normal organiza-
tion again.

3. This can be done without modifying the genetic character of the

cells.

A continued study of these facts, and of others in this field, will cer-
tainly prove very fruitful. Abnormal development is only development
under unusual conditions, and the wider spectrum of morphogenetic
information thus made available provides the student of development
with a powerful tool for the study of some of his most difficult problems.

PART THREE

Morpho genetic Factors

CHAPTER 12

Introduction to Factors

In earlier chapters various morphogenetic phenomena were discussed,
but relatively little was said as to the factors that produced them. There
now remains the task of relating these phenomena to changes in the
outer or inner environment of the plant and attempting to account for
their origin. This is really a part of the broader field of plant physiol-
ogy, and no sharp line can be drawn between the two. Much of physiol-
ogy, particularly those parts of it that deal with the various metabolic
processes, is not of primary interest for morphogenesis. Other parts of
it, however, such as photoperiodism, vernalization, auxin action, water
relations, and the carbohydrate-nitrogen ratio, for example, have much
significance for the morphogenetic phenomena of polarity, differentia-
tion, regeneration, and others. To present these morphogenetic implica-
tions adequately would mean going more deeply into plant physiology
and its vast literature than can be attempted in the present volume. No
discussion of the problems of plant morphogenesis would be com-
plete, however, without some mention of the physiological factors which
influence development so powerfully. The purpose of this final section
of the book is to introduce the reader to the more important of these
factors and to provide him with an entry into the literature of the sub-
ject. No attempt will be made to discuss them thoroughly from the point
of view of plant physiology.

It is first necessary to consider the relation between the two chief
sorts of factors— environmental and genetic. A living plant is an or-
ganized system maintaining itself in a complex and changing environ-
ment. Its genetic constitution (or genotype) remains unaltered save for
occasional doubling of the chromosomes in local areas or the rare oc-
currence of somatic mutations. Despite this, the plant does not remain
unchanged. Its appearance (or phenotype) is often greatly modified as
the environment is altered, and we commonly say that this change is
the result of an environmental factor. So, in a sense, it is, but there is
often difficulty in disentangling the effects of heredity and environment
in morphogenetic changes. One should remember that both are always

303

304 Morphogenetic Factors

operating. A visible trait is the developmental reaction of a specific
(and constant) genetic constitution to a specific environment. Every
trait is therefore inherited since it will always be produced if the en-
vironment is of a certain sort. In some traits the expression of the genetic
constitution is essentially the same under a wide range of environments.
The relative position of the floral parts, for example, the arrangement
of the leaves, or the character of the pitting on the side walls of the
vessels in the wood is usually quite unchanged under various condi-
tions of light, moisture, temperature, or auxin concentration. Such
traits, for this reason, are especially useful in taxonomy. Others, such
as the height of the plant, the thickness of the cuticle on its leaves, and
whether it flowers or not, may be very different under different condi-
tions of nutrition, water supply, and photoperiod. Such traits
are usually said to be determined by environmental factors. Actually,
both types of traits are inherited and both are environmentally deter-
mined. In the former, the repertoire of responses of the genetic constitu-
tion to changes in the environment is relatively meagre whereas in the
latter it may be very wide. Under a given length of day, for example,
salvia plants will flower but lettuce plants remain entirely vegetative.
What promotes or inhibits flowering is not simply the day-length but
the different inherited responses of these two plants to this day-length.

Where the developmental response of a plant varies widely under
different environments as it often does when such factors as light or
water or auxin concentration are changed, the obvious way to study the
morphogenetic processes concerned is to use genetically uniform ma-
terial but to change one or another of the environmental conditions
under experimental control. This method has proved very successful and
has yielded a great body of information as to the relations of environ-
ment to plant development. This has been by far the most fruitful
method of morphogenetic analysis since it lends itself so readily to ex-
perimental attack.

Traits in which environmental changes have little effect on the de-
velopmental expression of the genetic constitution can be studied by the
usual techniques of genetics. These consist primarily in maintaining a
constant environment, crossing genetically pure stocks that show dif-
ferent aspects of the trait to be studied, and analyzing the results in
subsequent generations. There is much less opportunity here to modify
the variables, for the genes themselves can be altered only with great
difficulty and in an unpredictable fashion. The rise of biochemical
genetics, however, is providing a much wider basis for experiment here.

A question often raised in the discussion of these environmentally in-
duced characters is whether they are adaptations and thus may serve to
maintain the life of the plant. Many structural traits, such as the much

Introduction to Factors 305

reduced leaf size of microphyllous xerophytes, the nectaries in many
flowers, or the wound cork produced on an injured surface, are present
under almost all environments and are so deeply embedded in the
genotype, so to speak, that the only way they may be changed is
through genetic mutation. They have doubtless arisen by means of
natural selection, and their adaptive character is due to this fact.

Other traits, such as the shape and structure of the leaf blade in
heterophyllous plants, the degree of development of vascular tissue in
the stem, or the place of origin of roots and shoots along a regenerating
axis, are often subject to very wide differences, depending on light, water,
auxin concentration, mechanical stresses, and other factors. Though they
can be greatly modified experimentally, these changes seem in most
cases clearly advantageous under natural conditions and are thus to be
regarded as adaptations. The adaptation here (doubtless also the result
of natural selection) is not a specific and unchanging structure but the
tendency to react developmentally in a favorable way as conditions
change.

It seems clear, however, that in many other cases, where there is a
wide range of developmental differences induced by changes in the en-
vironment, these are not adaptive or favorable for survival but are
neutral in this respect. The degree of lobing in a leaf as affected by
temperature, the relative abundance of male and female flowers as
affected by nutritional factors, or the shape of the fruit as affected by the
size to which it is able to grow seem none of them to have significance
for survival. Such traits appear to be simply accidental developmental
results of the interaction between genetic constitution and environment.
Among these, particularly the ones induced by extreme environmental
changes, are some of the most interesting for morphogenesis. It is there-
fore necessary to divorce completely the problem of adaptation, which
is an evolutionary one, from that of the environmental induction of
characters, which is a morphogenetic one.

In studying the various factors that are important in plant develop-
ment, emphasis in some cases is put on changes in the environment-
external and internal— and in others on changes in the genetic constitu-
tion. This is purely an arbitrary classification, however, and simply for
convenience. In the present treatment of the subject morphogenetic
factors will be discussed in several general groups. Some, such as light,
temperature, gravity, and some mechanical factors, originate chiefly in
the external environment though their effects, of course, are produced
internally. They may be grouped together as physical factors. Among
these is included water, since its morphogenetic effects (as opposed
to its physiological ones) are due not so much to its chemical composi-
tion as to the physical processes of its absorption and evaporation.

306 Morpho genetic Factors

A second group are the chemical factors, which derive their impor-
tance primarily from their participation in the chemical processes going
on in the plant. Some substances, notably those in mineral nutrition,
come into the plant from the outside, but many originate internally as
products of the plant's metabolism. Especially important in morpho-
genesis are the various growth substances.

A third group of factors, the genetic ones, may also be regarded as
part of the internal environment. Here are to be considered the genes,
permanent and self-perpetuating; the chromosomes, which may have
certain morphogenetic effects apart from the genes they contain; and
the cytoplasm, the intermediary between genes and developmental
processes. These factors, though doubtless effective because of their
physical or chemical character, are difficult at present to reduce to such
terms and are best considered by themselves.

The effects of these various factors on development are complicated
by the fact that they are operating on an organized living system which
tends to regulate its activities in conformity to a specific norm. Three
consequences of this should be borne in mind:

First, a given factor does not lead directly to a given result but serves
instead as a stimulus or evocator that sets off a reaction in the organism.
What this will be depends on the state of the system at the time. The
effect of light on a photographic plate is easily predictable, but its effect
on a plant depends on the part of the plant concerned, the age of the
plant, and its physiological condition.

Second, the effect of one factor may be greatly modified by another.
The photoperiodic effect of light, for example, may depend in a given
case on the temperature of the environment, so that one factor may
sometimes be substituted for another. Although the essence of good
experimental work is to deal with only one variable at a time, this often
is impossible in morphogenetic experiments (and in biology generally)
for no one factor can be studied entirely independently of the others.
What it will do depends on the rest of the environment and on the state
of the organism.

Third, the organized system is not a constant one but tends to change
in character from one phase in its life cycle to the next and from one
region of the body to another. The potency of a cell (the repertoire of
developmental possibilities open to it), high at first, is reduced as the
cell grows older. Doors continually close behind it, so to speak. The
reactivity of a cell (the response it will make to a given environmental
change) also is different at successive developmental stages. Both
potency and reactivity may be unlike in different parts of the organism.

An investigation of the effects of various factors on plant develop-
ment, particularly environmental ones, though not as simple as might

Introduction to Factors 307

at first appear, may still be very fruitful. It is often possible to examine
the effects of changes in one factor without serious complications from
others, and the organism does remain essentially constant over short
periods. The very considerable knowledge now available as to the
factors that modify plant development has proved most important for
an understanding of the problems of morphogenesis, and there are wide
possibilities for extending it much further. The next seven chapters are
devoted to a brief consideration of the operation of these factors.

CHAPTER 13

Light

Light is a powerful factor in determining the course of development in
plants and has a much more important morphogenetic effect on them
than it does on animals. This is to be expected, since light is necessary
for photosynthesis and thus for the production of food. Experiment has
made it clear, however, that the morphogenetic influence of light is
much more subtle and indirect than this and results from its control not
only of food production but of various physiological activities in the
plant by which this food is distributed in the processes of growth and
differentiation. The role of light in plant development has been studied
actively for many years and is the basis of an extensive literature. Among
the more inclusive reviews of this field are those by MacDougal ( 1903<7 ) ,
Burkholder (1936), and Parker and Borthwick (1950).

Many of the early results are invalid because of the impossibility in
those days of exact control of light, as to its intensity and quality, in
experimental work, but most of these difficulties have now been over-
come, and light in a plant's environment can be manipulated with
relative ease.

It is a matter of common observation that plants reach their greatest
size and vigor in good light and that insufficient illumination results
in weak and spindly growth even if water, soil nutrients, and tempera-
ture are at their optimum levels. Most of the experimental work with
light has involved not merely differences between light and darkness
but measured differences in the light stimulus itself. Three of these are of
chief importance: the intensity, the quality, and the duration of the
light. Intensity is the brightness of the illumination, the actual energy
of the radiation. Quality concerns the wave length of the light. Dura-
tion refers to the relative lengths of the alternating periods of light and
darkness to which the plant is exposed. These differences are not always
sharply separable, and one often modifies the effects of another.

308

Light 309

INTENSITY OF LIGHT

Since rate of photosynthesis increases with light intensity, up to a cer-
tain point, the growth and vigor of a plant are generally proportional,
within limits, to the brightness of the light to which it is exposed.
Shirley (1929) grew a variety of plants in different intensities of day-
light and found that at low ones dry weight was directly proportional
to intensitv but that at higher ones growth was relatively less. He ob-
served that intensity also affected certain qualitative traits, such as ratio
of root to shoot, strength of stem, thickness of leaves, and development
of vascular tissue.

It has frequently been observed that plants grown in shade have rela-
tively small root systems. In general it may be said that stem elongation
varies inversely with light intensity but that width varies with it directly
( Popp, 1926 ) . The effect of light may be different on different parts of
the plant and at different stages of development. Some morphological
effects of light may be quite specific though the mechanisms involved
are unknown. Some herbaceous stems, for example, have zig-zag form
in the light but are straight if grown in the dark. Plants that twine in the
light usually lose this ability in darkness.

Light is also important morphogenetically for some plants lacking
chlorophyll. In certain mushrooms, for example, the fruiting body will
not develop normally in complete darkness although the whole vegetative
mycelium is subterranean (Borriss, 1934b).

Etiolation. The most conspicuous effect of differences in light intensity
on plant structure is to be seen in the phenomenon of etiolation. It is a
familiar fact that green plants growing in darkness or relatively weak
light tend to be tall and spindly, with small, pale leaves, weak roots, and
poorly developed vascular tissues. Such plants soon die unless consider-
able reserve food is available in seeds or other storage organs, in which
case etiolated growth may continue for some time. The early work of
Kraus ( 1869 ) showed that etiolation involves a considerable increase
in cell length, though in most cases this is accompanied by some increase
in cell number in the longitudinal dimension.

Different parts of the plant and different species differ considerably
in their manifestations of etiolation. Only shoots etiolate and not roots,
flowers, or fruits. Avery, Burkholder, and Creighton ( 1937a ) observed
marked differences between the first internode and the coleoptile as to
their elongation in various light intensities. Intensity may also affect the
proportions of parts. In Tropaeolum plants, for example, which are grow-
ing in weak light the ratio of petiole length to lamina width becomes
progressively greater as the leaves develop, whereas under normal

310 Morpho genetic Factors

illumination the two dimensions grow at about the same rate (Pearsall,
1927).

As to the causes of etiolation there has been much discussion but no
final agreement. Auxin is undoubtedly involved, for it is well known
that sensitivity to it increases in darkness. Wave length of light is also
important here, for etiolation may be very different in red light and in
blue. The two processes of leaf growth and stem elongation may be
affected differently.

Priestley (1926b) called attention to the fact that in etiolated stems
the endodermis tends to be well developed and to have thick-walled
cells. An etiolated stem is thus somewhat like a root in structure. He
suggests that for this reason water and nutrients, coming from the roots

Fig. 13-1. Effect of etiolation on cell shape. Longitudinal section of cortical paren-
chyma of the stem of Vicia faba when grown in light ( left ) and in darkness ( right ) .
( After Kolda. )

into the vascular cylinder, may be confined there and prevented from
passing outward. This would tend to accelerate growth at the tip of the
shoot and to check the development of leaves.

The relation of light to normal and etiolated growth evidently involves
the problems of cell division and cell enlargement. In beans Brotherton
and Bartlett (1918) found that in the epidermis about a third of the
added growth in length of etiolated as compared with normal plants
was due to more cells and about two-thirds to longer cells, the rate of
both processes of division and enlargement being inversely proportional
to light intensity. Cell elongation has been shown in many other cases
to increase with diminished light intensity (Fig. 13-1). This is evident
not only in green plants but in fungi (Castle and Honeyman, 1935).

Light 311

Whether light produces its effect on cell size by changing osmotic
concentration, permeability of cell membranes, attraction of protoplasm
for water, character of the cell wall, or other processes is not clear. It is
significant that not merely is cell size increased in low light intensity but
size along the polar axis of the cell.

Meier (1934) studied the effects of the intensity of light on cell di-
vision in the unicellular alga Stichococcus bacillaris and found that its
multiplication in culture is proportional to the intensity of illumination
up to a certain point but that high intensities check it.

Thomson (1954) grew seedlings of oats and of peas with different
amounts of light and reports that light accelerates whatever growth
processes are going on while it acts, its effect depending on the stage
of development of the tissues concerned. Exposure early in the course of
either the cell-division phase or that of cell elongation hastens the

Fig. 13-2. Light and vascular development. Portion of the vascular cylinder of the
stem of Vicia faba grown in darkness (left) and in the light (right). (From Borg-
strom. )

completion of that phase of growth, but after it is under way light
hastens the transition to the next phase and thus reduces the final num-
ber or length of cells.

Shape traits may be modified by light. Smirnov and Zhelochovtsev
(1931) found that in Tropaeolum leaves the reduction of blade expan-
sion in weak light modified the fundamental growth pattern. Njoku
(1956a) reports that differences in light intensity change the leaf shape
in Ipomoea.

Anatomical characters are also affected. Penfound ( 1931 ) observed
that stems of Helianthus and Polygonum growing in full sunlight have a
much greater amount of xylem and more and thicker-walled cells in the
mechanical tissue than those in shade. The much reduced vascular tissue
of etiolated plants is well known (Fig. 13-2). Bond and others have
found that as light intensity is reduced the development of the endo-
dermis increases in the stem, where it normally is weak or absent. That

312 Morphogenetic Factors

this tissue is much better developed in roots than in stems may be re-
lated to the fact that roots normally grow in darkness and stems in light.
Leaf structure is often different in different light intensities. It has
long been known (for example, Nordhausen, 1903) that in many cases
leaves on the south side of the tree ("sun leaves") are thicker and better
differentiated than those on the north side or the interior of the crown
("shade leaves"; Fig. 13-3). This has been discussed by Lundegardh
(1931) and others. A particularly striking case is described by Cormack
( 1955). The question has been raised (p. 327) as to whether this effect is
actually due to light intensity or to differences in water relations, par-

Fig. 13-3. Transverse sections through the blades of sun leaves (above) and shade
leaves ( below ) of a, Acer; b, Quercus; c, Fagus; and d, Tilia. ( After Schramm. )

ticularly rate of transpiration, for sun leaves tend to be xeromorphic in
character. Talbert and Holch (1957) studied the leaves of 37 species
and found that sun leaves usually had smaller laminar area, shorter blade
perimeter, deeper lobes, more pronounced veining and marginal serra-
tions, more hairy surfaces, and shorter petioles than shade leaves.

Anderson ( 1955 ) studied the development of sun and shade leaves in
Cornus and Viburnum and finds that in the latter the large leaf size is
the result of earlier and more rapid growth. The greater thickness of sun
leaves is due to greater cell elongation. Differentiation takes place earlier
in shade leaves.

Light 313

QUALITY OF LIGHT

Much work has been done on the effects of different wave lengths
(colors) of light. Many of the early results here are of doubtful value
since it was often difficult to change the wave length without at the same
time modifying intensity. There are many well-established facts, how-
ever, from which conclusions can be drawn.

It seems clear, for example, that the longer wave lengths, notably
those in the red, promote a marked elongation of cells and thus of tissues,
whereas the blue rays (and white light) check this effect and tend to
prevent elongation. Teodoresco (1929) describes many examples of this,
especially from less highly organized forms such as young plants of liver-
worts or fern prothallia growing from spores. In these cases where white
or blue light is used, a rather compact group of cells develops from the
spore, but in red light a much elongated, spindly cell. The same effects
are evident in fungi. An important fact is that the plane of cell division
is usually controlled by the light. Mohr ( 1956 ) finds that in young fern
prothallia in red light cell division tends to be at right angles to the
polar axis of the structure so that filaments of elongate cells are formed,
whereas in blue light division is in various planes, so that a plate of cells
develops. In a normal and growing fern prothallium transferred to red
light, many of the cells grow out to form filaments.

The same effects are to be seen in the more complex higher plants. Thus
Teodoresco finds that blue light checks petiole elongation but increases
blade area, and Vince ( 1956 ) that in many plants, when grown under
lights of equal energy levels, total stem length, internode length, and
leaf length increase with increase in the wave length. Not all plants
react alike, however. Whether the mechanism by which the red rays
promote elongation is like that by which low light intensity does so is
not clear, but presumably the same processes are affected by both factors.
Wassink and Stolwijk ( 1952 ) used equipment by which it was possible
to grow plants in various wave lengths of monochromatic light, and
under these conditions there was strong elongation of the stem and curl-
ing of leaves and petioles in green, yellow, and red light but essentially
normal growth in blue. Fortanier (1954), however, observed that only at
high light intensities is stem elongation greatest in red, yellow, and
green. At low ones it is greatest in blue. Leaf number was not affected by
wave length.

Quality of light also affects flowering. Curry and Wassink ( 1956), work-
ing with annual Hyoscyamus niger, found that flowers were produced in
blue and infrared-plus-red radiation but that neither stem elongation nor
flower-bud formation occurred in green or red light.

314 Morphogenetic Factors

The relation of wave length to auxin production and other problems
of photomorphogenesis have been discussed by Stolwijk (1954).

Other developmental traits are affected by light quality. Thus Funke
(1931) observed that in heterophyllous water plants, where the juvenile
immersed leaves are ribbon-like, these never develop into anything else if
the plants are grown in red or in green light. In blue or white, however,
normal mature foliage is produced. This change may be reversed by
changing the wave length of the light. In root cultures of peas, red light
inhibits the formation of lateral roots more effectively than blue or
green, perhaps by inactivating substances necessary for root growth
(Torrey, 1952). Many other instances of the effects of light of different
wave length on development in higher plants have been reported.

Less work has been done with lower plants. Meier (1936), again with
the alga Stichococcus, found that in cell culture the individual cells in a
given time multiplied fourfold in white light, threefold in blue, but
only twofold in yellow and red. Green light proved to be destructive to

them.

In the slime mold Didynium nigripes, light is necessary for the develop-
ment of sporangia (Straub, 1954). Green light has no effect but red
and blue have. If plasmodia treated with these wave lengths are killed
by freezing and fed to living plasmodia, the latter produce sporangia
after a briefer exposure to light and much more rapidly than control
plasmodia which had been fed untreated ones. Evidently a substance con-
ducive to sporangium production is formed by the action of light of cer-
tain wave lengths. Gray (1953), using the slime mold Physarum poly-
cephalum, found that continuous irradiation with monochromatic light
in the blue and green and a narrow band in the yellow induced fruiting
bodies, the rate of their formation being inverse to the wave length of the
light used. He suggests that a changed acidity resulting from the irradia-
tion may be responsible for the production of sporangia.

There are general discussions of the morphogenetic effects of different
wave lengths of light by Parker and Borthwick (1950) and Wassink and
Stolwijk (1956).

DURATION OF LIGHT

One might expect that the longer a plant is exposed to light favorable
for photosynthesis, the more it would grow and the more vigorous it
would be. Keeping plants in continuous light, however, is often found to
result in less vigor and in a disturbance of the normal reproductive
cycle. It is evident that the production of flowers and fruits is not some-
thing that inevitably occurs but rather that it will happen only when
environmental factors are favorable for it. In 1920 Garner and Allard pub-

Light 315

lished the results of their pioneer observations which showed that flower-
ing is not determined by the intensity or the quality of light alone but by
the length of daily exposure to light, or the photoperiod. What essentially
is involved is the relative length of the alternating light and dark periods,
or, perhaps more accurately, the length of the dark period for some
plants and of the light period for others. This phenomenon of photo-
periodism has now been subjected to intensive study. A history of the
work on it until 1948 was written by Murneek (1948). Other surveys
of the subject or particular aspects of it are those by Garner (1937),
Burkholder (1936), Hamner (1944), Leopold (1951), and Naylor

(1953).

All plants do not respond alike to photoperiodic stimulation. In the so-
called short-day forms, flowering is induced by relatively short periods
of daily illumination ( and thus longer dark periods ) . Such plants flower
naturally in fall or early spring. Long-day plants require a longer period
of light and in nature are summer-flowering forms (Fig. 13-4). Many
plants, such as the tomato, are day-neutral and will flower under long
or short photoperiods or continuous illumination.

This classification is not a very exact one, for different steps in the
reproductive process may each have their optimal photoperiod. Thus most
strawberries flower under a relatively short day but fruit under a long
one, and Phlox is a long-day plant for flowering but is day-neutral for
fruiting. The optimal period for the formation of flower primordia at a
growing point may be different from the one determining the later
growth and opening of the flowers. These relationships have been dis-
cussed by Roberts ( 1954 ) .

There is a close relation between temperature and photoperiodism
which has been studied by a number of workers, among them Purvis
(1953) and Vlitos and Meudt (1955). High temperature will sometimes
induce flowering even when day-length is not favorable for it. In vernali-
zation (p. 339) it is necessary not only to expose the germinating seeds to
low temperature but to provide the proper photoperiod for later growth.
Schwabe (1951) concludes, from experiments with vernalized short-day
and long-day Chrysanthemum cuttings, that the effects of vernalization
and of day-length in this plant are operative at different stages in the
train of reactions leading to flower initiation. Sometimes a high level of
nutrition, especially of nitrogen, may be substituted for day-length. Short-
day soy plants have a higher concentration of nitrogen than do long-day
ones. In many cases an exposure for a few days to a photoperiod favorable
for flower production will result in flowering regardless of the one to
which the plant is later exposed. Plants vary in their sensitivity to this
photoperiodic induction.

Plant parts affected by photoperiodic stimulation in most cases are the

316

Morpho genetic Factors

Fig. 13-4. Above, long-day plant, Nicotiana sylvestris. Below, short-day plant, Nico-
tiana tahacum, var. Maryland Mammoth. At left, under long days; at right, under short
days. ( From Melchers and Lang. )

young but fully developed leaves. Evidence indicates that a flower-form-
ing substance is produced in these which then diffuses through living
cells to the meristem and there stimulates the formation and growth of
floral primordia (p. 397). This substance can be transmitted by grafting
from a plant in flower to one which is not, and the latter plant, even

Light 317

though kept under a photoperiod unfavorable for flowering, will then
flower. The age of the plant may change its photoperiodic response. In
Kalonchoe, for example, young plants 3 months old flower only in short
days, but after 5 months they have become day-neutral (Harder and
von Witsch, 1940« ) .

Even though the initiation of floral primordia has begun under a given
photoperiod, the later differentiation of the various structures can be
greatly altered by changing the length of the period. Thus in the stami-
nate inflorescence of maize, after the initiation of primordia, later growth
under longer photoperiods will cause the flowers to be infertile and
even to show progressive changes toward a vegetative condition. The
glumes develop ligules and the lemmas differentiate into blade, ligule,
and sheath until the spikelet becomes much like a vegetative shoot and
can be propagated as such (Galinat and Naylor, 1951). When trans-
ferred to a photoperiod unfavorable for flowering, buds which would
have produced flowers will sometimes grow into abnormal vegetative
shoots (phyllody), as reported by Behrens (1949) and others. Skok and
Scully (1955) present evidence that floral development is associated
with a dark-dependent mechanism and the elongation of the main axis
with quite a different and light-dependent one.

The length of the photoperiod may affect the differentiation of the
sexes. This is well shown by the work of Schaffner ( 1931) on sex reversal
in staminate plants of hemp, Mercurialis annua (Fig. 13-5). He planted
seeds in the greenhouse every 2 weeks from July 15 until May 15 and
found that in the beginning, when days were long, the flowers were all
staminate but that the percentage of pistillate ones steadily increased
up to the plantings of Nov. 1 and 15 (which came to flower during the
shortest days) and that the percentage of these flowers gradually de-
creased after this until in the long days of spring the plants were all
staminate again. Long days obviously favor the production of staminate,
and short days, of pistillate, flowers. Similar results were obtained by
others, as by Jones ( 1947 ) in Ambrosia.

In Cannabis sativa under a 16-hour day flowering takes place in from
4 to 6 weeks, the leaves become more complex (with up to nine leaflets),
and the plants are about half males and half females. Under 8-hour days,
however, development is more rapid, flowering is reached in 3 or 4
weeks, and the plants are about half hermaphrodites and half females
(Petit, 1952).

Day-length also affects reproduction in the lower plants. In the alga
Vaucheria sessilis (League and Greulach, 1955) the production of sex
organs was earlier and more abundant under 18-hour days than under
8-hour ones. Addition of glucose and peptose to the culture medium
hastened their formation under short days. Sex organs were not produced

318 Morpho genetic Factors

unless there was a high concentration of fat globules near the point of
origin. These authors believe that this is not a case of true photoperiodism
but that the low production under short days results from a limited
availability of food.

Klein (1948) reports that in the fungus Pilobolus there is a definite
cycle of asexual reproduction caused by periods of light and darkness,

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Fig. 13-5. Graph showing percentage of reversal of staminate flowers to pistillate ones
in genetically staminate plants of Mercurialis annua planted at different dates. Day-
length markedly affects sex expression. ( From Schaffner. )

sporangiophores maturing at the end of a dark period and new ones re-
maining immature at the end of the light one. Light is essential to growth,
but a dark period seems necessary to establish a periodicity of growth
and maturation of the fruiting bodies. Periodicities other than those
found in nature could be established in this plant by artificial illumina-
tion. Among these were light-dark cycles (in hours) not only of 12-12

Light 319

but 16-16, 15-9, and 9-15. The 16-16 period was quite consistent and evi-
dently had been acquired by the plant.

The physiology of photoperiodism presents many problems which are
too compiex to be discussed here. One hypothesis proposes that in the
light a substance is produced which persists in the subsequent dark
period. In the latter another is formed which is destroyed by a very
brief exposure to light. These substances interact to make a flower-
forming substance. In the short-day species Kalanchoe Blossfeldiana,
which has been studied intensively ( Harder, 1948 ) , a single leaf borne at
the tip of the plant ( those above it having been removed ) if exposed to
a long day will almost completely prevent flowering in the plant below.
Harder, Westphal, and Behrens (1949) conclude that in it is formed a
substance which inactivates the flower-forming hormone before this
reaches the floral primordium. Auxin presumably is involved in some of
these processes. This has been discussed by various workers, among them
Konishi (1956).

In some cases the photoperiodic reaction can be changed. Working
with an early-blooming variety of peas which is day-neutral, Haupt
( 1957 ) reduced flowering by removing the cotyledons and modifying
the soil nutrients. The plants now reacted as though they were long-
day and late-blooming types. He found that a true late-blooming
variety which is normally a long-day plant lost its photoperiodic reac-
tion and bloomed early if a scion from a blooming plant was grafted
into it.

Earliness of blooming may be due to other factors than day-length.
Thus in an early-blooming and a late-blooming variety of Chrysanthe-
mum, both grown under short days, Doorenbos and Kofranek ( 1953 )
found that the initiation of the florets took place at the same rate, but the
time from the end of this stage until the date of blooming was 28 days
in the early variety and 42 days in the late one.

Photoperiodism has been studied chiefly in relation to the differentia-
tion of reproductive structures, but it has a pronounced effect on others
also. Among instances of this are the following:

Pfeiffer ( 1926 ) grew buckwheat with daily illuminations of 5, 7, 12,
17, 19, and 24 hours and found that maximum stem length and diameter
were produced in the 17-hour day.

The effect of the photoperiod is different on different parts of the plant
and under different conditions. Hall (1949) grew gherkins under green-
house conditions from seedling to maturity. At high nitrogen levels,
plants given a 16-hour day had larger stems than those under 8 hours
but at low nitrogen levels this was reversed and plants under the shorter
days grew larger. Under the 8-hour photoperiod more nodes and leaves

320 M or pho genetic Factors

were produced but the total leaf area was smaller and there were fewer

roots.

Deats ( 1925 ) , studying tomato and pepper, found that the amounts of
both phloem and xylem varied directly with the length of day.

Garner and Allard ( 1923 ) made the significant observation that as the
photoperiod becomes less favorable for vegetative growth the structure
of the plant becomes somewhat xeromorphic— the stem tends to become
more branched, underground parts to enlarge, pubescence to increase,
abscission layers to cause leaf fall, and flowers to appear.

In a study of heterosis in beans, Malinowski (1934) crossed two races
and grew them and their hybrids under long and short days. In long days
the Fx plants were larger in every way than the parents. In short days
they were about the size of the parents and flowered 6 weeks earlier than
under long days. This acceleration of flowering seems to have cut down
their vegetative growth and reduced heterotic vigor.

Mac Vicar and Struckmeyer (1946) grew soybeans with a deficiency
of boron in different photoperiods. The deficiency symptoms were much
more severe under long-day treatment than under short. The boron
content of all the plants was much the same, and these authors believe
that the effect of day-length was to alter the boron requirement of the
plants.

The relative size of the leafy shoot to roots or tubers is markedly in-
fluenced by day -length. Radish, for example, grown under short days,
as in a greenhouse in the winter, forms a very large root and a small
shoot, but in the longer days of spring the root is relatively much
smaller. Other plants with storage roots behave in the same way, as do
potatoes in the ratio of tops to tubers ( Pohjakallio, 1953). Zimmerman
and Hitchcock (1929) observed that in dahlias short days produce heavy,
fleshy root systems but long days, fibrous ones. These workers also found
( 1936 ) that growing Jerusalem artichokes under short days stimulated
tuber production but that the same result was obtained by subjecting
only the tip of the stem to short days by capping it part of the time with
black cloth. This indicates that the control of tuberization by day-length
is centered in the growing tip and its young leaves. In general, the
growth of underground storage regions is stimulated by day-lengths
different from those favorable for the vegetative growth of the shoot.
Where the photoperiod is such that the shoot in its growth is unable to
use carbohydrate beyond a certain amount, this accumulates in storage
regions. Jenkins (1954) reports that long days and relatively high tem-
peratures are necessary for bulb formation in shallots. In Poa, long days
favor the growth of bulbils and short days of ears ( Schwarzenbach,
1956).

In potatoes (Chapman, 1958), short photoperiods induce tuber for-

Light 321

mation. A tuber-forming stimulus is produced near the growing points
of the plant and moves basipetally. It is able to cross a graft union and
produce tubers in a noninduced plant. In plants with forked stems,
one half was given short periods and the other long. Tubers were
produced on that part of the stolon below the short-day branch.

Reduction of growth of the axis, with the formation of leafy rosettes,
is favored by relatively short days. Thus Oenothera forms rosettes in the
fall and tall flowering stems in the next spring. Lettuce makes compact
heads in the short days of early spring but shoots upward in the longer
ones of June.

In strawberries, long days increase leaf size and cell number (Arney,
1956). Ashby (1950b) reports that day-length also affects leaf shape in
Ipomoea, In 16-hour days, plants begin to flower at the fifteenth or
sixteenth node and lobing begins at the fifth to seventh node. Under 8-hour
days, however, flowering begins at the first node and lobing is almost
entirely suppressed.

Gotz (1953) has made an intensive study of the effect of day-length
on the formation of plantlets on the leaves of three species of Bryo-
phyllum. In short days neither plantlets nor their primordia are formed
nor are flowers produced, and the leaves become somewhat more suc-
culent. Under long days, however, plantlets appear in abundance. The
effect of different day-lengths on plantlet production can be studied in
different leaves on the same plant. Neither grafting a scion from a long-
day plantlet-producing plant into a short-day plant, or injecting sap
from one, will induce the formation of these structures.

The photoperiod also affects rooting of cuttings. Some species root
best under long days and others under short (Stoutemyer and Close,
1946). The photoperiod under which the stock plant has been growing
actually affects the rooting of cuttings taken from it more than does that
under which the cuttings themselves are grown (Pridham, 1942).

As to leaf structure, Glimmer ( 1949 ) found that in Kalanchoe a change
in the photoperiod affects the thickness of the epidermal cell walls, the
size of the vein islets, and the form, size, and number of mesophyll cells
but that the number of stomata responds more slowly and the size and
form of the epidermal cells are unaffected. In the ten species she studied,
plants grown under short days had thicker leaves than under long ones,
and this was almost entirely because of greater size of the mesophyll
cells, which elongate at right angles to the surface of the lamina. They
also increase somewhat in width. If a single leaf on a Kalanchoe plant
growing under long days is itself exposed to short days, it grows con-
siderably thicker and changes its form somewhat. It is significant that
these changes are transmitted to other leaves directly above this one,
suggesting that a morphogenetic substance is involved. Detached and

322 Morphogenetic Factors

rooted leaves respond to day-length by the same changes in form and
structure as do those that remain attached to the plant ( Schwabe, 1958 ) .

In many woody plants studied, both flowering and vegetative growth
are markedly affected by the photoperiod (Wareing, 1956; Downs and
Borthwick, 1956). In general, short days induce dormancy and long ones
prolong growth. Marked ecotypes as to photoperiod have been found in
a number of species.

Cellular characters are also affected. Von Witsch and Fliigel (1952)
found that in leaves of Kalanchoe Blossfeldiana ( 2n = 34 ) formed in long
days the mesophyll cells have chromosome numbers between 128 and
135. Under short days these cells are much larger and the degree of
polyploidy is increased, the chromosome number going up to about 540.
In tetraploid plants of Hyoscyamus niger produced by colchicine, the
critical day-length for flowering and the time preceding the elongation
of the internodes were both shortened, the number of leaves was re-
duced, and the time of flowering delayed, as compared with diploid
plants (Lang, 1947).

The problems of photoperiodism are complicated by the fact, empha-
sized by Biinning ( 1956 ) and others, that there are endogenous rhythms
in certain of the physiological processes of the plant. It has been found,
for example, that a light period of 12 hours alternating with 12 hours of
darkness gives in many plants a different result from an alternation of 6
hours of light and 6 hours of darkness and thus two cycles in a day. The
total amount of light and darkness are the same but their effects are not.
There is evidently a changing sensitivity in the reaction of the plant
during the day to various environmental factors. This fact is of much
importance for plant physiology but its significance for morphogenesis
has as yet not been very fully considered. The existence of innate rhythms
may account for the conflicting results obtained in experiments on the
morphogenetic effects of various environmental factors.

RELATION TO OTHER FACTORS

The various morphogenetic effects of light provide an excellent example
of the complexity of interaction of factors in plant development. Light
powerfully influences flowering, but so do temperature, growth sub-
stances, nutrition, and genes, and in some cases water supply and gravity.
They often have parallel effects on vegetative structures as well. These
factors frequently can be interchanged to some extent and produce the
same result, as when temperature is substituted for photoperiod, and
vice versa. Auxin is closely concerned with many of the traits that light
affects, but the exact relation between light and auxin is not clear. Some-
times light seems to destroy it and sometimes to stimulate its produc-

Light 323

tion. Specific photoperiodic reactions have been found to be gene-con-
trolled. The.morphogenetic effects of bright light and of limited water
supply are sometimes hard to disentangle. It is difficult, as has been
said before, to separate any one factor sharply from the others and to
study it in isolation. All are concerned with the entire organized system
that is the plant.

CHAPTER 14

Water

Water is closely involved with many activities of the plant, especially
photosynthesis and transpiration. It fills the cell vacuoles and constitutes
the bulk of protoplasm. It maintains the turgidity of the tissues and thus
is an important factor in growth. Botanists still are very far from explain-
ing the complex problems of the water relations of plants. These have
been discussed in an extensive physiological literature (see Crafts, Cur-
rier, and Stocking, 1949; Kramer, 1945, 1955; Meyer, 1938; and Walter,
1955).

Xeromorphy. Water is also of significance in problems of plant struc-
ture and thus for morphogenesis. Where it is relatively scarce or the
amount that can be absorbed is limited for other reasons (as in saline
soils) or where evaporation is excessive, plants display characteristic
structural features. Such xerophytes tend to have reduced leaf surfaces,
heavy cuticle, small and thick-walled cells, high stomatal frequency,
abundant mechanical tissue, and large root systems, and they often are
spiny or succulent. These traits, collectively termed xeromorphy, have
been regarded as adaptations which increase absorption or reduce tran-
spiration and thus maintain a sufficient water supply under dry condi-
tions. Xerophytes may show other adaptations such as hairy surfaces,
rolled leaf blades, and stomata sunken in pits or otherwise protected
against undue exposure to evaporation. The characteristic structures of
xerophytic plants have long attracted the interest of ecologists and pro-
vide much of the subject matter for the science of ecological anatomy.

Such traits presumably have arisen through the action of natural se-
lection and are thus not ultimately attributable to the direct effect of the
environment. Many plants, however, if grown under conditions where
water is scarce or transpiration high, have been observed to assume
some degree of xeromorphism. Leaf surfaces will tend to be somewhat
reduced, cells smaller and thicker-walled, and mechanical tissue more
abundant. Such structural changes are clearly the result of an environ-
mental factor— a reduction in amount of available water. What is in-
herited here is this specific response to the environment.

There has been considerable controversy, however, as to whether or

324

Water 325

not such changes are adaptive and are advantageous to the plant. That
they should be so is a plausible conclusion, and for such traits as heavy
cuticle it may be correct. Its general validity has been challenged by
a number of people, notably Maximov, who has reviewed the problem
comprehensively ( 1929, 1931 ) , especially as to the physiological basis of
drought resistance. Maximov called attention to the earlier work of
Zalenski (1904), published (chiefly in Russian) a quarter of a century
before and largely neglected outside the country of its origin. Zalenski
observed that the veining of the leaves in plants growing in dry, open
spaces was much more abundant than in the leaves of those in the shade
or in protected spots. These observations he then extended to a com-
parative study of the structure of leaves on the same tree. Here he
found that, as a rule, leaf structure changed with the level of insertion
on the tree, the structure being more xeromorphic with increasing dis-
tance from the root. The progressively higher leaves had smaller cells
throughout, smaller stomata and more of them per unit of area, greater
vein length per unit of area, thicker and less sinuous walls in the epi-
dermal cells, a greater contrast between palisade and spongy layers, less
intercellular space, and better developed mechanical tissue. These re-
lationships were later called "Zalenski's law" and were independently
discovered by others, among them Yapp ( 1912 ) . Zalenski's results are
evident in herbaceous as well as in woody plants. Some data that he
presents for Dactylis glomerata are shown in Table 14-1. Salisbury ( 1927)

Table 14-1. Variations in Anatomical Elements of Leaves of Different
Tiers in Dactylis glomerata *

Tier 1 2 3 4 5

Height of insertion ( cm. ) 0 10.2 25.2 37.0 51.0

Length of leaf ( cm. ) 7.1 10.3 18.5 18.0 13.2

Breadth of leaf (cm. ) 0.30 0,35 0.54 0.52 0.45

Length of vascular bundles

(mm./sq. cm. of leaf surface) 371 511 557 625 626
Mean diameter of cells of

upper epidermis ( mm. ).. . 0.0418 0.0294 0.0272 0.0217 0.0189

Number of stomata in field .. . 34 42 61 80 64

Length of stomata ( mm. ).. . 0.0434 0.0415 0.0403 0.0356 0.0384

o

From Maximov (1929), after Zalenski.

found that stomatal frequency per unit area increases with the height at
which the leaf is borne but that the stomatal index (ratio of stomata to
epidermal cells in the same region) changes relatively little. This is a
necessary implication of Zalenski's observations.

These structural characters are among those regarded as typically
xeromorphic. Zalenski, Yapp, and others, however, have explained them

326 Morpho genetic Factors

without relating them to water conservation but simply as direct or
indirect results of decreasing cell size with progressively higher leaf
insertion. Small cell size, in turn, grows out of the greater difficulty
with which water is obtained by the higher leaves, since they have to
lift it farther and against the competition of the lower ones. It follows
that at the critical period of rapid leaf growth, which results primarily
from cell expansion through the absorption of water, the cells of the
upper leaves cannot attain the size of the lower ones. The other struc-
tural traits are a consequence of this basic difference. That such a con-
clusion is correct is indicated by other evidence, such as the fact that if
lower leaves are removed while the upper ones are still growing the
latter will resemble in structure leaves that would normally be lower
on the stem.

Xeromorphy in these upper leaves therefore seems unlikely to be an
adaptation for reducing water loss. Indeed, it was later shown that
upper leaves may transpire more rapidly than the lower ones. These
results have cast doubt on the adaptive character of the traits of
xerophytes in general. Maximov calls attention to the fact that when
water is abundant many xerophytes transpire more rapidly than meso-
phytes and it is only under drought conditions that their water loss is
markedly cut. He attributes this, and therefore the quality of drought
resistance in general, not to any structural traits but to protoplasmic
characters, notably osmotic concentration and changes in cell colloids
that would enable the plant to conserve its water supply and thus
endure dry conditions better than other plants. Eckardt (1953) agrees
with this conclusion. The physiology of drought resistance has been re-
viewed by Iljin (1957).

In earlier years a number of Russian investigators, assuming that types
with small cells were more resistant to drought than those with large
cells, determined for various cereal varieties their "anatomical coefficients"
(chiefly cell size), hoping to find a means of identifying resistant types
by direct inspection. This possibility was not supported by the work of
Maximov. More recently, however, Lai and Mehrotra (1949), working
with sugar cane, have found that some cell characters, notably small
size, seem in certain cases to be associated with drought resistance.

Farkas and Rajhathy ( 1955 ) reexamined anatomical gradients in some
herbaceous plants, particularly tomato, and found that cell size in
leaves decreases from below upward and that number of stomata per
unit area increases, thus again confirming Zalenski (Fig. 14-1). Under
dry conditions this gradient is much steeper. They found several other
physiological gradients some of which may be explained as dependent
on that for water. In others the relation to the latter is not clear. Stage
of development of the leaves also complicates the problem here.

Water

327

Shields (1950), who has reviewed the whole subject of xeromorphy,
agrees in general with Zalenski, Maximov, and Yapp that this type of
structure has little significance as an adaptation in drought resistance.
She also emphasizes the importance of physiological factors in relation to
water loss. Many of the structural characteristics of xerophytes, she sug-
gests, may be the result of physiological differences. Thick cell walls and
abundance of mechanical tissue may result from active photosynthesis
in a plant where all its products cannot be used in growth because of
the shortage of water.

Ashby ( 1948Z? ) , however, presents evidence that the relative xeromorphy
of the upper leaves, at least as indicated by cell size, is not due to corn-

er

16
15
1U

~ 13

<-> 12

^ 10

% 9

150

m

130
120
"10
100
90
80
70
50
SO

w

120
110
100
90
80
1 70
- I 60
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uo

30
20
10

7^

^^t

t\

V

=**

VB/aftf/ache

'pidermiszellen-
grolie

-"

A \

y

2 3

2 3

2 3

2 3

1. Blatter

2 Blatter

3. Blatter

*. Blatter

Fig. 14-1. Gradient of cell size in tomato leaves. Graph showing stomatal number (in
a given microscopic field ) , epidermal cell size ( in microns ) , and leaf surface ( in square
centimeters) for the first four leaves of five young tomato plants. These are arranged
in each case according to the ascending order of stomatal number for each leaf class.
( From Farkas and Rajhdthy. )

petition for water but to the influence of immature leaves on those above
them, an influence which may be hormonal in character.

Leaves on the outside, and particularly the south side, of the crown
of a tree (sun leaves, p. 312) are often considerably thicker and more
xeromorphic in appearance than those in the center (shade leaves).
This has been attributed to the direct action of light. This difference may
be due in part to water relations, for Hanson ( 1917 ) showed that, on
the outside of the crown, conditions favored much more rapid evaporation
than in the interior. He found that leaves on the outside are smaller,
more deeply lobed, and lower in water content and that they transpire
faster per unit of area (Fig. 14-2). This has frequently been confirmed.
Huber (1926) agrees that sun leaves result from a water deficit. Soding

328 M 01 -pho genetic Factors

( 1934 ) grew trees in pots and found that, by adding a small amount of
salt to the soil, leaves like sun leaves were formed by the plant. Light,
however, probably has a share in the production of xeromorphy, for

Fig. 14-2. Effect of environment on leaf structure. Sections of leaves of Acer saccharum
from 1, south periphery of the tree; 2, center of crown; 3 and 4, base of crown. Various
factors are doubtless involved in these changes, but differences in rate of transpiration
( higher in exposed leaves than in the others ) seem especially important. ( From
Hanson. )

bright light has been shown to reduce leaf area and to increase blade
thickness. The xeromorphy observable in many tropical plants may check
the harmful effects of too intense insolation.

Still other factors are probably involved in the development of this sort

Water 329

of leaf structure. Miiller-Stoll (1947b) has evidence that xeromorphy of
plants in peat bogs is due to a deficiency of nitrogen rather than of water.
He fertilized such plants and observed a marked increase in leaf area and
cell size and a decrease in stomatal frequency, cell- wall thickness, and
venation. Lack of nitrogen and lack of water thus seem to produce
similar structural changes. These two factors are associated in other
morphogenetic phenomena.

Experimental Work. Many experiments have been performed to de-
termine directly the effect on plant structure of varying amounts of
water in the soil or in the air. Only a few of these can be mentioned

here.

Rippel (1919) studied white mustard growing in moist and in dry
soil. Vein length per unit area of leaf surface was considerably greater
in dry soil. In both, it increased progressively from the first leaf to the
fifth, and this gradient was steeper in dry soil than in wet.

Penfound (1931) paid particular attention to stem anatomy and found
that, although increased soil moisture reduced xeromorphic traits, it in-
creased the relative amount of xylem in the stem.

Cain and Potzger (1940) brought Gaijlussacia plants into the green-
house. They varied the amount of available water and also grew some of
the plants in front of a fan. Though dry air and fan induced some
xeromorphy, the mesophyll was considerably thicker in plants in the
moister soil, contrary to most earlier observations.

Simonis (1952) studied four genera grown in soils of high and low
water content. In all, the leaf surface was reduced under water deficit,
but the morphological responses of different plants were somewhat dif-
ferent. Water content tended to be unchanged under dry conditions,
or sometimes even was increased, and succulence was generally greater.
Simons (1956) grew year-old apple seedlings in greenhouse pot cul-
ture in moist and dry soil. Reduction in water supply affected leaf area
and also thickness and size of cells in epidermis, palisade, and xylem.

Fewer experiments have been done on the morphogenetic effects of
differences in the humidity of the air. Eberhardt (1903) grew a wide
variety of plants under bell jars, maintaining light and temperature the
same in all but changing the humidity. Dry air tended to produce the
ordinary xeromorphic traits and also an increase in hairiness ( Figs. 14-3
and 14-4). The results of Lebedincev (1927) and Rettig (1929) were
much the same. The effects of dry air were more pronounced when the
soil was also dry.

At the opposite extreme from xeromorphy, produced by water deficit,
are those changes that result from submersion in water. As a rule, the
roots of such plants are small or lacking, the vascular and mechanical
tissues poorly developed, the leaves thin and often much dissected, the

330 Morpho genetic Factors

stomata vestigial or absent, and the cell walls thin. These traits are gen-
erally regarded as adaptations to an aquatic habitat. A few heterophyllous
water plants (p. 216) can live either submersed or growing in the air with

Fig. 14-3. Diagram of cross sections of stems of Achyranthes, showing relative de-
velopment of tissues in air which is dry ( I ) , normal ( II ) , and humid ( III ) . b, xylem;
1, phloem; s, sclerenchyma; m, pith. Dry air tends to reduce size of pith and cortex
and to increase development of xylem and sclerenchyma. ( From Eberhardt. )

their roots in soil. Among these are Polygonum amphibium and the
water buttercup, Ranunculus aquatilis. In these plants the land form,
essentially mesophytic in structure, is very different from the water form

3

»=ss

c

I II

Fig. 14-4. Outer cortex and epidermis of Aster sinensis grown in air that is of normal
humidity ( I ) and that is dry ( II ) . The latter shows greater wall thickness in collen-
chyma and larger bundles of sclerenchyma. E, epidermis; C, cortex; S, sclerenchyma.
( From. Eberhardt. )

and in some cases was not at first recognized as belonging to the same
species. Occasionally, as in the buttercup, foliage transitional from one
to the other may be found. In plants like the mermaid weed, Proser-
pinaca palustris, leaves borne in the air are broad and little-lobed

Water

331

Fig. 14 5. A species of Myriophyllum, an "amphibious" plant, showing differences be-
tween leaves grown in water and in air. ( From Fassett. )

whereas the submersed ones are much dissected (Fig. 14-5). Potamogeton
and similar forms are entirely aquatic but in some species there are
both broad floating leaves, exposed on their upper surfaces to the air, and
delicate submersed ones.

Various explanations have been proposed (p. 216) for the differencs

332 Morphogenetic Factors

between shoots grown in water and in air, especially in Proserpinaca.
Transpiration, seasonal differences, and reversion to juvenile stages may
be involved. Combes (1947) found that in Oenanthe low temperature
is effective in producing deeply incised leaves. Allsopp (1955) has
studied the water fern, Marsilea, grown under various conditions, and
has discussed the general problem of the structure of water plants. The
land form of leaf has four leaflets, and there are stomata on both sur-
faces, but the water form is merely lobed and lacks stomata in the lower
epidermis (Fig. 14-6). Raising the osmotic concentration of the culture

5% U. E.

I7.U.E.

5% L.E.

I%LE.

Fig. 14-6. Comparable sporeling leaves of Marsilea Drummondii, an "amphibious"
plant. Form of leaf and structure of upper and lower epidermis in leaves grown in
media containing 5 per cent glucose (left) and 1 per cent (right). The former re-
semble typical land forms and the latter, water forms. ( From Allsopp. )

medium by adding glucose produces the land type of leaf. Whether this
is an osmotic or a nutritional effect is not certain. Allsopp concludes that
it is the water balance of the developing tissues, determined by the
osmotic pressure of the surrounding liquid, and the relative humidity of
the air or, in general, the diffusion pressure deficit of the water of the
environment, which produce the structural features distinctive of land
or water forms. Here, again, the morphogenetic problem involves much
more than the direct effect of a single environmental factor.

Effect of Transpiration Stream. Another aspect of the problem of the
morphogenetic effects of water involves the influence of water supply

Water

333

and transpiration rate on the development of vascular tissue. Does a
strong transpiration stream stimulate the formation of conducting cells
and thus serve as a "functional stimulus"?

There is clearly a quantitative relation between a transpiring surface
and the vascular tissue supplying it. D. J. B. White (1954), in a study of
the relation of laminar area to petiolar xylem in the bean leaf, found
that there is an allometric developmental correlation between the two,
the cross-sectional area of xylem growing about two-thirds as fast as
laminar area (Fig. 14-7). There have also been a good many measure-
ments of the amount of vascular tissue at different levels in the stem, both
absolutely and in proportion to the area of leaf lamina above. Reliable

L09X
2-5

" Immature

20

V5

0-5 10 Log L 15 20

Fie. 14-7. Relative growth of area of lamina (L) and cross-sectional area of petiolar
xylem (X) in immature leaves of bean. (From D. ]. B. White.)

data as to the amount of transpiration in relation to cross section of
vascular tissue are difficult to obtain. Riibel (1920) measured the xylem
area at different levels on a sunflower plant and the total leaf area above
each level. In plants grown in a normally sunny situation there was
about 0.21 sq. mm. of vascular tissue per square decimeter of leaf area,
as compared with 0.10 sq. mm. in shaded plants. Since there is more
transpiration in the sun, there is evidently a relation here between
transpiration and the amount of conducting tissue. In the lowest stem
levels there was from Vi to V3 sq. mm. of cross section of conducting
tissue to every gram of dry weight of leaves above it, but in young and
vigorous leafy plants this increased to V2 sq. mm., again showing a
presumptive relation to transpiration. The proportion of wood to phloem

334 Morphogenetic Factors

decreased at upper levels. The leaves at different levels transpired at
about the same rate.

Alexandrov, Alexandrova, and Timof eev ( 1927 ) observed that in
Bryonia (a running vine) the number of vessels in any part of the stem
varies with the dimensions of the leaves in that region. The size of
the vascular tissue in a petiole is also related to the area of its lamina.

In fir, spruce, and beech, Huber ( 1928 ) found that the relative con-
ducting surface (the ratio of the area of conducting tissue to the fresh
weight of leaves above it) increases from base to apex in the stem. In
lateral branches this ratio was smaller than in the main stem, a fact
presumably related to the dominance of the latter. The relative conduct-
ing surface and the amount of transpiration were determined for various
plants by Huber and the rate of flow of water through the vascular sys-
tem calculated. This was found to be relatively high for herbaceous
plants, low for conifers and xerophytes, and intermediate for broad-
leaved trees, thus seeming to be related to the amount of transpiration.
Huber also observed ( 1924 ) that in oak branches growing in bright sun-
light a square decimeter of leaf area transpired 75 mg./hour and was
supplied through a cross-sectional area of 0.42 sq. mm. of vascular tissue.
In branches growing in shade there were 46 mg. of water transpired
through a vascular cross section of 0.20 sq. mm. In other words, the
greater the transpiration stream passing through the vascular system,
the larger this system was. He believes, however, that the amount of
water carried upward depends primarily on the osmotic pull exerted
by the leaves and the resistance to flow in the vascular tissues rather
than solely on the size of the vascular tissue itself.

These various facts show that there is a definite correlation between
the amount of water passing through the vascular tissue and the amount
of such tissue that is developed. This, consequently, suggests that the
transpiration stream itself acts as a formative stimulus for the differentia-
tion of vascular tissue. Doubt as to the correctness of such a conclusion,
however, is raised by some remarkable results reported by Werner ( 1931 )
in maize. He was able to grow a plant of almost normal size (suspended
in the air in a transpiration experiment) that was connected to its root
system in the soil by only a single extremely thin root about 10 cm.
long. The entire water supply for this plant, the stem of which was
several centimeters wide, passed through a vascular strand only about
0.5 mm. in diameter. Here, at least, there is little evidence that a heavy
transpiration flow stimulates a proportionate development of vascular
tissue. Similarly, in a frond of Osmunda, all the water transpired by a
large blade area is drawn through a leaf trace which is very small as it
leaves the stele. At the base of the frond this expands into a ring of
large bundles.

Water

335

In such cases as these, one is forced to conclude that much more vascu-
lar tissue is normally developed than is required to carry the normal
transpiration stream. The relation so frequently observed between
area of transpiring surface and cross-sectional area of conducting tissue
may therefore be simply another instance of developmental correlation,
of one tissue keeping step with another (p. 107), and may be without
causal significance for the differentiation of vascular tissue.

There are other ways in which water may have morphogenetic sig-
nificance. Positive hydrostatic pressures often occur at the time of early
and rapid leaf growth, and leaves developing then tend to be large and
to have shallow lobes. A little later, when sap pressure is lower or absent,
the leaves are smaller and the lobes deeper. Experiments of Pearsall

•OOi n n n

75-

PERCENT

OF

FLORETS

CLEISTOGAMOUS 5Q
BLACK,

CHASM06AM0US
WHITE 25

PERCENT OF WATER

Fig. 14-8. Relation between the percentage of water in the soil and the percentage
of cleistogamous florets in Stipa. ( From W. V. Brown. )

and Hanby (1926) tend to confirm this, since when they applied con-
siderable hydrostatic pressure to stems while the leaves were develop-
ing, the lobes were shallow, but they were deeper under less pressure.
The angle at which the lateral veins go off in palmate leaves seems to
affect their ability to deliver water. Where this angle is more than 90°
the flow of water under pressure is reduced. This fact may be related
to the determination of leaf shape.

Osmotic pressure has important morphogenetic effects since it is one
of the factors determining the amount of cell enlargement. Various cir-
cumstances affect the osmotic concentration of the cell sap. One of these
is chromosome number, for Becker (p. 40) observed that in a polyploid
series of moss cells the concentration varied inversely with the degree of
polyploidy. Schlosser ( 1935 ) found in tomato that maternally inherited
differences in osmotic concentration in the cytoplasm, as well as in the

336 M or pho genetic Factors

environment, affected the expression of genes for plant height. The
character of growth may also be influenced. If the alga Stigeoclonium
is grown in relatively high osmotic concentrations, its cells round up
and divide in all planes to form a so-called palmella colony. In weaker
solutions vegetative activity is increased and the cells become cylindri-
cal, divide in only one plane, and form filaments (Livingston, 1900).

Water may also affect differentiation in other ways, such as the in-
creased proportion of cleistogamous flowers formed as soil moisture
decreases (W. V. Brown, 1952; Fig. 14-8).

A study of the water relations of plants, and especially of the forma-
tive effects of water on plant growth, has recently been somewhat
neglected. These relations provide a promising opportunity, however, to
approach some of the problems of plant morphogenesis from a direction
different from that of most experimental work today.

CHAPTER 15

Temperature

Temperature is obviously of much importance for the physiological ac-
tivities of a plant since the rate of metabolic processes is markedly
affected by it. Though its chief significance is in physiology, it also
influences development in various ways. These have been summarized
by Went (1953).

Both light and temperature apparently produce their morphogenetic
effects by speeding up or slowing down particular physiological processes.
What the effect in a given case will be evidently depends on the sensi-
tivity of the plant to these stimuli in a particular part of its body or on a
particular phase of its development. The effect of temperature is especially
important on rate of growth. The optimum temperature for this may be
different in different regions of the plant, at different stages of develop-
ment, or even at different times of day. This may result in a change in
proportions of various parts and thus of form and structure. Biinning
(1935), for example, observed that the later in the season the seeds of
beans mature, the shorter is the epicotyl of seed and seedling and the
quicker do the primary leaves reach maturity. This he found to be a
temperature effect, for high temperature during the 5 weeks preceding
seed maturity produces longer epicotyls and a slower development of
primary leaves.

In Ipomoea, Njoku ( 1957 ) found that the higher the night tempera-
ture (with a good level of mineral nutrition) the less deeply lobed were
the leaves (Fig. 15-1). Here what temperature seems to affect directly
is the rate of production of leaves at the growing point, and this, in turn,
is correlated with depth of lobing. Many other cases have been found
where temperature thus exerts an indirect effect on form and structure
because of the fact that different parts are differently susceptible to
its influence.

Thermoperiodism. There is often a daily rhythm in reaction to tem-
perature as there is to light. At any temperature that is constant through-
out the 24 hours many plants will grow less rapidly than if their environ-
ment is relatively cool at night and warm during the day. The optimum

337

338 Morpho genetic Factors

temperature for growth may therefore be different under different con-
ditions. This thermoperiodism affects growth in various ways (Went,
1944, 1945, 1948). Went found in tomato, for example, that if the green-
house temperature is held constant the optimum is about 26.5°C, at which
there is a steady growth in length of 23 mm. per day. At all other tem-
peratures, growth is less (Fig. 15-2). Plants kept warm (26.5°) during
the day, however, but cooler at night ( 17 to 20° ) grow still better, about
27 mm. per day. It is significant that this low temperature is effective only
if it is applied during the dark period of daily growth. The same thermo-
periodism is evident in fruit development, the best fruit set occurring
when the night temperatures are 15 to 20°. Evidently two different

3-5P

30

X

(II

c

01

a

<T3

25

-5 20

1 5"

J L

-L

a L

Fig. 15-1. The effect of low and of
high night temperature on shape of
successive leaves in Ipomoea caerulea.
Shape index measures degree of lob-
ing. ( From Njoku. )

23456789
Leaves, numbered from base

processes are involved, one going on in the light and the other in the
dark, and with different temperature optima. Plants differ considerably
in their response to thermoperiodism ( Knapp, 1956 ) . Sproston and Pease
( 1957 ) have shown that thermoperiodism is related to the production of
the sexual stage in the fungus Sclerotinia.

There is a close relation between temperature and photoperiodism,
for it has frequently been shown that a particular temperature can be
substituted for day-length in determining the balance between vegetative
growth and flowering. Thus in Rudbeckia, a long-day plant, flowers are
produced in shorter days if the temperature is kept high (Murneek,
1940). Flowering in beets can be controlled by manipulating the relation

Temperature 339

between temperature and the photoperiod (Owen, Carsner, and Stout,
1940), a technique which has been termed photothermal induction.

The problem of dormancy, of why plants or parts of them fail to grow
until particular conditions are satisfied, has implications for morpho-
genesis, particularly in relation to buds, since there are usually very many
buds on a plant that do not develop. Whatever determines the particular
ones that are to grow has an important influence on the form of the plant.
Factors that inhibit or stimulate growth of these meristematic regions
have been studied chiefly in connection with growth substances (p. 386),
but others are involved. Among them temperature has an important place.
It is well known that low temperature is one of the most effective means
for breaking the dormancy of seeds, buds, and other plant parts. The

30 -""Vday

20-

10

day temperature 16.5*
night temperature as
indicated on abscissa

temperature, constant
day and night

3k>- 2S° 20° 15° 10° S'C

Fig. 15-2. Thermoperiodicity in tomato. Stem growth (in millimeters per day) in
plants kept constantly at the indicated temperature ( lower curve ) and for 8 hours dur-
ing the day at 26.5 °C but at night at the temperature indicated (upper curve). (From
Went. )

influence of temperature on bud growth has been widely studied by
horticulturists because of its practical importance (see Chandler et al.,
1937).

Vernalization. A more significant effect of temperature for morpho-
genetic problems is evident in the processes of vernalization, by which
flowering is accelerated through the application of low temperature at a
particular stage of development. Horticulturists have known for many
years that the chilling of seeds or seedlings will in many cases force
plants into bloom earlier than would otherwise occur. Scientific study
of this effect, however, began in comparatively recent years and at first
was explored chiefly by Russian plant physiologists, especially Lysenko.
A conspicuous example of the effect of vernalization is the speeding up

340 Morphogenetic Factors

of flowering in some of the cereal grains so that "winter" varieties,
superior in certain respects, can be treated like "spring" varieties. A win-
ter race of rye, for example, is normally sown in the fall and flowers and
fruits the next season. If planted in the spring it will produce abundant
vegetative growth but no flowers. A spring race sown in the spring will
fruit in that growing season. If seed of winter rye is soaked in water,
however, and is then exposed to low temperature (0 to 10° C or there-
abouts) for a few hours or days, it can be sown in the spring and will
bear flowers and fruit just as rapidly as spring rye does. Grain germi-
nated at 1°C and then planted will produce rye that flowers in 68 days,
but if germinated at 18 °C, flowering does not take place for 150 days
(Gregory and Purvis, 1938). The vernalized seed may be kept dormant
for some time or even dried and it will still grow like spring rye when
it is planted.

These facts are explained on the assumption that development is to a
great extent independent of growth, that in an annual seed plant there
is a specific series of developmental stages, each a necessary precursor
to the next, and that these stages require for their completion different
environmental conditions, especially as to temperature and light. This
is an aspect of the general concept of phasic development previously
discussed (p. 205).

In these cereals the first stage is the one in which the floral initials
are formed, and for this process low temperatures are necessary. Winter
rye sown in the fall will produce these initials because it is exposed to
the low temperatures of winter but if it is sown in the spring the tem-
perature is not low enough for this to happen. Vernalization thus acts as
a substitute for winter temperature.

The next stage, the development of the flowers themselves, usually
requires higher temperatures but also relatively long days. Flowering
will be delayed indefinitely if plants at this stage are exposed to short
light periods. In the long, warm days of spring, both winter and spring
varieties will thus come into flower. The difference between them is that
spring varieties will form floral primordia in these warm days and winter
varieties will not do so without treatment.

In certain plants a definite number of primordial structures are formed
at the growing point of the embryo, and it can be shown that the fate of
some of these has not been determined in the seed but that leaves or flow-
ers will form from them, depending on environmental conditions. Thus
in winter rye there are usually 25 embryonic primordia. The first seven
will always develop into leaves. The next 18 are indeterminate, and the
lower the temperature to which they are exposed, the more of them will
develop flowers. At high spring temperatures, none of them will do so
unless previously chilled.

Temperature 341

Different plants respond very differently to vernalization, and in some
it is without effect (Kondratenko, 1940). Vernalized plants may be de-
vernalized, usually by high temperature following the cold treatment,
and they may sometimes even be revernalized (Lang and Melchers,
1947).

The induction of flowering by low temperature is by no means limited
to the cereal grains or to seed treatment. Young plants beyond the seedling
stage may be vernalized and thus forced into flower, and some biennial
varieties will flower in their first season if subjected to cold. The grow-
ing stem tip is the region sensitive to the vernalizing influence. Low-
temperature effects on growing plants, particularly as to flowering,
have been widely investigated. This work is reviewed by Thompson
(1953).

The exact way in which low temperature produces its effects in ver-
nalization is not clearly known but in some cases it has been thought to
influence the production and distribution of auxin and perhaps also of
substances that stimulate flowering (p. 397). Hatcher (1945), however,
finds that the auxin content of grains of winter and spring races of
cereals is the same and that there is no detectable amount of auxin in
the embryos either at normal or low temperatures. He concludes that it
is not concerned in the process of vernalization.

Although the most conspicuous effect of vernalization is the acceleration
of flower development, vegetative characters may also be affected, such as
leaf size. Hansel ( 1953 ) found that early leaves were longer if germina-
tion temperatures were slightly below 0°C than if they were slightly above
this (Fig. 15-3). Internal differentiation is also affected (Roberts and
Struckmeyer, 1948).

The literature of vernalization and of its relation to photoperiodism
and phasic development is extensive. The history of research in this gen-
eral field has been reviewed by McKinney (1940) and Whyte (1948).
The latter is one of a series of papers on this general subject brought to-
gether by Murneek and Whyte (1948). Among other related publica-
tions are those of Gregory and Purvis ( 1938), and Whyte (1939).

Other Temperature Effects. There are many other instances where
morphogenetic effects of temperature have been observed. Some typical
examples of recent investigation in this field are the following:

Burstrom ( 1956 ) finds that under higher temperatures the final length
of cells in roots is reduced because of the shorter period of cell elonga-
tion. Cell-wall plasticity and calcium requirement are also reduced.

Schwabe (1954), working with Chrysanthemum, limited low-tempera-
ture treatment to the growing tip and confirmed earlier conclusions that
this is the region where the stimulus of vernalization is perceived. The
stimulus did not p^tss across a graft union but it was translocated to

342 Morphogenetic Factors

lateral buds that were distant from the one that was chilled and had
formed some time after it was treated.

Wittwer and Teubner ( 1957 ) observed that in tomato low-temperature
treatment of seeds had no effect, but exposure of very young seedlings to
low night temperatures (10 to 13°C) for 2 or 3 weeks induced earlier
flowering and more flowers in the first cluster, in contrast to those grown
at higher temperatures (18 to 21°C). Cold treatment of older seedlings
increased the number of flowers in later clusters. Other factors, especially

16
I2h

• 1st Lamina
a 2d Lamina
O 'Scores'

B

o

c

la

O

-J

- •

140

Co

3o 3

J L

I I I

an- "3 -2 -60 *l *3
treated Temperature of Vern. oq

2o

lo

Fig. 15-3. Effect of vernalizing temperatures on length of lamina of first (A) and
second ( B ) leaves in winter rye, and on stage of differentiation of spike as meas-
ured by an arbitrary scale of "scores." Controls at left. ( From Hansel. )

nitrogen nutrition, also affect flower formation and complicate the prob-
lem of studying it.

Hall (1950) compared buckwheat plants in culture with their roots and
shoots at different temperatures with others where the entire plant was
grown at either high or low temperature. Development was more normal
under the latter condition. High temperature for the shoot checked vege-
tative growth and hastened flowering, maturity, and senescence, and low
air temperature there prolonged ontogeny. Increase in duration of the

Temperature 343

vegetative phase, however, did not result in the production of more plant

material.

L. D. Tukey ( 1952 ) subjected bearing branches of sour cherry to sev-
eral different night temperatures and found that higher temperatures
accelerated development during stages I and II (early growth and stone
formation) but checked it in stage III (fleshy pericarp growth) (Fig.

2-5). . .

Leopold and Guernsey (1954) treated germinating peas with various

growth substances and followed this with low temperature. The combi-
nation of chemical with temperature stimulation they termed chemical
vernalization. It hastened flowering, but only if carbon dioxide was later
present. Changes in day-length had no effect. They conclude that there
are two stages in the growth of young pea plants which are affected, the
first requiring auxin and low temperature and the second requiring
carbon dioxide. The function of carbon dioxide here is not understood.

Chaudri, Biinning, and Haupt (1956) observed that the exposure of
young onion plants to 3 hours of low temperature during the dark por-
tion of the photoperiod hastened the development of bulbs. This effect
was greatest when the low temperature was applied during the latter
part of the dark period.

Fisher ( 1954 ) worked with a trifoliate New Zealand species of Ranun-
culus in which the juvenile leaves are undivided. Sometimes the adult ones
show a partial reversion to this juvenile form. He grew plants under
controlled conditions and found that when the temperature was relatively
high (20°C in the daytime and 15°C at night) there was a complete
reversion to the undivided juvenile leaf shape but that at lower tem-
peratures ( 10 and 5° ) the adult form persisted.

Steinberg (1953) studied Mammoth Rustica tobacco, a type which
came originally from a cross between Nicotiana rustica and N. tabacum.
This is indeterminate in growth and very rarely flowers, but it can
readily be made to do so if the night temperatures are dropped to 50
or 60°F, regardless of day-length. In this respect it is unlike Maryland
Mammoth (p. 316), which also is indeterminate in growth but flowers only
in short days, regardless of temperature. The indeterminate character of
growth in both is due to the fact that flowering is prevented, in one type
by high temperature and in the other by long days. Steinberg suggests
that there may be a separate genetic basis for the two types of reaction.

Benson-Evans and Hughes ( 1955 ) observed that in the liverwort
Lunularia cruciata, which is world-wide in distribution but rarely repro-
duces sexually except in a "Mediterranean" type of climate, the induc-
tion of archegoniophores requires subjection to low temperature, later
followed by higher temperature and long days, thus fitting it to its par-
ticular ecological distribution.

344 M or pho genetic Factors

Margalef ( 1953 ) found that in cultures of the green alga Scenedesmus
obliquus low temperatures cause cell size to increase, although other fac-
tors have a minor effect on it. Since cells in this species grow faster
in length than in width, large cells have a more slender shape than
small ones, so that temperature indirectly affects cell shape.

CHAPTER 16

Various Physical Factors

There are a number of other morphogenetic factors which may be grouped
together as physical ones in a general sense, notably such clearly me-
chanical factors as external compression, tension, bending and swaying;
gravity and inner tissue tension, together with absolute size and bio-
electrical factors, each with its bearing on development.

Those factors which may be called mechanical in the strict sense are
relatively simple in character in comparison with light, electricity, and
many chemical ones and evidently produce most of their morphogenetic
effects indirectly through modifying physiological processes in the living
cells. Much of the early work in this field was done by Schwendener
( 1878, 1898 ) . Among other problems, he emphasized the importance of
such factors in determining the arrangement of leaf primordia at the
apical meristem.

Mechanical effects are in many cases much like the ones produced by
other factors, suggesting that both are acting upon the same proto-
plasmic mechanisms. Such parallel effects are familiar to the student of
morphogenesis and emphasize again the importance of the complex re-
acting system rather than that of the relatively simple stimulus or evo-
cator. There has been a good deal of disagreement as to experimental
results in this field, much of which is probably due to the fact that the
reactivity of the plant is very different at different stages of its develop-
ment and under different environmental conditions.

In studying these effects it is sometimes difficult to separate various
plant movements and tropisms from more strictly form-producing and
morphogenetic phenomena. Changes in the positions of parts, as in the
leaves of Mimosa, the fly-traps of Dionaea, the stamens of various plants,
and other structures, are due chiefly to changes in turgor brought about
by specific substances. This is essentially a problem in plant physiology
and offers opportunity to study the mechanisms of stimulus and response,
with their various chemical and electrical correlates.

Tropistic responses to gravity and light, however, are usually due to
more rapid cell elongation on one side of the axis than on the other and
are thus, in part, growth reactions. The various thigmotropisms, or

345

346 Morpho genetic Factors

responses to contact, involve more definitely morphogenetic changes.
When the tip of a tendril is lightly touched on one side, as by a small
branch or wire, the tendril will coil around it and thus tend to anchor
the plant to a support. This coiling results from the more rapid growth of
that side of the tendril not touching the support. There is evidence that
the stimulus of contact tends to produce a substance that checks growth,
although the mechanism which makes a tendril react thus, and later
contract in a coil, pulling the plant toward a support, is not well under-
stood.

Mechanical factors are also concerned in other growth reactions. Biin-
ning and his colleagues (1941, 1948, 1954), working with Mimosa, Si-
napis, and Vicia, have forlnd that mechanical stimulation (stroking with
paper or agitating on a shaking machine) checks the lengthening of
stems in darkness ( etiolation ) in much the same way that light does. The
internal structure of stems grown in darkness but mechanically stimu-
lated is quite different from that of etiolated stems and hardly to be
distinguished from ones growing in the light (Fig. 16-1). He suggests
that both mechanical stimulation and light partially inactivate auxin ac-
tion. Both stimuli are more effective if repeated at intervals than if applied
continuously, a fact which may be due to a refractive stage following
the stimulus.

Borriss ( 1934£> ) showed that Coprinus fruiting bodies which would not
have matured in the darkness will do so, at least partially, if mechanically
stimulated, and Stief el ( 1952 ) finds that the stipe of the fruiting body of
Coprinus responds to mechanical stimulation and to light just as do the
stems of higher plants, both stimuli tending to check elongation.

Mechanical pressure may have an important morphogenetic effect by
determining the plane of cell division in meristematic tissue (p. 49), the
plane of division tending to be parallel to the direction of the pressure.

It is with the more specifically morphogenetic effects of mechanical
stimuli, however, that we are particularly concerned here. Chief among
these are tension, compression, bending, swaying, and the omnipresent
stimulus of gravity.

Tension. Much work has been done on this problem, especially in
earlier years, but the results are often contradictory. Hegler (1893)
stretched seedlings of sunflower and petioles of Helleborus by attaching
weights to them. After a 2-day application of 150 gm., it required a
pull of 350 gm. to break these structures as compared with only 160 gm.
in the controls. Traction seemed to have increased the tensile strength,
and Hegler found that traction had increased the cell-wall thickness and
the amount of collenchyma.

Newcombe (1895) reviewed the very considerable amount of early
literature in this field. His own work confirmed Hegler's. He also found

Various Physical Factors 347

that if stem bases were enclosed in plaster and thus relieved of mechani-
cal strain they produced less mechanical tissue.

Ball (1904), however, repeated Hegler's experiments, using pulleys
and carefully comparing stretched plants with their controls, but found
no difference between them in structure or tensile strength. Hibbard
(1907) confirmed Ball. Still later Bordner (1909) studied the problem
again and confirmed Hegler's results, using similar material. In stretched
plants the amount of vascular tissue and the tensile strength were in-

Fig. 16-1. Vicia faba. Outer portions of
transverse sections through the second
internode. a, grown in darkness without
shaking; b, grown in light; c, grown in
darkness and shaken. Mechanical stimu-
lation has much the same effect on
growth as does light. ( From Bunning. )

creased. He found that no effects were produced unless the plants were
growing, a fact that may help explain the conflicting results of these
various workers.

Flaskamper (1910) and others subjected flower and fruit stalks to ad-
ditional weighting but found no change in histological structure. Wieders-
heim ( 1903 ) hung weights on branches of a weeping variety of beech
and reported that these grew less rapidly and had shorter cells but formed
no additional vascular tissue.

In all this early work on mechanical factors the suggestion was natural

348 Morpho genetic Factors

that the plant would tend to react in such a way as to oppose the effect
of the factor and, in the cases here discussed, to develop more mechanical
tissue which would resist traction and prevent breakage of the plant.
Vochting (1878), with his versatile interest in all such problems, asked
the practical question as to whether plant axes, subject to different ten-
sile strains in nature, showed structural differences as a result. He com-
pared the pedicels of squash fruits hanging from trellises with similar
ones growing on the ground and found more vascular tissue in the
former. However, when such a fruit was supported on a platform beside

Fig. 16-2. Effect of tension on wood structure. Left, transverse section of wood of
Fagus sylvatica from a root grown under strong tension; right, section of root of the
same species not under tension. Note generally thicker cell walls in the former. (From
Jaccard. )

a freely hanging one, he found the same amount of vascular tissue in
the stalks of both. Vochting suggested that the differences first observed
were due to differences in the amount of transpiration rather than to
tension. He also tried to induce mechanical tissue by traction in weak,
poorly vascularized plants, but without success. However, he grafted a
normal shoot on such a weak one and observed the development in the
latter of a marked increase of vascular tissue.

It might be objected that stems are not usually subject to tension but
that roots are, and it was evidently important to study these organs as
well. Wildt (1906) fastened the seedling stem and the adjacent part of

Various Physical Factors 349

its root in plaster and pulled gently. The soft central tissue disappeared
and a solid vascular core resulted. Flaskamper, who repeated and con-
firmed this, found that roots which had been subjected to traction had
somewhat less tensile strength than the controls. Newcombe (1895)
stretched roots of sunflower and squash and observed that they grew
somewhat stouter and were definitely stronger than the controls. Jaccard
(1914) studied some experiments of nature in this field, notably cases
where a small root crosses a larger one and is stretched by the growth in
diameter of the latter. In the root under tension the cell walls of the
wood were thicker than in the control (Fig. 16-2). The amount of me-
chanical tissue was less, however.

Fig. 16-3. Effect of tension on a tendril.
Device for subjecting part of a tendril
to tension by weight over pulley (A)
and for relieving the other part by hav-
ing a cord bear all the tension ( B ) .
Stimulus of contact is the same in both.
( From Brush. )

Among the organs of a plant most commonly subject to tension in na-
ture are tendrils. Many experiments have been undertaken with them
to determine whether traction (pulling) affects their structure. Much
difficulty was found by early workers in separating the effects of contact
(to which stimulus tendrils are particularly susceptible) from traction.
Brush (1912) placed a tendril in lengthwise contact with a thread to
the free end of which, thrown over a pulley, weights were attached. In
the control, this thread was continuous and sustained all the pull. In the ex-
perimental one the thread was interrupted in the middle so that the
tendril itself bore all the pull. Each tendril was thus in contact with the
thread through all, or almost all, its length, but one was under tension
and the other was not (Fig. 16-3). In both, there was more xylem than

350 Morphogenetic Factors

in tendrils having no stimulus of contact, but in the one under traction
the walls of the fundamental tissue cells were markedly thicker than in
the other tendrils.

Compression. Because of technical difficulties, not as many attempts
have been made to produce the opposite sort of mechanical stimulation,
compression in the lengthwise direction.

Pennington (1910) hung weights on woody and herbaceous stems of
various sorts as they were growing in height but found no appreciable
effect on structure or mechanical strength. Himmel (1927) used more

S

0RA.K5 FRJ533DRK

Fig. 16-4. Graph showing growth of Podophyllum petioles, in inches per hour, under
lengthwise pressure from various weights. Upper curve, control; lower, experiment.
Growth is markedly reduced by pressure. ( From Himmel. )

favorable material, the growing petioles of the large, umbrella-like leaves
of Podophyllum. On the apices of these petioles he hung weights which
were periodically increased as growth continued. He found that growth
rate in the weighted petioles was less than in the controls but that growth
in the former finally equalled that in the latter (Fig. 16-4). The rigidity
of the petioles was somewhat increased.

Rasdorsky ( 1925 ) , working with sunflower and marigold, approached
the problem in another way. He held up the plant by a gently stretched
thread attached to the upper part of its stem and thus relieved it from

Various Physical Factors 351

supporting its own weight. Plants thus treated were definitely weaker
than the controls. No structural changes are reported. The upward pull,
weak as it was, may have stimulated growth in length and thus tended
to make the plant top-heavy.

Newcombe (1895) supported the base of the stem in young sunflower
and squash plants by encasing it in plaster, thus relieving it of mechani-
cal strain. In that part of the stem under the cast much less mechanical
tissue was formed, although this developed rapidly when the cast was
removed. Other effects of such treatment, especially on respiration, might
account for the results obtained.

The studies on experimental traction and compression are contra-
dictory and indecisive, and many factors other than mechanical ones
may well be involved. Little work has been done in this field in recent
years. Schwarz ( 1930 ) subjected the problem of mechanical factors in
development to critical review and concluded that they have little effect
and that the results attributed to them may well be due to nutritional
influences and transpiration. Rasdorsky (1931), however, took issue
with him strongly.

Bending and Swaying. There is much more agreement as to the effect of
bending and swaying plant organs. Most workers find that, when grow-
ing herbaceous stems are bent, the cells (especially collenchyma and
bast fibers) on the convex side are smaller in cross section and thicker-
walled than corresponding ones on the concave side. The same results
are evident in plants grown on a clinostat, showing that gravity is not
involved.

A good discussion of this problem is presented by Biicher ( 1906 ) . To
this result of bending he gave the name camptotrophism. Since cells on
the convex side of the bend are evidently under tension and those on the
concave side under compression, the histological differences observed
seem related to the type of mechanical strain involved. These effects
agree with the ones from the experiments just reported where tension
seems to increase wall thickness and reduce cell size, and compression
produces the opposite result. Biicher obtained more direct evidence in
support of this conclusion. He enclosed in plaster most of the lower
portion of a growing hypocotyl of Ricinus. The upper part was enclosed
in another casing of plaster, leaving a short portion of hypocotyl unen-
closed between the two. The weight of the upper layer of plaster was
supported by the hypocotyl, which was thus subjected, particularly in
its free portion, to considerable lengthwise compression (Fig. 16-5). In
the control plants the hypocotyl had relatively small and thick-walled
cells. In the compressed hypocotyls, however, the cells were much
larger and had very thin walls. This sort of experiment seems worth re-
peating with modern techniques of analysis. What, for example, would

352 Morphogenetic Factors

the electron microscope show as to the character of such cell walls laid
down under pressure?

Biicher found that when a growing shoot, negatively geotropic, is
forcibly kept horizontal the cells of the upper side are smaller and
thicker-walled than those of the lower. This phenomenon he called
geotrophism and explained it on the assumption that since the lower
side grows more rapidly (tending to bend the stem upward) it must
be under compression and the upper side under tension. To test the
relative effects of gravity and bending, he inverted a plant of Ricinus
and held its tip bent at 90° to the axis (and thus horizontal). Campto-
trophism and geotrophism should thus be brought into opposition. Actu-

Fig. 16-5. Effect of vertical compression on hypocotyl of Ricinus. At left, young
seedling, protected by sheath and cotton plug, held in two blocks of plaster and there
subjected to compression from weight of plaster. At right, bast bundle from upper part
of such a hypocotyl ( above, under compression ) and from the normal control ( be-
low), showing increase in cell size and reduction in wall thickness as a result of com-
pression. ( From Biicher. )

ally, the plant reacted as it would to gravity, with smaller cells on the
upper, concave side. Perhaps in such a case it is the difference in degree
of tension that determines the result.

Vochting ( 1908 ) placed the stem of a potted plant in a horizontal po-
sition and put a support under it at some distance from the pot. On the
free end he hung weights and observed a considerable increase in the
cross section of the stem, especially of its vascular system. This was most
marked near the point of support, where the strain was greatest, and on
the upper and lower sides. Growth of the stem in length had ceased,
so that these changes resulting from mechanical stimulation were evi-
dently in the secondary tissues. Haerdtl (1927) found similar results.

Various Physical Factors 353

Many experiments have been conducted, beginning with Knight
(1811), on the effect of continually swaying plants as they grow. The
swaying was done by clockwork and pendulum, water wheel, or motor.
Observers are generally agreed that the cross section of the axis tends to
be elliptical under these conditions, with its wider dimension in the
plane of sway (Fig. 16-6), and that more vascular and mechanical tissue
is developed than in the controls (Rasdorsky, 1925; Burns, 1920).

It may be objected that in these swaying experiments conditions are
so abnormal that results may be due to other factors than purely mechani-
cal ones. The experiments of M. R. Jacobs (1954) are significant here. He
supported the trunk of a young pine tree with guy wires attached about

Fig. 16-6. Effect of swaying on sunflower stem, cross sections. At left, control. At
right, stem swayed for 3 weeks in the vertical plane of the figure. ( From Rasdorsky. )

20 feet from the ground so that lateral movement below this point was
prevented although the trunk above the point of attachment was sub-
ject to ordinary wind sway. This portion increased normally in thickness
but the unswayed lower portion grew much less rapidly than the upper
or than the unsupported controls. When the guy wires were removed,
this part grew rapidly in thickness until its normal diameter had been
attained. Evidently in such cases swaying stimulates cambial activity.
This may be a factor in producing the relatively slender trunks of trees
in a forest as compared with those grown in the open.

A somewhat similar case has been reported by Venning (1949) for
celery, an herbaceous plant. One series of seedlings was grown in con-

354 Morpho genetic Factors

stant wind and another in a windless environment. The former developed
50 per cent more volume of collenchymatous tissue than the latter. In all
such cases, however, it is difficult to separate mechanical effects from
those caused by increased water loss.

Ultrasonics. The morphogenetic effect of a quite different mechanical
factor, intense ultrasonic vibration, has been reported by several work-
ers. Takashima and others ( 1951 ) found that in germinating radish seed-
lings exposed for 16 minutes the shoots were much deformed. In peas
similarly exposed, length of root and shoot was increased through in-
creased cell size.

Gravity. Gravity is unlike the mechanical factors just discussed in
that it is continuous, unchanging in intensity, and constant in direction.
It is one of the most important formative factors, for plants must con-
tinually regulate their growth to it. The upright position of main-shoot
axes, the downward growth of primary roots, and the various inter-
mediate orientations of leaves and lateral branches and roots are mani-
festations of geotropic growth reactions. The general growth pattern of
the plant body is a specific reaction to gravity. The problem of tropisms
is primarily one for plant physiology but the student of morphogenesis
should not lose sight of the fact that these tropisms, whether reactions
to gravity, light, or other stimuli, are continually molding the pattern of
the plant.

One can distinguish between the tropistic effects of gravity in the strict
sense, which involve the orientation of parts, and its truly formative ones.
Conspicuous among the latter are the modifications of symmetry from
radial to dorsiventral or vice versa (p. 176). Many years ago Wiesner
(1868) and others studied the dorsiventral symmetry of plant struc-
tures, especially leaves, when the axis on which they were borne was
horizontal instead of vertical, and succeeded in inducing form changes in
them experimentally. For such a difference in form between the upper
and the lower leaves of a horizontal branch or between the upper and
lower sides of such leaves, Wiesner proposed the term anisophyllij (p.
171). Goebel later distinguished between anisophyllous forms which are
constant and hereditary and those which can be reversed by changing
the relation of the growing structures to gravity.

Gravity has been found to modify internal structure also. Brain (1939)
grew various plants horizontally on a clinostat and found that this modi-
fied the cells somewhat, those on the clinostat being generally shorter
and wider, presumably because of the greater extensibility of their cell
walls. Larsen (1953) found that gravity has little effect on rate of cell
elongation when acting on roots growing in the normal direction but
checks such elongation when acting in the opposite direction or at right
angles to it. Imamura ( 1931 ) was able to change the position of palisade

Various Physical Factors 355

and spongy parenchyma by reversing the orientation of Iris japonica
leaves to gravity. Kreh (1925) examined changes in the fruiting bodies
of the fungus Lenzites which had been turned through an angle of 180°
with relation to gravity and found that in new growth the original
dorsiventral structure was restored. Many other cases of the effect of
gravity on structure have been reported.

It is often difficult to distinguish the effects of gravity from those of
light, since a change in the relation to one usually produces a change
in the relation to the other unless experimental conditions are carefully
controlled. Wiesner (1892c) in a later paper recognized that his earlier
results in anisophylly were due to light as well as to gravity, and
Bussmann ( 1939, 1941 ) found the same to be true of induced dorsiven-
trality in fern prothallia.

Gravity presumably does not modify plant structure directly but acts
through its influence on other factors. It produces tension and compres-
sion of tissues with consequent effects on cell division and expansion.
The reaction of woody plants in developing stem tissues strong enough
to resist bending and wind sway has been mentioned, and there must be
the same regulatory control of growth to resist weight of trunk (Esser,
1946). In this sense, gravity acts as a mechanical factor. Opatowski
(1946) explains the oblique growth of trees under the action of prevailing
winds as a mechanical response, based on the concept of maximum
strength.

Equally important is the role of gravity in the distribution of growth
substances. Just how this occurs is not clear, but differential distribution
of substances under the stimulus of gravity must be involved (p. 380;
Brauner, 1927). This presumably affects the form of structures when
symmetry is changed from radial to dorsiventral, for example. It also
has less direct effects. Van Overbeek and Cmzado ( 1948 ) and Fisher
(1957) have shown that flower formation is geotropically stimulated in
horizontally placed pineapple and soybean plants, presumably by
alteration in the distribution of growth substances. Other phenomena
of differentiation may perhaps be explained in the same way.

Gravity serves as the frame of reference to which the whole pattern
of plant growth is regulated. A plant develops under the constant and uni-
form stimulus of gravity, and its tropistic and morphogenetic responses—
hardly to be distinguished from each other here— are such that a spe-
cific bodily form is produced. Without this regulation to a steady orient-
ing directive, the general pattern of the plant body would doubtless be
much less specific and might even fail to be developed. Because of their
being anchored in one spot, plants are much more sensitive of such
gravitational form control than are animals.

Reaction Wood. The example of such control that has been worked

356 Morphogenetic Factors

out most fully is one which was first observed in the development of
reaction wood of conifers and later in similar tissue in angiosperms.
Students of wood structure have long noticed that horizontal branches
of coniferous trees are excentric in cross section (p. 175), with the pith
nearer the upper side than the lower. Below the pith is a wedge-shaped
sector of wood, reddish in color when freshly cut, and hence often
called "rotholz." Since the lower side of a branch is obviously under
compression, this was long regarded as the cause for the development
of this sort of structure, and it was called "compression wood." Its cells
are somewhat shorter than those of normal wood, and the micellae in
their walls are less steeply pitched. Such wood is absent, save exception-
ally, in vertical axes and thus in the main trunk but develops wherever
such an axis is forced to grow at an angle from the vertical, as in a tree
bent partly over. Such wood grows somewhat more in length than does
normal wood and thus produces considerable longitudinal compression.
If a tree grown in an oblique position is sawn across, beginning on the
lower side, the saw therefore tends to bind.

This tissue has now been shown not to be the result of growth under
compression but to have a nature and function of much morphogenetic
significance. It is now more correctly called reaction wood. Together
with the corresponding tissue in angiosperms, it has been studied by
various wood anatomists, especially Hartmann (1932, 1942, 1943), whose
work has been extended somewhat by Sinnott (1952). In young conifers,
especially pines, before the growing season began, these workers tied
some of the lateral branches downward and others upward. They also
tied the tip of the main axis into a position out of the vertical, sometimes
even in a loop. When new shoots of the current year developed from
the terminal buds of these various axes, these new shoots tended to have
the same direction of growth that they would have had if the shoot out
of which they grew had not been fixed in an atypical position (Fig. 16-7).
The main axis bent around so that it again grew upward. The lateral
branches (in white pine) grew out at an angle of about 70° from the
main trunk and thus from the directional pull of gravity. In other words,
there was, in a sense, a regeneration of the normal growth pattern of
the tree.

In this process the reaction wood performs an essential function, for it
always occurs in such a place that its greater lengthwise growth will tend
to bend the new shoot (and the free portion of the old shoot) into a
direction which would be normal for it. If a lateral branch has been
bent upward, for example, the reaction wood will be on the upper side,
for this will push the branch down. Such a change continues until the
orientation of the shoot is normal, when reaction wood again develops on
the lower side, as in ordinary branches. Its function here seems to be to

Various Physical Factors 357

counteract, by its upward push, the downward pull caused by the
weight of the branch. A bent-over terminal shoot develops reaction wood
on its lower side and thus pushes the axis up to vertical. If the terminal
shoot is removed, an excess of reaction wood begins to develop on the
under side of the lateral branches just below the tip and one of them
is finally pushed up to the vertical and becomes a new "leader." Some-
times two share this leadership, neither becoming quite vertical.

Fig. 16-7. Development of reaction wood in pine in three branches which had been
bent upward artificially. Reaction wood normally is formed on the lower side but in
the new growth on these branches it develops on the upper side after bending and
thus tends to push them back to their normal orientation. (From Sinnott.)

Angiosperm branching is regulated in much the same way except that
the reaction wood here is normally on the upper side of a branch and
acts by producing tension rather than compression, thus pulling the
branches into place instead of pushing them. Wardrop ( 1956 ) believes
that the distribution of tension (reaction) wood in Eucalyptus is regula-
tory and operates to maintain normal tree form much as reaction wood
does in the conifers.

That compression itself is not responsible for the formation of this
wood is shown by the fact that when a terminal shoot is bent around and

358 Morpho genetic Factors

tied in a vertical loop, reaction wood is formed on the under side of both
the upper and lower parts of the loop. In the former, the wood is under
compression but in the latter under tension. That gravity is not directly
responsible is shown by the appearance of reaction wood on the upper
sides of branches which are being pushed down. In every case the de-
velopment of this wood is such that it will bring back the normal pattern.

The reaction of each part of the plant seems to be a specific orienta-
tion to the direction of gravitational pull. This reaction is different in
different parts of the growth pattern of the tree. In herbaceous material
(branches of Aster) the author has found that a lateral branch tied out
of position will tend to assume its normal angle to gravity rather than
its normal angle to the main axis of the plant. When gravity is replaced
experimentally by centrifugal force, reaction wood is also produced
(Scott and Preston, 1955).

Auxin has been shown to be responsible for the relation between a
terminal bud and lateral ones below it (p. 386), and it is presumably
concerned with the production of reaction wood (Wershing and Bailey,
1942). The problem of morphogenetic significance is why there is just
enough auxin (and thus enough reaction wood) at just the right place
and time to produce such a specific pattern of branching that this can
be used as a diagnostic character for the species. Here is the problem
of organic form in one of its simplest but most puzzling manifestations.

Spurr and Hyvarinen ( 1954a ) have reviewed the literature of reaction
wood in the conifers.

Tissue Tension. Another factor, mechanical in its nature, which may
be of some morphogenetic importance is tissue tension. Not all the cells
in a tissue are equally turgid, and cell walls differ in their elasticity and
their plasticity. Tissues also grow at different rates. These differences
often cause tensions between cells or groups of cells which, since plant
cells adhere firmly to each other, cannot be reduced by cellular readjust-
ments in position.

In an early and thorough paper Gregor Kraus (1867) examined this
problem. He measured the length of a piece of growing herbaceous inter-
node and then sliced it into longitudinal strips, each consisting of only
one tissue (pith, wood, cortex, or epidermis). When he measured the
length of these, he found that the outer ones had shrunk in comparison
with their original length before isolation but that the inner ones had
expanded. Evidently there was considerable tension between them in
the intact internode, the outer tissues being stretched and the inner ones
compressed.

The degree of tissue tension is not constant but is usually low in young
internodes, increases farther back, and finally decreases in most cases
to zero as growth finally ceases. The distribution of tension among the

Various Physical Factors 359

tissues also changes. Schiiepp (1917) found that there was tension in the
growing point but that here it was opposite in its distribution from that
in tissue which was extending. Schneider (1926) found no tension in the
growing point itself but saw it first in the leaf primordia, which for this
reason tend to bend inward.

What bearing tissue tension may have on differentiation or on the de-
velopment of form is not clear but it may be of some importance. In
young ovaries, however, where presumably form and structure are being
determined, there seems to be little tension though this increases in
later stages of development. A remarkable instance of tension in dead,
dry wood has been reported by M. R. Jacobs ( 1945), who found that if a
board which includes the whole width of the log is sawed at one end part
way down by a series of parallel longitudinal cuts the strips thus sepa-
rated tend to spread apart fanwise, indicating the existence of a very
considerable degree of tension between the inner and the outer parts of
the log.

Absolute Size. Another morphogenetic factor, which in a sense may
be regarded as physical, is absolute size itself. It is clear, as Galileo long
ago pointed out in his principle of similitude, that as any body increases
in size its volume enlarges as the cube of the diameter but its surface
only as the square. Thus the ratio of surface to volume will progressively
decrease. In a living organism, where physiological activity is often
limited by the amount of available surface for interchange of material
between organism and environment, or between one tissue and another,
the surface-volume relationship is of much importance and is obviously
related to changes in shape and structure.

This shows most simply in the increased elaboration of bodily form
as size increases. Among algae, for example, the smaller types are
relatively simple and compact but the larger ones, through branching
or surface convolution, have a much more elaborate conformation, with
the result that the ratio of surface to volume is not very different in the
two. A good example of the same thing is the difference between the
small, rounded chloroplasts of higher plants and the very much larger
chromatophores of some of the lower ones, which are elaborately branched
and dissected. Internal anatomy displays the same tendency, for in the
sporeling of a fern the vascular cylinder is a solid rod but as the plant
grows this soon opens out to form a hollow tube. It may later be broken
up into a ring of bundles or even a series of concentric rings or tubes.
The radial thickness of each strand thus tends to be approximately the
same, with the result that the surface of contact between xylem and
phloem, so important in the physiology of the plant, remains relatively
constant. Every unit mass of phloem tissue has essentially the same
"frontier" on the xylem as every other one, and none is limited in its water

360 Morpho genetic Factors

supply. Similarly, as roots increase in size, the number of radial arms
increases, with the result that the xylem-phloem surface remains relatively
constant.

There are many examples of this correlation between absolute size
and complexity of conformation, a fact which Bower (1930) was the

N

*

/

rv*

Fig. 16-8. The effect of absolute size on structural complexity. Steles of Lycopodium
scariosum of seven progressively larger sizes showing the increase in complexity that
accompanies increased size. ( From Bower. )

first to bring forcefully to the attention of botanists ( Fig. 16-8 ) . Although
the advantage of such a correlation is obvious, the problem of how it is
brought about morphogenetically is not clear. The advantage is not
effective physiologically until the structures are mature and functioning
but the pattern is laid down in the meristem. It may be that this is simply
a case of inheritance of a particularly advantageous developmental pat-

Various Physical Factors 361

tern which has arisen through natural selection, as have other embryonic

characters.

The relation between size and form here seems to be too immediate,
however, to be accounted for in this long-range fashion. An inherited
pattern ought to be evident in a small and stunted as well as in a large
individual, but the effect of size seems to be more direct. One is tempted
to see here another example of the regular spacing of structures to which
attention has earlier been called (p. 199). In the same way there may be
maintained a constant ratio between primary xylem and phloem, a ratio
which originates within the tissues of the primary meristem. This morpho-
genetic problem, which has an important bearing on the origin of differ-
entiation and of structure in general, seems especially favorable for
biochemical and perhaps even mathematical attack.

Bioelectrical Factors. For many years the possibility that electricity,
in one way or another, might affect the physiological and developmental
activities of plants has interested botanists, and there is a very consider-
able literature on the subject. Unfortunately, this is a field that is theo-
retically and technically so complex that few workers are qualified to
obtain dependable results in it, and much of the published work is there-
fore of doubtful value. The present writer is certainly not competent to
review it critically.

Students of tropisms have discussed the possibility that differences in
electrical potential may be involved in these activities. Went (1932)
suggested that the polar flow of auxin is an electrophoretic process.
Clark (1938) raised doubt as to this idea and pointed out that it is pos-
sible by certain chemical treatments to abolish the polarity of auxin trans-
port without changing the electrical polarity, protoplasmic streaming, or
other characters of the system (p. 385). Schrank, however, who has dis-
cussed the problem in some detail ( 1957 ) , has shown that in the trans-
verse distribution of auxin in the Avena coleoptile, a transverse electrical
polarity precedes the movement of auxin, thus tending to support Went's
theory. The early work on the electrical control of polarity was reviewed
by Thomas (1939).

Morphogenetically the most significant result of the work with elec-
tricity is the evidence that in many organisms there are continuous bio-
electrical currents and a distribution of electrical potential differences
so constant that a bioelectrical field is set up in the organism. By the use
of a very delicate micropotentiometer Burr was able to demonstrate
the existence of such a field in amphibian eggs (1941). Even in the
young ovaries of cucurbits such relations between the form of the ovary
and the bioelectrical pattern could be shown (1944). Burr and Northrop
( 1939 ) have discussed the general problem of electrodynamic fields in
living organisms. Lund ( 1931 and others ) carried out a series of studies on

362 Monpho genetic Factors

electrical potential differences in trees, as related to the phenomena of
polarity, dominance, and correlation in them.

If bioelectrical fields are actually concerned with the specific character
of development, it would seem possible to change them by applying
other electrical fields externally and thus perhaps to modify organic
form. This turns out to be very difficult to accomplish, however. Never-
theless, Lund ( 1945 ) was able to inhibit completely the growth in length
of an onion root by passing an electric current upward through it, al-
though the same current passing downward produced little or no inhi-
bition.

It is tempting to explain all form differences as results of these constant
bioelectric fields, and they may well be concerned with the control
of organic development. Such fields are doubtless related to the fine
structure of protoplasm and the complex pattern of surfaces which this
presents. Whether the fields are the cause of developmental changes or
are themselves the result of chemical or physical factors is an important
theoretical question. The problem of bioelectric factors is too complex for
easy solution, but it should certainly continue to be attacked vigorously
by those who are qualified to do so.

The volume by Lund and his collaborators ( 1947 ) presents a good ac-
count of the problem of bioelectrical fields and their implications for
morphogenesis. Rosene has gathered for it a bibliography of 1,406 titles.

CHAPTER 17

Chemical Factors in General

Chemical factors are of paramount importance for metabolism and for
physiology generally, but they also have an important part in the de-
termination of form and structure. Physical factors-light, water, tem-
perature, gravity-produce their effects on development chiefly through
the external environment, but chemical ones operate morphogenetically
both from inside and outside the organism, and in studying them it is
necessary to recognize this fact. Nitrogen, for example, by its presence in
the soil, markedly affects the growth and development of a plant rooted
there, but it does so because of what happens after it has entered the
living system of the plant. Here it may be moved from place to place and,
as a constituent of protoplasm, it affects the course of development in
many ways. The student of morphogenesis concerns himself, therefore,
not only with the visible effects of changing amounts of nitrogen in the
soil but with the history of this element as a part of the organic mecha-
nism. This is true for other chemical substances, whether taken in from
the outside or synthesized within the plant. Much of differentiation re-
sults from differential distribution of substances throughout the plant

body.

Many effects of these substances are local. In studying them experi-
mentally it is therefore not enough to examine their effects upon the
plant as a whole but to discover what happens in particular parts of the
plant as their concentration in these parts is altered. The most important
discoveries in the field of growth substances, for example, have been
made by studying their local effects on a developing root or leaf or ovary.

The role of chemical substances in development also changes with time,
for the life of the plant is a life history and this history consists of specific
progressive changes. These are reflected not only in alterations in struc-
ture, as between juvenile and adult foliage, but in physiological changes
that go on within the plant. Some of these are gradual but others are
more sharply marked. Such is the transition from the vegetative to the
flowering state (p. 184), in which meristematic activity shifts from one
region and one type to others that are quite different and where there is

363

364 Morphogenetic Factors

often a radical redistribution of substances in the plant body. The plant's
life history is composed of such progressive steps. This concept is of
importance for morphogenesis and perhaps especially for its chemical
aspects.

The subject of chemical factors in plant life, and particularly of the
biochemistry of metabolism, is one of the chief concerns of physiology,
but the only aspect of this field germane to the science of morphogenesis
is the somewhat limited portion of it which deals directly with the rela-
tion of chemical substances to development. The present discussion will
necessarily treat this subject in nothing more than a very brief and
general fashion. One chapter will be devoted to the role of the elements
and the compounds that are primarily significant for their role in nutrition
rather than in morphogenesis. A second chapter will deal with those
substances that, even in very minute amounts, have been found to exert
profound effects on growth and development and are commonly called
growth substances.

ELEMENTS

It has long been known that only a few of the chemical elements are
essential for plant life. These, in addition to carbon, oxygen, hydrogen,
and nitrogen, are sulfur, phosphorus, calcium, magnesium, potassium, and
iron, together with a number of others, notably boron, zinc, copper,
manganese, cobalt, and a few others which, in very small amounts, are
essential for the nutrition of most plants and are known as trace elements.

Several of the elements, or simple compounds of them, have been
found to have some effect on development and are thus of morphogenetic
importance, though except for nitrogen this is relatively minor.

Nitrogen. This element is of outstanding significance in many ways.
It is an essential constituent of all proteins and thus of protoplasm, and
from its presence in the nucleoproteins it is concerned in the production
of new living stuff and thus in all growth and reproduction.

That nitrogen tends to increase the vegetative growth of plants has
long been known, but it may also have certain specific effects on their
structure. Burkholder and McVeigh (1940) grew maize (both inbred
and hybrid ) with varying applications of nitrogen in sand culture. Where
nitrogen was abundant, as compared with plants where this was limited,
meristems were better developed, length and diameter of stem were
greater, cell size and cell number increased as did the size and number
of the bundles, there was greater differentiation especially in the phloem,
and both sieve tubes and vessels increased in diameter (Fig. 17-1).

Plants growing with little available nitrogen tend to be woodv and to
have thick cell walls, presumably because much of the carbohydrate is

Chemical Factors in General

365

deposited in these structures, whereas if nitrogen were abundant it
would be used in protein synthesis. Shields and Mangum (19.54) studied
the content of total and of amino nitrogen in the leaves of '40 species of
plants and found it highest in thin, mesophytic herbaceous leaves, next
in small xeromorphic dicotyledons, and least in monocotyledons with
much mechanical tissue.

L3X 38-11

/ 38-1 1

0 0.032 0.16 08 4.0

MILLIMOLES OF N PER LITER

Fig. 17-1. Nitrogen and hybrid vigor. Two inbred lines of maize and their hybrid
grown in sand culture with various amounts of nitrogen. The increase in size with
added nitrogen is much greater in the hybrid than in either parent. (From'Burk-
holder and McVeigh. )

Nitrogen supply may be related to the differentiation between male
and female sex organs, for Kocher (1941), studying the dioecious species
Melandriurh album, found markedly more nitrogen (as percentage of
dry weight) in leaves of female plants than of male. This difference
was slight in seedlings, rose until flowering took place, and then disap-
peared.

There may be interaction between nitrogen and other factors. In onion,

366 Morpho genetic Factors

for example, Scully, Parker, and Borthwick ( 1945 ) observed that,
with plants grown at photoperiods longer than necessary for bulb pro-
duction, variations in nitrogen had little effect, but when the photoperiod
was close to the critical one for bulbs, bulb development was consider-
ably greater at low nitrogen levels than at high ones.

Cohen ( 1953 ) reports the effect of a nitrogen compound, ammonia, on
the development of the slime molds Dictyostelium and Polysphondylium,
two members of the Acrasiaceae ( p. 223 ) . Treatment with a low concen-
tration of ammonia greatly simplifies the morphogenetic expression of
these forms and reduces the degree of their differentiation. The sorocarps
produced resemble those of the genera Guttulina and Guttulinopsis.

Carbohydrate-Nitrogen Ratio. Many other instances of the develop-
mental effects of nitrogen could be cited. More widespread than these
changes produced by nitrogen directly, however, are the ones that re-
sult from the balance between nitrogen and carbohydrates. Horticul-
turists know that nitrogen stimulates vegetative growth, that weakly
vegetative plants tend to flower early, and that in vigorously vegetative
ones flowering is either scanty or does not occur until the amount of
available nitrogen is reduced. This problem was first studied intensivelv
by Kraus and Kraybill (1918) in tomatoes. They found that in strongly
vegetative plants bearing few flowers or fruit the C/N ratio was low.
Those producing fruit abundantly had a high C/N ratio but had been
given a good supply of nitrogen at the beginning of their growth. They
interpret these facts to mean that when nitrogen is abundant all the
carbohydrate produced by the plant will be used in forming new vege-
tative tissue. If nitrogen is in short supply, however, carbohydrates will
tend to accumulate, and when the C/N ratio becomes high enough, the
development of reproductive structures will be stimulated. This hap-
pens early in weakly vegetative individuals, but such plants are too small
to produce a large crop of fruit. Maximum yield results from an abundant
supply of nitrogen at first and an active production of carbohydrates
later by the fully grown vegetative structures. This is what normally
happens under favorable conditions. The important morphogenetic as-
pect of this hypothesis is that it maintains that the differentiation of
reproductive organs is dependent on the accumulation of carbohydrate in
the plant. Until this happens, vegetative structures take priority over
reproductive ones in the use of available carbohydrate.

In general, the younger the tissue, the lower is the C/N ratio. From
a low point in the seedling it increases as foliage develops and as the
ratio of top to root grows larger until it reaches the point where reproduc-
tive structures are formed. This would explain why flowering normally
is deferred until the plant has reached a considerable vegetative develop-
ment.

Chemical Factors in General 367

The relation of the C/N ratio to flowering is evident in many ways. In
biennially bearing apple trees, for example, it is high in the bearing
years and low in the "off" ones. In fruit spurs where the buds are de-
veloping into flower buds, starch content tends to be high and nitrogen
low, whereas in barren spurs the opposite is true. Potter and Phillips
(1927), however, found that flower-bud formation in fruit spurs was
more closely related to the amount of nitrogen than to any ratio be-
tween this element and carbohydrates.

Loomis ( 1932 ) has emphasized the fact that the effect of water on
development resembles that of nitrogen, both tending to stimulate vege-
tative growth. He believes that the balance is not so much between carbo-
hydrate and nitrogen as between the factors that tend to produce growth
and those that tend to induce differentiation. The former include both
water and nitrogen together with any other factors, such as temperature,
that favor the synthesis of new protoplasm. Differentiation, on the other
hand, requires an excess of available carbohydrate. Why this is so is by
no means clear, though there may be a selective advantage in a mecha-
nism which tends to defer the development of reproductive structures
until a plant has reached the size where it is large enough to produce
fruit abundantly.

The carbohydrate-nitrogen ratio is related to other structures than
reproductive ones, notably the shoot-root ratio. In general, the higher the
C/N ratio, the larger is the relative size of the root. When nitrogen is
abundantly available in the soil, the increased growth tends to occur
in the shoot more than in the root. Hicks ( 1928b ) found that in willow
cuttings the carbohydrates pass downward and the nitrogen upward so
that the C/N ratio is higher at the base, where roots develop, than at
the tip, where shoots are formed. Da vies (1931) also observed that in
willow cuttings roots develop in regions where nitrogen, as a percentage
of dry weight, is low and shoots where it is high. These facts obviously
have a bearing on the problem of polarity in regeneration (p. 119).

Reid (1924) made stem cuttings from tomato plants that were high in
C/N ratio and from others that were low and found that the former made
better roots than the latter. She also observed (1929) that the relative
development of the root in seedlings of various species was related to
the proportion of carbohydrate to nitrogen in the seed from which
they grew. Where this was high the seedlings had stronger roots than
where it was low.

Despite the evident relation between the C/N ratio, as observable in
the chemical composition of the plant, and the processes of flowering and
root formation, there is now a good deal of evidence that this ratio may
not be the cause but rather an accompaniment of these activities. In a
number of instances, such as the soybean (Murneek, 1937) and wheat

368 Morphogenetic Factors

(Polster, 1938), floral initiation begins some time before the change
from low to high C/N ratio takes place. In various plants that have been
brought to flowering by other means, such as chemical or photoperiodic
stimulation, the increase in C/N is much less conspicuous than under
natural conditions. In many cases, also, there is no precise ratio that may
be counted upon to induce flowering. Both in carbohydrates and com-
pounds of nitrogen there are many different chemical forms, and it is a
matter of doubt whether the ratio should regard total, soluble, or easily
available carbohydrate, on the one hand, and total, protein, or soluble
nitrogen on the other.

Despite these criticisms, the general concept that in the living plant
there is at any particular stage a balance between various chemical
constituents and that a shift in this balance is related to a change in the
activities of the plant is an important one. The organism tends to maintain
a homeostatic equilibrium among its various processes but this is not a
static condition, for the equilibrium changes progressively as the or-
ganism develops from one phase to the next. This is so complex that
the ratio between any two chemical substances will usually give only an
incomplete picture of it. A study of the C/N ratio, whether this be
cause or effect of the onset of the reproductive phase, will doubtless
continue to provide information about this major step in the life history
of the plant.

Other Elements. Much of what is known about the morphogenetic
effects of the other essential elements comes from observation of changes
in development produced when each is deficient in amount. These changes
are usually differences from the normal amount of growth or are ab-
normalities of various sorts, "hunger signs" resulting from insufficient
nutrition. The literature of physiology and pathology is full of such in-
stances. Venning (1953) has described the developmental effects of
deficiencies in sulfur, calcium, nitrogen, potassium, phosphorus, and iron.
The effects of the various trace elements have been reviewed by several
workers, among them Brenchley (1947) and Wallace (1950).

A few of the effects of various elements are of morphogenetic interest.

Phosphorus is of much importance in physiology and genetics because
it is a constituent of the nucleic acids. Morphogenetically it is significant
in relation to mitosis. Phosphate promotes cell division in roots but has
little effect on cell elongation, whereas nitrate promotes elongation but
not division.

Stanfield ( 1944 ) analyzed roots and tops of staminate and pistillate
plants of Lychnis dioica and found that the staminate had a higher per-
centage of phosphorus than the latter in both vegetative and early flower-
ing phases.

Pierce ( 1937 ) observed that in violet plants grown in nutrient solu-

Chemical Factors in General

369

tions without calcium the chromosomes in root-tip cells were markedly
smaller than when grown in complete nutrient. When phosphorus was
in excess, however, the chromosomes were about twice normal size.
These differences were also reflected in the size of the nucleus.

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added to the medium at the times indicated by arrows. Dash lines show growth
without further addition of zinc. ( From Skoog. )

There is a good deal of evidence that phosphate fertilizers increase the
growth of roots as compared with tops, particularly in root crops.

Calcium is closely connected with the formation of the cell wall. When
it is deficient in amount the cytoplasm tends to break down, the walls
to fall apart, and meristems to degenerate. Calcium itself does not enter

370 M or pho genetic Factors

into the composition of the wall but produces its effects through changes
in the cytoplasm ( Sorokin and Sommer, 1929 ) .

More conspicuous effects of calcium have sometimes been observed.
Pearsall and Hanby (1925), for example, found that in Potamogeton

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excess calcium made the leaves broader and their cells more numer-
ous.

In field plots abundantly fertilized with potassium, plants of flax,
ramie, oats, and willow showed marked increase in number and size of
bast fibers (Tobler, 1929). Hemp was but slightly affected.

Chemical Factors in General

371

Robbins and his colleagues (1929) have observed a shape difference re-
lated to potassium. Sweet potato plants grown with little potassium have
longer and more slender roots as compared with "chunkier" ones on
plants grown where this element is abundant. The difference seems to be
due to the greater cambial activity in the well-nourished plants as a
result of increased protein synthesis resulting from an abundance of
potassium.

Zinc has indirect morphogenetic importance since it seems to be
necessary for the maintenance of auxin in an active state (Skoog,
1940; Fig. 17-2).

Boron evidently is concerned with the development of the cell wall
and affects the process of carbohydrate condensation into wall material
(Spurr, 1957; Fig. 17-3). Reduction in amount of boron produces hyper-

lAA+Co

Fig. 17-4. Effect of cobalt on etiolated pea
stem segments supplied with auxin alone
(below) and auxin plus cobalt (above).
( From Miller. )

O

12 3 4

PER CENT SUCROSE

trophy and hyperplasia of tissues, especially the cambium, in tomato,
turnip, and cotton and affects the number and the maturation of the fibers
(Palser and Mcllrath, 1956). MacVicar and Struckmeyer (p. 320) ob-
served that day-length altered the boron requirement of soybeans.

Cobalt has been found by several workers to increase the size of cells,
particularly in association with sucrose. Miller (1954) reports that in
etiolated pea stems cobalt salts plus auxin produced only slight elonga-
tion. Sucrose alone had the same effect, though it considerably increased
fresh weight ( Fig. 17-4 ) . When sucrose and cobalt were applied together
to the pea stem there was greatly increased elongation. He believes that
water uptake and wall growth are separate processes and suggests
that sucrose tends to increase cell volume but that cobalt promotes the
ability of the cell to enlarge its surface.

372 M or pho genetic Factors

Lyon and Garcia (1944) studied the effects of anions and cations on
stem anatomy of tomato plants in over 40 nutrient solutions varying in
the relative proportion of nitrogen, sulfur, and phosphorus, and of calcium,
potassium, and magnesium. Differences in stem diameter and in relative
amounts of phloem, xylem, and pith, as well as cellular differences in
parenchyma of pith and cortex, vessels, fibers, phloem cells, and pericycle
fibers, were correlated with specific differences in the nutrients.

Makarova ( 1943 ) examined the relation of various nutrient elements
to traits described by Maximov as xeromorphic and found that, in gen-
eral, such traits were intensified by phosphorus, boron, and manganese
and diminished by potassium and iron. These effects chiefly concern cell
size.

MORE COMPLEX SUBSTANCES

Sucrose itself may have certain morphogenetic effects. Yates and Curtis
( 1949 ) found that the root-shoot ratio in orchid seedlings growing in
nutrient media is not related to the C/N ratio, as in so many cases, but to
the concentration of sucrose alone, the optimum concentration for root
growth being markedly higher than for shoot growth. At the best con-
centration for root growth, shoot growth was reduced.

In sporelings of Marsilea grown with varying concentrations of glu-
cose, Allsopp ( 1954 ) observed that in low concentrations the plants
showed many of the traits of the water forms of amphibious plants, and
those at higher concentrations resembled land forms. This presumably
is not owing, however, to the specific morphogenetic effect of glucose
but to the fact that in the lower concentrations water is more available
osmotically and conditions therefore to some extent simulate aquatic
ones (p. 332).

By using glycogen, soluble starch, or dextrin as a carbon source in-
stead of sugar, Nickerson and Mankowski (1953) were able to convert
the normal budding yeast type, in Candida albicans, to a filamentous
mycelial type.

Sossountzov (1954) tried various amino acids instead of inorganic
nitrogen as nitrogen sources in the culture of fern prothallia and found
that under these conditions they tended to be atypical but that in most
cases the proportion of filamentous prothallia to cordate ones was con-
siderably increased.

Hammett and Walp (1943) studied 10,000 fertilized Fucus eggs, half
of which were exposed to proline and half were not, and observed that
proline increased differentiation here (as measured by the production
and growth of rhizoids) much as it has been shown to do in ani-
mals. Barghoorn (1942), however, found no definite evidence that pro-

Chemical Factors in General 373

line stimulates the differentiation of protoxylem in roots of cotton and

beans.

By adding certain chemical substances to the medium, Tatum, Barratt,
and Cutter ( 1949 ) produced various nonheritable morphological changes
in Neurospora and Syncephalastrum which they termed paramorphs.
Anionic surface-active agents such as Aerosol induced the formation of
compact colonial paramorphs. Sorbose proved to be the most effective
paramorphogen. Discovery of the mechanisms by which these substances
cause the production of such specific forms in these very simple organisms
might yield important information on the origin of forms at higher levels.

There is a considerable group of chemical substances, the vitamins,
which are of great importance in animal nutrition. Many of them are
synthesized by plants, and some are now known to be essential for the
growth of certain plants or plant structures. Vitamin Bx (thiamin), for
example, can be shown to be necessary for the growth of excised roots in
culture, but it is synthesized in the shoots. Nicotinic acid also seems to be
essential for root growth, but what other vitamins may also be necessary
for the life of plants is not certainly known. All the vitamins are effective
in extremely small concentrations.

The morphogenetic importance of the vitamins for plants seems not
to be very great. Reid (1941) has evidence that vitamin C affects cell
size in the meristematic region, and there are a few similar instances.
Schopfer (1950) has reviewed the problem of the vitamins in morpho-
genesis.

CHAPTER 18

Growth Substances

The chemical substances discussed in the previous chapter are primarily
important in the nutrition of the plant, and most of them are required
in relatively large amounts since they contribute to the composition of
protoplasm. In relatively few cases, however, have they been shown to
be of any very great morphogenetic significance.

There is another group of physiologically active substances which are
not concerned with nutrition and which, although present in most
cases in very low concentrations, are of great importance for the growth,
development, and differentiation of plants. They have been given various
names-hormones, inductors, Wuchsstoffe, activators, evocators, growth
regulators, and growth substances. They were first studied in animal
physiology but in recent decades they have assumed major importance
for an understanding of the development of plants as well. They are
diverse in character and effect and are the chemical means by which
many morphogenetic processes are controlled. Among these processes
are growth, tropisms, many correlations, and the determination and
differentiation of specific organs and structures in the plant body. Indeed,
as our knowledge of these substances increases, more and more of the
activities in development and differentiation are found to be affected by
them, and, in interaction with the genes, they seem to be the chief
agents in morphogenesis. It must not be forgotten, however, that they
are agents merely and that the ultimate control of development lies in
the factors that determine the concentration, distribution, and interaction
of these and other chemical and physical mechanisms. Here lies the ulti-
mate problem.

Many of these substances, in great diversity, are produced and con-
trolled by the plant itself and are thus of particular interest in normal
morphogenesis. It has been shown, however, that a large number of
synthetic compounds have effects comparable to naturally occurring ones,
and this has greatly extended the means for experimental attack on de-

374

Growth Substances 375

velopmental problems (Zimmerman and Wilcoxon, 1935; Zimmerman,
1951b; and an extensive series of other papers ) .

The literature in this active field is large, and in a brief space little
more than a very general introduction to it can be made. The student
may be referred to a number of books, symposium volumes, and reviews,
among which are the following: Boysen-Jensen (1936); Went and Thi-
mann (1937); Avery and Johnson (1947); Thimann (1948); Skoog
(1951); Soding (1952); Audus (1953); Leopold (1955); Wain and
Wightman (1956); and the Eleventh Symposium of the Society for Ex-
perimental Biology (1957).

The term hormone was first used by Starling in 1904 with reference to
secretin, a substance important in animal physiology. Such hormones are
regarded as "chemical messengers" since they are produced in one part
of the body and carried to some other part, where they affect develop-
ment and various physiological processes. Their discovery marked a great
advance in an understanding of the chemical control of growth and
differentiation.

With the demonstration that there are substances in plants which are
physiologically active in similarly small amounts, the term hormone was
carried over into plant physiology by Fitting (1909) in relation to a
substance in orchid pollen which produced swelling of the ovary. Various
phytohormones are now recognized. This word is not a particularly
happy one, however, for plants lack the efficient circulatory system of
animals. Indeed, many of these substances exert their effects in the
region where they are produced and thus are not "messengers" at all.
The most important natural plant hormones, the auxins, also differ
from typical animal ones in being relatively nonspecific and involved in
a great variety of growth processes rather than in particular ones. Huxley
( 1935 ) discussed the relationship of these various substances, in animals
and plants, and suggested a classification and terminology for them.
Evidently there are many compounds and processes involved, and for
plants, at least, it seems preferable to use for all such morphogenetically
active materials the relatively noncommittal term growth substances. This
will be employed in the present discussion to refer to those substances
of whatever sort or activity that, in low concentration, are involved in
the control of growth, development, and differentiation. It should be
recognized that some of these substances are effective in retarding these
processes rather than in their stimulation.

The history of the work on growth substances has been reviewed by a
number of authors (Leopold, 1955, Chap. 1; Went, 1951a; and Audus,
1953). Most of it dates from about the beginning of the second quarter
of the present century and was largely confined, at the start, to workers
in continental Europe. Among early students of the subject were Boysen-

376 M or pho genetic Factors

Jensen, Cholodny, Dolk, Fitting, Kogl, Laibach, Paal, and Went. The
modern understanding of auxin was established by an important paper
by the last-named botanist in 1928.

Growth substances have been shown to be present in many species
and throughout the plant kingdom, in algae, mosses, ferns, and a great
variety of seed plants. They have relatively less effect on the growth of
fungi.

TYPES OF GROWTH SUBSTANCES

There are many growth substances but the best known and those ap-
parently of the greatest general importance are the ones that occur
naturally in plants and are usually termed the auxins. These were identi-
fied first in the oat coleoptile but are now known to be present in almost
all plants and to be concerned in a great variety of developmental
processes. There has been a good deal of discussion as to how many
auxins there are, but one of them, identified by Kogl and his colleagues
(1933) as 3-indoleacetic acid, seems to be of primary importance, and
all known auxins are related to it chemically. In the present discussion the
term "auxin" will be generally limited to this and chemically similar
compounds.

Our knowledge of indoleacetic acid (IAA) is now very substantial
but there are a considerable number of other naturally occurring growth
substances, or substances which have been thought by many to exist in
plants, which are unrelated to this chemically but are important in various
ways. About these we know much less. Here belong the wound hormones
( traumatins ) ; the various flower-forming substances (florigens); the so-
called root-forming, stem-forming, and leaf -forming substances or calines;
the gibberellins; the hormones concerned with the determination of sex;
various substances that amplify or antagonize the effects of auxin; and
others. About the chemical nature of most of these little is known, and
the very existence of some of them is in doubt. The conception of "organ-
forming substances," in the narrow sense, is far from being established
and has been involved in the general discussion of determination. It is
clear, however, that there are a great many compounds, some of them
very specific in their influence, which in minute amounts have important
effects on one or another of almost all phases of plant development. An
understanding of their nature and mode of action is proving of much
importance for the solution of morphogenetic problems.

It should again be emphasized that most growth substances in plants
are much less specific in their effects than are the hormones of animals.
Thus IAA is concerned in cell expansion, cell division, cambial activity,

Growth Substances

377

abscission, parthenocarpy, tumor formation, root production, dominance
relationships among buds, nastic responses, and tropisms generally. The
effect in each case must evidently be a function of the specificity of the
responding system, including other biologically active compounds, rather
than of a particular evocating substance.

The developmental effects of growth substances are chiefly of three
sorts: on growth in general (defined as permanent increase in volume),
on the correlations of growth, and on development and differentiation of
specific structures. These may involve very different problems.

GROWTH SUBSTANCES AND PLANT GROWTH

Growth of the plant as a whole may be controlled by various growth
substances. Van Overbeek (1935) showed that in genetically dwarf races

12 3 4

STAGE OF DEVELOPMENT

I 2 3

STAGE OF DEVELOPMENT

Fig. 18-1. Yield of diffusible auxin from long shoots (left) and short shoots (right)
at successive stages in development in Ginkgo. ( From Gunckel and Thirnann. )

of maize there was much less auxin than in plants of normal height, indi-
cating that auxin was associated with growth in stem length. The
dwarfing gene here effects a more rapid destruction of auxin rather than a
lesser production of it. Von Abrams (1953) sprayed IAA on etiolated
plants of dwarf and tall varieties of peas. The dwarf increased 30 per
cent in height but the tall one was slightly reduced, an instance of the
frequently observed fact that the effect of auxin is different with different
material. In a number of other cases the dwarfing of plants has been
shown to be related to a deficiency of auxin.

Auxin particularly affects growth in length, especially of the stem, and
in many cases has been found to be the factor that determines length
growth of the internodes. Gunckel and Thirnann (1949) compared the

378 Morpho genetic Factors

amount of auxin in developing short shoots and long shoots of Ginkgo and
found that elongation of the latter was associated with a sharp rise in
auxin content (Fig. 18-1).

Auxin is also involved in the growth of fruits (Fig. 18-2), though not
all the steps in the process are yet well understood (Murneek, 1954;
Lund, 1956). There are reviews by Nitsch (1952) and Luckwill (1957).
An increase in auxin content often occurs at pollination, again at fertiliza-

Fig. 18-2. Centers of origin of auxin in the development of a fruit. 1, from mother
plant; 2, from pollen; 3, from developing ovules. (From Nitsch.)

tion, and usually during endosperm growth and the development of the
seeds. This increase of auxin in the ovary is often followed by its increase
in the pedicel and adjacent regions.

That fruit development is stimulated by growth substances is made
clear by the occurrence of parthenocarpy, or growth of fruits without
fertilization and seed development (Fig. 18-3). Gustafson (1936) in-
duced parthenocarpy in cucurbits by applying synthetic growth sub-
stances to the pistil, and this has now been done frequently with other

Growth Substances 379

plants. He also showed that fruits which are naturally parthenocarpic
have a much higher concentration of auxin than do seed-bearing ones.
In some cases parthenocarpy does not require application of a growth
substance to the unfertilized ovary but simply the presence in the air of
the greenhouse of vapor of a specific substance. Induction of partheno-
carpy is by no means universally possible and has been found more
frequently in members of the Solanaceae and Cucurbitaceae than in
other families. The subject has been reviewed by Vazart (1955).

Fig. 18-3. Parthenocarpy. Left, normally pollinated tomato fruit with many seeds.
Right, parthenocarpic fruit produced by treatment with synthetic growth substance.
( Courtesy Boyce Thompson Institute. )

Davidson (1950) found that several marine algae were stimulated in
their growth by synthetic substances in the sea water (Fig. 18-4). Al-
though auxin seems rarely to be concerned with the growth of fungi,
Fraser (1953) reports that indoleacetic acid stimulates growth in the
common mushroom.

Cell Enlargement. The primary effect of auxin on plant growth seems
to be its promotion of increase in cell size, especially in the stem and
in its longitudinal dimension. In phototropism the side of the axis away
from the light grows faster than the lighted one, and Went ( 1928 ) and
others showed that auxin is more abundant on this shaded side. Avery

380 M or pho genetic Factors

and Burkholder (p. 30) found that the more rapid elongation here was
the result of increase in cell length rather than in cell number.

Most tropisms have now been shown to be due to greater growth on the
convex side because of longer cells there (Fig. 18-5). In both photo-
tropism and geotropism, however, the role of auxin is different in root and
shoot. If a young plant, for example, is placed in a horizontal position,
auxin can be shown to accumulate on the lower side, though how this
occurs is not well understood. In the stem, this results in a bending
upward of the axis. The young primary root, however, will bend down-

THALLUS

HOLDFAST

NO. HOLDFASTS

CONCEN TRATION

Fig. 18-4. Effect of different concentrations of indoleacetic acid on the growth of
Fucus, as measured by length of thallus and length and number of holdfasts, in com-
parison with untreated controls. ( From Davidson. )

ward, the cells elongating faster on its upper side. Evidently the same
concentration which stimulates cell elongation in the stem checks it in
the root, another example of the difference in the effect of auxin under
different conditions. Geiger-Huber and Huber (1945) found that by
continually decapitating a root its auxin content was markedly reduced
and that it now bent upward instead of downward.

How much of the difference in cell size among the various tissues of
the plant is due to auxin it is hard to say but, directly or indirectly, this
substance is probably involved in most of the differences in degree of

Growth Substances

381

cell enlargement that occur between the meristematic condition and ma-
turity. Gibberellin acts in a similar manner.

Cell Division. Growth substances are also associated often with cell
division and with meristematic activity generally. Buds, especially as they
begin to expand, are rich in auxin. Cambial activity is closely related to
the presence of auxin (Snow, 1935; Fig. 18-6; Soding, 1936), and the
progressive awakening of the cambium in the spring from the stem tips
downward is accompanied by a progressive increase in auxin concen-
tration (Avery, Burkholder, and Creighton, 1937b; Fig. 18-7; Gouwentak
and Maas, 1940).

Fig. 18-5. Cell size in geotropic curva-
ture. Lengthwise section through the con-
vex side (upper) and the concave one
(lower) of a root of Zea bending down
geotropically. Bending is produced by
the greater elongation of the cells on the
upper side resulting from a relatively
weak concentration of auxin there. ( After
MacDougal. )

Various synthetic growth substances have been found to stimulate
cell division even in tissues which are mature or nearly so. Such a sub-
stance, applied to a young stem, will often produce there a callus-like
mass of cells, so that it is easy to see why growth substances are associated
with the formation of galls and tumors. This ability to produce cell
division in older tissues has often been used for the determination of
chromosome numbers in their cells, since it is now possible to observe
mitotic figures there.

The various wound hormones produce their effect by increasing the
division of cells below wound surfaces.

382

Morphogenetic Factors

Cells which
normally '
form fibres

Phloem

Primary ,
xylem

Secondary
xylem

Primary
xylem

Fig. 18-6. Stimulation of cambial activity by auxin. Above, two bundles from control
plant, decapitated but no auxin applied. Below, a similar region from a plant in which
auxin had been applied to the decapitated tip. Cambial growth is markedly stimu-
lated by the auxin. ( From Snow. )

Growth Substances

383

*ft

I

I

7.8

5.4

9.2
10.0

7.3
6.8

8.2

2.7
78

6.2

4.0
3.5

0.0

0.0

Fig. 18-7. Concentration gradient of growth hormone (in terms of Avena curvature)
at various levels in a twig of Aesculus on May 16, when the growth of the current
year ( above arrow ) was just completed. ( From Avery, Burkholder, and Creighton. )

GROWTH SUBSTANCES AND CORRELATION

Of much significance for morphogenesis is the role of growth sub-
stances in the correlation of growth (Thimann, 1954/?). Here is involved
the whole problem of organized development. These substances seem to
be the agents by which many such correlations are achieved, but one
should hesitate to call them "growth regulators" since the actual regula-
tion must go further back, to the mechanism that controls their distribu-
tion and local concentration and binds the parts and processes into an
organism.

Differential Movement. An important fact about auxin is that in living

384 Morphogenetic Factors

cells it does not move in all directions but has a definitely polar flow,
going from the more apical regions of the plant downward ( p. 141 ) . This
was first observed in the oat coleoptile, where auxin is formed at the tip
and then passes basipetally, regardless of how the axis is oriented. If a
portion of the coleoptile is cut off and inverted and auxin is then applied
to the end now uppermost, it will not move downward, though auxin
placed at the other end will move up, in the original polar direction.
Such polar transport is also shown in the stem axis, in which auxin
moves down through the phloem. Inverted stems, after some time and
apparently after the development of some new vascular tissues, may gain
the ability to transport auxin in the opposite direction from the original
one (Went, 1941).

Auxin transport may not invariably be polar, for Jacobs (1954) has
reported that, if relatively weak concentrations are used instead of the
strong ones commonly employed in experiments, there is a good deal of
upward translocation. In a young internode of Coleus he found that
about one-third as much auxin moved upward as downward. He also ob-
served that in young bean hypocotyls, although auxin transport was al-
ways basipetal, the ability to transport it at all was lacking in very young
seedlings but increased as they grew older. It was greatest in the upper
portion of the hypocotyl and decreased toward the base. Oserkowsky
( 1942 ) concluded that where auxin moves only basipetally it is carried
in living cells but that transport in both directions may result from
diffusion through dead cells or cell walls. Leopold and Guernsey (1953fl)
showed that in Coleus the flow was clearly basipetal in the shoot and
in the opposite direction in the root ( Fig. 18-8 ) and that flowering stems
transport auxin in both directions. Haupt (1956), however, reports that
polar transport of auxin is as clear in the floral structures he studied as it
is in vegetative shoots. Niedergang-Kamien and Skoog ( 1956 ) were able
to reduce or inhibit polar flow by triiodobenzoic acid (Fig. 18-9) and
suggest that the reported effect of this substance on growth correlations
is due to this fact.

Nevertheless, polar transport of auxin seems to be a general phenome-
non and is obviously of much morphogenetic importance since it under-
lies the marked structural differentiation between the two ends of the
plant axis. It is probably involved in the polar character of regeneration
(p. 119) and in many other developmental events.

Auxin flow may show a transverse as well as a longitudinal polarity,
notably in geotropic movements. The accumulation of auxin in the
lower half of a horizontally placed axis, although doubtless a response to
the stimulus of gravity, is not simply a downward diffusion but is made
possible by differential and unidirectional changes in the permeability
of the cells. Such transverse polarities have been emphasized by de

Growth Substances

385

Haan (1936), who reexamined the fact earlier noted by Noll that when
primary roots are bent, lateral roots grow chiefly from their convex sides
(Fig. 18-10). He observed that in such cases the root primordia, push-
ing out through the cortex, bend toward what is at that point the convex
side of the root (Fig. 18-11), and he interprets this as the result of a
transverse polar gradient in a root-forming hormone. Such transverse
reactions of plants are extensively discussed by Borgstrom (1939), who
shows their importance in many structural and physiological characters
of plants.

TIP

0 0 2 0.4 06 08 1.0
CONC TIBA IN MG./L

Fig. 18-8. Relative amount of basipetal Fig. 18-9. Effect of 2,3,5-triiodobenzoic
transport of auxin in various regions of acid on polar transport of auxin. Graph
the vegetative and of the flowering axis showing reduction in amount of auxin

of Coleus ( From Leopold and Guernsey. )

transported basipetally in sunflower epi-
cotyl cylinders which had been pre-
treated for 2/2 hours with various concen-
trations of TIBA. (From Niedergang-
Kamien and Skoog. )

No satisfactory explanation of polar auxin transport is available (p. 361).
The suggestion of Went (1932) that electrophoretic diffusion might ac-
count for it has been shown by Clark ( 1938 ) to be doubtful, since the
polar transport of auxin can be abolished by the application of sodium
glycocholate without producing any change in the electrical polarity.
Schrank, however, in a series of papers ( 1957 and others ) presents evi-
dence that electrical polarity is the essential basis for the polar transport
of auxin. The question of auxin transport is part of the more general one
as to why many substances move about the plant in certain directions
more than in others. Auxin is doubtless important in the development of
growth patterns, and an understanding of the mechanism of its differen-
tial movement would clear up many morphogenetic problems.

386 Morphogenetic Factors

Dominance, Inhibition, and Stimulation. Whatever the mechanism for
the differential distribution of growth substances may be, there is no ques-
tion that it has much to do with the effect of one part on another and
thus with growth correlation in general (Chap. 4).

Meristematic regions are commonly centers of auxin production, and
from them this substance moves to others where it may either stimulate
or inhibit growth. The most familiar example of this is the so-called
dominance of apical buds. It is well known that in most cases, if such a

Fig. 18-10. Curved primary root of a lu-
pine seedling, showing lateral roots grow-
ing from convex sides only. (After Noll.)

Fig. 18-11. Cross section of a curved root
like that in Fig. 18-10, showing that the
lateral root, in its course through the
cortex, bends toward the convex side, X.
(After Noll.)

bud is present, the buds below it will not grow but that they will do so
if the apical bud is removed. Thimann and Skoog (1934) showed that if
this apical bud is cut off and paste containing indoleacetic acid placed
on the stump the lower buds will not develop, though in the controls,
with paste alone, they do so. Such a result has been confirmed many
times and has led to the widely held view that auxin inhibits growth of
the lower buds and thus produces the dominance of the apical one.

Snow, in a series of papers (1937, 1940, and others), calls attention to
some facts that are not easily explained on this hypothesis. He finds that

Growth Substances 387

buds farthest from the apex are most inhibited, which does not seem
logical if auxin from the terminal bud is the inhibitor. Furthermore,
inhibition may sometimes pass upward, although auxin typically passes
downward. Snow believes that auxin is either changed into an inhibiting
substance (for which Libbert, 1955, has evidence) or stimulates the pro-
duction of one and that the greater the distance from the apex, the
greater the amount of the inhibitor. Such a substance is not polar in
movement and can thus pass into lateral buds as auxin presumably can-
not.

Champagnat ( 1955 and others ) has studied especially the effects upon
bud growth of the cotyledons or leaves that subtend them and comes to
the conclusion that both inhibitory and stimulatory substances are in-
volved.

Thimann (1954£>) is inclined to think that auxin itself is the major
inhibiting influence and that the various apparent objections to this
hypothesis may be met by assuming that auxin may sometimes move in
an apolar direction and that its effects may be different under different
circumstances. He does not rule out the possibility of the existence of
other and specifically inhibiting substances.

Meanwhile other workers have emphasized the importance of nu-
trition in apical dominance. Van Overbeek (1938) observed that after
removal of the terminal bud the auxin content of the stem decreases. He
believes that in some way auxin blocks the passage of nutrients to the
lateral buds, which have only a poor vascular connection with the main
cylinder. When the amount of auxin is reduced a better connection is
established, nutrients enter the buds, and thev begin to develop.

The nutrient theory of apical dominance is strongly supported by
Gregory and Veale (1957). They suggest that the degree of dominance
is proportional to the supply of available carbohydrate and nitrogen and
that competition among the various buds explains the difference in relative
bud growth. Auxin is concerned in this competition since a high auxin
content prevents the formation of the vascular connections between bud
and vascular cvlinder.

The underlying mechanism in such an apparently simple phenomenon
as bud dominance is still by no means clear. The general fact of domi-
nance is established, however, and helps toward an understanding of
some of the differences among plants in their bodily patterns, for what-
ever determines bud growth determines the shape of the plant. There are
usually a great number of potential growing points on an axis but most
of them do not develop into shoots, apparentlv because of inhibitory'
action mediated in one way or another by growth substances. Plants differ
in the degree of this inhibition. For example, in Aster novaeangliae there
is one main stem with only a few floral branches at the top. Aster

388 Morpho genetic Factors

multiflorus, on the other hand, is much branched and bushy. Delisle
( 1937 ) found that in the former species the concentration of auxin at the
tip was high (Fig. 18-12). In the latter it was much lower, suggesting
that the copious branching resulted from weak inhibition. After re-
moval of the apex in the young plant, A. novaeangliae became much
branched, and application of auxin to the tip of A. multiflorus resulted
in the growth of a main stem with relatively small branches. Thus an
important taxonomic character is related to the amount of auxin present
in the plant.

Many of the effects of growth substance in correlation are stimulatory
rather than inhibitory. There is a close relation, for example, between the
presence of growing seeds and the development of a fruit, the seeds pro-
ducing the auxin necessary for fruit growth. In some cases, as has been

20

5 15

8

»

20

30 40 SO

LENGTH Or TIP IN MM

60

SO

Fig. 18-12. Effect of auxin on inhibition of branching in Aster. Auxin concentrations
at successive distances from apex in A. novaeangliae, an unbranched species. The
amount of auxin in A. multiflorus, which is more branched., is considerably less. ( From
Delisle. )

mentioned, synthetic growth substances may be substituted for the
natural auxin and seedless fruits produced. Growth of the receptacle
may also be related to seed production. When Nitsch (1950) removed
the growing achenes from a strawberry, the fleshy portion stopped grow-
ing, but if synthetic growth substance replaced the achenes, the normal
development of the strawberry was resumed (Figs. 18-13, 18-14). If
only some of the achenes were removed, the weight of the mature ripe
fruit was proportional to the number of achenes remaining. Nitsch found
that the achenes contained a large amount of auxin but that this was
absent from the receptacle.

Galston ( 1948 ) has described an example of competitive correlation
in asparagus. Root primordia, stimulated by auxin, are formed during

Growth Substances

389

a period of minimum stem growth, but once they are laid down, stem
growth again accelerates. Compensatory correlations (p. 98) of various
sorts also have their basis in auxin action. Removal of the root tip almost
always stimulates growth of lateral roots below it, somewhat as in

Fig. 18-13. Relation of presence of achenes to growth of strawberry. All achenes
have been removed early in development except three vertical rows ( left ) or three
horizontal ones (right). Growth of the receptacle is limited to the region in contact
with the achenes. ( From Nitsch. )

Mar., 1950]

30

25

20

15

10

DIAME TER
IN MM.

I
2

O o- — o o o

le

is

18

21

25

DAYS AFTER POLLINATION
Fig. 18-14. Auxin and growth of the straw-
berry. Curve 1, control. Curve 2, growth of
fruit from which all achenes were removed
and auxin in lanolin paste substituted. Curve
3, like 2 but without the auxin. (From
Nitsch. )

Fig. 18-15. Effect of 2,4-D on
leaf shape. Below, leaf of un-
treated plant of Pisum sativum.
Above, plant treated with 2,4-D
paste. ( From Wenck. )

390 Morpho genetic Factors

apical-bud dominance. Active growth of lateral roots may also inhibit
apical growth (Street and Roberts, 1952).

Correlations of position may be the result of auxin activity in many
cases. Thus where an upright terminal shoot of a coniferous tree is re-
moved, one of the lateral branches will swing up from its nearly horizontal
position to a vertical one and replace the lost leader, evidently in re-
sponse to the absence of auxin previously produced by the apical bud. In
woody plants the orientation of branches with reference to the main
axis and to gravity also seems to be due to auxin action since it is regu-
lated by the production of reaction wood ( p. 356 ) , which seems to result
from the presence of auxin. The precise amount of auxin (and thus of
reaction wood formed) determines the angle that a given branch
will assume and thus the branching pattern and form of the whole tree.

The form of individual organs, ultimately the result of dimensional
correlations, may be affected by growth substances, particularly in leaves
(von Denffer, 1951; Linser and others, 1955; Wenck, 1952; Fig. 18-15).

Such correlating activities are doubtless present in the lower plants as
well. Moner (1954) describes the action of a substance, as yet unidenti-
fied, which is concerned with the development of the precisely formed
colonies of the alga Pediastrum.

Much evidence is therefore available that the correlated and integrated
character of the plant, whatever its final cause may be, is the immediate
result of specific amounts of growth substances at specific places and
times. What controls this precise production and distribution of these
substances is a more difficult problem.

GROWTH SUBSTANCES AND THE DETERMINATION

OF STRUCTURE

The effect of growth substances on the specific form and structure of
plants has attracted more attention than any other of their morpho-
genetic activities.

Tropisms and other auxin-mediated orientations of plant parts to cer-
tain factors in the environment, notably gravity and light, account for
many features of external form, though the familiar patterns of plant
growth are produced by interaction between these tropisms and certain
specific inner factors. Sometimes a simple tropism may produce such
a profound change in plant form as to be significant morphogenetically.
In "lazy" maize (van Overbeek, 1936), for example, the stalk grows
flat on the ground, not through mechanical weakness but because of the
characteristic distribution of auxin in it. Tropisms are primarily the
concern of physiology, however, and there is no room here to consider
the extensive literature in which they are discussed.

Growth Substances 391

The arrangement of structures in a radially symmetrical pattern doubt-
less involves differential distribution of auxin, but little is known
about this. When such radially symmetrical structures are placed in a
horizontal position they often tend to become dorsiventral, as in certain
flowers and stems. Since most such direct effects of gravity seem to be
produced by differential distribution of auxin, as in the well-known
cases of geotropism, auxin presumably is involved in structural dorsi-
ventrality as well. Its role here in young liverwort plants has been
described by Kohlenbach ( 1957 ) .

Of wider morphogenetic interest are the effects of growth substances
on the determination of specific structures. From his study of flower
production Sachs (1882) suggested that organ-forming substances are
operative in plants, especially in the determination of flowers and roots.
The growth of knowledge of morphogenetically effective substances
revived interest in this hypothesis, and it has stimulated a wide range of
experiments which have thrown much light on the mechanisms of de-
velopment. Organ-forming substances of many types have been postu-
lated in the formation of roots, stems, leaves, flowers, galls, sexual struc-
tures, and others. Just how such substances produce their effects is not
known, and the actual existence of some of them is not yet proved, but
the theoretical, and also the practical, importance of these problems is
great. The most obvious way to account for development is to postulate
the operation of a series of such substances. The difficulties of this con-
ception, however, are obvious, for a very large number of them would be
necessary. The tendency today is to assume the activity of a relatively
small number and to explain the variety and specificity of their effects
through their interactions and in other ways.

Root Formation. Van der Lek (1925) observed that a piece of stem
(used as a cutting), on which there was a bud or young leaf, formed
roots at its base, whereas a naked stem piece did so much less readily or
not at all. This suggested that there was a substance, formed in buds
and leaves, that moved downward and stimulated root production. Went
( 1929 ) demonstrated this by showing that an extract from the leaves of
Acalypha, applied to the apex of a cutting, promoted root formation at
its base. Several workers soon discovered that auxin and various natural
and synthetic substances also have this effect and that cuttings could
be made to root by the application of such substances.

In 1935 Laibach and Fischnich described a technique by which indole-
acetic acid in lanolin paste applied to a stem would promote root for-
mation. In the same year Zimmerman and Wilcoxon ( 1935 ) reported
that several synthetic substances such as indolebutyric, indolepropionic,
phenylacetic, and naphthaleneacetic acids had this effect and could
be used in horticultural practice to hasten the rooting of cuttings when

392 M or pho genetic Factors

this was otherwise slow or difficult. The root-forming activity of
2,4-dichlorophyenoxyacetic acid, 2,4-D (Zimmerman and Hitchcock, 1942),
was especially conspicuous. By their application in paste or other means
under favorable conditions root initials may be produced almost any-
where on the plant. These substances are not equally active, and some of
them which have less value in root formation show other morphogenetic
effects. "Root-forming hormones" are now familiar aids in plant propa-
gation (Fig. 18-16). These substances are chiefly effective in the produc-
tion of root primordia and in most cases they actually check the later
growth of the roots. Because of their great theoretical and practical in-
terest, much work has been done on the root-forming effects of growth

Fig. 18-16. Effect of "root hormones" on cuttings of holly. At left, controls. At right,
plants treated with mixture of indolebutyric and naphthaleneacetic acid. (Courtesy
Boyce Thompson Institute. )

substances. There are a number of general reviews of this work, among
them Pearse, 1939; Thimann and Behnke, 1947; and Avery and Johnson,
1947.

The movement of synthetic substances, like that of natural auxin, is
polar except when their concentration is high. If applied at the apical
end of a cutting, they tend to pass downward and to stimulate root for-
mation at the base. If applied basally, they form roots there. The experi-
ments of Czaja and others have previously been described (p. 124) in
which regeneration in pieces of root is also polar in character, shoot buds
forming on the upper end and root primordia on the lower. This is evi-
dently owing to the accumulation of auxin at the lower (distal) end and
its consequent relatively low concentration at the upper one, a low con-
centration being related to shoot growth and a higher one to root growth

Growth Substances

393

(Fig. 18-17). When slices were repeatedly trimmed off from the lower
surface, shoot primordia began to appear there, presumably because of
the removal of auxin and the consequent reduction in its concentration.
When concentrations of growth substances are much higher than in
natural conditions, they tend to have a local effect and to produce a
downward bending of the leaves (hyponasty ) and the formation of callus.
Upon the latter, root primordia often appear. Growth substances ap-
plied to the soil may be absorbed, carried up in the transpiration stream,
and affect the structure of the growing plant.

.INCREASE
AUXIN

UNTREATED

DECREASE
AUXIN

INTACT
ROOT

ROOT
SEGMENTS

AFTER
REGENERATION

Fig. 18-17. Auxin and regeneration. In a root segment of Taraxacum, placed hori-
zontally (2), regeneration is normally polar, shoots developing at the proximal end
and roots at the distal one (see Fig. 6-4). When the amount of auxin is increased at
the proximal end, roots are produced there ( 1 ) . When it is decreased at the distal
end, shoots develop there ( 3 ) . ( From Warmke and Warmke. )

It is recognized that growth substances are not the only factors con-
cerned in root formation. A supply of sugar is necessary. Indeed, the
stimulating effect of leaves on root formation may be due in part to their
production of nutrients. In grafting experiments between rooting and
nonrooting varieties of Hibiscus, van Overbeek and Gregory (1945)
found that something formed in the leaves, in combination with auxin,
is required for root growth, and van Overbeek, Gordon, and Gregory
(1946) showed that this is not a hormone since it can be replaced by
sucrose or nitrogenous substances. The importance of a high carbohy-
drate-nitrogen ratio in root determination has already been discussed

394 Morpho genetic Factors

(p. 367). Torrey (1950) observed that pea root tips transferred directly
to a culture medium provided with IAA produce lateral roots at once
but that tips transferred after growing a week in culture do not do so for
some time. A substance (not auxin) stimulating lateral root formation
seems to originate in the lower part of the root and moves upward,
producing laterals in acropetal succession.

It has been observed that the rooting response is often altered (gen-
erally increased ) when two different substances, such as indoleacetic acid
and naphthaleneacetic acid, are combined. Went (1939) applied dif-
ferent substances successively rather than in mixtures and found that
cuttings of etiolated pea seedlings, which do not root after treatment
with auxin alone, will do so if phenylacetic acid is first used, though
this substance by itself is ineffective. He believes root formation results
from the interaction of two factors and suggests that phenylacetic acid
may act to mobilize or activate a specific root-forming factor, rhizocaline
(Bouillenne and Went, 1933; Bouillenne, 1950; Libbert, 1956). The
question of the existence of such a specific factor has been studied by a
number of workers. Evidence for it is largely indirect, and rhizocaline
has not been isolated; but auxin is evidently not the only factor operative
in the initiating of root primordia.

It must not be concluded that growth substances can produce roots
anywhere on the plant. They are often formed, to be sure, in unusual
places, as along the surface of the stem. Even in such instances, how-
ever, the initiation of root primordia does not take place anywhere and
indiscriminately but only in certain cells or at certain zones that are
potentially capable of forming them. At such points roots may be formed
under the stimulus of other factors such as ethylene, carbon monoxide,
wounding, or abnormal nutrition. The nature and location of such re-
gions are variable and depend on the general growth pattern of the plant
treated. There is a difference, for example, between monocotyledons and
dicotyledons as to rooting response. Treatment with growth substances
is one of the methods by which knowledge may be gained as to the
potentialities of various cells and tissues, not only for root formation but
for other developmental activities.

Auxin and Rhizoids. Auxin is present in the coenocytic alga Bryopsis
and is most abundant in that part of the plant where rhizoids are com-
monest. Jacobs (1951) finds that an application of indoleacetic acid
stimulates rhizoid formation in the region where these are least abundant.
He regards this as analogous to the effect of auxin on root initiation in
higher plants.

Leaf Formation. Attempts have been made to find substances which
might be involved specifically in the development and growth of the
leaf blade. In some cases leaf growth is dependent on the presence of a

Growth Substances

395

factor coming from the cotyledons. Pilet (1952) observed that Semper-
vivum leaves parasitized by Endophyllum sempervdvi contain much
more auxin than normal ones and, presumably for this reason, are accel-
erated in their development. The effectiveness of adenine in leaf formation
has been observed by various workers (D. Bonner and Haagen-Smit,
1939). Auxin does not seem to promote the growth of the blade as a whole,

V

Fig. 18-18. Section through leaf blades
of Kalanchoe Blossfeldiana. At left, from
a plant grown under long days. At right,
from one grown under short days. The
difference in thickness is entirely due to
cell size. ( From Harder and von Witsch. )

however, although when embryonic leaves are treated with it, various
changes may be produced (Laibach and Fischnich, 1936; Zimmerman,
1951k; Applegate and Hamner, 1957). These are probably to be looked
upon as injuries rather than formative effects. Wenck (1952) has studied
the stimulatory and inhibitory effects of auxin and of various auxin
antagonists on leaf growth in a number of species.

396 Morpho genetic Factors

Went ( 1938 ) here postulated a phyllocaline, analogous to rhizocaline.
Later ( 1951/?) he extended his concept of the calines more fully into the
details of leaf form and structure. He calls attention to the importance of
adenine for mesophyll growth and shows that vein tissue, on the other
hand, can be increased by auxin without affecting mesophyll develop-
ment. There are thus two morphogenetic tendencies in leaf development:
one toward the formation of veins and induced by auxin and the other
of mesophyll, induced by adenine. Whatever factor induces the former
( as well as the stem and petiole ) may be called a caulocaline and the lat-
ter a phyllocaline, whatever their chemical nature may turn out to be.
Leaf shape is affected by the balance between the two. Leaves with a
dominance of phyllocaline will tend to be palmate for they will have an
excess of mesophyll, whereas those with more caulocaline will tend to be
pinnate or parallel-veined, since they will have relatively more vein
tissue. One may question, however, whether the problem of organic form
can be solved quite as simply as this.

Harder ( 1948 ) observed that in certain succulents, such as Kalanchoe
Blossfeldiarui, variations in leaf shape and structure depend on the day-
length. Plants grown under short days have short, apetiolate, and markedly
succulent leaves (Fig. 18-18). A single leaf subjected to short days will
transmit this "short-day shape" to the immature leaves above it which are
developing under a long day-length. This effect Harder and von Witsch
(1940b) attribute to a growth substance they call metapkisin, which is
not identical with either auxin or florigen.

Stem Formation. It has proved difficult to demonstrate any substances
specifically related to the growth of the stem. Went (1938) decapitated
pea seedlings and measured the length of the secondary lateral branches.
He gives evidence that stem growth here depended on the roots, not on
the cotyledons, and suggests that it was due to caulocaline in conjunction
with auxin. In later experiments neither auxin from the apex nor water
supply from the root appeared to control stem growth, and Went again
attributed this to caulocaline coming from the stem base and the root
system.

Flower Formation. The existence of flower-forming substances has a
firmer foundation. They were postulated by Sachs, who held them re-
sponsible for changing a plant from a vegetative to a reproductive state.
The demonstration that such a change could be induced by altering the
carbohydrate-nitrogen ratio (p. 366) and by photoperiodism (p. 315) cast
doubt upon this idea. More recent work, however, has come to its support.
Kuijper and Wiersum (1936), for example, found that if a soybean plant
is brought to a flowering state by exposure to short day-lengths and
another kept flowerless by long days a shoot of the former grafted into the
latter causes the flowerless plant to form flowers abundantly. Hamner

Growth Substances 397

and Bonner (1938) reported that this effect could be produced in
Xanthium through a barrier of lens paper without actual union of tissues.
Withrow and Withrow ( 1943), however, failed to confirm this and showed
that where transmission of the flowering stimulus had occurred there
had been a slight fusion between cells which had grown through the lens
paper. Nevertheless, in grafting experiments like these, a substance evi-
dently passes from scion to stock across the graft union and induces
flowering. To such a substance the name florigen has been applied.

Other experiments in photoperiodism also suggest the operation of such
a flower-forming substance. Cajlachjan (1938), by localizing the recep-
tion of the photoperiodic stimulus, showed that this was received by the
leaves but was effective in flower induction at growing points considerably
distant and had therefore apparently passed, as a specific substance, down
the petiole, along the stem, and into a lateral branch. Borthwick, Parker,
and Heinze (1941) with soybeans found similar results. Harder (1948)
observed that in Kalanchoe this substance passes directly down the stem
from the site of induction but does not cross it, so that one side of the
plant flowers but the opposite one does not.

Unlike auxin, the movement of which is usually polar, the flower-
inducing agent seems able to travel in any direction in the plant. Since
local applications of cold, heat, or narcotics reduce or inhibit the trans-
port of such substances from centers of production to those of action,
it seems probable that living tissue is involved, a conclusion supported
by girdling experiments of Galston ( 1949 ) and others, who showed that
the floral stimulus cannot pass across a water gap.

From the leaf of a unifoliate species of Streptocarpus that was ready to
flower, Oehlkers (1955) made a series of cuttings. Those from the base
of the leaf produced flowers at once, those from a little farther up pro-
duced them soon, and cuttings from near the tip formed only vegetative
shoots. Oehlkers believes this was because of the differential distribution
of a flower-forming substance.

Genie differences may also be involved. One variety of Hyoscyamus
niger (henbane) is biennial and does not flower until its second year.
Another variety is annual. If from the annual form a flowering scion, or
leaf from one, is grafted into a plant of the biennial race during its first
year, the latter will flower in this season (p. 264). It was also shown that
the substance here concerned was not limited in action to this species for
a flowering scion of tobacco or petunia (genera in the same family) has
the same effect on biennial Hyoscyamus.

This nonspecificity of the flowering stimulus is also evident in certain
host-parasite relationships. Orobanche minor (one of the broomrapes),
when parasitizing clover, flowers only when the host plant flowers ( Holds-
worth and Nutman, 1947). Cuscuta Gronovii (dodder) flowers only

398 Morpho genetic Factors

in a long day if it is parasitic on the long-day plant Calendula, but in a
short day if it is parasitic on the short-day plant Cosmos (von Denffer,

1948).

These various lines of evidence, about which a great body of facts has
now been gathered, suggest that there are one or more specifically flower-
forming substances. None of these florigens has yet been isolated nor is
there any knowledge as to their chemical nature. Some substance that
under certain conditions stimulates flowering is certainly able to pass
across a graft union and thus seems hormonal in character. This sub-
stance is evidently closely involved with photoperiodism, though what it
does depends to a great extent on the amount of auxin or other growth
substances present. Thus J. Bonner and Thurlow (1949) completely pre-
vented flowering in the short-day plant Xanthium canadense, grown
under short days, by spraying it with auxin, and leaves thus treated did
not transmit the flowering stimulus by grafting. Substances that antago-
nize auxin action, such as triiodobenzoic acid, increased flowering in soy-
beans (Galston, 1947). De Zeeuw and Leopold (1956) report that low
auxin concentrations applied to two short-day species promoted floral
initiation if applied before the induction period but are less effective
afterward. In a Xanthium plant defoliated to a single leaf, Salisbury
( 1955 ) found that auxin inhibited flowering if applied before the flower-
ing stimulus (produced by photoperiodic induction) had been com-
pletely translocated from the leaf but promoted it if applied afterward.
Leopold and Guernsey ( 19535 ) , using the position of the first flower in
peas as a measure of flower initiation, observed that a number of sub-
stances, notably sucrose, malic acid, and arginine, tended to inhibit flower-
ing but that this inhibition was removed by auxin. Although flowering
is usually an "all or none" reaction, structures intermediate between
flowers and vegetative shoots sometimes occur. Such phyllody has been
produced through manipulation of the flowering stimulus by Harder and
his colleagues (1947). Gibberellin is often effective in flower induction
(Lang, 1957).

The pineapple (Clark and Kerns, 1942) produces flowers abundantly
if naphthaleneacetic acid or certain other growth substances are applied
by spray to the center of the plant. Van Overbeek (1946«) has shown
that plants thus treated will flower under long days, which ordinarily
inhibit flowering in pineapple. In the sweet potato, also, Howell and
Wittwer ( 1955 ) reported that flowering can be induced experimentally by
a growth substance.

The problem of the relation of growth substances to flowering is evi-
dently a complex one. It is the basis of a considerable literature, much
of which can be found in Melchers and Lang (1948), Lang (1952), Bon-
ner and Liverman ( 1953), and Liverman ( 1955).

Something analogous to the control of flowering by specific substances

Growth Substances

399

is even to be found in the algae, for von Denffer and Hustede (1955)
were able to shift the sexual phase of Vaucheria sessilis to the vegetative
one by treatment with indoleacetic acid (Fig. 18-19).

Sex Determination. Both in the determination of the sex of individual
plants and in the development of the sex organs, growth substances of
various sorts seem to be effective.

In the dioecious species Cannabis sativa (hemp) it is possible to dis-
tinguish genetically male from genetically female plants before they
flower. Heslop-Harrison (1956) grew plants under controlled photo-
periodic conditions and during the period of differentiation of flower
buds applied naphthaleneacetic acid to leaves at the third and fourth
nodes. In genetically male plants, female flowers were produced, sug-

-10 -11 .
m m 0

JES 9/anJ

Fig. 18-19. Effect of different concentra- Fig. 18-20. Young prothallia of Pteridium
tions of IAA on the proliferation of an- aquilinum 11 days after spore germina-
theridial primordia in Vaucheria. (From tion. A, grown on agar to which a water
von Denffer and Hustede. ) extract of prothallia was added. B, grown

on ordinary agar. The extract stimulates
early development of antheridia. (From
Dbpp. )

gesting that sexuality is determined by the concentration of native auxin
during the period of primordium differentiation and that femaleness is
associated with a relatively high auxin level. In Mercurialis ambigua
he found ( 1957) that carbon monoxide much reduced the number of male
flowers in genetically monoecious types, presumably by its effect on
auxin. Laibach and Kribben (1951) painted the lower surfaces of the
leaves of cucumber, a monoecious plant, with naphthaleneacetic acid
in lanolin and caused an increase in the proportion of female flowers,
sometimes altogether suppressing the differentiation of males. Indole-
acetic acid they found to be less effective and 2,4-D more so. Extending
his work to other plants, Laibach concludes (1953) that, in general,
female flowers or female parts of flowers tend to differentiate under

400 Morphogenetic Factors

higher concentrations of growth substances than do male flowers or
parts.

It has been suggested that hormones comparable to those of the animal
body may influence sex in higher plants. Love and Love ( 1946) found that
in Melandrium dioicum sex expression is influenced by various animal
sex hormones applied in lanolin to the axils of leaves in which flower
buds are to develop. Crystalline estrone, estradiol, and estradiol ben-
zoate shifted the sex of the flowers toward femaleness, whereas testos-
terone and its propionate promoted maleness. In general, hormones
promoting maleness or femaleness in animals have the same tendency
in Melandrium. Some doubt has been cast on these conclusions by Kuhn
(1941), who studied dioecious species of Cannabis and Mercurialis.
There is no evidence that substances identical with animal sex hor-
mones are formed by plants. If sex in dioecious plants is determined by
specific substances, these have not been isolated nor can they be passed
from one plant to another of opposite sex by grafting (Yampolsky,
1957).

Maleness in ferns seems to be related to specific substances. Dopp
(1950) made a water extract of the prothallia of the bracken fern which
stimulated the production of antheridia in sporelings 4 to 8 weeks
earlier than in untreated prothallia (Fig. 18-20). This can be carried in
agar media. Naf (1956) confirmed this and was further able to induce
antheridium formation on a variety of other related ferns even though
these did not normally produce them in culture. The extract from
prothallia of types of ferns that form antheridia under the conditions of
culture used was several thousand times more effective than were extracts
from types that do not form antheridia under these conditions. Such ex-
periments suggest that in the prothallia of all polypodiaceous ferns there
is a substance that stimulates the formation of male sex organs.

Sex hormones have also been found in all the thallophytes except the
red algae and the basidiomycetes. Burgeff (1924) reported that in non-
aquatic types such as Mucor mucedo, the hyphae of two different sexes
("plus" and "minus" races) influence each other by means of diffusible
substances. Kohler (1935) confirmed these results, and Plempel (1957)
has reported the activity of four substances in sexual interactions in this
species. Kohler found that in Phy corny ces Blakesleeanus two diffusible
substances are produced by each sex. Krafczyk ( 1931 ) showed that in
Pilobolus crystallinus at least three different processes are chemically
controlled: the characteristic swelling and branching of the hyphae, the
growth of hyphae toward each other, and the delimitation of the game-
tangia. Machlis ( 1958 ) has found in the water mold Allomyces a hor-
mone, sirenin, excreted during female gametogenesis that attracts the
male gametes to the female ones.

Growth Substances

401

Similar processes have been more fully studied in the water mold
Achlya by J. Raper (1939-1957), especially in A. bisexualis and A. ambi-
sexualis (Fig. 18-21). Experiments involving the transfer of mycelia
into water where plants of the opposite sex had been growing, and the
use of cellophane membranes, gave evidence that in the very regular
sequence of the sexual process four diffusible substances are concerned.

A1 Augments
'tf Inhibits — -

Production of

Antheridial Hyphae

<r-

— A Initiate
Mutually Aug.
— ^Initiates

A- Complex

AttractioW^^TVv

Anth. HypriafF^

Delimitation \.\\
of Antheridia ^

Production of
pi Initials

Delimitation of
Oogonia

ifferentiation of
heres

>

Maturation of
Oospores

Fig. 18-21. Sex hormones in Achlya. Specific activities of substances A, B, C, and D
in the development and function of the sex organs. ( From J. Raper. )

402 Morpho genetic Factors

In the male mycelium antheridial branches are first induced by hormone
A, produced by the female mycelium. The antheridial branches then
form hormone B, which induces the production of oogonial initials in
the female plant. These structures now form hormone C, which causes
the antheridial branches to grow chemotropically toward the oogo-
nial initials. Lastly, it appears that hormone D, presumably formed
in the antheridia, causes the oogonial initials to delimit the oogonia
from their stalks. The chemical nature of these substances is still un-
known.

The most complex examples of the effects of specific substances in
sexual reproduction and sex determination in the lower plants are those
described by Moewus ( 1940 and many other papers ) in the unicellular
green alga Chlamydomonas eugametos, in which the biochemical and
the genetic basis of the various hormonal mechanisms were subjected to
detailed analysis. A thorough reexamination of this work indicates that
many of the facts and conclusions of Moewus are not well founded and
that the contributions of the Chlamydomonas work to our understand-
ing of sexuality in the lower plants are much less considerable than
they were once thought to be.

Work on the sexual processes and substances in thallophytes has been
reviewed by J. Raper (1952, 1957). Hawker (1957) has reviewed the
whole field of reproduction in the fungi.

Wound Hormones. The substances first proved to have a determining
effect on morphogenetic processes were the wound hormones, or necro-
hormones. It has long been observed that in the vicinity of dying and
necrotic cells there occur divisions in other cells which under ordinary
conditions would not have shown such division. These have a definite
relation, both in distribution and orientation, to the accumulation of de-
composition products released by the injured cells. Wound meristems are
thus developed which produce layers of cork that cut off the injured
region and protect the healthy tissue underneath.

Haberlandt (1921, 1922) was the first to attack this problem directly.
He found that if the cut surface of a potato tuber is washed and the
contents of the injured cells thus removed only a few cell divisions
occur. It might be thought that in such cases the reduced access of
oxygen to the flooded tissues would account for the reduction in
metabolic activity and thus of cell division. The action of a definite
substance, however, is strongly indicated by later experiments of
Haberlandt and others in which the juice, debris, or extracts of tissues
produced an effect on cell division much exceeding that from mere
wounding (Fig. 18-22). When sap from crushed tissue was injected into
small intercellular spaces, active cell division, presumably from wound
hormones, was found to occur (Reiche, 1924). These substances are not

Growth Substances

403

species-specific, for those from one species will produce this effect in quite
unrelated ones.

Much work has been done in isolating wound hormones and deter-
mining their chemical nature. Standard material for estimating relative
effects of hormone activity was first sought. Wehnelt (1927) used the
layer of parenchyma cells which lines the immature pod of the common
snap bean. Such tissue responds sensitively to various types of stimula-
tion by abundant cell division and the formation of intumescences, the
size of which provides a rough measure of the intensity of the stimulus.
This "bean test" has been used by many students of wound hormones
(Jost, 1935; Umrath and Soltys, 1936). On such pod surfaces Bonner
and English (1938) placed droplets of extract from crushed tissue

Fig. 18-22. Effect of wound hormones.
Section of internode of Kalanchoe below a
wound, showing how cortex cells have been
induced to divide frequently, and parallel
to the wound surface. ( From Sinnott and
Block. )

(chiefly bean pods) and found that the height of the intumescence
which developed after 48 hours was proportional to the concentration
of the wound hormone present in the extract. These proliferations are
usually higher than the ones induced by other chemical or physical means.

Considerable progress has been made toward a knowledge of the
chemical nature of these wound hormones. Bonner and English isolated
from bean-pod juice a substance which in low concentration was very
active in the bean test and named it traumatin. English, Bonner, and
Haagen-Smit later (1939) purified from the same source a crystalline
dibasic acid similar in its effects. Traumatin appears to be active on only
a few types of cells, such as those of the potato tuber and the bean pod.

To understand wound reactions in any plant, organ, or tissue, account
must be taken of many internal and external factors as yet imperfectly
known (Bloch, 1941). Workers have often been puzzled by differences

404 M or pho genetic Factors

between cells in their response to wounding or wound hormones. Such
cells evidently differ in character and reactivity. Thus the root pericycle
and the vascular cambium respond to injuries by the production of
wound tissue much more readily than do adjacent cells of the ground
parenchyma. Auxin may be one factor which produces such specific
reactivity. In Populus balsamifera, Brown (1937) found that the cam-
bium was stimulated to active growth both by wound hormones released
from dead cells and by a substance, presumably auxin, coming from buds
and leaves distal to the wound. Application of auxin above the wound
considerably increases a local wound reaction (Brown and Cormack,
1937). Other observations confirm this (Bloch, 1941).

GROWTH SUBSTANCES AND INTERNAL DIFFERENTIATION

Numerous instances have been reported where specific changes in in-
ternal structure are related to the action of auxin or one of the synthetic
growth substances.

In the regeneration of buds on the decapitated hypocotyl of flax (p.
245), Link and Eggers (19466) found that this was largely prevented if
indoleacetic acid in lanolin was applied to the cut surface. Even the
transverse division of epidermal cells, the first visible step in bud pri-
mordium differentiation, was usually inhibited.

Nysterakis and Quintin (1955) report that application of 2,4-D to
growing stems of Araucaria excelsa reduced the length of the tracheids
by more than half and changed the pitting from circular to scalariform.

Jacobs (1956) finds that the regeneration of severed xylem strands
and the distribution of auxin proceed together, and from this and other
evidence he concludes that auxin is usually the limiting factor in the
differentiation of xylem. The chief distinction of xylem cells is their
thick secondary wall. The facts that auxin is effective only in plants-
organisms with cellulose walls-and that the only plant group where
auxin seems to have little effect on growth is the fungi, which have
chitinous rather than cellulose walls, both suggest that auxin acts on the
cell wall.

Native auxin and synthetic growth substances have been shown to be
effective in preventing the abscission of leaves and fruits. If a leaf
blade is removed but the petiole left, this will soon drop off by abscission.
If one of several growth substances is placed on the cut petiole stump,
however, abscission will not take place. Presumably when the leaf is in-
tact auxin is continually moving down the petiole and inhibits the
differentiation of an abscission layer at the base. The use of sprays of
various growth substances to prevent the fall of leaves or fruits under
certain conditions is now a common horticultural practice. What the

Growth Substances 405

mechanism is by which the abscission layer is produced or inhibited is
not known.

Sprays of this sort are also used to stimulate rather than inhibit
abscission, notably for the purpose of thinning young fruits when too
many have been set. How, one may ask, does the same substance act
in two such different ways? Evidently a normal growing and functioning
organ will produce enough auxin to prevent its abscission. When this
production ceases, the organ will drop off unless a fresh supply is avail-
able through external application. Anything which checks or deranges
normal growth, however, will tend to check auxin production and thus
lead to abscission. Sprays of some substances and in certain concentra-
tions will tend to do this, and hence their usefulness in the thinning of
fruit. An answer to the problem of this double effect has been proposed
by Jacobs ( 1955 ) , who has shown that in addition to the inhibiting
effect of auxin on abscission there may be a speeding effect produced
by auxin formed in young nearby leaves. This stimulates the abscission
of a petiole whenever the flow of auxin from its leaf blade is reduced.
Abscission is thus controlled by an "auxin-auxin balance."

The differentiation of more specialized tissues may be stimulated by
auxin. Camus (1949) grafted buds of Cichorium to pieces of storage
tissue and found that vascular strands began to differentiate just below
the bud and continued to develop until they established connection with
the vascular tissue beneath. Buds encased in cellophane and inserted
into tissues cultivated in vitro produced the same effect, indicating that
a diffusible substance, possibly auxin, was involved (Fig. 18-23).

Of significance here is the work of Wetmore ( 1956 ) on the induction
of xylem in callus tissues. Into homogeneous callus maintained in culture
from parenchyma cells in the cambial region of lilac, a growing lilac
stem apex was grafted by inserting it into a V-shaped cut. After tissue
union was effected, strands of xylem began to differentiate into the
homogeneous callus tissue below the graft. That auxin was the factor
responsible for this is suggested by the fact that when the cut was filled
with agar containing auxin but without a stem tip vascular tissue ap-
peared below it in the same way, the distribution of the strands depend-
ing on the concentration of the auxin. It is significant that only xylem
tissue was thus differentiated and not phloem. This was also the case
in the regeneration of severed vascular strands in the stem of coleus
(p. 242). It may be that the factors which stimulate xylem develop-
ment are different from the ones involved in phloem production.

More profound effects of growth substances on the anatomy of plants
have been described. Much of the work here has been done by Kraus and
his colleagues at the University of Chicago, who have tried a variety of
substances in different concentrations and on many plants. Their gen-

406 Morpho genetic Factors

eral conclusions are that most of the changes produced are in the ab-
normal distribution and proportions of tissues rather than in the produc-
tion of new structures. Important factors in these changes are nutrition
and the age and state of the tissues when treated. Marked differences
in reaction to various substances were found, and morphogenetic
processes may thus in part be manipulated. A review of this work has
been made by Beal ( 1951 ) .

Fig. 18-23. At left, effect of a bud grafted to the phloem region of a piece of chicory
root in culture. The bud stimulates the development of vascular tissue below it, pre-
sumably because of a growth substance it produces. At right, a similar experiment
except that a sheet of cellophane, CL, has been placed between the bud and the tissue
below. The same effect is produced, indicating that organic continuity is not neces-
sary. B, bud; P, phloem; V, vascular parenchyma; C, cambium; A, histologically
altered tissue; L, line of contact between bud and stock. (From Gautheret, after
Camus. )

OTHER FORMATIVE EFFECTS

Various other substances of morphogenetic significance have been
postulated, but little is known about them. Thus in Dictyostelium, the
remarkable life cycle of which has been described earlier (p. 223), the
factor controlling the aggregation of the myxamoebae into a pseudoplas-
modium appears to be chemical in nature and diffusible (J. T. Bonner,
1949). To this substance Bonner has given the name acrasin.

In a few traits, such as time of fruit ripening in dates ( Swingle, 1928 )
and staple length in cotton (Harrison, 1931), pollen seems to have a

Growth Substances 407

direct effect not only on the embryo but on the tissues of the ovary
itself, tending to make these somewhat resemble ones of the paternal
parent. This metaxenia must evidently be due to gene-produced chemi-
cal factors introduced through the pollen tube and modifying the de-
velopment of such maternal tissues as the pericarp and the seed coat.

The development of galls with specific external and internal struc-
tures (p. 285) produced by fungi or insects seems to be dependent on
various chemical substances. In insect galls these may be injected into
the plant by the insect but more probably they result from secretions
from the growing larva.

In other galls, particularly the one most actively studied— crown
gall— auxin is clearly involved (p. 294). Experiments with tissue cultures
have shown that cells of normal tissue in many cases are unable to
grow unless supplied with auxin. Cells of bacteria-free crown-gall tissue,
however, can do so. This fact suggests that the change from normal to
tumor tissue may result from the acquirement by tumor cells of the
ability to synthesize auxin. It is probable, however, that the problem is
more complex and that changes in the ability to form other growth
substances are also involved. Thus Braun and Naf ( 1954 ) have extracted
from crown gall a biologically active substance which is not auxin but
which, in association with auxin, produces active proliferation of to-
bacco-pith tissue in culture. Neither this nor auxin alone has a growth-
stimulating effect of this sort. The question of the relation of auxin to
crown-gall formation has been actively investigated. The subject has been
reviewed by Braun and Stonier (1958).

Growth substances are also involved in the production of other gall-
like structures. Swellings and malformations somewhat resembling typical
root nodules associated with nitrogen-fixing bacteria have been induced
by application of synthetic growth substance on the roots of several types
of leguminous plants (Allen, Allen, and Newman, 1953).

A number of other growth substances deserve mention here. Adenine,
for example, has been found to possess significant properties, especially
for leaf growth, and the balance between it and auxin seems to determine
the character of development in some cases (p. 414, and Skoog and
Tsui, 1951).

The synthetic growth substances are too numerous to be discussed
here. Of particular note is 2,4-dichlorophenoxyacetic acid (2,4-D), im-
portant because of its wide use as a herbicide. It produces such profound
growth abnormalities that death usually ensues (Kaufmann, 1955; Fig.
18-24). For some unknown reason it has relatively little effect on
monocotyledonous plants. Work with it has been reviewed by Wood-
ford, Holly, and McCready (1958).

Maleic hydrazide is important in that it inhibits growth in a wide

408 Morphogenetic Factors

variety of plants without causing obvious morphological abnormalities.
Plants treated with it tend to lose dominance in their apical buds and
show certain other effects (Naylor and Davis, 1950). It seems to inhibit

Fig. 18-24. Median longitudinal section of young adventitious root apices in rice. Left,
of untreated plant. Right, of plant treated with 2,4-D. There is a great increase of
periclinal divisions in the latter, which produces massive, abnormal roots. (From
Kaufman. )

mitosis (Greulach and Atchison, 1953) and also checks the formation of
flower primordia in both long-day and short-day plants (Klein and
Leopold, 1953; Fig. 18-25).

£3

O CL
Ul

u. Q-

°<

oc o
uj or
m o

15

10

o o

\

0 .1 I 4 10 40100 MG/L.

CONC. OF MALEIC HYDRAZIDE

Fig. 18-25. The effect of maleic hydrazide on the total number of flower primordia at
the first five nodes of soybeans. ( From Klein and Leopold. )

Substances such as triiodobenzoic acid and coumarin under some
conditions increase the effect of auxin and under others markedly inhibit
growth. A number of substances occur that inhibit or antagonize auxin
action (J. Bonner, 1949) and have been termed antiauxins (Fig. 18-26).

Growth Substances

409

Some gases have been found to exert strong formative effects on
plants and thus deserve to be included among the growth substances,
although chemically they are very different from the rest. In studying
the effects of illuminating gas and its constituents on greenhouse plants,
workers at the Boyce Thompson Institute found that in tomato plants
exposed under bell jars to atmospheres containing 1 per cent of carbon
monoxide the stems became covered after a few days with an abundant
growth of roots. Other gases produced similar effects. Carbon monoxide
was found to induce rooting in many other plants (Zimmerman, Crocker,
and Hitchcock, 1933 ) . These results led to the investigation of the effects
of ethylene, acetylene, and propylene (Zimmerman and Hitchcock,
1933). All were found to induce rooting and root-hair formation, leaf

0.01

100.0

0.1 1.0 10.0

IAA CONCENTRATION: MG./L.
Fig. 18-26. Growth of Avena coleoptile (upper curve) induced by various concentra-
tions of indoleacetic acid. The degree of inhibition of this growth by an auxin an-
tagonist ( 4-chlorophenoxyisobutyric acid) at concentrations of 1, 10, and 50 mg. /liter
is shown in the three successively lower curves. ( From Foster, McRae, and Bonner. )

epinasty, proliferation of callus-like masses of tissue, and abscission of
leaves, flowers, and fruits. These gases, however, do not stimulate growth
in the absence of auxin. The relation of ethylene to auxin has been
discussed by Michener (1938).

In Puerto Rico Rodriguez (1932) discovered that ethylene induces
flowering in the pineapple, and in Hawaii it was found soon afterward
that acetylene will accomplish the same result (Lewcock, 1937). The
effect of these gases on pineapple is much like that of the synthetic
growth substances which induce flowering (p. 398).

In addition to the growth substances which have here been discussed-
auxin, various other naturally occurring substances, and the synthetic
compounds— another is now being actively studied and is assuming an
important place in morphogenetic problems. This is gibberellin.

410 Morpho genetic Factors

In a disease of rice produced by the fungus Gibberella fujikuroi, it
was observed some years ago that many of the infected plants grew
taller than uninfected ones (Kurosawa, 1926). Young and uninfected
rice plants treated with culture filtrates of this fungus grew unusually
tall. A similar increase in growth was observed when this filtrate was ap-
plied to some other plants, both monocotyledons and dicotyledons. Sev-
eral different but related substances were purified from Gibberella and
are now commonly termed the gibberellins. Their nomenclature is still
somewhat confused but they may be named gibberellin Als A2, and A:i,
the last being the best known and often called gibberellic acid.

Gibberellin commonly produces a very marked increase in stem
elongation ( Fig. 18-27 ) . This is particularly conspicuous in certain dwarf

600

500

400"

Sprayed with 20 ppm.
Gibberel lie Acid

E
«
10

«

>
4

300-

200

weeks after spraying
Fig. 18-27. Relation between concentration of gibberellic acid and plant height in
bean plants. ( From Gray. )

plants, notably peas. Brian and Hemming (1955) induced a fivefold
increase in height in such plants, bringing them up to the size of tall
races, by applying a little of this substance to one of the leaves. It had
no effect on plants of the tall races. The length but not the number of
internodes was increased. The so-called "slender" mutants of peas,
which are tall but spindly, showed no effects of gibberellin treatment.
Phinney ( 1956 ) found that gibberellin caused some dwarf mutants in
maize to grow as tall as the normal plants from which they had been
derived but some other dwarf races showed little response. Tall plants
were unaffected. The relation of gibberellin to dwarfing is evidently a
complex one. Most of the elongating effect is caused by increase in cell
length rather than in cell number. There are a few cases, however, where
cell division as well as cell elongation has been stimulated.

Growth Substances 411

Leaf growth is affected by gibberellin and is often, though not always,
increased. Radish leaves floated on a gibberellin solution in the dark
grew larger than the controls. It is perhaps significant that kinetin has
much the same effect and that when both substances are applied the
increase in growth is equal to the sum of their separate effects.

Although gibberellin and auxin are similar in some respects, notably
in stimulating cell elongation, they differ chemically and in other im-
portant ways. Gibberellin fails to produce typical epinasty nor does
it induce callus formation, both of which usually result from auxin ac-
tion. It also fails to show the polar transport within the plant so character-
istic of auxin. It does not inhibit the growth of lateral buds but tends
instead to stimulate their development. It does not check leaf abscission.
It inhibits rather than promotes root initiation but does not inhibit root
growth.

Gibberellin evidently has some relation in its effects on development
to those produced by light, though this relation is not clear. Lang ( 1957 )
found that it induced biennial Hyoscyamus to flower the first season, re-
gardless of day-length. The usual inhibition of growth produced by red
light is removed by treatment with gibberellin. The effects of this sub-
stance much resemble etiolation but are independent of light. This
is unlike the effect of auxin.

In its influence on dwarf plants, which seems to be its diagnostic
feature, gibberellin perhaps substitutes for some essential factor that is
normally present and which may have been lost by mutation. No effects
of gibberellin have as yet been found in any of the lower forms. Sub-
stances essentially like it have now been extracted from several higher
plants (Radley, 1958), and it is probably widely spread in the plant king-
dom.

The literature in this field has been reviewed by Stowe and Yamaki
(1957). Further study of gibberellin should yield important information
on the factors governing plant development.

MECHANISM OF ACTION

Relatively little is known chemically about most of the growth sub-
stances. Some of them, like the calines, are little more than inferences.
The existence of others, such as florigen, can be proved by experiment,
though they have not been isolated. Others can be isolated, at least
partially, but their chemical nature is not well known. As to auxin,
gibberellin, and traumatic acid, fairly complete chemical information is
now available.

Many attempts have been made to find some common features of
chemical structure among these substances which have formative effects

412 Morphogenetic Factors

and thus to gain a clue as to how these effects are produced. These sub-
stances vary considerably. Having studied many such compounds,
Koepfli, Thimann, and Went (1938) concluded that the minimal struc-
tural requirement for a substance to stimulate growth, at least in the
pea test for auxin, is to possess an unsaturated ring system with a side
chain adjacent to a double bond in the ring, and with a carboxyl group
in the chain separated from the ring by a carbon atom. Thimann (1957)
points out that there are a considerable number of biologically active
compounds which do not have this structure and at least one that does
not even contain a ring. It seems doubtful that an understanding of
the mechanism of action, either of auxin or similar synthetic substances,
will be gained by a knowledge of their chemical structure without an
equal knowledge of the reacting systems that they stimulate. The general
question of the chemistry and mode of action of plant growth substances
was discussed at the Wye College symposium (Wain and Wightman,
1956).

Just how growth substances produce their morphogenetic effects is
not well understood. The first visible result of auxin action is a speeding
up of protoplasmic streaming, indicating that some aspect of metabolism
is being accelerated. The marked influence of auxin on growth also sug-
gests this, since growth requires the release of energy. Some physiologists
believe that auxin acts as a respiratory coenzyme and thus has an im-
portant share in the respiratory cycle. No enzyme has yet been found,
however, that can be activated by auxin in physiological concentrations.

Since what appears to be the primary effect of auxin is cell enlarge-
ment, it seems plausible to conclude that water uptake is controlled by
it, and there is some evidence for this. The suggestion has been made
that auxin increases the osmotic concentration of the cell sap and thus
increases cell size. Cell growth may take place, however, even with a
decreasing osmotic concentration. Burstrom (p. 41) believes that cell
enlargement is not primarily caused by water uptake.

Interest at first focused on auxin-induced changes in the cell wall as
related to growth, and Heyn (1940) has reviewed the evidence that
auxin directly increases the plasticity of the wall and thus its irre-
versible extensibility. Some workers believed that the effect of auxin
was indirect and only through its influence on the cytoplasm. Recent
studies, however, support Heyn's view. Thus Cleland and Bonner ( 1956 )
present evidence that auxin directly induces a loosening of the cell-wall
structure and thus a relaxing of wall pressure, which makes possible an
expansion of the cell. The effect of auxin is independent of cell expan-
sion. Auxin may affect the wall by altering pectin metabolism.

The relation of growth to protoplasmic viscosity and to the swelling
capacity of cell colloids suggests that auxin may have something to do

Growth Substances 413

with these qualities. Northen (1942) observed that auxin usually de-
creases viscosity of protoplasm. He regards protoplasm as a "reversibly
dissociable-associable system," in which auxin (and other agents)
cause dissociation of cellular proteins and increased swelling pressure. As
the result of such action, it is thought that components of the fine struc-
ture of the cell may undergo reorientation and the reactivity of the
cell may be changed.

Of greater morphogenetic interest is the direct relation of growth sub-
stances to the development of organs or structures. The situation here
is even less clear than in the control of growth. In a number of cases one
is faced with a curious antithesis between the action of auxin in dif-
ferent situations. For example, at a given concentration it stimulates the
growth of stem tissue but inhibits that of the primary root, with the
result that differential geotropic bending occurs. It stimulates the de-
velopment of root primordia and hence is useful in the rooting of cut-
tings, but it checks the elongation of the roots after their emergence. In
some cases its effect is to accelerate flowering and in others to inhibit it.
Sometimes it prevents bud growth and sometimes it stimulates this. In
certain cases its effect is to stimulate the growth of roots rather than buds
but in other cases it has just the opposite influence.

In this confusing situation the hypothesis of specific organ-forming sub-
stances appeals to many, especially those who seek direct and primarily
chemical solutions to morphogenetic problems. To be sure, development
often does seem to be the result of the action of such substances, as in the
formation of roots, flowers, and abscission layers. But where, one may
ask, does this specificity end? In the flower, are there separate substances
for sepals, petals, stamens, and ovaries, for anther and filament, style and
stigma? Does each tissue and each type of cell have its appropriate
"caline"? It is easy to reduce to absurdity the more naive statements of
this hypothesis.

To what, then, can one attribute the highly specific results of plant
development? One answer is that the specificity lies in the protoplasmic
system rather than in the growth substance and that the latter serves
primarily as a trigger or evocator that calls out a specific response. We
should remember that auxin, the substance about which most is known,
is markedly nonspecific. A few such biologically active substances,
stimulating responses from a highly organized protoplasmic system,
might account for development. A dime, it has been said, will open
a turnstile, activate a dial telephone, or bring a tune from a juke box, but
the dime, like a molecule of auxin, is identical in every case. The dif-
ference lies in the complexities of the responding mechanism. The answer
to morphogenetic problems is more difficult to come by on this conception
than on that of specific formative substances since it involves an under-

414 Morpho genetic Factors

standing of the whole protoplasmic system. This is a far goal, but, as
Thimann (1957) has remarked, "It begins to look as though the whole
cell were necessary to auxin activity."

But part of the living system in a plant evidently includes other
biologically active substances. A good deal is known about several of these,
and although they may not be "organ-forming" in the earlier sense of the
word, their share in the control of developmental processes is more
important than that of most other chemical compounds. A hopeful
method of attack on morphogenetic problems is to study the relationship
between these substances. It is now well known that there are com-
pounds which enhance or which inhibit the effects of auxin. Still more
promising are results such as those of Skoog and Miller ( 1957 ) on the
relationships between auxin and adenine (or its derivative, kinetin). The
presence of both seems to be necessary for vigorous growth, at least of
tobacco callus in culture. If the proportions of the two are changed, how-
ever, the character of the growth is different. Relatively high levels of
auxin and low ones of kinetin, either in cultures of tobacco callus or in
cuttings, will tend to produce good root growth but little bud develop-
ment, whereas high kinetin and low auxin levels favor growth of buds
instead of roots. To be sure, kinetin is a substance which has not yet
been found in the living plant, and its balance with auxin has been
demonstrated in only a few cases, but the picture this balance pre-
sents of the possible control of differentiation through alteration in pro-
portions within a relatively simple chemical situation opens up encourag-
ing possibilities.

Other factors are doubtless concerned in these cases, and the problem
must involve more than a simple two-compound interaction, but the
idea that there may be a relatively small number of active but non-
specific substances, with the possibilities for complex interactions among
them that this offers, makes understandable how an essentially infinite
number of different structures might be produced without the necessity
of postulating the activity of substances specific for each of them. Only
12 different kinds of chessmen can produce, by their various relation-
ships, an almost limitless number of combinations on the board.

The study of plant growth substances has been of great significance
and stimulation for morphogenesis, but it has done little more as yet than
pose a series of deeper problems. Chief among these are three:

1. What is it that controls the distribution of growth substances as to
space, time, and concentration?

2. What is it that determines the specific response which a given cell
or tissue makes to them?

3. How do they interact in their control of development?

These problems are part of the deeper one of biological organization.

CHAPTER 19

Genetic Factors

The factors discussed thus far are effective chiefly through the environ-
ment of the plant, either its external surroundings or its inner physiologi-
cal processes, which are open to relatively simple analysis. It is obvious,
however, that these factors alone are not enough to explain all mor-
phogenetic phenomena. There are also inborn differences, rooted in the
specific constitution of each individual organism, which powerfully affect
what it is and does. These differences are inherited, and it has been the
great service of genetics to biology since the turn of the century to show
that their physical basis is primarily in the genes, located in the chromo-
somes of the nucleus.

GENES

The various environmental factors exert their effects against this
specific genetic background, the entire system of genes in the plant.
Genes are sometimes thought of as though these bodies, known to be
independent in inheritance to a certain degree, were also independent
in development. This evidently is not true, however, for in their control
of growth and differentiation the action of all the genes must be closely
coordinated, in space and time, if an organism is to be produced. How
these distinct entities are thus so precisely correlated in their action is a
major problem for both genetics and morphogenesis. It is also clear that
a gene does not produce its effect by determining a precise series of steps
leading to the development of a specific trait, for the same genotype
may have a very different effect if the environment is different. A gene
simply determines a specific response to a specific environment. The
genetic constitution that distinguishes a tall plant from a short one, for
example, will not produce this difference unless the conditions of tem-
perature, moisture, and soil fertility are such as to make vigorous growth
possible.

The problem of gene action, of how a gene or group of genes produces
its effects, is now one of the central concerns of genetics and is being

415

416 Morphogenetic Factors

actively investigated. The role of genes in the synthesis of enzymes and
other substances and thus in the determination of successive steps in
metabolic processes is yielding much information as to the relations
between genetics and physiology. Increasing knowledge of those re-
markable compounds, the nucleic acids, is leading to an understanding
of the chemistry of the gene and of the manner in which it reproduces
itself. Indeed, desoxyribonucleic acid ( DNA ) has such significant proper-
ties that some biologists hopefully believe that it will finally produce an-
swers for most of the basic problems of their science. All this, however,
has as yet thrown little light on how it is that genetic factors affect the size,
shape, and structure of plants and their parts. This is a much more diffi-
cult problem than working out the biochemical steps in the synthesis of an
organic compound produced in plant metabolism. How a single pair of
genes can determine, for example, whether a tomato plant will have the
familiar deeply lobed leaves or the unlobed "potato-leaf" type is very
difficult to see. Here something more than a series of chemical steps seems
to be concerned. Growth relationships are being controlled, and at present
we must admit that very little is known about how such control is exer-
cised. A solution of this problem must start with a knowledge of what
actually happens in the inheritance of form and structure. To make such
a descriptive analysis and at the same time seek hopefully for clues that
will lead to a knowledge of the mechanisms involved is the chief task at
present of the student of morphogenesis who is interested in the genetic
aspects of his science.

Genes and Growth. The underlying problem in growth is the increase
of living substance, due ultimately to the reduplication of genes. How this
is accomplished and how the DNA molecule divides into two new ones
like itself are now beginning to be understood. Traits of size, either of body
or organ, are markedly affected by environmental factors, but there is also
a genetic basis for most of them. Since the pioneer work of East and
Nilsson-Ehle it has been recognized that most quantitative traits depend
not on single genes but on a series of multiple factors or polygenes, cumu-
lative in their effect and in most cases without dominance. Such traits are
difficult to analyze genetically since it is rare that the effect of individual
genes can be followed, though there are statistical methods for determin-
ing the number of genes by which two individuals differ for a given trait.
That polygenes are operative in quantitative inheritance is indicated by
the fact that the variability of the F2 is markedly higher than that of the
parents or the Fi, as would happen if segregation were taking place.
There is now a substantial body of evidence that confirms the multiple-
factor hypothesis.

In a few cases the inheritance of size is not so complex, and the effect
of individual genes can be traced. One of these, vine height in peas, was

Genetic Factors

417

found by Mendel himself and is due to a single pair of genes, tall being
dominant over short and segregating clearly in the F2. De Haan (1927,
1930) has shown that in addition to this gene there are two (perhaps
four) others that tend to inhibit growth. In this case a group of several
genes, all modifying the same trait, can be recognized and their indi-
vidual effects distinguished. In a considerable number of other cases it
can be shown that two, three, four, or more pairs of genes are concerned
in the inheritance of a size trait. Thus Quinby and Karper (1954) have
evidence that in cultivated sorghum varieties, ranging from 2 to 15
ft. in height, four pairs of genes are operative.

Genes of this sort are cumulative in their effect. Sinnott (1937), Pow-
ers (1939), Charles and Smith (1939), and others have shown that
this additive effect is geometric rather than arithmetic, each gene

Fig. 19-1. Geometric action of genes determining size. A, graph of fruit weight of an
Fa population of cucurbit fruits consisting of 244 individuals plotted in arithmetically
equal classes. B, the same population plotted in classes equal logarithmically. The
first population is skewed, the second nearly symmetrical. ( From Sinnott. )

contributing not a certain definite amount of height or weight but a
certain percentage increase of the effect of the rest. This is shown by
the fact that the Fx is closer to the geometric average of the parents than
to their arithmetic average and is thus somewhat nearer to the smaller
parent in size. Furthermore, if a segregating F2 is plotted in classes that
are arithmetically equal, it skews toward the upper side, whereas if the
scale is a logarithmic one, the F2 population is symmetrically distributed
around the geometric mean (Fig. 19-1).

A developmental study of inherited size differences shows that some
are attained by differences in rate of growth and some in its duration. The
size differences between plants showing hybrid vigor and their parent
inbreds are related to a more rapid rate of growth, and some other size
differences also have their basis in genetically controlled growth rates. In
other cases the difference in size is due to longer duration of growth.

418 Morpho genetic Factors

Large pumpkins differ from small gourds, for example, simply because
they grow for a longer time (Sinnott, 1945b, and p. 16). The actual
growth rate of these two varieties in terms of compound-interest growth is

the same.

Inherited size differences are also related to cellular characters (p. 34 ) .
Most of them are due to differences in number rather than size of
cells, large size being the result of more cell divisions during develop-
ment. Less frequently the period of cell expansion is more extensive in
the larger forms and their cells are consequently larger, though usually
not in proportion to body size.

In the many cases where there are inherited differences in cell size,
it is usually not the size of the meristematic cells that is different but the
amount of increase that occurs after division ceases. Thus the fruits of
large races of pumpkins have much larger cells than do small gourds,
but this difference is not evident at the meristem. Some of it appears in
the growth of the young ovary but most of it during the enlargement of
the ovary in fruit development (Sinnott, 1939). Sugar beets have much
larger cells (and leaves) than do table beets, but only in their mature
structures. The meristematic cells are much the same size in both.

Many cases have been found in which there is not a gradation be-
tween large and small types but the small ones are so markedly dif-
ferent as to be regarded as somewhat abnormal dwarfs. In most such
plants there is a single gene difference from normal which seems to
control one important growth factor. A number of these occur in maize,
and the auxin relations of some have been worked out (p. 377). Some
dwarfs are small-celled but a few have cells larger than those of normal
plants. There are also a number of gigas forms which are due to gene
differences. Large and small types are also frequently related to chromo-
some number (p. 438).

Differences in height may result from mutations that alter a determi-
nate type of growth to indeterminate. These have been found, for ex-
ample, in tobacco (Jones, 1921) and maize (Singleton, 1946). Each
shows single-gene segregation with normal determinate plants. The dif-
ference between bush and climbing varieties of beans, also due to a
single gene, is really a difference between determinate and indeterminate
growth.

Another important effect of genes on size is to be seen in cases of
hybrid vigor or heterosis. The Fi plants, in crosses between parents that
are homozygous or essentially so, are often much larger and more vigor-
ous than either parent (Fig. 17-1), and this fact has wide economic ap-
plication, especially in maize. The difference is closely associated with
heterozygosity and disappears with inbreeding. Various suggestions have
been made to account for it— the stimulating effect of the heterozygous

Genetic Factors 419

condition, the dominance of linked genes, increased embryo size, and
others— but no satisfactory explanation has yet been reached. Gene ac-
tion in heterosis has been discussed by Jones (1957), and there is a
wide literature in this field (Sprague, 1953).

Genes and Form. The chief morphogenetic significance of genetic fac-
tors, however, is in their relation to the development of organic form. Here
it is not the total amount but the distribution of growth that is impor-
tant. Genes must in some way control relative growth— the amount of
growth in one dimension as compared with that in each of the others
so that specific shapes are produced. Many instances could be cited
where the shape of leaf or flower or fruit is certainly inherited and where
differences in it segregate and can be analyzed in mendelian terms, at
least to some degree. Only a few can be mentioned here.

Leaf shape in cotton has had particular attention. In one of the earliest
analyses of shape inheritance, Leake (1911) found that in crosses be-
tween broad-lobed and narrow-lobed forms the F^ was intermediate and
the F2 showed segregation into i/4 narrow, V> intermediate, and 1 4 broad.
Peebles and Kearney ( 1928 ) crossed shallow-lobed and deep-lobed types
and found Fx to be intermediate and a ratio of 1:2:1 in F2. In some
varieties of cotton the genetic situation is much more complex. Both
Hutchinson (1934 and others) and Silow (1939) postulate a series of
multiple alleles, chiefly affecting lobing. They believe that the genes are
"compound" and vary qualitatively as well as quantitatively. Hammond
(1941) showed the importance of developmental analyses of shape in
individual leaves and of changes of leaf shape along the stem. This
method was carried further by Stephens ( 1944 ) .

In the Japanese morning glory, Pharbitis, Imai (1930) and a number
of other Japanese geneticists have studied the complex situation presented
by the inheritance of leaf shape in crosses among its many varieties.

Among other traits of form the inheritance of which has been analyzed
in mendelian terms are fruit shape in Bursa (Shull, 1914), root shape in
radish (Uphof, 1924), and leaf lobing in Tropaeolum ( Whaley, 1939).

Evidence for the Existence of Genes for Shape. The problem under-
lying all these instances of the inheritance of form is to find the method
by which genes determine what the form is to be. The fact that such
traits show segregation suggests that genes control them directly, but
it is difficult to see how this is done. Some geneticists have tried to sim-
plify the problem by assuming the operation of genes for individual
dimensions only, as in the case of vine length in peas. Thus in tobacco
flowers Anderson (1939) studied the inheritance of tube length and
limb width in crosses between Nicotiana Langsdorfii and N. alata, species
which differ in corolla shape. He observed that in F2 there was much
sharper segregation for length than for width, suggesting that fewer

420 Morpho genetic Factors

genes were operative in the former character than in the latter. There
was by no means free recombination of length and width in F2, however,
as independent assortment would require. The combinations that did
occur were only a narrow segment of those theoretically expected. When
length was plotted against width in F2, these were confined to a narrow
segment of the total, running from combinations rather like one parent
to those like the other through others resembling the Fj. He suggests that
factors hindering free recombination might be gametic elimination,
zygotic elimination, pleiotropism, and linkage. He believes that all of
these may here be operative and suggests that all quantitative characters
of an organism may be tightly linked, surely a radical conclusion. An
extreme instance of the hypothesis that shape is the result of genes
determining dimensions has been proposed by Frets (1947), who postu-
lates that in the inheritance of seed shape in beans there are a series of
independent genes for length, breadth, and thickness, respectively.

H. H. Smith (1950) studied a cross much like that made by Anderson
and comes to the conclusion that there is a developmental restriction to
free recombination but that this is due to a "correlated growth pattern."
In simpler words, there are genes that control shape directly rather than
through individual dimensions.

Evidence for the existence of such genes has been presented by Sin-
nott (1935), chiefly from studies of the inheritance of fruit shape in the
Cucurbitaceae. This evidence is of several types, as follows:

1. If a race with flattened, disk-shaped fruits is crossed with a spheri-
cal one, the F! shows complete dominance of the disk shape and in the
F2 there is sharp segregation into % disk and y± sphere. In another case,
two different types of spheres, when crossed, show evidence of the ac-
tion of complementary genes, for the Fx is disk-shaped and in the F2
there is dihybrid segregation into %6 disk, %6 sphere, and y16 elongate.
Other shape differences can be analyzed in equally simple mendelian
terms, though more genes are usually involved.

2. In the disk-sphere cross, F2 segregation for shape index (ratio of
length to width) is sharp but those for length and for breadth are much
less so, suggesting that the segregating genes control shape directly and
not through dimensions.

3. In one disk-sphere cross, the fruits of the disk parent were con-
siderably larger than those of the sphere. The size of the Fx was close to
the geometric mean between the two parental sizes, and the means of the
segregating F2 disks and spheres were essentially similar to each other
and close to that of the F\. This can be explained by assuming that
size is determined by a series of genes but that the gene for shape is
independent of these and molds into a particular form the material
made available by the genes for size.

Genetic Factors 421

4. In a considerable series of crosses between races genetically more
complex and differing in both the size and the shape of their fruits, a
positive correlation was observed in each case between fruit length
and fruit width in the parents and the Fj (where presumably all size
differences are caused by environmental factors) but a negative one in
F2 where segregation occurs. This again can be explained by assuming
that shape is inherited independently of size. A certain amount of ma-
terial is genetically available for every fruit, and if its shape genotype
tends to produce an elongate one, this will be relatively narrow, and
hence the negative correlation. Maximum parental length is never com-
bined in F2 with maximum width, or minimum length with minimum
width, as they should be if dimensions are directly determined genetically
and recombined independently.

5. In the F2 the coefficient of variation for length is twice as large as
that for width, which is to be expected in a radially symmetrical organ
where shape and size are genetically independent, for if the amount of
material for growth is fixed, a unitary change in width (equatorial
diameter) should produce a much greater change in length, since volume
is essentially width X width X length.

Further evidence that genes for shape are actually operative is found
in the fact that in a number of plants, such as the tomato (Lindstrom,
1928; Butler, 1952), genes for fruit shape are linked with others and can
be definitely located on chromosome maps (Fig. 19-2). If it were dimen-
sions that are directly controlled, presumably their genes would occupy
different loci.

If genes determining shape actually exist, the difficult problem arises as
to how they produce their effects. The ultimate mechanisms are by no
means clear but the visible steps in the process can be described. In
some cases the shape of an organ, such as a fruit, is established when it
is a very small primordium. After this, growth rates in the various dimen-
sions are equal, and as the structure grows its shape remains constant. The
critical step in establishing growth relationships here is taken very early.
This is what happens in fruits of pepper, tomato, some races of Cucurbita
pepo, and various other plants. It is usual in organs that are nearly iso-
diametric at maturity.

In many fruits and in most leaves, especially where the dimensions are
markedly unlike, the primordium is a roundish mass of cells and the shape
of the organ is produced by differential growth among the dimensions
(Sinnott, 1936b). In various races of the gourd, Lagenaria siceraria, for
example, mature fruit shape varies from long and narrow through round
to flattish. All are alike in early primordia. In elongate types (like the
"Hercules club") length increases faster than width and as the organ
grows in size it becomes progressively more elongate. Conversely, the

422

Morpho genetic Factors

I

Normal (M) Mottled (m)

Smooth (P) Hi Peach (p)

Normal (0) Oblate (o)

Woolly (Wo/wo) I Normal (wo)

1

Normal (Ne) U Necrotic (ne)

Simple Inflor. (S) ■ Compound Inflor, (s)

Non-beaked (Bk) I Beaked (bk)

Few Locules (Lc) ■Many Locules (Ic)

Fig. 19-2. Map of chromosome 1 of tomato. Two genes for fruit shape, and genes for
other structural characters, have places on it. ( From Butler. )

Genetic Factors

423

flattish types grow more rapidly in width. In all such instances, form
changes as size increases. Where a particular race is genetically small,
its fruit shape at maturity will be different from one which is genetically
larger but has the same shape genotype. This fact complicates a study
of the inheritance of shape in cases where the parents differ in both shape
and size.

In types where shape changes during development the dimensional
relations, if plotted logarithmically, are allometric, the points falling
along a straight line the slope of which measures the relative growth rate
of the two dimensions (Fig. 5-8). It is this relative rate which the genes
control, for if two races of Lagenaria differing in the slope of this line

6O-1
50-

40
30

20-

O

z
u

10

8

6-

— r~
4

-j—
6

-i 1 —

8 10

20 30

WIDTH. MM

Fig. 19-3. Segregation of relative growth rates. Allometric growth of length to width
of fruits in an F2 from a cross between a rather elongate and a rather flat variety of
cucurbits. The two F2 classes resemble in general the parental forms. The Fi was
like the elongate type. What is segregating is the character of the relative-growth
line. (From Sinnott.)

are crossed, the trait which segregates in F2 is the steepness of this slope
(Fig. 19-3), the value of k in the allometric equation (p. 105; Sinnott,
1958).

It should be remembered that what is being controlled is not simply
the relationship between two dimensions but between all the dimensions
that make up the organic pattern. In the "bottle" gourd, for example, the
length of the axis during growth is related to the width of the upper,
sterile lobe; of the isthmus; and of the lower, fertile lobe. Relative to the
axis, the lower lobe grows fastest, the upper next, and the isthmus least.
The form of the whole structure thus changes in a precise and predict-
able fashion.

This concept of shape inheritance may be illustrated most simply by

424 Morpho genetic Factors

inscribing the lengthwise profile of an organic form like that of a fruit
in a series of rectangular coordinates, as D'Arcy Thompson ( 1942 ) has
done with various structures, and then seeing how other forms may be
derived from it by deforming these coordinates in a particular fashion
(Fig. 19-4). A change such as might be produced by a single gene dif-
ference is evidently not a localized one but involves, at least to some
degree, the pattern as a whole.

The objection may be raised that in some cases a single dimension does
seem to be inherited, as in vine height in peas. In a strongly polarized
organ like the stem, height may be changed with little reference to stem
diameter. In such cases height seems to be a direct expression of size in

— ?^--^ —

f-f-"-f^

I I -

\-\-J-t

V ~ /

Fig. 19-4. Geometric modification of fruit shape. The fruit at the upper left has its
longitudinal profile inscribed in a grid of equal coordinates. This may be changed to
various other shapes by changing these coordinates. ( From Sinnott. )

which the major effect of the genes is channeled in one particular dimen-
sion, that of the polar axis. Ear length in maize, one of the first characters
to be analyzed in terms of multiple genes, is the major dimension of a
polarized organ and thus strongly affected by any genes that control
total amount of growth. Here, however, ear width is also involved to
some extent, and there are differences in the relation of length to width
in various races. Such a case may perhaps be regarded as intermediate
in genetic control between one in which genes for shape express them-
selves in a weakly polarized structure (like a fruit), thus producing a
wide range of patterns, and one in which growth is essentially limited
to the polar dimension.

Genetic Factors 425

The evidence therefore favors the view that in most cases, certainly,
genes control form directly. How this is done poses one of the most
difficult problems of genetics and morphogenesis and one closely in-
volved with that of biological organization itself. Most of the work on
gene action has indicated that genes control the production of specific
substances; but how, one may ask, does a substance control the de-
velopment of a specific form? This involves the control of relationships,
like that between length and width in a developing fruit, and not only
single relationships but a whole series of them organized into a pattern.
The amount of growth in one dimension is related precisely to the
amounts in all the others. For a specific substance to do this involves the
old question of organizers and organ-forming substances which are so
easy to postulate and so difficult to picture in physical terms. These
gene-produced substances seem rather to act as evocators, calling out or
modifying formative potentialities in the living stuff of the organism. We
need to assume the immanent presence in protoplasm of something that,
for want of a better simile, can be compared to a system of coordinates in
three dimensions.

A specific substance may be thought of as bending or otherwise modify-
ing these coordinates in a particular way and thus regulating growth in
such a fashion that a specific pattern is produced. The problem remains
as to the nature of this underlying formativeness. It may be thought of,
perhaps, as a molecular pattern in the cytoplasm (p. 455). To call it a
"field" is to give it a name but not an explanation. It is evidently involved
in the nature of the living, organized system that an organism is. To
recognize that it exists, even though one cannot yet explain it, is a step
in advance and may save us from a too naive conception of the nature
of gene action in development.

Other Structural Traits. Aside from pure forms in the geometrical sense,
various other structural characters are under gene control, or at least
show mendelian segregation after crossing. Thus the zigzag stem that
appeared in descendants of a certain cross between Tom Thumb pop-
corn and Missouri dent (Eyster, 1922) behaves as a double recessive to
normal stem. "Corn grass," a mutation in maize with narrow leaves,
many tillers, and few male flowers, is a single-gene dominant ( Singleton,
1951 ) . In peas, relatively long distance between first and second flowers as
compared with the total length of the inflorescence was found by
Lamprecht ( 1949 ) to be the result of three genes. Abnormalities of
various sorts have also been shown to have a genetic basis. Among them
are double flowers in many plants, as for example Tropaeolum (Eyster
and Burpee, 1936), where doubleness is recessive but where a dominant
"super-double" strain appeared, female sterile and with about 135
petals. Peloria in Linaria vulgaris and Digitalis purpurea has been shown

426

M 01 pho genetic Factors

by various workers to differ in some types by a single gene from normal
flower. Fasciation is a single-gene recessive to normal in Nicotiana
(O. E. White, 1916). In both peloria and fasciation individuals are found
which are usually normal but occasionally produce these abnormalities,
presumably because of some genetic predisposition in this direction. These
should be of particular interest in studies of the basis of gene action.

There are two traits in the nature of abnormalities ("tufted" and
"polycladous"), presumably gene-determined, in the liverwort Spliaero-
carpos (Allen, 1924, 1925) which are of particular interest in that they
occur in the haploid gametophyte generation so that the effects of a single
gene are directly visible, unmodified by the influence of its allele.

Fig. 19-5. Cross section of the stem of Aquilegia. Left, normal plant. Right, mutant
with thicker cell walls. ( From Anderson and Abbe. )

Anatomical characters have also been shown to be directly affected
by genes. In Aquilegia canadense a dwarf race with bushy, compact
growth and stiff, brittle branches has been shown by Anderson and
Abbe (1933; Fig. 19-5) to differ from normal by a single gene. The
direct effect of this gene is to cause precocious secondary thickening of
the cell walls, from which all the other differences follow. Piatt, Darroch,
and Kemp ( 1941 ) report that in wheat, solid stem differs from normal
hollow stem by three or four pairs of recessive genes.

In all these cases where the form or structure of a particular plant part
has been found to be controlled by a gene or group of genes, much
valuable information as to the method of control may be gained by a
study of the development of this structure. In a few cases this has been
done, as in cotton leaves and cucurbit fruits described above; in dwarf
mutants in maize by Stephens (1948); in structure and growth rates of

Genetic Factors

427

inbred and hybrid maize by Weaver (1946), Heimsch, Rabideau, and
Whaley (1950), and Stein (1956); in a leaf mutant in maize by Mericle
( 1950 ) ; and in the leaves of two species of Tropaeolum and their hybrid
by Whaley and Whaley ( 1942 ) . In this last piece of work it was found
that the pattern was essentially determined by early differential cell
division in certain regions, the final form being attained by uniform
cell expansion. Much more work of this sort, even at the purely descrip-
tive level, needs to be done, for it will doubtless pose more sharply the
problems which have to be solved and may suggest new methods of
attacking them.

Fig. 19-6. Acetabularia. A, A. mediterranea. B, A. wettsteinii. C, a stalk piece (shaded)
of the former species grafted to a rhizoid of the latter, which contains the nucleus. The
regenerating "hat" resembles that of A. wettsteinii and thus seems to be determined
by the nucleus. ( After Hiimmerling. )

Acetabularia. In a few cases more direct proof of gene control over
form characters has been obtained. One of the most notable of these is
presented by the coenocytic marine green alga Acetabularia (p. 136). This
plant has a branching, rhizoidal base from which rises a stalk several
centimeters high, surmounted by a "hat" something like the "umbrella"
of a mushroom. At most stages of its life history, Acetabularia has but a
single, large nucleus, located in one of the basal rhizoids. Two species
of the genus differ in size and especially in the form of the hat. If a
long piece of the stalk of the taller species ( A. mediterranea ) is cut out
and grafted to a decapitated basal portion of the other (A. wettsteinii),
which contains the nucleus, a new hat will be regenerated at the apex
of the grafted stalk. At first this hat will resemble that of the species
which contributed the stalk but at length it comes to be like that of the

428 Morpho genetic Factors

species at the base and thus like the one to which the nucleus belongs.
Evidently the nucleus, with its genes, determines the form of the hat
(Fig. 19-6). The delay in expressing this determination is thought to be
due to the persistence for a time of specific substances in the cytoplasm
of the stalk, produced previously by the nucleus of the species from which
it came. Acetabularia has provided material for many experiments im-
portant for genetics and physiology as well as for morphogenesis, most
of them by Hammerling ( see, for example, 1946 ) .

Genes and Sex Structures. A particularly complex problem in genetics
and one of much importance in morphogenesis is the inheritance of sex
and the determination of the structures in which sexual differences are
expressed.

In animals most individuals definitely belong to one sex or the other,
and the production of both male and female gametes by the same or-
ganism is rare. In plants, however, it is much commoner than the uni-
sexual condition. Among higher forms, staminate and pistillate flowers
may be separate but on the same individual (the monoecious condition)
or the flowers may be perfect and hermaphroditic. There are a consider-
able number of cases, however, where the two types of sexual structures
are borne on different individuals (the dioecious condition). Such forms
are strictly comparable to unisexual animals.

In determining just what the sexual character of a plant will be, how-
ever, the environment has a much greater effect than it does in animals.
Sex reversal or the production of one sort of sexual structures rather
than another due to physiological or environmental changes is rare in ani-
mals but in plants this is relatively easy to accomplish. In monoecious
angiosperms the ratio of staminate and pistillate flowers to each other
or to the perfect flowers which sometimes occur on such plants may be
determined by light or by growth substances, or it may be an aspect
of the general phasic development of the plant (as in cucurbit flowers;
Nitsch, Kurtz, Liverman, and Went, 1952 ) . The problem of sex expression
in plants is therefore in large measure a developmental rather than a
genetic one. Although there is a definite genetic basis for most of the
sexual differences, this wide variability in its expression makes genetic
analysis particularly difficult. There is a large literature on this subject
only a very small part of which can be mentioned here.

With the rediscovery of Mendel's law there were many attempts to
analyze sexual differences in dioecious plants in mendelian terms. Among
the early workers were Correns (1907), Bateson (1909), and Shull
(1910). The plants on which they first worked were Melandrium (Lych-
nis) and Bryonia. Correns concluded from his experiments that in Melan-
drium the egg cells all carry a tendency toward femaleness and that the
male is heterozygous for sex, half the male gametes bearing female

Genetic Factors

429

tendency and half male. This plant could therefore be regarded as hav-
ing the XY type of sex inheritance and to be comparable to Drosophila.
The later discovery by Blackburn (1923) of an unequal pair of chromo-
somes in Melandrium strongly supported this conclusion, and it is now
generally accepted. It has been strengthened by the fact that definitely
sex-linked traits have been found here, notably a difference in leaf shape
(Fig. 19-7).

Sex chromosomes are not confined to vascular plants. In the liverwort
Sphaerocarpos Donnellii Allen (1919) reported that the four spores of
each tetrad produce two male and two female gametophytes. The females
have a very large chromosome, apparently the X, and the males its much
smaller homolog, apparently the Y ( Fig. 19-8 ) . This is the XY type of

Fig. 19-7. A sex-linked trait in Melandrium. At left, normal plant. At right, a narrow-
leaved mutant, the gene for which is located in the X chromosome. ( From Shull. )

sex determination but expressed in the gametophyte generation. A good
many other dioecious liverworts and mosses have been found to possess
a similar pair of sex chromosomes. It is significant that when such
gametophytes are made diploid they become monoecious, evidently be-
cause they now possess both types of chromosomes, though in such
cases the gametes usually fail to function. The genetics of bryophytes has
been reviewed by Allen ( 1935, 1945 ) .

There are a number of complications in the chromosome theory of sex
determination in the higher plants, however. Bryonia, which, like
Melandrium, is clearly male-heterozygous on breeding evidence, has no
unequal chromosome pair, and it turns out that visibly unequal chromo-
somes, presumably sex chromosomes, are present in only about half
the genera of dioecious plants. In some cases, also, like Dioscorea, the
female is XX and the male XO, with one chromosome less than the female.

430 Morphogenetic Factors

In others, like the dioecious species of the strawberry, Fragaria, it is the
female that is the heterozygous sex and all male gametes are alike. Other
difficulties appear. In Rumex, for example, the female has two X chromo-
somes and the male one, but the male has two different Y chromosomes.
In Humulus lupulus, hops, the female apparently has two pairs of dif-
ferent X chromosomes and the male has one of each of these plus two
different Y chromosomes.

The situation is so complex and the results reported often so conflict-
ing that some botanists, among them Schaffner and Yampolsky, have
entirely repudiated the chromosome theory of sex, particularly since in
some cases, notably in Cannabis, sex can readily be reversed by various
environmental factors, as Schaffner was able to do by altering the

Fig. 19-8. Chromosomes of Sphaerocarpos. From female gametophyte, above, showing
X chromosome, and from male, below, showing Y. ( From C. E. Allen. )

photoperiod (p. 317). McPhee (1924) obtained similar results. He showed
that this does not invalidate the genetic basis for sex but simply demon-
strates that the range of expression for the genotype in hemp in response
to the environment is very wide.

The early ideas that two X chromosomes produce a female and one X
a male are clearly too simple. The modern view of sex determination
conceives of a balance between several, probably many, genes of which
some are in the so-called sex chromosomes and others may be in the
autosomes. This theory of balance is well shown by the results of several
workers (Warmke and Blakeslee, 1940; Westergaard, 1940; and Warmke,
1946) with a dioecious race of Melandrium which had been made tetra-
ploid by colchicine treatment. Here the female had four X chromosomes
and four sets of autosomes, 4A + XXXX, and the male 4A -f- XXYY. By
crosses among these and with diploids, the investigators were able to pro-

Genetic Factors 431

duce types with one or with two Y chromosomes combined with two,
three, or four X's, the number of autosomes being kept the same in each
combination. The Y was thus the only variable. They also combined one,
two, three, and four X chromosomes with one Y, again with the same
number of autosomes, so that the number of X chromosomes was the
variable. The results as to male, female, and hermaphrodite flowers led
to the conclusion that the autosomes have little sexual tendency ( as they
do have in Drosophila), that the Y contains strong male-determining
genes, and the X, weaker female-determining ones. The ratio of X to Y
chromosomes determines what the sex will be. It can also be shown
that there are at least three genes for maleness in the Y chromosome.

Experiments like these support the hypothesis that genes with tenden-
cies to produce male structures or female ones are carried by the X, the
Y, or the autosomes and that the balance between them determines the
particular expression of sex. These genes may be present in chromosomes
where there is no morphological difference between members of the pair,
and such difference is obviously not significant for sex determination. The
sharp distinctions between maleness and femaleness in animals and the
relative scarcity of intersexual forms among them make genetic analysis
of sex much less difficult there than in plants.

Aside from the determination of sex in individuals as a whole, the de-
gree of sex expression within the individual has also been shown to be
under gene control. Typical illustrations of this are the following: In
several cucurbits the monoecious condition is dominant over the andro-
monoecious (where some flowers are hermaphroditic and some stami-
nate), and a single gene is involved (Rosa, 1928). Poole and Grimball
(1939) extended this for Cucumis by demonstrating a two-factor dif-
ference between hermaphroditic and monoecious, since a cross between
these types gave in F2 nine monoecious: three gynomonoecious: three
andromonoecious: one hermaphroditic. In Carica, Hofmeyr (1938) re-
ports that three alleles, Ml5 M2, and m, are responsible for maleness,
hermaphroditism, and femaleness, respectively (M^m is staminate; M<jn,
hermaphroditic; and mm, pistillate). Homozygous Mi or M> are lethal.
Janick and Stevenson (1955) find that the monoecious character in
spinach is allelic to the XY pair of genes concerned in sex determination.

A notable example of the effect of genes on sex determination which
could lead directly to the production of a dioecious condition from a
monoecious one was demonstrated by Jones (1934) with maize. In this
plant there are several recessive genes for tassel seed (ts) on chromo-
some 1, in which the staminate florets are replaced by pistillate ones
and the plant is thus essentially female. The recessive silkless gene (sk)
in chromosome 2 sterilizes the female flowers and thus produces a plant
essentially male. The silkless gene has no effect in the presence of tassel

432 Morpho genetic Factors

seed and the double recessive sksk tsts is thus female. If this is crossed
with a plant sksk Tsts, which is male, half the offspring are Tsts (male)
and half tsts (female). Interbreeding such plants, which are incapable
of self-fertilization, will continue to produce offspring of which half are
staminate and half pistillate, so that these plants, if prevented from
crossing with other types of maize, will constitute a dioecious race. In this
case chromosome 1, on which tassel seed is located, functions as a sex
chromosome although no morphological difference is visible.

A detailed review of the genetic basis for sex expression in flowering
plants has been written by Allen (1940).

Genes and Growth Substances. Since growth substances so powerfully
affect growth and development it is natural to expect that in many cases
gene action will involve the production and distribution of these sub-
stances, and in a considerable number of cases this has proved to be the
case. Thus in the profound changes in growth habit of "lazy" maize
(p. 390) the character is due to the fact that auxin, instead of accumu-
lating on the lower side of a horizontal stem, remains evenly distributed
so that the stem does not turn upward. Its failure to do so is not the re-
sult of mechanical weakness but of abnormal auxin relations.

Mention has already been made (p. 264) of the single-gene difference
between the annual and the biennial varieties of Hyoscyamus niger and
the fact that this is apparently due to a growth substance which can
be transmitted by grafting, to make the biennial form flower in its first
season. It is probable that a growth substance may also be operative in
other similar cases, like those of beets and white sweet clover, where the
difference between annual and biennial forms has been shown to be due
to a single gene. In the single-gene mutants reported by Stein (p. 265)
which were grafted to normal stock, some of the effects of the gene seemed
able to cross the graft union but others did not.

A particularly interesting case is reported by Scheibe ( 1956 ) for peas,
where a recessive fasciated mutant, differing from normal by a single
gene, has a higher concentration of natural auxin than the normal.
Furthermore, fasciation can be produced in the normal type by appli-
cation of indoleacetic or naphthaleneacetic acid. Here the difference be-
tween the two genes seems to be in their ability to produce a growth
substance.

Genes are also concerned with photoperiodic response. The Mammoth
mutant of tobacco differs from most strains by a single gene which,
among other effects, has changed the normal day-neutral type to one
that flowers only under short day-lengths. Chandraratna ( 1955 ) has
shown that, in rice, races sensitive to photoperiod differ from day-neutral
types by a single gene.

Goodwin ( 1944 ) crossed several races of a short-day species of Solidago

Genetic Factors 433

differing in flowering time and found that a considerable number of
genes were involved in the determination of this character, probably
distributed among all nine chromosome pairs.

Since developmental traits involve reaction of the genetic constitu-
tion of the organism to various other environmental factors— water, tem-
perature, light, mechanical factors, and others— it is obvious that genes
or their combinations must take part in these reactions, and although
there are not yet many cases in which the action of individual genes
has yet been analyzed as successfully here as it has in the biochemical
genetics of lower organisms, this will doubtless be accomplished and
will give information of value for the solution of the problems of de-
velopment. This knowledge will be second in significance only to that
which may be gained as to the mechanisms by which these innumerable
gene reactions are so organized in the growth and activity of the indi-
vidual that it becomes an organism.

CYTOPLASM

The fact that an entire and normal plant may be produced by regenera-
tion from a single cell (p. 253) or a group of similar cells in different
regions and from different tissues is evidence that all the cells of the plant
are genetically alike. This implies that all the nuclei are similar, a conclu-
sion supported by the fact that in all cells (save in cases of polysomaty)
the number and structure of the chromosomes are constant.

If this conclusion is valid, the basis of differentiation would appear to
lie in the extranuclear portion of the cell, the cytoplasm. Much less is
known about the cytoplasm than about the nucleus, and events in it are
not as dramatic and easily observed. It is clear, however, that beneath
its relatively homogeneous superficial appearance there must be a high
degree of chemical and physical diversity, an understanding of which
is necessary before the problems of differentiation can be mastered. The
basis for cytoplasmic differentiation is doubtless at the submicroscopic
level. Weiss (1956), Schmitt (1956), and some others have shown that
the elements of the macromolecular pattern are markedly different from
one another in size and distribution (see also Tartar, p. 455). A wide field
of research at this level is now developing.

There are a few cases where the cytoplasm can be shown to be im-
mediately concerned in determination of structural characters. This is
particularly true of the cell wall, which is directly produced by the
cytoplasm and is a primary element in many differences between cells.
Examples of this are seen in the regenerative conversion of thin-walled
parenchyma cells into xylem cells with reticulate lignified walls. The pat-
tern of these lignified thickenings is preceded in development by an

434 Morphogenetic Factors

identical pattern of granular cytoplasmic strands on which the thickenings
are laid down (p. 193). Other markings in the cell wall have also been
traced to cytoplasmic differences.

The cytoplasm may be concerned in the development of characters
above the cellular level. In the cells of air roots of orchids, the bands
of wall thickening ( p. 201 ) that keep these cells from collapsing are laid
down by the cytoplasm in each cell. They are not isolated structures in
single cells, however, but a thickening in one cell is directly adjacent to
one in the next, so that a continuous system is produced extending from
cell to cell and forming a histological pattern over a considerable mass of
tissue. The differential fiber patterns in Luff a (p. 197) and similar cases
doubtless originate in the cytoplasm.

The distribution and configuration of the cytoplasm probably have a
more deeply seated relation to development, however, than in these ex-
amples of cellular patterns. The plane in which a cell divides, at least
in vacuolate cells, is foreshadowed by the orientation of a cytoplasmic
plate some time before the axis of the spindle is established (p. 25), a
fact which suggests that cell polarity, and thus the direction of growth
and ultimately organic form itself, may have their immediate basis in the
distribution and patterning of the cytoplasmic body.

The relation of cytoplasm to such differences in form may be well
seen in the coenocytic bodies of many red algae, notably the genus
Caulerpa. Here there are no cellular barriers to the passage of cytoplasm
from one part of the plant to another, and much streaming takes place.
Differences may be observed in various parts of the plant body as to the
character of the cytoplasm, part of which is fixed to the inner wall and
does not stream. In such plants the differential distribution of the cyto-
plasm seems to be related to the differentiation of the plant body, though
the mechanisms involved are unknown. The disadvantage in such or-
ganisms and the probable reason why they have never been able to de-
velop very highly differentiated bodies is their difficulty in keeping the
various components of their living material sufficiently isolated so that
physiological differences can be maintained effectively and a high degree
of organization thus made possible.

Even in multicellular plants visible differences in distribution of cyto-
plasm are related to differentiation. This is especially evident in cases of
unequal cell division, as in the formation of trichoblasts in many roots
(p. 190). In the mother cell, which is to divide unequally to form a
small trichoblast and a larger hairless cell, much of the cytoplasm (and
the nucleus) moves toward the end at which the trichoblast will be cut
off, so that even before division there is a difference in cytoplasmic dis-
tribution. The formation of the new wall finally separates two regions
which had already become cytoplasmically different. In the formation

Genetic Factors 435

of stomatal mother cells, initials of trichosclereids, and many other ex-
amples of unequal cell division the same differential distribution of cyto-
plasm, before division, is evident.

In such cases, unlike the coenocytes, the differences which arise in the
cytoplasm cannot become distributed beyond the limits of the original
mother cell. If in each cell division, however, there were a quantitatively
or qualitatively unequal distribution of cytoplasm between the two
daughter cells, cellular differentiation would result. It seems reasonable
to suppose that many cell divisions are thus cytoplasmically unequal
even though the differences are not visible and may be at the submicro-
scopic or chemical level. Such inequality would provide the necessary
cytoplasmic basis for differentiation.

If differentiation proves to be primarily a matter of cytoplasmic distribu-
tion, the mechanism by which this distribution is controlled must evi-
dently be one of the major problems of morphogenesis. In some cases
the cause may be ascribed to polarity. Certainly polarity is involved, as
we have seen, in many axes other than the major one of the plant body
and is evident in many developmental patterns. It may be that the mecha-
nisms which are effective in the extreme and conspicuous cases of un-
equal and polar cell division may also be involved in all differential di-
visions (Bunning, 1958).

That the cytoplasm contributes to the determination of developmental
processes through inheritance is clear from a number of facts, particularly
in cases where the offspring of reciprocal crosses are unlike. Where the
offspring tends to resemble the maternal parent this difference is evi-
dently due to that which only this parent contributes to it, the cytoplasm.
In traits where plastid differences are involved the influence of the
cytoplasm is clear, since the plastid primordia are carried in it. In other
cases it is more difficult to see what the mechanism of transmission is.

Crosses in Epilobium, where reciprocal hybrids are often markedly dif-
ferent in size, have been studied intensively. Lehmann (1936) showed
that in such cases the smaller hybrids have a lower concentration of auxin
than the larger ones. When Schlenker and Mittmann (1936) applied
auxin to the smaller plants their size was considerably increased. These
facts suggest that something carried in the cytoplasm stimulates the
synthesis of auxin. It may be, as has sometimes been suggested, that
sensitivity to auxin is determined by the genes but that auxin synthesis
is carried on in the cytoplasm. Michaelis (1938) disagrees with Lehmann
and believes that the facts can be explained by specific interactions be-
tween genes and cytoplasm. This Epilobium work, however, and the
great body of evidence obtained by von Wettstein (1924) and his col-
leagues in experiments with mosses show that the genes are not inde-
pendent in their effects but that what they do is determined to a con-

436 Morphogenetic Factors

siderable degree by the cytoplasm with which they are associated.
Whether the specificity of the cytoplasm results from self-perpetuating
bodies such as the often postulated plasmagenes or from persisting
effects of genes on the cytoplasm (Mather, 1948) has not been de-
termined. This question is primarily of genetic rather than of morpho-
genetic importance.

When a knowledge of the cytoplasm is more complete, that part of the
cell, somewhat neglected by genetic investigations in the past, will doubt-
less contribute much more significantly to our understanding of develop-
ment and differentiation. What has been called protoplasmatic plant
anatomy is concerned with some of these problems. Its contributions have
been summarized by Reuter ( 1955 ) .

CHROMOSOMES

The control of development and form lies chiefly with the genes and
their reaction to the environment, but it must also be recognized that
differences in the number and character of the chromosomes, apart from
the genes they contain, may be of considerable morphogenetic signifi-
cance.

Polyploidy. Most plants in the sporophyte generation are diploid, the
cells containing two sets of chromosomes, one coming from the male
parent and one from the female, each chromosome belonging to a pair
of homologous ones. In some plants, however, the number of sets has
been multiplied so that every chromosome is represented by more than
two homologs. Such plants are polyploids. There are many cases where
the number of sets is doubled, to form tetraploids. Hexaploids, octoploids,
and many other polyploid types are known, though polyploidy cannot
be increased indefinitely throughout the plant because of loss of vigor in
higher members of the series. Individual cells, however, or groups of
cells may become very highly polyploid.

Polyploids are often found in nature, many species belonging to so-
called polyploid series where each species has a particular multiple of a
basic number of chromosomes.

Various ways of producing tetraploids artificially are known, and many
polyploids used in experimental work have arisen in this way. One
effective means is treatment with colchicine or certain other chemicals
which check mitosis after chromosome division but before the new
nuclear membrane is formed, so that the two daughter cells have the
double chromosome number. Colchicine may be applied to seeds or to
the whole plant. Growth after the latter treatment, as compared with
normal development, has been described for cranberry by Dermen
(1944). Many large cells in normal plants are polyploid, and a bud

Genetic Factors 437

developing in such a tissue will be a tetraploid or higher (Jorgensen,
1928). In mosses and ferns gametophytes may be regenerated from
diploid tissue under favorable conditions (p. 234) and are thus diploid
in character. From them tetraploid sporophytes may arise. Haploid
sporophytes in higher plants have been produced by various chemical
and physical treatments and sometimes occur in twin seedlings ( Christen-
sen and Bamford, 1943). These cases prove that the differentiation into
sporophyte and gametophyte does not result simply from difference in
chromosome number.

The primary effect of a multiplication of chromosome number is an
increase in the volume of the nucleus and the cell. Most other distinctive
traits of polyploids follow from this one. The relationship between num-
ber of chromosome sets and cell size is not always a simple proportional-
ity, however. A study of such a series as that in Datura stramonium (Sin-
nott, Houghtaling, and Blakeslee, 1934), for example, where In, 2n, 3n,
and 4n plants can be compared directly, shows that the increase in cell
size is different in different tissues. In epidermal cells it is not far from
1:2:4:8. In xylem cells the increase is a little greater, but in the paren-
chymatous cells of the fundamental tissue in the petiole, the tetraploid
is usually much more than eight times the diploid.

In such cases, each added chromosome complement does not simply
add an amount proportional to the increase in chromosome number but
multiplies cell size by a certain amount. In other words, the addition is
geometric rather than arithmetic. This is evident to some degree in the
pedicel cells of Datura but particularly in the large ones of the petiole.
It is well seen in mosses, where von Wettstein ( 1924 ) produced diploid
gametophytes by regeneration of protonemata from sporophyte (2n)
tissue so that haploid and diploid gametophytes could be directly com-
pared. When this was done, Tobler (1931) found that the increase in
cell size of diploid over haploid was different for different races and
that in crosses between them it was a character which seemed to segregate.
The effect of polyploidy may be different in related species ( H. H. Smith,
1943).

In some polyploid series, like that reported by Harriet E. Smith (1946)
for races of Sedum pulchellum with two, four, and six chromosome sets,
cell size increased with number of sets. In many cases, however, mem-
bers of such a polyploid series in nature do not differ appreciably in cell
size. An observation of von Wettstein's (1938) may indicate the reason
for this. He grew a diploid race of Bryum, which he named Bryum
corrensii, from a regenerated diploid protonema. It had large leaves and
cells about twice the haploid size and was quite sterile. Under vege-
tative propagation its size gradually became reduced until after 11
years it had returned to a practically normal condition as to leaf and

438 Morpho genetic Factors

cell size and fertility, although its chromosome number was still diploid.
This suggests that regulation to a physiologically optimum cell size had
taken place. In polyploid series in the higher plants it may be that regu-
lation, through natural selection or otherwise, has produced an optimum
cell size even with widely different numbers of chromosomes. In poly-
ploid series of recent origin, however, such as those produced by colchi-

>

w

V

4

*

V

%

Fig. 19-9. Flower of diploid (left) and tetraploid (right) in Antirrhinum majus.
( Courtesy W. Atlee Burpee Co. )

cine, there is almost always a close relationship between chromosome
number and cell size.

The increased cell size of polyploids may be reflected in larger plant
size (Fig. 19-9). Oenothera gigas, which proved to be a tetraploid, was
named for its size, and "gigas" tetraploids of many species are now known.
Frequently, however, the tetraploid plant is little larger than the diploid,
and it may even be smaller. It usually has stouter stems and thicker

Genetic Factors

439

leaves, and its flowers are larger. Haploid plants are universally smaller
than diploid ones. Triploids may be intermediate between tetraploids and
diploids but are often indistinguishable from the latter.

Genetic differences may sometimes determine the effect of polyploidy
on plant size. Flax ( Linum usitatissimum ) has been selected commercially
in two directions, toward the production of linseed oil and of flax fiber.
Pandey (1956) compared the tetraploid with the diploid forms of both
types of plants in this species and found that in the linseed type the An
is a gigas form whereas in the flax type it is actually smaller than the 2n.
The linseed tetraploid grows faster than its diploid but the flax tetraploid
grows more slowly. The two tetraploids also show certain morphological
differences.

SHOOT
APEX 10

LEAF 10

SHOOT
APEX 10

LEAF 10

Q 10 mm.

Fig. 19-10. Shoot apex and leaf primordium in Zea mays. Left, diploid; right, tetra-
ploid. Difference in size is due entirely to larger cells of the tetraploid. (From Ran-
dolph, Abbe, and Einset. )

The origin of size differences in members of a polyploid series has
been studied developmentally in a few cases. The apical meristem of the
tetraploid is always broader than that of the diploid. Sometimes it is
relatively flat, as in Vinca rosea (Cross and Johnson, 1941), or it may
be the same shape as the diploid but doubled in size, as in maize
(Randolph, Abbe, and Einset, 1944; Fig. 19-10). In the development
of the cucurbit fruit, Sinnott and Franklin (1943) found that the ovary,
from primordium to the time of flowering, was almost twice the volume
in An as in 2n and thus was proportional to the volume of its cells (Fig.
19-11). In these plants, growth of the ovary into the fruit is chiefly by
cell expansion. This second phase of growth is much less extensive in An
than in In, so that the mature fruit is almost the same size in both, as
are the cells of which it is composed. In these cases the flower is "gigas"
but the fruit is not.

440 Morpho genetic Factors

Members of a polyploid series often differ in other respects than size.
There is a general tendency in tetraploids for organs to be relatively
shorter and wider than in diploids. This difference is well shown in the
series of capsules in Datura from In to An (Blakeslee, 1934). The
haploid has a slender capsule and becomes progressively flatter in the
upper members of the series. Fruits of tetraploid cucurbits produced by
colchicine were in every case changed toward a flatter, or at least a less
elongate, form. The leaves of tetraploid varieties of most plants show
the same shape changes in comparison with the diploid. Straub (1940)
observed that flower size changes in the same way, flowers from higher
members of a polyploid series being relatively wider. In Torenia the
position of the anthers with reference to the corolla is changed in the
octaploid.

40

60 ao ioo

8 10 20

OVARY DIAMETER mm
Fig. 19-11. Graph showing general relations between cell size and ovary size in de-
veloping fruits of diploid and tetraploid cucurbits. In early stages the 4N is larger in
both respects but after flowering the growth of the 2N is greater and at fruit ma-
turity (vertical bar) the two are essentially alike. (From Sinnott and Franklin.)

This shape difference probably originates at the meristem itself.
Cross and Johnson found that in Vinca rosea the tetraploid apex was con-
siderably wider but no deeper and that the increase in size of its com-
ponent cells was also chiefly in width. Riidiger (1952) has shown that
in various plants the cells of the tetraploid are somewhat shorter and
wider than those of the diploid. Organ shape may thus be a reflection
of cell shape, though in other cases cell shape seems not to be markedly
different in An and 2n. Why there should be such a shape difference,
either in cell or organ, is not clear. Cell size alone is not enough to ac-
count for it, for there are large-celled races which do not differ in
shape from small-celled ones of the same species.

Certain more general biological facts are related to polyploidy. Steb-
bins (1938), for example, has studied polyploidy in a large number of
woody and herbaceous genera and finds that polyploid series are more

Genetic Factors

441

abundant in perennial herbs than in annuals or woody plants (Fig.
19-12). The basic chromosome numbers, however, are significantly
higher in woody genera.

Much work on polyploidy has been done by students of ecology and
plant distribution ( Miintzing, 1936 ) , though most of this has little direct
concern with morphogenesis. In general, polyploids can endure extremes
of climate better than diploids. The distribution of polyploids as to
latitude has been discussed and the literature reviewed by Love and Love
(1949).

Polyploids are of importance for evolution not only in matters of selec-
tion and distribution but from the fact that by their means sterile
hybrids can become fertile and genetic lines, separated by incom-

35--

1

EL

n

tl WOODY

■ HERBACEOUS

U WOODY b HERBACEOUS

nln hi

m.

Lii

LtiL

m.

5 & 7 8 9

BASIC HAPLOID NUMBER

Fig. 19-12. Distribution of basic chromosome numbers in herbaceous and woody
genera of dicotyledons. Dotted lines indicate genera known only tentatively. Herba-
ceous types tend to have smaller numbers. ( From Stebbins. )

patibilities, thus be brought together. Many species will hybridize but
the offspring are usually sterile. If their chromosome number is doubled
(to form an allopolyploid), as sometimes happens in nature, fertility
is restored since there are now pairs of homologous chromosomes and
normal meiosis can take place.

Somatic Polyploidy ( Polysomaty ) . Polyploidy is concerned with an
important aspect of differentiation, for investigation has shown that many
somatic cells, particularly the larger or physiologically more active
ones, are polyploid and often to a rather high degree. This condition is
termed polysomaty. In some cases, such as the meristematic region of
the root of spinach (Gentcheff and Gustafsson, 1939; Berger, 1941),
chromosomes of certain of the dividing cells, particularly in the periblem,
are twice, or sometimes four times, the normal diploid number. This seems
to be the result of an additional doubling in the prophase before the

442 Morphogenetic Factors

mitotic figure is formed. Polysomaty of this type has been reported in
other cases, as in Cucumis (Ervin, 1941).

In many instances it has been shown that a process of endomitosis
takes place in certain cells by which the chromosome number is doubled
(or further multiplied) even though the cell is mature, the nuclear
membrane intact, and no mitotic figure has been formed (Geitler, 1949).
That this doubling has taken place is indicated by the fact that the num-
ber of visible chromocenters, presumably corresponding to the chromo-
somes, is doubled. The chromosome number may be definitely determined
by inducing these cells to go into typical mitosis, either through wound-
ing or by application of growth substances. Under such conditions the
chromosomes can readily be counted. Grafl (1939) was thus able to
prove that among mature and normally differentiated cells of Sauromatum
guttatum some were tetraploid, some octaploid, and some 16-ploid. This
situation has now been found in many other cases. D'Amato (1950), by
the use of 2,4-D, observed it in roots of a number of monocotyledons,
and Holzer (1952), by treatment with indoleacetic acid, in the roots of
27 species of angiosperms. Holzer found that the distribution of these
polyploid cells was not at random but formed a pattern which was similar
in groups of related plants. Often it is not the number of chromosomes
(or chromosome centers) that increases but the number of strands per
chromosome.

The connection between polyploidy and the volume of cell and
nucleus has important morphogenetic implications. In certain animal
tissues, among them the cells of the developing salivary glands of
Drosophila, it has been observed that nuclear volume falls into definite
classes, each approximately twice the volume of the one next below it.
Such "rhythmic" distribution was observed in plants by Monschau ( 1930).
The relation between polysomaty and nuclear volume has now become
well established (Bradley, 1954, and others). This makes it possible to
determine with some accuracy the degree of polyploidy in a mature and
differentiated cell by measuring the volume of its nucleus or even of the
cell itself, in comparison with related cells and ultimately with those in
which the chromosome number can be determined directly. Thus in
various angiosperm species, Tschermak-Woess and Hasitschka (1953«)
have estimated the degree of polyploidy of certain cells in a tissue as
various multiples of the basic number, up to 256-ploid (Fig. 19-13).
Somatic polyploidy, as estimated either by direct count or by nuclear
size, commonly increases with distance from the apical meristem (Fig.
19-14) and with age (Fig. 19-15).

All this obviously has a Very important bearing on the problem of
differentiation. Wipf and Cooper (1940) for example, found a close rela-
tion between the presence of naturally occurring tetraploid cells and the

Fig. 19-13. Cereus spachianus. Cells showing increasing chromosome numbers during
development, a and b, 2n; c, 32n; d, 64n; e, highly polyploid resting nucleus from an
older portion of the cortex; /, young polyploid resting nucleus with chromocenters,
2 to 3 mm. behind the shoot apex; g, a part of the differentiated cortex showing marked
differences in cell size, presumably because of somatic polyploidy. ( From Fenzl and
Tschermak-Woess. )

443

MONOSOMATIC CELLS

DISOMATIC CELLS

TETRASOMATIC CELLS

100 lM MO 230 300 350 400 450 500 550 600 630 700 750 870 830 600 050 1000 1050 1100 1130 l!00 1250 ~I300

MICRONS FROM EXTREME TIPS OF ROOTS

Fig. 19-14. Frequency distribution of mitoses with one, two, or four times the basic
number of chromosomes, in the root of Cucumis. Chromosome number increases with
distance from the apex ( left. ) ( From Ervin. )

5600

! NUCLEAR VOLUME

5320

yC

5040

4760

4480

4200

3920

3640

3360

3080

2800

2520

2240

I960

1680

1400

1120

840

560

.

280

.AB

.An

UJi>

0

14 20

25.

' DAYS

Fig. 19-15. Changes in nuclear volume (cubic
microns ) during development of maize endo-
sperm. C, central region. AB and AD, surface
layers. Nuclear growth here is due to endomi-
tosis, with increase in number and size of
strands per chromosome. Number of chromo-
somes presumably does not increase. ( From
Duncan and Ross. )

444

Fig. 19-16. Endopolyploidy in tri-
chomes of Bryonia, a, glandular
hair with basal cell 256-ploid;
b, hair of filament, the basal cell
128-ploid, and others 16-ploid. The
epidermis is diploid. ( From Tscher-
mak-Woess and Hasitschka. )

Genetic Factors 445

origin of root nodules in legumes. Von Witsch and Fliigel (1952) found
that meristematic tissue of Kalanchoe Blossfeldiana was diploid but that
as the leaves differentiated the mesophyll became polyploid, as could
be shown by wounding and observing mitoses in the wound callus. Inci-
dentally, the mesophyll was only 8-ploid if the leaf had developed under
long days but 32-ploid under short-day conditions. Steffen (1956) esti-
mated from nuclear volume that chalazal haustoria in Pedicularis were
96-ploid and micropylar ones 384-ploid. An illuminating study of endo-
mitotic polyploidy in the differentiation of the trichomes of angiosperms
has been made by Tschermak-Woess and Hasitschka (1954; Fig. 19-16).

Somatic polyploidy has now been shown to be so frequent as to make it
probable that much of the differentiation of plant cells, so far as cell size
is concerned, is related to it, cell size being roughly proportional to the
degree of polyploidy. Exceptions have been found to this relationship,
and no firm generalization about it can yet be made. Obviously, too,
there is much more to differentiation than change in size. However, the
possibility certainly exists of learning much about the mechanism of
cellular differentiation and of developing what has been called "karyologi-
cal plant anatomy," a subject outlined in some detail by Tschermak-Woess
(1956). D'Amato (1952) has also reviewed the field of polyploidy in
differentiation, and Geitler's book (1953) discusses endomitosis more
fully.

Other Effects of Chromosome Differences. There is sometimes a rela-
tion between cell size and total chromosome bulk. In 13 species of Crepis
differing in number and length of chromosomes Navashin ( 1931 ) meas-
ured total chromosome length at a comparable stage of mitosis, using
this as an indication of chromatin mass. In each species he plotted this
against the volume of comparable cells in the root meristem and found
a close correlation between the two, suggesting that the total bulk of
chromosome material affects the size of the cell (Fig. 19-17). In some
cases, notably in mutants of Primula and Phragmites (p. 35), both
chromosomes and cells are markedly larger than normal, and this is also
reflected in the size of the plant itself. Neither of these types is polyploid.
In some plants there are "accessory" chromosomes which seem to have
little or no genetic effect, but Miintzing and Akdik (1948) find that
their presence causes an increase in the size of stomatal cells.

The influence of extra chromosomes was studied in Crepis tectorum by
Schkwarnikow ( 1934 ) . This species has four pairs of chromosomes called
A, B, C, and D, and four races were available in each of which one of
these chromosomes was represented by three instead of two members.
Plants in which B or C was present as a trisome had cells larger than the
normal diploid. Those in which A or D were the extra ones, however,
had smaller cells than normal. Here evidently something more than bulk

446

Morpho genetic Factors

5000-

i

1 i
i

'Z 4000-

i

1

l

■

3

o

i

d>

E

3
O

* 3000-
O

i
i

i

2000-

i

■ i i i i i

i i

i i i

i i i i

Chromosome length (relative units)

Fig. 19-17. Correlation between average cell volume (of dermatogen cells in root tip)
and average total chromosome length (chromatin mass) in 13 species of Crepis. The
length of bar for each species indicates the probable error for that determination.
( Redrawn from Navashin. )

of chromosomes was concerned with cell size. This presumably was de-
termined by the genes the chromosomes carried (Table 19-1).

Table 19-1. Average Cross-sectional Area (in Square Microns) of Primary

Dermatogen Cells in Root of Diploid Crepis tectorum and in

Four of Its Trisomies *

Diploid 260.0 ± 5.3

Trisomic A 235.5 ± 3.6

Trisomic B 282.6 ± 4.0

Trisomic C 271.0 ± 2.4

Trisomic D 228.5 ± 5.5

° From Schkwarnikow (1934).

A somewhat similar result was found by Sinnott, Houghtaling, and
Blakeslee (1934) in the primary chromosome mutants of Datura stra-
monium. This species has 12 pairs of chromosomes, and in each mutant
race there are three representatives of one of these chromosomes. The 12
trisomic races differed very considerably from one another, both ex-

Genetic Factors

447

ternally and internally. In some the cells in certain tissues were larger
and in some smaller than in the diploid. Such traits as the size of the
bundles, the amount of internal phloem, and the development of peri-
cycle fibers differed among the mutants. It is significant that for each
trait the diploid was approximately the average of the 12 mutants, a good

2N

i-i-

I 2-

22-

3 3

— 3-4

5-5-
5 6 —

77-

II II

1112 —

1313

13-14

14 14--

15-15-
15 16-

17 17 —

23 24-

IN-

6 6

■7 8

—910
1010

9 3

■1718

19-19

19-20

•21-22

2 N

■3N

■4W

210 2.58 3.06 3.54 4 02 451 5.00

Fig. 19-18. Genie balance in Datura stramonium. Cross-sectional area of flower stalk
in various chromosomal types (in square millimeters). Vertical line marks normal
value for the diploid. Areas larger or smaller than this are shown by the lengths of the
horizontal lines for each type. IN, 3N, and 4N are below. Above, the primary mutants
have solid lines, the secondaries dotted ones. Each chromosome is numbered by its
two ends, the primaries being 1.2, 3.4, etc., and the secondaries 2.2, 3.3, etc. The
geometrical mean of the primaries is almost exactly the value for the diploid. (From
Sinnott, Houghtaling, and Blakeslee. )

example of genie balance (Fig. 19-18). Evidently each chromosome
contributed something to the character of the plant, and when this
chromosome was represented by three instead of two, this contribution
was increased. Such a result seems clearly to be due to the genes which
the chromosome carries, however, rather than to something specific in

448 Morphogenetic Factors

the chromosomes as such. It may be that all the effects now attributed to
chromosomes may ultimately be found to be due to their genes.

It must regretfully be admitted that not very much of substantial impor-
tance has yet been contributed by genetic analysis to a solution of the
problems of morphogenesis. Its most significant addition to our knowl-
edge of development thus far is perhaps the discovery of the relation be-
tween the size of a cell and the degree of its internal polyploidy, with the
bearing this fact has on the control of histological differentiation. Behind
the other problems of morphogenesis still lurks the unanswered question
of how genes control the development of form and structure and thus
the orderly and integrated growth of an individual as an organism. En-
vironmental factors have an important influence on the character of this
organism, but the organizing process itself seems to be centered in proto-
plasm and thus to be under the control of the directive and self-multi-
plying elements in protoplasm, the genes. It is to this general problem of
organization that attention in our final chapter is directed.

CHAPTER 20

Organization

Underlying the various phenomena of morphogenesis that have here been
discussed stands a single basic problem: how a mass of living stuff is
organized into a system, so well termed an organism. Organization is evi-
dent in various ways but most vividly in the development of form in
living things. Form is not simply a trait to be described and classified.
It is also the visible expression of a self-regulatory equilibrium which
tends to be attained in development, maintained during life, and restored
when disturbed. Every individual has a specific equilibrium of this sort,
a morphogenetic norm, so to speak, to which it tends to conform. This is
the unifying factor that gives continuity to an organism. It is a pattern
for development in which every part, in its growth and activity, is related
to all the others and by which the fate of each is determined by its posi-
tion in the organized whole.

The manifestations of a given norm are various. It is not constant in
expression but may change, in a precise and regular fashion, from embryo
to maturity. It may produce very different results under different en-
vironmental conditions. Its basis is established in the genetic constitu-
tion of the individual. The nature of this norm, how it is modified in ex-
pression by factors inside and outside the organism, and how develop-
ment is regulated in conformity to it are the basic questions with which
the science of morphogenesis must deal.

To attack this problem hopefully one should break it down, if possible,
into simpler components. These have already been discussed in earlier
pages, but it will be useful here to bring them briefly together into focus
on the main problem.

One of these components is polarity. All plants, at least at certain
stages, are organized around an axis which provides a basis along which
development takes place and in relation to which the lateral organs are
formed. The two poles of this axis (save in rare cases) are unlike. The
axis may be vertical or horizontal, and if lateral axes arise from it, these
often have specific orientations, so that the plant body is really a pattern
of polarities. In many cases transverse as well as longitudinal ones may

449

450 Morphogenetic Factors

be seen. Polarity is manifest in physiological activities as well as in struc-
ture.

The universal presence of polar phenomena in plants suggests that
there is in living stuff an innate tendency toward polarization, although
most eggs and undifferentiated cells at first are unpolarized. This provides
a concrete point of attack on developmental problems. The suggestion is
obvious that organic polarities may be related to those evident in the
inorganic world, and especially to chemical and electrical ones, but this
has proved somewhat difficult to establish experimentally. Polarity has
been shown in some cases to be modified by specific factors in the en-
vironment.

Not only are the two ends of the polar axis unlike but other differences
appear in graded series backward from each apex. These gradients are
evident in the rate of various metabolic processes and in the form and
structure of lateral organs arising successively at the growing point. Here
is a simple place to study the origin of differentiation. One school of
biologists regards these axial gradients as the most important factors in
development.

The polar axis is not only a gradient axis but an axis of symmetry. In-
deed, the symmetrical arrangement of parts around it is a conspicuous
aspect of axiation. Organic symmetry, an expression of the basic regu-
larity in the arrangement of plant structures, is manifest at every level
from the internal structure of a cell to the configuration of a tree. It is
obviously an important element in the orderly formativeness that living
organisms display.

Radial symmetry— the regular spiral distribution of lateral structures
around an axis— is best displayed in vertical plant axes where the stimuli
of gravity and light affect all sides of the axis almost equally. Under these
conditions, the symmetrical arrangement of the lateral organs seems to be
traceable to an inherent spirality in living stuff itself. This has as yet
received little experimental study, but its widespread occurrence in
phyllotaxy, the spiral grain of wood, the spiral character of the cell wall
and of protoplasmic streaming, and the spiral movements of the plant
body suggest that spirality is another basic fact in organization.

Spirality is masked to a considerable extent in those axes which are
horizontal and thus exposed differentially to gravity and light, but the
dorsiventral symmetry of these structures provides good material for a
study of the interaction of polarity, spirality, and environmental factors
in the development of plant form.

We may therefore recognize several components in the general phe-
nomenon of plant organization: polarity, differential gradients, symmetry,
and spirality. These seem to be distinct characteristics and may have dif-
ferent bases in protoplasm. They certainly can be investigated separately.

Organization 451

All of them, or their rudiments, seem to be present in all plants. They
provide the basic ingredients, so to speak, out of which the developmental
norm is produced. Just what a specific norm will be depends on the
interaction between these inherent protoplasmic traits and two other
factors: the genetic constitution of the individual and the environment
in which it develops.

The genetic constitution is the complement of genes in the organism.
These act on the protoplasmic traits just mentioned to produce the form
characteristic of that organism. This form, however, is not a specific pat-
tern of polarities, gradients, spiralities, and symmetries but results from
a specific reaction to a specific environment. Neither genes nor environ-
ment alone determines what an organism is, for their action is comple-
mentary and one cannot be separated from the other. In practical experi-
mental work, however, much can be learned by studying the effects of
different genotypes under the same environment or of the same genotype
in different environments. The latter method has so far been much more
fruitful, as is shown by the vast literature in the fields of the morpho-
genetic effects of light, water, temperature, mechanical factors, and
various chemical substances. There is still opportunity for much fruitful
work in all these fields. A study of gene action, on the other hand, al-
though actively pursued, has thus far been concerned chiefly with the
effects of genes on metabolic processes or on the synthesis of specific
substances. How genes control developmental relationships, and thus
the production of organic form, is almost unexplored territory.

In a given individual, therefore, through the interaction of its genotype
and the particular environment in which it lives, both acting on the basic
tendencies toward polarization, gradients, symmetry, and spirality, there
is at any given stage of its development a norm to which it conforms.
This involves more than a mere interaction between organism and en-
vironment. What emerges from the developmental process is an organized
system in which the various parts are related and mutually interdependent
and which controls its own development by a process of self -regulation.
This is to be seen most clearly in the familiar phenomena of growth. A
plant or animal exists in an environment of which the chemical constitu-
ents (atoms, molecules, or larger particles) are a heterogeneous mass and
dispersed at random. When these particles are drawn into the organism
they lose this randomness and each now comes to occupy a particular
place in the living system. By some means this orderly disposition of new
material into an organized whole is controlled. When death ensues, the
control disappears and the dispersive tendencies of lifeless matter break
down the system. This system is specific and is different in every indi-
vidual. The mass of data now accumulated from studies of regeneration
suggests that all the cells, at least at their beginnings, are totipotent and

452 Morphogenetic Factors

that the basis for the norm of the organism is present in the living stuff
of every cell.

The omnipresence of the developmental norm is suggested by that
quality in development termed by Driesch equifinality, the attainment of
the same developmental goal in very different ways. There is no single
or linear progression of steps by which a structure is formed, but the or-
ganism may shift its course of development according to circumstances.
This is much more difficult to explain than is a linear step-by-step series
of changes, each a precursor of the next. A regulatory mechanism of some
sort must be involved. What gives unity to the individual is not so much
its unchanging genetic constitution, important as this is, but rather this
developmental norm, immanent in the organism from the first and often
reached over different routes.

It should be emphasized that what is involved here is not inherent
adaptability by which an organism naturally reacts in a favorable way to
environmental changes, for a given norm may hinder survival. The "lazy"
mutation in maize, for example, which causes the plant to grow flat on
the ground, would not persist in nature. Most normative reactions of
plants evident today tend to be favorable since they are the ones that
have survived in the winnowing process of natural selection, but the fact
of normativeness has no relation to adaptability.

The self-regulatory character of living things has often been observed
and discussed. In bodily activities it is the basis of the homeostatic re-
actions so evident in physiology. Its most conspicuous manifestations,
however, are structural and are seen in those cases where a portion of an
organism is experimentally isolated from the rest and then proceeds to
restore its missing parts so that a single whole is produced. Each of the
first two cells from a Fucus egg, or the first two blastomeres in a frog
embryo, if isolated, will develop not into half an organism but into a whole
one. Single cells from the epidermis of a plant, under appropriate condi-
tions, will develop into whole individuals. Cuttings restore lost roots.
Missing shoots are replaced by others. Severed vascular strands are united
by the growth of connecting bundles. The literature of plant regeneration
is full of such examples. Many of these were brought together by Ungerer
( 1926 ) , but botanists have in general been less concerned with this prob-
lem than have zoologists. Regeneration is such a dramatic fact that many
attempts have been made to account for it. Actually, however, regenerative
development is no more and no less difficult to explain than normal
development. The real problem is not regeneration but self-regulatory,
normative development.

Many suggestions have been made to explain this central enigma of
morphogenesis, but it must be admitted that none has yet been proposed
which is generally acceptable. The problem is enormously difficult and

Organization 453

doubtless cannot be solved by any simple or single hypothesis. It is essen-
tially one of synthesis, in which evidence from many sources must be
coordinated. For discussions of it the reader is referred to the publications
of Agar (1951), von Bertalanffy (1952), Child (1941), Driesch (1937),
Holmes (1948), Lillie (1945), Meyer (1935), Needham (1936), Reinke
(1922), E. S. Russell (1933), Smuts (1926), Troll (1928), Ungerer
(1926), Wardlaw (1955c), Weiss (1950), Whyte (1954), and Woodger
(1929). Woodger's discussion of the concept of organism (1930, 1931)
is particularly useful.

The position that a biologist assumes toward this problem will usually
be determined more by his attitudes and predilections than by the con-
flicting and inconclusive evidence that is now available. To those who
assume that all organic traits must have been produced by natural selec-
tion, both normal and regenerative development will be regarded as the
result of a long-continued selective process. Holmes (1948) and others
have supported this view, and it is probably held by a majority of biol-
ogists who have considered the matter. Aside from the general presump-
tion in its favor, there is some positive evidence for this position in the
fact that organized, regulatory development is not invariable but some-
times breaks down. There are many examples of this in the various types
of abnormal growth. Sometimes, as in teratological structures, only the
last developmental stages become confused and irregular, but when the
breakdown is more complete, tumors, galls, and other amorphous struc-
tures are produced. Finally, in tissue culture, all traces of multicellular
organization seem to have vanished. There evidently are various levels
of organization, and it is reasonable to suggest that the more complex
ones have gradually evolved from the simpler because of the presumptive
advantages that a highly organized system has.

There are some difficulties with this hypothesis, however. In the break-
down of visible regulation the organizing capacity itself has not been
lost, for such abnormal structures as fasciations may revert to normal
growth again, and in amorphous galls and tissue cultures growing points
may appear which develop into typical plants. Single cells from a tissue
culture may produce normal organisms. There is no necessary connection
between the genetic constitution of the individual (which is what is
presumably modified by natural selection) and the appearance, or lack
of it, of a visible state of organization. Furthermore, it must be remem-
bered that even where gross visible organization has broken down, the
living cells themselves are small organized systems with a complex
though often submicroscopic structure and with a very considerable de-
gree of physiological self -regulation. Indeed, if all organization disappears,
death ensues. Organization seems to be a fundamental quality of living
things, explain it in whatever way we can, rather than a simple trait

454 Morpho genetic Factors

comparable to those upon which natural selection is effective. One cannot
discount the possibility, of course, that in the very beginning this regula-
tory normativeness may have arisen by a selective process and later be-
came established as a general characteristic of all life.

An essential aspect of organization and of the organic forms that result
from it is that these involve much more than a series of successive chemi-
cal steps, for form is concerned with relationships. In an earlier chapter
evidence has been presented that relationships, and thus form, are
genetically determined, but how genes act to produce this trait is far
from clear. An organized system is a complex pattern of such relation-
ships and one that is not static but changes during development and
restores itself if altered. Whatever its origin, the problem still remains as
to how, in terms of protoplasmic activity, such a self-regulating, pat-
terned system is produced.

One of the simplest explanations is that proposed by Child ( 1941 ) and
others who point out that an organized system does not develop unless
a polar axis is first established in originally homogeneous material by the
influence of an environment that differs on the two sides and that a
gradient arises along this axis. The essential importance, at least at the
beginning of development, of an asymmetric environment must not be
forgotten, an environment which, so to speak, "lines up" the undif-
ferentiated egg or mass of tissue in one direction and so orients it that
it can then organize its developmental pattern in an orderly fashion. Grav-
ity and unilateral light are the commonest asymmetric environmental
factors for plants. They make one side of the structure different from
the other and thus begin the continuing process of differentiation. Plants
grown where these factors are uniform on all sides are usually amorphous
(p. 137). The interaction between the polar gradient and the genes of the
organism is an important factor in producing a specific form. For some
biologists this explanation is sufficient to account for organic form, but
it does not give a clear picture of how such interaction works nor does it
explain the complex correlations that occur during development.

Among other suggested explanations one of the most promising is the
concept of a biological "field" in conformity to which development takes
place. Gurwitsch ( 1923 ) assumes such a field to be present around a
developing organic structure, but this is difficult to describe in physical
terms. In Gurwitsch's hands it acquires an almost mystical character and
seems to resemble nothing so much as an astral body immanent in and
around the growing organism. Where such a beautifully precise structure
as a fungus fruiting body molds itself out of a complex and intertwining
tangle of sliding hyphae, or where from a throng of individual myx-
amoebae a specifically fashioned sorocarp develops through their inter-
action, we must assume that in the mass of living stuff there is a formative

Organization 455

factor of some sort, but it should be possible to describe this in more pre-
cise terms than does Gurwitsch.

Fields of various sorts have often been postulated in animal develop-
ment, but in a somewhat more descriptive sense, as the developmental
influence of a given region over structures in it. If the rudiment of a
young and growing amphibian tail, for example, is transplanted at an
early age into the region of a leg it will grow into a leg since it is now in a
leg field. If it is somewhat older before transplanting it will become a
tail, since its own tail field is now operative. This conception of a morpho-
genetic field recognizes the formative influence acting within a given
region or throughout the embryo but offers little explanation of this
action. Fields have been discussed by Weiss (1950), Raven (1943),
and many other experimental embryologists. In botanical morphogenesis
the field concept has been employed by the Snows and Wardlaw to ac-
count for the localized development of lateral structures at the apical
meristem.

More specific is the suggestion of Burr and others (1932) that the
morphogenetic field is a bioelectric one. Burr has found that around a de-
veloping structure, such as a fertilized egg in animals or a developing
ovary primordium in plants, a micropotentiometer will reveal an orderly
pattern of potential differences that is a correlate of the form which will
develop from them. Burr and Northrop (1935) support the view that
the primary entities in nature are fields and not particles and that the
former determine the activities of the latter instead of the other way
around. Both physical and biological phenomena certainly are electrical
in their ultimate nature, but Burr's theory goes much further than that
in assuming the organized biological pattern, manifest to our eyes, to
be the visible expression of an underlying bioelectrical pattern. The ori-
gin of such a pattern and what determines the changes in it are yet un-
known.

One of the difficulties in accounting for an organic pattern is to see how
it can arise in a semifluid and formless protoplasmic system. How, one
asks, can such a flowing and unstable material as protoplasm produce
the very specific forms which come out of it? It is obvious that proto-
plasm, homogeneous though it seems to be, must have a structure of
some sort. The electron microscope is beginning to show what this
structure, at the macromolecular level, actually is (Weiss, 1956; Frey-
Wyssling, 1953). The organized pattern which we see emerging from
living stuff seems to be rooted in these submicroscopic configurations
of molecules. The developmental norm or pattern must in some way be
prefigured in the specific constitution of an organism's protoplasm. The
possibility that there may be a persisting pattern in the cytoplasm is sug-
gested by the work of Tartar (1956) on the ciliate protozoan Stentor,

456 Morpho genetic Factors

where such a pattern is passed from one generation to the next in the
ectoplasmic striping, which is divided between the daughter cells. Tartar
concludes that "it is possible that the complex activities of the cyto-
architecture of stentor may forecast an appreciation that some homologous
cytoplasmic pattern is common to all cells and is as important in its way
as the chromosomal nucleus which also has its orderly arrangements."

How such configurations originate is not clear, but some biologists,
among them Needham (1936), look for suggestions to the paracrystalline
state of matter ( "liquid crystals" ) . The molecular solutes in most solutions
are distributed at random but in some it can be shown that these dis-
solved particles are arranged in a very regular fashion. This may de-
termine such cellular events as differential growth and plane of division
and thus provide a basis for organic orderliness.

A number of workers, among them Baitsell (1940), have gone still
further and endeavor to translate molecular pattern into cellular pattern.
The molecule is a specific and organized structure. Perhaps, so goes the
argument, the forces that pull the atoms together into the orderly con-
figuration shown by a large and complex protein molecule, for example,
are of the same nature as those that bind together a vast number of such
molecules into the system which is a living cell, the unitary structure of
all organisms. On such a hypothesis the cell is to be looked upon as an
enormous molecule. If this concept is carried one step further, the whole
organism might be regarded as a single molecule and integrated by the
same forces that organize simpler ones.

A promising hypothesis has come from Turing (1952), who suggests
that a homogeneous system of substances which react on each other and
are diffusing through a tissue may become unstable because of random
disturbances in it and may thus produce a pattern. Turing analyzes a
hypothetical example mathematically and shows that six different forms
may result from a simple "diffusion-reaction" system of this sort. He seeks
a mechanism by which genes determine structure and suggests that well-
known physical laws, with their mathematical implications for develop-
ment, are enough to account for many of the phenomena of organic
form. Wardlaw (1953a, 1955c) has written a constructive discussion of
Turing's rather involved theory and its applications to morphogenetic
problems in plants.

Rashevsky in a series of papers (1944, 1955, 1958, and others) has
approached the problems of biology from a physical and especially a
mathematical point of view and in particular has endeavored to interpret
biological processes in terms of position and relation.

The problems of growth and form have been discussed by Sir D'Arcy
Thompson in his classic volume by that name (1942) already mentioned
frequently in this book. He marshals evidence from physics, chemistry,

Organization 457

and mathematics in considering such diverse questions of botanical in-
terest as growth, surface-volume relations, size and form, phyllotaxy, cell
shape, least-surface configurations, growing points, spiral growth, and
the theory of transformations in biology. Perhaps his most important
contribution is what seems a very simple one: the demonstration that,
if a given organic form is inscribed in a series of rectangular coordinates,
endless modifications of it may be derived by deforming these coordi-
nates in various ways. This method is particularly useful in evolutionary
studies by showing the progressive changes by which a structure has been
modified. Its significance for development is also important in the
demonstration that change of form is not a localized and particulate
process but that a given form is an integrated pattern and changes as a
whole, so that alterations in one region affect many others. This method
of analysis somewhat resembles that of allometry in expressing relation-
ships mathematically. If allometry could be extended to three dimensions,
as Richards and Kavanagh suggest (1943), it could be used to make a
more precise statement of developmental relations than D'Arcy Thomp-
son has done. By these means the changes in a growing organic form may
be described graphically and expressed in mathematical terms, surely
an important advance; but they provide no clue as to what the proto-
plasmic basis of such a form may be.

In this impasse we grope for clues wherever they may be found. The
science of cybernetics, for example, points to the resemblance between
the giant electronic calculators, with their "feedback" mechanisms, and
the nervous system, in which the brain is continually receiving reports
from the peripheral organs and sending back messages to them. There
well may be more than a curious resemblance between these complex
machines and a living organism, and in seeking to understand biological
organization we should not neglect the feedback principle. The fact
that there is no differentiated nervous system in plants need not mean
that this principle is not operative in them, for in plants the functions of
the nervous system seem to be performed by unspecialized protoplasm.
From other sources which at first seem very unlikely to offer any help
in this problem, clues may come. Information theory, with its systems of
coding, which has been found useful in so many fields, may not be without
significance for problems of development. In living stuff itself there may
perhaps be "coded," so to speak, a mass of data on which the developing
organism may draw and which may even be the basis of the morpho-
genetic norm that has here been discussed.

Since organization exists at other levels than the living organism, sug-
gestions as to the mechanism for it there may come from simpler types of
systems. In Whitehead's philosophy, the concept of organism holds a
key position, from atoms to man. He has called physics the science which

458 Morphogenetic Factors

deals with very small organisms ( atoms and molecules ) and biology the
one which deals with much larger ones. We know that the atom, far from
being simple, is itself a system with many kinds of particles within it,
bound together into a complex whole. Pauli has shown that the basis of
this may reside in the fact that two electrons cannot occupy the same orbit
and that the orbit of one is related to the orbit of another. This fact may
perhaps be regarded as the germ of other organizational relationships
higher in the scale.

In an exploration of the problem of organic form the obvious hypothe-
sis, and the simplest one with which to work, is that there are formative
substances. The quest for these has resulted in a vast deal of useful ex-
perimental work on various "organ-forming substances": chemical com-
pounds that make roots or shoots or flowers; calines, organizers, hor-
mones, growth substances, and other chemical bodies that are supposed to
produce specific structures directly. All such ideas, if carried far enough,
face the serious problem of how it is possible for a substance to become
translated into a form. This was the difficulty on which Spemann's
"organizer" came to grief. Today it seems much more likely that these
various substances, the effects of which undoubtedly result in the pro-
duction of form changes, act rather as evocators, releasers, or triggers
which call forth specific responses by the organized living system.

The problem of organic form seems to be centered in the patterned
character of protoplasmic structure rather than in its specific chemical
constitution. Here are manifest those basic tendencies mentioned at the
beginning of this chapter: polarity, spirality, and symmetry. It will be
noted that almost all the suggested explanations of organic formative-
ness discussed in earlier paragraphs involve physical rather than chemi-
cal factors, relationships rather than substantiveness. To be sure, these
are ultimately not easy to distinguish from each other; but for the im-
mediate future it seems more likely that morphogenesis will find new,
constructive ideas if it explores the many possibilities of biophysics
rather than relying as exclusively on those of biochemistry as it tends to
do today.

The fact is that we have as yet no idea of what the physical basis of
biological organization really is. This problem is closely concerned with
the origin and nature of life. Biochemists and biophysicists are beginning
to make some shrewd guesses as to how simple organic molecules may
have been synthesized in earth's primeval seas and even how such a
complex entity as a virus particle was put together. A knowledge of the
nucleic acids makes it possible to see how genes multiply. What happens
in gene mutation is also fairly well understood. All this has led many to
the optimistic belief that we now know how life originated, how it re-
produces itself, and how it evolves. An essential trait of every living

Organization 459

thing, however— its self-regulatory organization— must still be explained
before we claim that we know what life is. This may well involve princi-
ples, still undiscovered, which are distinctively biological and different
from the presently understood ones of the physical sciences. This is the
position taken by men like Delbruck ( 1949) and Schrodinger ( 1945). The
line between the physical and the biological sciences steadily grows less
distinct, but this does not necessarily mean that biology is simply a
specialized kind of physics and chemistry. Says Prof. Wald ( 1958 ) : "If
biology ever is 'reduced' to chemistry and physics, it will be only because
the latter have grown up to biology. At this point it will be hard to say
which is which."

Here the problem touches deeper questions of philosophy which lead
us away from purely scientific ideas. That biology, and perhaps especially
morphogenesis, is bound to have important philosophical implications
cannot be denied, but these questions are beyond the purpose of the
present discussion. It is important, however, for a student of the life
sciences to remember that back of all the phenomena of genetics, bio-
chemistry, and physiology stands the important fact that a living thing
is an organism, that there is an interrelationship among its parts, which is
manifest in development, and that if this system is disturbed it tends, by
a process of self -regulation, to restore itself. The most evident expression
of this organization is the form of the organism and its structures. Mor-
phogenesis, the study of the origin of form, thus assumes a central posi-
tion in the biological sciences.

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Name Index

Abbe, E. C, 34, 68, 426, 439

Abbe, Lucy B., 41

Abele, K., 31

Abessadze, K. J., 201

Abrams, G. J. von, 377

Acarar, P., 255

Agar, W. E., 453

Aitchison, J. A., 221

Akdik, Sara, 35, 222, 445

Albaum, H. G., 112, 121,240

Alexandrov, W. G., 110, 201, 334

Alexandrova, O. G., 110, 334

Allard, H. A., 164, 314, 320

Allen, C. E., 426, 429, 430, 432

Allen, Ethel K., 295, 407

Allen, G. S., 78

Allen, O. N., 295, 407

Allman, G. J., 118

Allsopp, A., 217, 332, 372

Amelung, E., 32

Amos, J. R., 260

Anderson, E., 41, 110, 419, 426

Anderson, R. E., 273

Anderson, Y. G., 312

Applegate, H. G., 395

Arber, Agnes, 216

Arens, K., 178

Arney, S. E., 321

Arutiunova, N. S., 35

Ashby, E., 33, 38, 98, 103, 201, 212

Askenasy, E., 66

Asseyeva, T., 271

Atchison, Earlene, 408

Audus, L. J., 375

Avakian, A. A., 262

Avers, Charlotte J., 78

Avery, A. G., 59, 89, 270

Avery, G. S., Jr., 19, 30, 31, 39, 86, 90,

187, 253, 309, 375, 379, 381, 383,

392

Baer, D. F., 68

Bailey, I. W., 26, 36, 37, 80, 81, 85, 111,

193, 358
Bailey, P. C, 40
Baillaud, L., 210
Bain, H. F., 245

Baitsell, G. A., 456

Baker, Rosamond S., 53

Ball, E., 69, 70, 72-74, 140, 237, 238

Ball, O. M., 347

Bamford, R., 437

Bannan, M. W., 37, 81-84, 199

Barclay, B. D., 58, 202

Barghoorn, E. S., Jr., 83, 84, 85, 372

Barkley, Grace, 193

Barratt, R. W., 373

Barthelmess, A., 163, 164

Bartlett, H. H., 310

Bartoo, D. R., 203

Basarman, M., 185

Batchelor, L. D., 263

Bateson, W., 271, 428

Bauer, L., 217, 234

Baur, E., 269

Bausor, S. C., 281, 282

Bayly, Isabel L., 81

Beadle, G. W., 42

Beakbane, A. Beryl, 260, 266

Beal, J. M., 406

Beal, W. J., 164

Beatty, A. V., 37

Becker, G., 40, 335

Behnke, Jane, 392

Behre, K., 125, 252

Behrens, Gertrud, 317, 319

Beissner, L., 214

Bellamy, A. W., 231

Benedict, H. M., 38, 212

Benson-Evans, K., 343

Bergamaschi, Maria, 38

Bergann, F., 270

Berge, H., 254

Berger, C. A., 184, 441

Bertalanffy, L. von, 453

Berthold, G., 44

Beyerinck, M. W., 280, 284

Beyerle, R., 121, 256

Biddulph, O., 295

Biddulph, Susan, 295

Biegert, F., 192

Bilhuber, E., 163

Bindloss, Elizabeth, 34

Bissett, I. J. W., 37

Bitters, W. P., 263

527

528

Name Index

Black, L. M., 290
Blackburn, Kathleen B., 429
Blackman, V. H., 16
Blair, D. S., 260
Blake, M. A., 505

Blakeslee, A. F., 59, 89, 185, 221, 222,
270, 272, 273, 296, 430, 437, 440,
446, 447
Blaringhem, L., 279, 282
Blaser, H. W., 91, 271
Bloch, B., 25, 77, 82, 118, 130, 131, 135,
171, 190-193, 197, 218, 219, 240-
242, 277, 282, 403, 404
Blondel, Benigna, 19
Boell, E. J., 73, 74, 140
Bohme, H., 262
Boke, N. H., 65
Bond, G., 197, 311
Bond, T. E. T., 278, 280
Bonner, D. M., 395
Bonner, James, 397, 398, 403, 408, 409,

412
Bonner, John T., 20-22, 224-226, 228,

229, 406
Bonnet, C, 151
Boodle, L. A., 245
Bopp, M., 195
Bordner, J. S., 347
Borgstrom, G., 123, 311, 385
Bormann, J., 250
Borowikow, G. A., 134
Borriss, H., 18, 21, 309, 346
Borthwick, H. A., 282, 308, 314, 322, 366,

397
Bosshatd, H. H., 80
Bouillenne, B., 394
Bouygues, H., 50
Bower, F. O., 360
Boy sen- Jensen, P., 190, 223, 375
Brabec/F., 270
Bradford, F. C, 259
Bradley, Muriel V., 442
Brain, E. D., 40
Brase, K. D., 259, 260
Braun, A., 151, 153
Braun, Armin C, 291-294, 407
Brauner, L., 355
Bravais, A., 151
Bravais, L., 151
Brenchley, Winifred E., 368
Brian, P. W., 410
Briggs, W. B., 187
Brink, B. A., 273
Broadbent, D., 42
Brotherton, W., Jr., 310
Brown, A. B., 404
Brown, J. G., 98
Brown, Nellie A., 290
Brown, B., 21, 29, 41, 42, 68, 78

Brown, W. V., 336

Bruhn, W., 214

Brumfield, B. T., 28, 76, 77, 268

Brush, W. D., 349

Biicher, H., 351, 352

Buchholz, J. T., 110, 206, 235, 236

Budde, H., 33, 111

Bullwinkel, B., 99, 100

Biinning, E., 118, 131, 133, 160, 192, 199,

200, 230, 322, 337, 343, 346, 347, 435
BurgefF, H., 400
Burkholder, P. B., 30, 31, 308, 309, 315,

364, 365, 380, 381, 383
Burns, G. P., 216, 353
Burpee, D., 425
Burr, H. S., 361, 455
Burstrom, H., 40, 41, 341, 412
Bussmann, K., 170, 355
Butler, L., 422
Buvat, B., 68, 232

Cain, S. A., 329

Cajlachjan, M. C, 397

Camefort, H., 68, 159

Camus, G., 72, 219, 405

Carlson, Margery C, 245, 247, 250

Carriere, E. A., 250

Carsner, E., 339

Carter, W., 284, 285

Carvalho, A., 189

Castan, B., 126

Castle, E. S., 21, 149, 165, 166, 310

Chalk, L., 37

Champagnat, P., 101, 387

Champion, H. G., 166

Chan, A. P., 64

Chandler, W. H., 339

Chandraratna, M. F., 432

Chao, Marian D., 18

Chapman, H. W., 320

Charles, D. B., 417

Chattaway, M. Margaret, 37

Chaudri, J. J., 343

Cheng, K. C, 274

Chester, K. S., 261

Cheuvart, C, 221

Child, C. M., 101, 140, 145, 231, 453,
454

Chowdhury, K. A., 86, 201

Christensen, Hilde M., 437

Chrysler, M. A., 237

Chung, C. W., 43

Church, A. H., 151, 153, 159, 163

Clark, H. E., 398

Clark, W. G., 361, 385

Cleland, B., 412

Close, A. W., 321

Clowes, F. A. L., 76-79

Name Index

529

Cockerham, G., 84, 86

Cohen, A. L., 366

Colby, H. L., 259

Collander, R., 221

Collins, J. L., 272

Colquhoun, T. T., 130

Combes, R., 332

Cooper, D. C, 442

Cormack, R. G. H., 86, 190, 312, 404

Correns, C, 233, 428

Coulter, J. M, 237

Courtot, Y., 210

Crafts, A. S., 324

Cramer, P. J. S., 267

Crane, H. L., 106

Crane, M. B., 269

Creighton, Harriet B., 309, 381, 383

Crist, J. W., 97, 274

Crocker, W., 409

Crockett, L. J., 156

Crooks, D. M., 245, 246

Cross, G. L., 439, 440

Crow, W. B., 151

Criiger, H., 193

Cruzado, H. J., 355

Currier, H. B., 324

Curry, G. M., 313

Curtis, J. T., 18, 372

Curtis, O. F., 128

Cutter, Elizabeth, 65, 70, 71

Cutter, V. M., 373

Czaja, A. T., 124, 134, 392

Dadswell, H. E., 37

D'Amato, F., 442, 445

Daniel, L., 261

Darroch, J. G., 426

Darrow, G. M., 282

Darwin, C, 1

Davidson, F. F., 379, 380

Davies, P. A., 367

Davis, E. A., 408

Dawson, R. F., 220

Deats, M. E., 320

De Candolle, Casimir, 151

Delbruck, M., 459

Delisle, A. L., 388

Demerec, M., 273

Denffer, D. von, 390, 398, 399

Denham, H. J., 166, 193

Dermen, H., 89, 271-273, 436

Desch, H. E., 36, 37

Deuber, C. G., 246

Dickson, A. G., 259

Diels, L., 212

Dippel, L., 193

Dobbs, C. G., 85

Dolezal, Ruth, 40

Doorenbos, J., 263, 319

Doposcheg-Uhlar, J., 123, 253

Dopp, W., 399, 400

Dore, J., 248

Dormer, K. J., 103, 164, 221

Dorries-Ruger, Kate, 43

Dostal, R., 104, 139, 233

Douliot, H., 75

Downs, R. J., 322

Doyle, J., 249

Driesch, H., 6, 118, 452, 453

DuBuy, H. G., 256

Duffy, Regina M., 53, 68

Duncan, R. E., 18, 444

East, E. M., 96

Eberhardt, P., 329, 330

Echols, R. M., 37

Eckardt, F., 326

Edgecombe, A. E., 140

Eggers, Virginia, 245, 404

Eichler, A. W., 167

Einset, J., 271, 272, 439

Elliott, J. H., 84

Enghsh, J., Jr., 403

Ensign, M. R., 38

Erickson, R. O., 18, 29, 66, 78

Eriksson, J., 75

Errera, L., 44

Ervin, C. D., 442, 444

Erxleben, H., 489

Esau, Katherine, 26, 78, 157, 158, 195,

204
Esser, M. H. M., 355
Evans, A. W., 234
Ewart, A. J., 39
Eyster, W. H., 425

Farkas, G. L., 326, 327

Felber, Irma M., 100

Felt, E. P., 284

Field, Carol P., 260

Figdor, W., 171, 233, 239

Finch, A. L., 106

Fischnich, O., 124, 391, 395

Fisher, F. J. F., 343

Fisher, J. E., 355

Fisk, Emma L., 68

Fitting, H., 121, 137, 170, 375

Flahault, C, 75

Flaskamper, P., 347, 349

Flemion, Florence, 260

Flugel, Anna, 322, 445

Fortanier, E. J., 313

Foster, A. S., 53, 63, 68, 89, 187-189,

191, 192, 208
Fourcroy, Madeleine, 240

530

Name Index

Frank, A. D., 281

Frank, H., 217

Frankel, R., 265

Franklin, Alicelia H., 35, 439, 440

Fraser, I. M., 379

Frets, G. P., 420

Freund, Y., 124

Freundlich, H. F., 243

Frey-Wyssling, A., 165, 166, 192, 455

Friesner, R. C, 103

Fritz, F., 241

Frohner, W., 493

Fulford, Margaret, 234

Funke, G. L., 40, 314

Furlani, J., 214

Gregory, L. E., 247, 263, 387, 393

Greulach, V. A., 317, 408

Grimball, P. C, 431

Grossenbacher, J. G., 81

Grundmann, E., 41

Guernsey, Frances S., 343, 384, 385, 388

Gulline, Heather F., 261

Gummer, Gertrud, 321

Gunckel, J. E., 65, 159, 189, 295, 377

Gunther, Elisabeth, 270

Gurwitsch, A., 40, 454

Gustafson, F. G., 378

Gustafsson, A., 39, 441

Gutsche, Alice E., 291

Guttenberg, H. von, 76

Galinat, W. C., 317

Galston, A. W., 53, 388, 397, 398

Garcia, C. R., 372

Gardner, C. O., 33

Gardner, F. E., 246, 290

Gardner, V. R., 274

Garner, R. J., 260

Garner, W. W., 314, 315, 320

Garrison, Rhoda, 67, 188

Gauchery, P., 34

Gautheret, R. J., 118, 292, 296, 298, 406

Geiger-Huber, M., 380

Geitler, L., 35, 50, 442, 445

Gemmell, A. R., 234

Gentcheff, G., 441

Georgescu, C. C., 282

Gessner, F., 217

Gibson, R. E., 274

Giese, A. C, 40

Giesenhagen, K., 48, 281

Gifford, E. M., Jr., 67, 68

Girolami, G., 187, 188

Glock, W. S., 85

Gliick, H., 216

Goddard, D. R., 78

Goebel, K., 6, 96, 98, 118, 122-124, 140,

151, 171-174, 190, 206, 209, 213,

230, 233, 239, 249-253, 279, 283,

354
Golub, S. J., 58
Goodwin, R. H., 77, 78, 432
Gordon, S. A., 247, 393
Gotz, O., 255, 321
Gouwentak, Cornelia, 381
Grafl, Ina, 442
Graham, R. J. D., 125
Gratzy-Wardengg, S. A. Elfriede, 121,

222
Gray, W. D., 314, 410
Green, P. B., 41, 166
Gregoire, V., 67
Gregory, F. G., 340, 341

Haag, Liselotte, 199

Haagen-Smit, A. J., 395, 403

Haan, H. de, 417

Haan, I. de, 385

Haberlandt, G., 6, 57, 121, 296, 402

Hackett, D. P., 194

Haddad, S. A., 21

Haeckel, E., 3, 149

Haerdtl, H., 352

Hagemann, A., 124, 249

Halbsguth, W., 170

Hall, W. C, 319, 342

Haller, M. H., 97

Halma, F. F., 260

Hammerling, J., 137, 233, 427, 428

Hammett, F. S., 11,372

Hammond, B. L., 237

Hammond, Dorothy, 209, 210, 419

Hamner, C. L., 395

Hamner, K. C., 315, 396

Hanby, Alice M., 217, 335, 370

Hansel, H., 341, 342

Hanson, H. C., 327, 328

Hanstein, J., 6, 60

Hanszen, A. H., 493

Hara, H., 515

Harder, R., 317, 319, 395-398

Harris, J. A., 96, 107

Harrison, G. J., 406

Harrison, R. G., 118, 148

Hartmann, F., 356

Hartsema, Annie M., 252

Hasitschka, Gertrude, 192, 442, 444, 445

Hatcher, E. S. J., 341

Hatton, R. G., 260

Haupt, W., 262, 319, 343, 384

Hawker, Lilian E., 402

Hawkins, Kate H., 125

Heald, F. D., 234

Hegler, R., 346

Heimsch, C, 19, 204, 427

Heinicke, A. J., 265

Name Index

531

Heinze, P. H., 397

Heitz, E., 137

Hemming, H. G., 410

Hertwig, R., 27

Heslop-Harrison, J., 277, 399

Heslop-Harrison, Y., 399

Heyn, A. N. J., 41, 165, 412

Hibbard, R. P., 347

Hicks, Phyllis A., 140, 367

Hieke, K., 261

Hildebrandt, A. C, 298

Himmel, W. J., 350

Hirmer, M., 151, 163

Hitchcock, A. E., 320, 392, 409

Hoblyn, T. N., 260

Hofler, K., 233

Hofmeister, W., 44, 80, 151, 159

Hofmeyr, J. D., 431

Hofsten, Angelica von, 54

Hofsten, R. von, 54

Holch, A. E., 312

Holdsworth, H., 397

Holle, H. G., 75

Holly, K., 407

Holmes, S. J., 453

Holzer, K., 442

Honeyman, A. J. M., 310

Hough, J. S., 284, 285

Houghtaling, Helen R., 33, 437, 446, 447

Howard, H. W., 262

Howell, M. J., 398

Hoxmeier, Sister Mary C., 221

Huber, R., 327, 334

Huber, H., 380

Huber, P., 82

Hughes, J. G., 343

Hurd, Annie M., 136

Hurd-Karrer, Annie M., 140

Huskins, C. L., 274

Hustede, H., 399

Hutchinson, J. R., 419

Huxley, J. S., 105, 375

Hyvarinen, M. J., 37, 358

Iljin, W. S., 326
Imai, Y., 273, 282, 419
Imamura, S., 354
Imhofe, Rarbara, 271
Irmak, L. R., 34
Isbell, C. L., 247
Iterson, G. van, 160
Iterson, G. van, Jr., 48

Jablonski, J. R., 37
Jaccard, P., 128, 348, 349
Jackson, R. T., 208
Jacobs, M. R., 214, 353, 359

Jacobs, W. P., 79, 99, 100, 131, 141, 204,

242, 384, 394, 404, 405
laffe, L., 136
Jahn, E., 29

Janczewski, E., 75, 78, 171
|anick, J., 431
janse, J. M., 118, 128, 139, 233

Jastreb, M. G., 463

Jenkins, J. M., Jr., 320

Jensen, W. A., 78

Johansen, D. A., 206, 207, 281

Johnson, Retty, 253

Johnson, Elizabeth R., 253, 254, 375, 392

Johnson, M. A., 62, 68

Johnson, T. J., 439, 440

Johnson, V. A., 33

Johnston, E. S., 99

Jones, D. F., 418, 419, 431

Jones, H., 217

Jones, J. Johanna, 103

Jones, K. L., 317

Jorgensen, C. A., 269, 437

Jost, L., 6, 242, 403

Kaan Albest, Anita von, 243

Kaeiser, Margaret, 37

Kane, K. K., 20, 21, 229

Kanna, R., 282

Karper, R. E., 417

Karzel, R., 237

Kaufman, P. R., 407, 408

Kavaljian, L. G., 78

Kavanagh, A. J., 21, 112, 456

Kawahara, H., 515

Kearney, T. H., 101, 419

Keeble, F., 35, 96

Kehr, A. E., 262, 295

Kelly, J., 282

Kelvin, Lord, 53

Kemp, H. J., 426

Kendall, J., 284, 286

Kerl, Irmgaard, 233

Kerns, K. R., 272, 398

Kerr, T., 193

Kienholz, R., 282

Killian, K., 233

King, J. W., 53

Kirschner, R., 493

Kisser, J., 290

Klebs, G., 6, 118, 120, 123, 124, 205, 282

Klein, Deana, 318

Klein, R. M., 291, 293, 294, 296

Klein, W. H., 408

Kleinmann, A., 80

Klieneberger, E., Ill

Knapp, E., 101, 135

Knapp, R., 338

Kniep, H., 135, 233

532

Name Index

Knight, T. A., 353
Knudson, L., 84
Kny, L., 49, 96, 125
Kocher, V., 365
Koepfli, J. B., 412
Kofranek, A. M., 319
Kogl, F., 376
Kohlenbach, H. W., 391
Kohler, F., 400
Kondratenko, F., 341
Konishi, M, 319
Korody, Elisabeth, 62
Kostoff, D., 35, 261, 265, 284, 286, 295
Kostrum, Gertrud, 136
Kowalewska, Z., 250
Krabbe, G., 81
Krafczyk, H., 400
Kramer, P. J., 97, 324
Kranz, G., 214
Kraus, E. J., 290
Kraus, G., 32, 309, 358, 366, 405
Kraybill, H. R., 366
Kreh, W., 355

Krenke, N. P., 210, 211, 266
Kribben, F. J., 399
Kribs, D. A., 36
Krieg, A., 289
Kroll, G. H., 78
Krug, C. A., 189
Kuhn, E., 400
Kuijper, J., 396
Kiinning, H., 86
Kupfer, Elsie, 230, 250
Kupila, Sirkka, 292
Kurosawa, E., 410
Kurtz, E. B., Jr., 210, 211, 428
Kiister, E., 6, 124, 128, 193, 241, 277,
279, 284, 286, 290

Labyak, L. F., 97

Ladefoged, K., 85

Laibach, F., 391, 395, 399

Laing, S., 37

Lai, K. N., 326

Lamb, Barbara, 272

La Motte, C, 126, 127

Lamprecht, H., 425

Lance, A., 65, 156

Lang, A., 316, 322, 341, 398, 411

Lange, F., 89

Larsen, P., 354

La Rue, C. D., 246, 249, 250, 261

Lawton, Elva, 256

League, Elizabeth, 317

Leake, H. M., 419

Lebedincev, Elisabeth, 329

Lebeque, A., 256

Leech, J. H., 65

Lehmann, E., 435

Lehmann, R., 33

Leighty, C. E., 96

Lek, H. A. A. van der, 100, 246, 391

Lemppenau, Christa, 346

Leopold, A. C., 217, 315, 343, 375, 384,

385, 398
Levey, R. H., 20, 21, 229
Levine, M., 290, 291, 294
Lewcock, H. K., 409
Lewis, F. T., 53
Libbert, E., 103, 387, 394
Liernur, A. G. M., 280
Lilleland, O., 98
Lillie, R. S., 453
Lindegren, C. C., 21, 35
Lindemuth, H., 39
Lindstrom, E. W., 421
Link, G. K. K., 245, 291, 293, 294, 296,

404
Linnemann, G., 201
Linser, H., 390

Liverman, J. L., 210, 211, 398, 428
Livingston, B. E., 336
Loeb, J., 118, 254
Lohwag, K., 121
Loiseau, J.-E., 156
Loomis, W. E., 182, 367
Lopriore, G., 237
Lorbeer, G., 35
Love, A., 280, 400, 441
Love, Doris, 280, 400, 441
Love, H. H., 96
Luckwill, L. C., 98, 378
Lund, E. J., 118, 135, 136, 361, 362
Lund, H. A., 378
Lundegardh, H., 125, 312
Lutman, B. F., 37
Lyon, C. B., 372
Lysenko, T., 262

Maas, A. L., 381
McCallum, W. B., 217, 230
McClintock, Barbara, 274
McClintock, J. A., 260
McCready, C. C., 407
MacDaniels, L. H., 128
MacDougal, D. T., 99, 308, 381
McGahan, M. W., 204
Machlis, L., 400
Mcllrath, W. J., 371
McKinney, H. H., 341
McPhee, H. C, 430
McVeigh, Ilda, 255, 256, 364, 365
MacVicar, R., 320, 371
Magness, J. R., 97
Magnus, W., 233, 284
Mahan, R. I., 493

Name Index

533

Maheshwari, Nirmala, 297

Maheshwari, P., 206

Mahlstede, J. P., 245

Makarova, N. A., 372

Malinowski, E., 320

Malins, Marjorie E., 320

Maltzahn, K.-E. von, 34, 65, 106, 210

Mangum, W. K., 365

Mankowski, Z., 372

Mapes, Marion O., 514

Marchal, El., 234

Marchal, Em., 234

Margalef, R., 344

Marquardt, H., 41

Marstrand, E. B., 37

Martin, J. P., 286

Mason, T. G., 102

Massart, J., 123

Masters, M. T., 277

Mather, K., 436

Matzke, E. B., 48, 53, 68, 167

Maule, D., 128, 289

Maximov, N. A., 325, 326

Mears, Kathryn, 514

Meeuse, A. D. J., 48, 83, 198, 199

Mehrlich, F. P., 255

Mehrotra, O. N., 326

Meier, Florence E., 311, 314

Meijknecht, J. C, 114
Melchers, G., 264, 316, 341, 398

Mendes, J. E. T., 189
Mer, fi., 102
Mericle, L. W., 427
Messeri, Albina, 86
Meudt, W., 315
Meves, F., 496
Meyer, A., 453
Meyer, B. S., 324
Meyer, D. E., 240
Michaelis, P., 435
Miehelini, F. J., 66
Michener, H. D., 409
Miehe, H., 133
Miller, C. O., 247, 371, 414
Miller, Helena A., 195, 204
Miller, J. C, 262
Millington, W. F., 68, 296
Mirskaja, Ljuba, 99, 237
Misra, P., 166
Mittmann, G, 435
Mobius, M., 34
Moewus, F., 43, 185, 402
Mohr, H., 137, 313
Mole-Bajer, Jadwiga, 39, 40
Molisch, H., 214
Molliard, M., 284
Monceau, D. du, 118
Moner, J. G, 390
Monschau, M., 442

Montfort, C, 210

Moquin-Tandon, A., 277

Moreland, C. F., 101

Morrow, Dorothy, 33

Morrow, Ielene B., 204

Mothes, K., 261

Miihldorf, A., 26

Muir, W. H., 298

Mullenders, W., 87

MUller, L., 210

Miiller-Stoll, W. R., 132, 135, 263, 329

Munch, E., 104

Miintzing, A., 35, 441, 445

Murneek, A. E., 96, 97, 99, 315, 338, 341,

367, 378
Murray, C. D., 108
Muzik, T. J., 261

Naf, U., 137, 400, 407

Navashin, M., 35, 445, 446

Naylor, A. W., 315, 317, 408

Naylor, E. E., 247, 253, 254, 256

Needham, J., 453, 456

Neeff, F., 81, 128-130, 166, 289

Neel, J., 192

Neilson-Jones, W., 124, 267

Nelson, M. G, 96

Nemec, B., 237, 242

Neurnbergk, E. L., 256

Newcombe, F. G, 346, 349, 351

Newman, A. S., 407

Newman, I. V., 60, 65, 156

Nickell, L. G, 261, 298

Nickerson, W. J., 43, 372

Niedergang-Kamien, Ethel, 384, 385

Nienburg, W., 135-138

Nightingale, G. T., 371

Nilson, E. B., 33

Nitsch, J. P., 210, 211, 297, 378, 388, 389,

428
Njoku, E., 108, 311, 337
Nobecourt, P., 296
Noll, F., 138, 385, 386
Nordhausen, M., 312
Northcott, P. L., 165
Northen, H. T., 413
Northrop, F. S. G, 361, 455
Nutman, P. S., 102, 397
Nysterakis, F., 404

Oehlkers, F., 397
Oehm, G, 34
Oexemann, S. W., 98
Opatowski, I., 355
O'Rourke, F. L., 100
Oserkowsky, J., 384
Ossenbeck, G, 247, 254

534

Owen, F. V., 339

Name Index

Palser, Barbara F., 371

Pandey, K. K., 439

Parke, R. V., 66

Parker, M. W., 308, 314, 366, 397

Parr, T. J., 285

Partanen, C. R., 296

Passmore, Sara G., 98

Pearl, R., 16, 18

Pearsall, W. H., 96, 107-109, 217, 310
335, 370

Pearse, H. L., 392

Pease, D. C, 338

Peebles, R. H., 419

Penfound, W. T., 311, 329

Pennington, L. H., 350

Penzig, J., 277, 282

Petit, J., 317

Pfeffer, W., 118, 123, 170

Pfeiffer, Norma E., 319

Philipson, W. R., 65, 67, 68

Phillips, T. G., 367

Phinney, B. O., 68, 410

Pierce, W. P., 368

Pilet, P.-E., 395

Pilkington, Mary, 69, 237

Pirschle, K., 264

Pirson, H., 35

Plantefol, L., 65, 151, 156, 157

Plateau, J. A. F, 44

Piatt, A. W., 426

Plempel, M., 400

Plett, W., 124, 245

Plumb, G. H., 285

Pohjkallio, O., 320

Pollard, J. K., 72

Polster, H., 368

Pomplitz, R., 177

Pont, J. W., 125

Poole, C. F., 431

Popesco, C. T., 263

Popham, R. A., 64, 68, 76, 156, 204

Popoff, M, 27

Popp, H. W., 309

Potter, G. F, 367

Potzger, J. E., 329

Powers, L., 417

Prakken, R., 274

Prantl, K., 237

Prat, H., 79, 140

Preston, R. D., 165, 166

Preston, S. B., 358

Prevot, P. C, 222, 252

Pridham, A. M. S., 321

Priestley, J. H., 81, 86, 118, 167, 201

244, 245, 310
Purvis, O. N., 315, 341

Quinby, J. R., 417
Quinlan, Mildred S., 228
Quintin, Simonne, 404

Rabideau, G S., 427

Radley, Margaret, 411

Rajhathy, T., 326, 327

Randolph, L. F., 35, 439

Raper, J. R., 401, 402

Raper, K. B., 143, 225, 227, 228

Rappaport, J., 296

Rasdorsky, W., 350, 351, 353

Rashevsky, N., 456

Rathfelder, O., 126, 204

Rauh, W., 245

Raven, C. P., 455

Reed, E., 254

Reed, H. S., 17, 18, 102

Reeve, R. M., 62, 65

Reiche, Hildegard, 402

Reid, Mary E., 37, 367, 373

Reinders-Gouwentak, Cornelia A., 221

Reinert, J., 298

Reinke, J., 63, 453

Reith, W. S., 21, 78

Renner, O., 217

Rettig, H., 329

Reuter, Lotte, 436

Richards, F J., 151, 161-163

Richards, O. W., 21, 112, 456

Richardson, S. D., 97

Rick, C. M., 265

Rickett, H. W., 234

Rickless, P., 41

Riehm, E., 102

Rietsma, J., 19, 222

Riker, A. J., 291,292, 298

Riley, H. P., 33

Rink, W., 234

Rippel, A., 329

Robbelen, G, 208

Robbins, W. J., 214, 217, 296

Robbins, W. R., 371

Roberts, R. H., 86, 97, 205, 260, 266, 315

341, 390
Robertson, T. B., 16, 17
Robinson, E., 21, 42, 78
Rodriguez, A. G, 409
Rogers, W. S., 260, 266
Romeike, A., 261

Ropp, R. S. de, 291, 292, 296, 298
Rosa, J. T., 431
Rosene, Hilda F., 362
Rosenwinge, L. K., 136
Rosier, P., 89
Ross, H., 284
Ross, I. K., 523
Roth, Ingrid, 91, 187

Name Index

535

Rouffa, A. S., 65
Roux, W.,3, 118
Riibel, E., 333
Riidiger, W., 53, 440
Ruge, U., 247
Russell, E. S., 453

Sacher, J. A., 188

Sachs, J., 6, 32, 44, 57, 63, 118, 221, 282,
391

Sagromsky, Herta, 192, 199, 200

Sahni, R., 209

Salisbury, E. J., 325

Salisbury, F. R., 398

Samuels, E. W., 259

Sanio, K., 30, 36

Sankewitsch, E., 295

Satina, Sophie, 59, 89, 185, 221, 222, 270,
272, 273, 296

Sax, Hally J., 35

Sax, K., 141, 260

Sax, Katherine R., 29

Sehaffalitsky de Muckadell, M., 209

Sehaffner, J. H., 317, 318, 430

Schander, H., 98

Schechter, V., 134

Scheibe, A., 432
Schenck, H., 281, 282
Schermerhorn, L. C, 371
Schilling, E., 290
Schimper, C. F., 151, 153
Schkwamikow, P. K., 445, 446
Schleiden, M. J., 23
Schlenker, C, 435
Schlbsser, L.-A., 335
Schmidt, A., 61, 62, 66
Schmitt, F. O., 433
Schneider, E., 359
Schoch-Rodmer, Helen, 82
Schopfer, W. H., 373
Schoser, G., 232
Schoute, J. C, 61, 151, 160, 281
Schramm, R., 208, 312
Schrank, A. R., 361, 385
Schratz, E., 33, 111
Schrodinger, E., 459
Schroeder, C. A., 33, 164
Schroter, H.-R., 261
Schiiepp, O., 63, 78, 112, 187, 359
Schulman, E., 86
Schumacher, F. X., 97
Schumacher, W., 141
Schwabe, W. W., 315, 322, 341
Schwanitz, F., 35
Schwarz, W., 89, 249, 351
Schwarzenbach, F. H., 320
Schwendener, S., 6, 151, 159, 345
Scott, D. R. M., 358

Scott, Lorna I., 86, 201

Scully, N. J., 317, 366

Seeliger, R., 215

Sensarma, P., Ill

Setchell, W. A., 233

Shaffer, R. M., 223, 228

Shank, D. R., 97

Sharman, R. C, 67

Shepard, H. R., 36

Shields, Lora M., 327, 365

Shirley, H. L., 309

Shull, G. H., 419, 428, 429

Sierp, H., 34

Sifton, H. R., 68

Silberschmidt, K., 261

Silow, R. A., 419

Simak, M., 98

Simon, S., 123, 131, 237, 241, 242

Simon, S. V., 141, 249, 261

Simonis, W., 329

Simons, R. K., 329

Singleton, W. R., 418, 425

Sinnott, E. W., 17, 20, 25, 27, 29, 31, 33,
35, 51, 77, 82, 106, 107, 110-112,
131, 142, 193, 197, 242, 356, 417,
418, 420, 421, 423, 437, 439, 446
Sinoto, Y., 34
Sirks, M. J., 282
Sitton, R. G., 259
Skok, J., 317
Skoog, F., 37, 247, 369, 371, 375, 384-

386, 407, 414
Smirnov, E., 311
Smith, E. F., 291
Smith, H. R., 39

Smith, H. H., 295, 417, 420, 437
Smith, Harriet E., 437
Smith, Joan, 514
Smith, K. M., 285
Smith, W. H., 33
Smith, W. K., 263
Smuts, J. C, 453

Snow, Mary, 69, 101, 151, 160, 161, 187
Snow, R., 69, 96, 101, 104, 151, 155, 160,

161, 163, 187, 381, 382, 386
Soding, H., 86, 327, 375, 381
Solereder, H., 280
Soltys, A., 403
Sommer, Anna L., 370
Sorauer, P., 288
Sorokin, Helen, 194, 370
Sorokin, S., 72, 204
Sossountzov, I., 372
Soueges, R., 206
Southwick, L., 265
Sparrow, A. H., 295
Spoerl, E., 291
Sprague, G. F., 419
Springer, Eva, 234

536

Name Index

Springorum, Brigitte, 398

Sproston, T., 338

Spurr, A. R., 65, 195

Spurr, S. H., 37, 358, 370, 371

Stafford, Helen J., 19

Stahl, E., 137

Stanfield, J. F., 221, 368

Stant, Margaret Y., 65

Starling, E. H., 375

Stebbins, G. L., Jr., 440, 441

Steeves, T. A., 71, 187, 188, 296, 297

Steffen, K., 445

Steil, W. N., 256

Stein, Emmy, 264, 432

Stein, O. L., 427

Steinberg, R. A., 343

Steinecke, F., 139

Stephens, S. G., 210, 419, 426

Stepka, W., 77, 78

Sterling, C, 159

Stevenson, E. C, 431

Steward, F. C, 51, 72, 75, 298

Stewart, K. D., 37

Stewart, L. B., 125

Stewart, W. N., 132

Stiefel, S., 346

Stingl, G., 237, 248

Stocking, C. R., 324

Stolwijk, J. A. J., 313, 314

Stonier, T., 291, 292, 407

Stoudt, H. N., 254, 255

Stout, G. J., 97

Stout, M., 339

Stoutemyer, V. T., 321

Stowe, B. B., 411

Strasburger, E., 6, 25, 29, 193, 256, 280

Straub, J., 40, 314

Street, H. E., 390

Struckmeyer, B. Esther, 97, 205, 320, 341,

371
Strugger, S., 165
Sunderland, N., 68
Surface, F. M., 500
Sussex, I. M., 71, 175, 188, 296, 297
Sussman, M., 223, 227, 228
Swamy, B. G. L., 127
Swarbrick, T., 259, 260
Swingle, C. F., 118, 244
Swingle, W. T., 267, 406

Takashima, R. H., 354
Talbert, Charlotte M., 312
Tammes, Tine, 107
Tandan, K. N., 86
Tartar, V., 433, 455
Tatum, E. L., 373
Tellefsen, Marjorie A., 38
Tenopyr, Lillian A., 53

Teodoresco, E. C, 313

Terby, Jeanne, 138

Teubner, F. G., 342

Thennan, Eeva, 292

Thimann, K. V., 21, 40, 96, 103, 118, 375,

377, 383, 386, 387, 392, 412, 414
Thomas, J. B., 361
Thompson, D'Arcy W., 18, 44, 45-47,

148, 151, 156, 180, 424, 456
Thompson, H. C, 341
Thompson, J. F., 72
Thompson, M. T., 284
Thomson, Betty F., 311
Thurlow, J., 398
Tieghem, P. van, 6, 75, 201, 245
Timmermann, G, 199
Timofeev, A. S., 110, 334
Ting, Y. C, 262
Tingley, Mary A., 140
Tischler, G., 26, 35
Titman, P. W., 189
Tobler, F., 134, 370
Tobler, Margarete, 437
Torrey, J. G., 79, 204, 221, 237, 298, 314,

394
Townsend, C. O., 291
Townsend, G. F., 35
Transeau, E. N., 38
Trecul, A., 124
Troll, W., 453

Trombetta, Vivian V., 28, 29, 111
Truscott, F. H., 237
Tschermak-Woess, Elisabeth, 40, 192,

442-445
Tsui, C, 407

Tukey, H. B., 18, 99, 259, 260
Tukey, L. D., 19, 343
Tulecke, W., 298
Tupper-Carey, Rose M., 128
Turing, A. M., 456

Ullrich, J., 33
Umrath, K., 185, 186, 403
Ungerer, E., 452, 453
Uphof, J. C. T., 419
Ursprung, A., 124

Van Fleet, D. S., 197, 222

Van Overbeek, J., 247, 355, 377, 387,

390, 393, 398
Vardar, Y., 255
Vasart, B., 379
Veale, J. A., 387
Veen, J. H. van der, 221
Venning, F. D., 197, 353, 368
Vince, Daphne, 313
Vischer, W., 216

Name Index

537

Vlitos, A. J., 315

Vochting, H., 6, 118-121, 127-130, 177,

217, 241, 244, 348, 352
Von Schrenk, H., 288

Wagenbreth, D., 265
Wagner, N., 26, 27, 40, 77
Wain, R. L., 375, 412
Wakanker, S. M., 98
Wakker, J. H., 139
Wald, G., 459
Walker, Rona, 261
Wallace, R. H., 288
Wallace, T., 368
Walp, L., 372
Walsh, J. P. de C, 37
Walter, H., 324

Wangermann, Elisabeth, 33, 38, 210
Wanner, H., 140
Ward, M, 102

Wardlaw, C. W., 68-72, 74, 151, 156,
160, 187, 206, 218, 222, 238, 239:
453, 456
Wardrop, A. B., 37, 357

Wareing, P. F., 86, 201, 322

Warmke, Germaine L., 124, 125, 393

Warmke, H. E., 124, 125, 393, 430

Wassink, E. C., 313, 314

Waterbury, Elizabeth, 260

Watson, D. P., 245

Way, D. W., 247

Weaver, H. L., 427

Webber, J. M., 256

Weber, Friedl, 223

Wehnelt, B., 402

Weide, A., 232

Weier, T. E., 194

Weiss, F. E., 267

Weiss, P., 433, 453, 455

Weissenbock, K., 233

Wellensiek, S. J., 263

Wenck, Ursula, 389, 390, 395

Went, F. W., 118, 129, 141, 210, 211,
337, 338, 361. 375, 376, 384, 385,
391, 394, 395, 396. 428

Werner, O., 334

Wershing, H. F., 358

Westerdijk, Johanna, 121

Westergaard, M., 430

Westphal, Maria, 319

Wetmore, R. H., 57, 58, 67, 69, 72, 73,
102, 111, 159, 189, 204, 219, 222,
297, 405

Wetter, C., 126

Wettstein, D. von, 137

Wettstein, F. von, 35, 234, 264, 435, 437

Whaley, C. Y., 427

Whaley, W. G., 20, 65, 419, 427

Whalley, Barbara E., 82

Whitaker, D. M., 135, 136

White, D.J. B., 110,333

White, O. E., 281, 282, 426

White, P. R., 292-294, 296

Whyte, L. L., 453

Whyte, R. O., 341

Wiedersheim, W., 347

Wiersum, L. K., 396

Wiesner, J., 124, 171, 174, 354, 355

Wightman, F., 42, 375, 412

Wifcoxon, W. F., 375, 391

Wildt, W., 348

Williams, B. C, 76, 77

Williams, S., 248

Wilson, C. M., 223, 228

Wilson, G. E., 274

Wilson, K., 132

Wilson, Katherine S., 262

Wilton, Ocra C., 86

Winkler, H., 6, 102, 118, 138, 233, 239,
248, 253, 266, 268

Winton, Dorothea de, 110

Wipf, Louise, 442

Withner, C. L., Jr., 262

Withrow, Alice P., 396

Withrow, R. B., 396

Witkus, E. R., 184

Witsch, H. von, 317, 322, 396, 445

Wittwer, S. H., 342, 398

Wolf, F. A., 19

Wolterek, Use, 216

Woodford, E. K., 407

Woodger, J. H., 453

Worsdell, W. C., 277-279

Woyciki, S., 214

Wright, C., 151, 152

Wulff, E., 121

Yamaki, T., 411

Yampolsky, C, 263, 400, 430

Yapp, R. H., 325

Yarbrough, J. A., 251, 254-256

Yarwood, C. E., 248

Yates, Ruth C., 372

Young, B. S., 204

Young, H. E., 97

Young, J. O., 18

Zalenski, V., 40, 325

Zeeuw, D. de, 217, 398

Zeller, O., 185

Zepf, E., 191

Zhelochovtsev, A. N., 311

Zimmerman, P. W., 271, 320, 375, 391,

392, 395, 409
Zimmermann, W., 121, 139, 233

Subject Index

Abies, 189

Abnormal growth, 275-299

amorphous structures in, 287

distinguished from pathological, 277

morphogenetic significance, 299

new structures produced by, 283

of organs, 277

produced by growth substances, 290

two concepts, 276
Abscission, stimulation and inhibition,

405
Absolute size, morphogenetic effects, 359
Acacia, 206, 209
Acalypha, 128
Acer, 84, 109, 129
Acetabularia, 136, 233, 427

nuclear control in, 427

polarity in, 137

regeneration in, 233
Achimenes, 124, 249, 253
Achlya, 400
Acrasiaceae, morphogenetic significance,

223
Acrasin, 223

effect on aggregation, 406
Actinomorphic flowers, 175
Adaptation not inherent in organization,

452
Adenine, and bud formation, 247

and leaf formation, 396
Adventitious buds, on leaves, 245

on roots, 245

on shoots, 251

and vascular development, 72
Agaricus, growth of sporophore in, 228,

229
Aggregation in Acrasiaceae, 223
Aging, significance in morphogenesis,

210
Agrobacterium, 291
Alkaloids, passage across graft, 261
Allium, 78, 107
Allometric constants, segregation, 113,

423
Allometry, 105
Allomyces, 400

Allopolyploidy and evolution, 441
Ambrosia, 317

Amino acids, in meristematic region, 72

in prothallial development, 372
Ampelopsis, 125
Amphibious plants, 216
Amphigastria, 171
Amphitropy, 171
Anacharis, 68
Anadendrum, 209

Anatomical coefficients and drought re-
sistance, 326
Angiosperms, shoot meristem in, 68
Angle meristem in Selaginella, 248
Animal hormones, effect on sex in plants,

400
Anisophylly, 171, 354

factors in, 171

habitual, 172

role of gravity in, 354
Annual rings, factors determining, 85

use in studying past, 86
Anomalous secondary growth, 87
Antheridium-forming substance in ferns.

400
Antiauxins, 408
Antirrhinum, 264, 282
Apical cell, 56

angiosperm root, 76

angiosperm shoot, 60, 65

fern leaves, 89, 187, 238

lower plants, 56, 75
Apical dome in shoot meristem, 60

cell relations in, 68

shape, 67
Apical meristem, determination of stelar
structure by, 72

development in embryo, 78

organization, 59

root, 75-79

self-determining region, 238

shoot, 59-68
Apogamy, 256
Apospory, 256
Aquilegia, 41, 426
Araucaria, 189, 214, 404
Aristolochia, 247
Aster, 358, 387, 388
Asymmetry, 173
Atropa, 261

538

Subject Index

539

Attraction center, 98, 140
Autocatalysis in growth, 16
Auxin, 376

in apical dominance, 387

in apical meristems, 72

in cambial activity, 381

in cell division, 381

in cell enlargement, 379

and cell wall changes, 404, 412

in crown gall, 407

in differentiation of vascular tissues,
72, 219, 405

and dorsiventrality, 391

in growth of fruits, 378

in growth correlations, 390

polar flow, 385

and protoplasmic viscosity, 413

in rhizoid formation, 394

in root growth, 78, 246, 391

in shoots of Ginkgo, 378

stimulatory effects, 388

transverse polarity in flow, 384

and tropisms, 380

use of term, 376

various effects, 377

in vein development, 395

and water uptake, 412
Auxin-auxin balance, 405
Auxin-kinetin interactions, 414
Available free space in phyllotaxy, 160
Avena, 31, 99, 141
Axiation in polarity, 144
Axillary buds, development, 67
Axis, polar, 116

Balance between parts in growth, 104
Begonia, 123, 147, 174, 192, 249, 252,

255
Bending, formative effects, 351
Benzimidazole and cell shape, 53
Bijugate spirals in phyllotaxy, 163
Bioelectric factors, in morphogenesis, 360

in polar flow of auxin, 361
Bioelectric fields, 362

and developmental patterns, 361

in organization, 455
Biological organization, 2
Biota, 214

Boron, role in development, 371
Bouvardia, 271

Brachysclereids, differentiation, 218
Brassica, 250

Bryonia, 110,334,428,429
Bryophyllum, 240, 247, 254, 321
Bryopsis, 138, 139, 169, 179, 233, 394
Bryum, 437
Buds, adventitious, 72

axillary, 188

Bulbils, 256

Bundle sheath, effect of wounding, 219

Burdo, 269

Bursa, 419

Byrnesia, 255

Calcium, role in development, 369

Calendula, 398

Calines, suggested roles, 376

Callithamnion, 232

Callitriche, 217

Callus, 244, 288

meristems formed in, 289
produced by growth substances, 290
Cambial cells, division, 80
polarity, 130
regulation of size in, 81
Cambial growth, and auxin, 86
differentiation in, 198
ratio, at fork, 87
seasonal changes in, 86
Cambium, 79-88
cork, 87

in herbaceous and woody stems, 86
physiology, 86
vascular, 79
Campanula, 217
Camptosorus, 256
Camptotrophism, 351
Candida, 372

Cannabis, 221, 317, 399, 400, 430
Carbohydrate-nitrogen ratio, 366
effect, on flowering, 366
on root growth, 79
on root-shoot ratio, 367
Carbon monoxide and root formation, 409
Cardamine, 251
Carica, 431
Carnegiea, 282
Cartesian diver technique, use in meri-

stem studies, 73
Casuarina, 130
Cataphylls, 188

Caulerpa, 104, 138, 139, 170, 233, 434
Caulocaline, 396
Causal morphology, 3
Cecidomyia, 280
Cell and organism, relations, 24
Cell division, 25-29
and cell size, 27
in culture, 51
differential, 192
duration, 30
experimental studies, 37
in fruit shape, 51
genetic factors in, 42
in living root tips, 77
rate, 28, 29, 41, 42

540

Subject Index

Cell lineage, 58

Cell multiplication in culture, 75
Cell number, methods for measuring, 28
orientation, 51
periodicity, 78
plane, 43-52
plate, 43
Cell shape, 52-54
ideal, 53

in leaves of different shapes, 53
at meristem, 53
Cell size, 29-37

in developing fruits, 33
in dwarfs, 34
effect of water on, 40
factors determining, 30, 37-40
genetic factors, 34, 437
inheritance, 418
in lower plants, 35
and organ size, 32
and position, 35
rate of increase in, 33
Cell theory as unifying concept, 23
Cell wall, fibrillar angle in, 37
growth, 41
plasticity, 41
polarity in, 132
in xylem, changes in, 85
Cellular basis of growth, 23-54
Cellular differences, origin, 189
Celosia, 282
Celtis, 285
Centradenia, 173
Cercidiphyllum, 189
Chamaecyparis, 210, 214
Chara, 149, 150, 203
Chemical elements, morphogenetic effects,

364
Chemical factors in morphogenesis, 363-

373
Chemical organization of shoot apex, 73
Chimeras, 266-272
mericlinal, 267
mixed, 267
periclinal, 61, 89, 268
breeding behavior, 269
complex chromosome situation in,

269
from Datura polyploids, 268
morphogenetic importance, 270
from tomato-nightshade grafts, 268
use in determining tissue origin, 272
in various cultivated fruits, 271
in vegetatively propagated plants,
271
sectorial, 267
Chitin molecules, angles, 165
Chlamydomonas, 402
Chondromyces, 228

Chromatography, use in meristem analy-
sis, 72
Chromosomes, 436-447
accessory, 35, 445

as morphogenetic factors, 436

number and cell size, 437

and sex^ determination in plants, 429

volume and cell size, 35, 445
Chrysanthemum, 156, 315, 319, 341
Cichorium, 405
Citrus, 164, 256
Cladonia, 170

Cladophora, 133, 134, 145, 232
Classification, natural, 1
Cleavage, 12

Cobalt, role in development, 371
Coelebogyne, 256
Coffea, 189
Colchicine, use in induction of polyploidy,

436
Coleus, 60, 65, 99, 126
Columnea, 173

Compression, formative effects, 350
Compression wood, 356
Connation in fasciation, 281
Control, evidence in growth, 95
Conversion of petiole to stem, 248
Coordination in development, 2
Coprinus, 21, 233, 346
Cork cambium, 87

origin in old tissue, 88
Cornus, 313
Corpus in meristem, 62
Correlation, 38, 95-115

compensatory, 98, 244

between dimensions, 111

in dwarf trees, 97

of embryo with maternal tissue, 99

genetic, 96, 104-115

inhibitory, 101

nutritional, 96

of part to whole, 105

between parts, 97, 107

physiological, 96-104

of position, 102

stimulatory, 100
Correlative inhibition, 39, 103
Corylus, 282
Cosmos, 398
Crassula, 255

Crataego-mespilus, 268, 270
Crataegus, 268
Crepis, 76, 445, 446
Crown gall, 291

absence of bacteria from, 293

cancer-like character, 295

capacity for autonomous growth, 292

conditioning phase, 293

induction phase, 294

Subject Index

541

Crown gall, permanent change in cells,
292

promotion phase, 294

secondary tumors in, 292

steps in development, 293
Cucumis, 249, 442

Cucurbita, 34, 41, 106, 210, 263, 421
Cuscuta, 397

Cybernetics and organization, 457
Cycas, 250
Cyclamen, 239, 245
Cyclophysis, 215

Cynipid wasps as gall inducers, 283
Cystosira, 135
Cytisus-laburnum, 268
Cytonuclear ratio, 27

Cytoplasm as morphogenetic factor, 433-
436

cell wall pattern, 433

dehydration, 40

in differentiation, 434

macromolecular patterns, 433

in reciprocal crosses, 435

structure, 49

unequal distribution at division, 435
Cytoplasmic pattern in development,

456
Cytoplasmic viscosity, 39

Dacrydium, 213

Dactylis, 325

Dasycladus, 233

Datura, 89, 222, 261, 270, 273, 296, 440,

446
Dedifferentiation, 181, 232
Dehydration of cytoplasm, 40
Delphinium, 273, 282
Deoxyribonucleic acid, 41, 165, 294, 416
Dermatogen, 60

Determinate structures, growth, 88-91
Development, contrasted with growth, 11

self-regulation in, 452
Developmental changes, progressive, 209
Dictyostele, 72
Dictyostelium, 143, 178, 226, 365, 406

mutants in, 227
Didymium, 314
Differentiation, 181-229

in Acrasiaceae, 223

at apices, 203

brachysclereids, 218

in cambial region, 84, 198

in cell lineage, 203

in cell size, 192

cell wall, 193

in cells, induced by others, 192

complex patterns, 202

cytoplasmic pattern in, 193

Differentiation, and development, 181,
202

in distribution of nucleic acids, 222

dormant primordia, 245

endodermis, 196

in external structure, 184-189

fiber patterns, 197

gametophyte from sporophyte, 185

and gradients, 218, 222

and growth, contrasted, 182
relative rates, 183

without growth, 223-229

growth substances in, 189, 219

histochemical, 197, 222

histological pattern, 195

in internal structure, 189-204

intracellular, 194

in Myxobacteriaceae, 228

during ontogeny, 205-215

origin, 186

in osmotic concentration, 222

physiological, 220-223

and polarity, 190

and position, 193

primordia at meristem, 187

in pseudoplasmodium, 224

in relation to environment, 215-220

between root and shoot, 220

between sexes, 185

between staminate and pistillate plants,
221

stomata, 199

in synthesis of alkaloids, 220

vascular tissue at apices, 204

between vegetative and reproductive
phases, 184, 205

veins, 198

vessels, 201

wall relationships in, 195

and water gradient, 218
Diffusion-reaction system of Turing, 456
Digitalis, 176, 283, 425
Dioecious form, origin in maize, 431
Dionaea, 345
Dioscorea, 123, 429

Diploid gametophyte, origin from sporo-
phyte, 234, 437
Divergence angles in polypeptid chains,

166
DNA, 41, 165, 294, 416
Dominance of apical bud, 101, 386

role in, of auxin, 386
of nutrients, 387
Dormancy and temperature, 339
Dorsiventrality, 170-178

in flowers, 175

and gravity, 176, 354

internal structures, 174

in leaves, 175

542

Subject Index

Dorsiventrality, physiological, 178

reversibility, 170

in roots, 170

in shoots, 171

in thalli, 170
Double-worked trees, 258
Drosera, 125, 249, 252
Drosophila, 429, 431, 442
Drought resistance, 326
Dryopteris, 69, 70, 72
Dwarfs, 260

genetic, 418

from immature seeds, 260

produced, by bark inversion, 259
by grafting, 259

Efficiency index, 16
Elaters, differentiation, 191
Electrodynamic fields, 361
Eleocharis, 246
Elodea, 65, 68
Embryo culture, 4
Embryology of plants, 206
Enation, 65, 280
Endogenous rhythm, 18, 322
Endomitosis, 442
Endophyllum, 395
Enter omorpha, 135
Entwicklungsmechanik, 3
Environment, and external differentiation,
215

and internal differentiation, 217

role in morphogenesis, 451
Epilobium, 160, 176, 435
Equifinality, 452
Equisetum, 58, 137, 179, 203
Eriophyces, 279, 280
Ethylene, and flower induction, 409

and root formation, 409
Etiolation, 309

causes, 310

and cell size, 40

in fungi, 310

structural changes in, 310
Eucalyptus, 206, 209
Evolution, 1
Exotrophy, 174
Experimental morphology, 3
Experimental studies, on cells, 37-43

on shoot apex, 68-75

Fagus, 77
Faciation, 280

inheritance, 282

origin, 281
Fibonacci series in phyllotaxy, 152
Ficaria, 107

Field, bioelectrical, 455

biological, 454

concept, 454
Florigen, 376, 397
Flowering, all-or-none reaction, 398

induction, by growth substances, 398
by low temperature, 341
by photoperiod, 315
Flowering stimulus, in host-parasite rela-
tionship, 397

nonspecificity, 398

transmitted by grafting, 262, 397
Foliar embryos, 127, 250

factors in growth, 254
Foliar helices, 156
Fontinalis, 151, 203
Form, organic, 1, 117, 449

and cell division, 52
Formativeness inherent in organisms, 425
Fractional series, in genetic spiral, 152

in parastichies, 155
Fragaria, 430
Fraxinus, 280
Friesia, 176
Fucus, 4, 50, 56, 117, 121, 135-137, 145,

169, 178, 233, 372
Funaria, 137
Functional stimulus, 110
Funkia, 256
Fusiform initials, 80

Gall stimulus, specificity, 285
Galls, 277-295

amorphous, caused by parasites, 290

cataplasmatic, 291

insect, 283
histology, 284

organoid, 279

prosoplasmatic, 283

artificial production, 285
Gametophytes, aposporous, 256
Gametophytic characters, inheritance, 426
Gases, morphogenetic effects, 409
Gaylussacia, 329
Gemmipary, 250
Gene action in development, 415
Gene effects transmitted by grafting, 264
Generative center in Plantefol's theory,

156
Genes, 415-433

"compound," 419

controlling growth relationships, 416,
421, 451

and duration of growth, 417

and environment, relation between, 451

as evocators, 425

and form, 418, 425

geometric effect, 417

Subject Index

543

Genes, governing shape, evidence for, 419

in photoperiodism, 432

and rate of growth, 417

and sex, 428

for shape linked with others, 421
Genetic constitution as factor in organiza-
tion, 450
Genetic factors, in morphogenesis, 415-
447

relation to environment, 305
Genetic reserve in meristematic cells, 232
Genetic segregation of allometric con-
stants, 423
Genie balance, 446
Georgia, 234
Geotrophism, 352
Germ layers in plants, theory, 59
Gibberella, 410
Gibberellin, 37, 376, 409

differences from auxin, 411

effect on dwarf plants, 410

morphogenetic effects, 410

and stem elongation, 410
Ginkgo, 159, 189, 237, 378
Gleditsia, 91
Gleichenia, 238
Gmelina, 201
Golden mean, 153, 156
Gradients, in cell size, 326

as components of organization, 450

histological, 140

metabolic, 73, 140
Graft hybrids, 268
Grafting, of bud into callus, 72

as morphogenetic technique, 258
Grafts, between male and female plants,
263

between tomato and tobacco, 261
Gravity, 354

and dorsiventrality, 355

effect, on growth, 354
on mitosis, 40

and flowering, 355

formative effects, 354

influence on other factors, 355
Griffithsia, 134, 233
Group effect in Fucus eggs, 136
Growth, 11-22

analysis, 13

cellular basis, 23-54

curve, sigmoid, 13

definition, 11

determinate, 19, 88

differential, 112

and differentiation, 182

direction, 51

distribution, 21

duration, 20

exponential, 15

Growth, of gourd fruits, 12

indeterminate, 19

physiology, 21

rate, 15, 20

relative, 105

and size, 20

variation in, 18
Growth substances, 374-414

in abscission, 404

in callus formation, 290, 393

in correlation, 383

in determination of structure, 390

differential movement, 384

in dominance and inhibition, 386

effects, on cells, 37

on genetic dwarfs, 377
various anatomical, 405

in flower development, 396

in growth stimulation, 386

in internal differentiation, 404

in leaf development, 394

mechanism of action, 411

minimal structural requirements for,
412

other terms for, 374

in plant growth, 377

polar transport, 384

in root development, 391

and root nodules, 407

in sex determination, 399

in stem development, 395

synthetic compounds as, 374

types, 376
Guttulina, 366
Guttulinopsis, 366

Gymnosperms, shoot meristem in, 68
Gynophore, intercalary meristem in, 79

Haploid sporophytes, 437
Hedera, 125, 179, 213, 217, 263
Helianthus, 311
Helleborus, 346
Heterauxesis, 105
Heteroblastic development, 206
Heterogony, 105
Heterophylly, 216
Heterosis and cell size, 35
Hibiscus, 393
Histogens, in root meristem, 75

in shoot meristem, 60
Hofmeister's rule, in cell division, 44, 80

in phyllotaxy, 159
Homeosis, 110
Homeostasis, 2, 452
Homoblastic development, 206
Hormone, use of term, 375
Horseradish roots, regeneration in, 248
Humulus, 430

544

Subject Index

Hyacinthus, 256

Hydrostatic pressure, effect on structure,

335
Hyoscyamus, 263, 264, 313, 322, 397,

411, 432
Hyperplasia of tissues, 288
Hypertrophy of tissues, 288
Hyponasty as effect of growth substances,

393

Ideal angle in phyllotaxy, 152, 155

Idioblasts, origin, 192

Impatiens, 151

Incompatibility between stock and scion,

260, 263
Individual in plants, 24
Indoleacetic acid ( I AA ) , 376
Information theory and organization, 457
Inheritance, cell size, 418

dimensions, 424

dwarf habit, 418

gametophytic characters, 426

pattern, 423

shape, 419
Inhibition, of buds, 387

of one primordium by another, 160

and stimulation in physiology, 103
Initiator cells in Acrasiaceae, 223
Intrusive growth, 82
Intumescences, 288
Ipomoea, 38, 107, 210, 262, 311, 321,

337
Iresine, 261
Iris, 33, 169, 175, 355
Isoetes, 126, 132, 171

Juncus, 279

June drop of fruit caused by auxin, 98

Jussiaea, 250

Juvenile stages, 205, 206

adapted to special environments, 217

and recapitulation, 209

reversal by gibberellic acid, 214

Kalanchoe, 127, 240, 254, 255, 317, 319,

321, 322, 396, 397, 445
Karyological plant anatomy, 445
Kinetin, 414
Kinoplasmosome, 80
Kohlrabi, reconstitution of tissue pattern

in, 244
Krenke's theory of physiological age, 210

Laburnum, 129
Lacunaria, 208

Lagenaria, 51, 130, 421, 423

Laminaria, 169, 233

Lateral meristems, 79-88

Lateral roots from convex side of main

root, 385
Layering in meristem, 62
"Lazy" maize, 390
Leaf, development, 89

primordium, changed to bud, 71
Least surface principle, 44
Leaves, effect on root formation, 393
Lecythis, 250
Light, 308-323

duration, 314

effect on reproduction, 315

intensity, effect on structure, 309

quality, effect, on differentiation, 314
on length growth, 313

relation to other factors, 322
Ligustrum, 89
Lilium, 250, 256
Linaria, 176, 245, 282, 425
Linum, 157, 187, 245, 439
Liquid film theory, in cell form, 44-49
Livia, 279
Living root tips, cell division observed in,

77
Long-day plants, 315
Luff a, 197, 201, 243, 250, 433
Lunularia, 121, 343
Lupinus, 69, 73, 160, 238
Lychnis, 221, 280, 368, 428
Lycopersicon, 34, 261
Lycopodium, 59, 171, 282

Madura, 124

Macromolecular pattern, 433

Male and female tendencies, balance, 431

Maleic hydrazide, 407

Manoilov reaction, 221

Marchantia, 121

Marsilea, 332, 372

Mechanical contact in phyllotaxy, 345

Mechanical factors, morphogenetic effects,

345
Meiosis, in Acrasiaceae, 224

in somatic cells, 274
Melandrium, 365, 400, 428-430
Melilotus, 263

Mercurialis, 185, 263, 317, 399, 400
Meristematic center in root, 77
Meristematic cells as genetic reserve, 232
Meristemoids, 201
Meristems, 4, 12, 55-91

apical, 56-79

determinate, 88-91

differentiation in culture, 75

diffuse, 13

Subject Index

545

Meristems, intercalary, 79

lateral, 79-88

residual, 67

rib, 47

zonation in, 64
Mespilus, 268

Metabolic gradient, 73, 140
Metaplasin, 396
Metaxenia, 101, 407
Metzgeria, 234
Microcycas, 64
Microfibrils in cell wall, 165
Middle piece, effect in grafts, 260
Mimosa, 345, 346
Mitogenetic rays, 40
Mitosis, 25
Mnium, 170
Monstera, 191, 218
Morphogenesis, defined, 3

early work in, 5-6

in lower plants, 6

phenomena in plants, 7
Morphogenetic factors, 7, 303
Morphogenetic movements, 5
Morphogenetic norms, 449
Morphogenetic point of view, 8
Morphogenetic problems, 5
Morphology, 1

idealistic, 1, 114
Mucor, 221, 400
Muehlenbeckia, 169
Multipotent primordia, 189
Myxamoeba, 23, 223
Myxobacteriaceae, 228

Narcissus, 65

Neurospora, 373

Nicotiana, 156, 261, 264, 282, 295, 296,

343, 419, 426
Nitella, 41, 149, 166
Nitrogen, effects, in development, 364

in slime molds, 366
and sex differences, 365
Normal curve, 16
Norms, morphogenetic, 449
Nothoscordum, 107
Nucellar embryos, 206
Nuclear size in relation to cell size, 27
Nucleic acids, 3
Nucleoplasmic ratio, 27
Nuphar, 71
Nymphaea, 71

Oenanthe, 332

Oenothera, 35, 321, 438

Onoclea, 137

Ontogeny, differentiation during, 205

Ophiostoma, 54

Opuntia, 169

Organ-forming substances, 376, 391, 413,

' 458
Organism, 2, 23

as fundamental biological fact, 459
Organismal theory, 23
Organization, 449-459

components, 449

as expression of molecular forces, 456

gradients, 450

mathematical relations, 456

not lost in abnormal growth, 453

polarity in, 449

regulatory mechanisms, 452

spirality in, 450

symmetry in, 450
Organizer, 156

Oriented behavior in polarity, 144
Orobanche, 397

Orthostichies in phyllotaxy, 153
Osmotic concentration, of cell sap, 40

and cell size, 40, 335

and plant form in algae, 336

and polyploidy, 335
Osmunda, 71, 188

Parabolic curves in meristem, 63
Paramorphs in fungi, 373
Parastichies, contact, 155

in phyllotaxy, 154
Parthenocarpy, 378
Pattern, cytoplasmic, 456

macromolecular, 455
Pediastrum, 179, 390
Pedicularis, 445
Pelargonium, 269
Pellionia, 173
Pelory, 176, 282
Pemphigus, 284
Periblem, 60
Petunia, 264, 265
Phalaris, 190, 222
Pharbitis, 282, 419
Phascum, 234
Phaseolus, 250, 274, 282
Phasic development, 205

and sex, 428
Phellem, 87
Phelloderm, 87
Phellogen, 87

origin in old tissue, 88, 201
Philodendron, 218
Phleum, 131

Phloem fibers, growth, 82
Phlox, 282, 315

Phosphorus, role in development, 368
Photoperiod, 315

546

Subject Index

Photoperiodic induction, 315
Photoperiodism, effect, 315

on chromosome number, 322
on flowering, 315
on leaf structure, 321
on lower plants, 317
on parasite and host, 397
on root-shoot ratio, 320
on sex determination, 317
on tuberization, 320
on vegetative structures, 319
Photothermal induction, 339
Phragmites, 35, 445
Phragmoplast, 25, 80
Phragmosome, 25, 43
Phycomyces, 21, 149, 165, 400
Phyllocaline, 396
Phyllocladus, 169, 208
Phyllody, 277, 317
Phyllogen, 89
Phyllotaxy, 66, 150
decussate, 151

experimental modification, 160
Fibonacci series in, 152
fractional divergence, 152
genetic spiral, 151

direction, 164
at meristem, 71
spiral, 151
theories, 156-163
Physarum, 314
Physiological age, 210
Phytohormones, 375
Picea, 189, 263
Pilobolus, 318, 400
Pisum, 250
Plagiotropic axes, 189
Plantefol's theory of phyllotaxy, 156
Plasmodiophora, 138
Plastochron, 66, 68
Plastochron index, 66
Plastochron ratio in phyllotaxy, 162
Plectranthus, 89
Plerome, 60
Pleurococcus, 119
Poa, 280, 320
Podophyllum, 187, 350
Podostemon, 237
Pogonia, 247

Polar patterns in organic form, 142
Polarity, 116-146

aspect of differentiation, 118
in auxin flow, 141

bioelectrical effect on, 361
cambial cells, 128, 130
cell, 131

in cell division, 131
cell wall, 132
in cellular slime molds, 143

Polarity, as component of organization,
449

definition, 117

determination, 137

and developmental pattern, 142

electrical, 139

in embryonic development, 126

in external structure, 119-126

factors of induction, 117

and gradients, 145

in grafts, 129

in isolated cells, 135

in leaf cuttings, 124

loss, 137

in lower plants, 121

of movement in phloem, 141

in plasmodia and coenocytes, 138

in pseudoplasmodium, 225

in regeneration, 119

reversal, 125

in root cuttings, 124

in root-hair cells, 131

in single cells, 134

in stem cuttings, 123

three aspects, 144

in tissue reorganization, 127

transverse, 123, 361
Polarized growth in leaves, 90
Polyembryony, adventive, 256

cleavage, 206, 235
Polygonum, 311, 330
Polyploid series, 35, 436
Polyploidy, 436

and cell shape, 440

and cell size, 35, 437

distribution among growth forms, 440

and organ shape, 440

and organ size, 439

and plant size, 438

produced by colchicine, 436

somatic, 441
Polypodium, 239
Polysomaty, 441

and cell size, 35

and cellular differentiation, 445

distribution in plant, 442

and photoperiodism, 442
Polysphondylium, 226, 366
Populus, 279, 282, 284, 404
Potamogeton, 192, 216, 217, 331, 370
Potassium, role in development, 370
Potency of cell, 306
Potentilla, 284
Pressure and plane of cell division, 49,

346
Primary tissues, origin, 79
Primula, 35, 70, 110, 238, 445
Proserpinaca, 216, 217, 330
Protein synthesis in root tip, 42

Subject Index

547

Protosiphon, 43

Protostele, 72

Primus, 279

Pseudoplasmodium in Acrasiaceae, 223

Pseudotransverse division in cambial cells,

81
Pseudotsuga, 78
Psilntum, 282
Pteridium, 175

Pteridophytes, shoot meristem in, 68
Pyronema, 233

Quiescent center in root apex, 78
Quincuncial arrangement of floral parts,
167

Ranunctdus, 216, 330, 343

Raphanus, 250

Ratio between rays and vertical cells in

wood, 83
Ray initials, at cambium, 80

origin, 83
Rays, uniform distribution, 83
Reaction wood, 103, 193, 355

in angiosperms, 357

and auxin, 358

in conifers, 355

longitudinal compression in, 356

regulatory action, 356
Reactivity of cell, 306
Recapitulation in juvenile traits, 1
Reciprocal crosses, role of cytoplasm in,

435
Reconstitution in regeneration, 235-244

basipetal character, 242

fem leaf, 239

fern prothallium, 240

in kohlrabi tuber, 244

root meristem, 236

shoot meristem, 237

after splitting of meristem, 237

tissue patterns, 240, 244
Regeneration, 230-257

bryophytes, 234

buds on hypocotyls, 245

defined, 231

epidermis under wound cork, 241

in flowers, 250

fungus fruiting body, 233

in gametophytes, 250

in higher plants, 235

indifferent primordia, 248

individual cells, 233

in inflorescences, 250

after injury, 230

in leaf cuttings, 249

in lower plants, 232

Regeneration, after physiological isola-
tion, 231

protonema from sporophyte, 234

by reconstitution (see Reconstitution
in regeneration )

redifferentiation in, 241

reproductive, 235, 250-257

by restoration, 235, 244-250

from root cuttings, 247

self-regulation in, 231

shoots from leaves, 252

from single cells in algae, 233

from single epidermal cells, 245, 253,
255

split meristems, 238

from stem cuttings, 245

vascular strands, 242

in vegetative propagation, 244
Rejuvenescence, 210
Relations, importance, 3
Relative conducting surface, 334
Relative growth, 105
Relative growth constants, segregation,

423
Reproductive apex, development, 67
Reproductive regeneration, 235, 250-

257
Reseau de soutien, 201
Restoration in regeneration, 235, 244-

250
Retinospora, 214
Reversibility of ontogenetic change, 214

effect of gibberellin on, 214
Reversion to juvenile state, 217
Rhizobium, 295
Rhizocaline, 394
Rhizophore, 248
Rhythms, endogenous, 322
Ricinus, 191, 351, 352
Ripeness to flower, 205
Robinia, 282
Root apex, 75-79

physiology, 78

in tissue culture, 78

tissue differentiation, 77

"types," 78
Root formation, effect of leaves on, 393
Root-forming hormones, 247, 392
Root nodules, as cataplasmatic galls,,
295

tetraploidy in, 442
Root-shoot ratio, 96
Rotholz, 356
Rudbeckia, 222, 338
Rumex, 185, 430

Sachs's rule in cell division, 44
Sagittaria, 216

548

Subject Index

Saintpaulia, 239, 253, 255

Salix, 128, 282

Samhucus, 279

Sanio's laws, 36

Sarracenia, 187

Sauromatum, 442

Scenedesmus, 343

Schizaea, 203

Schizostegia, 169

Scion in grafting, 258

Sclerotinia, 338

Scolopendrium, 239

Scorpioid cyme, 178

Secondary tissues, 80

Sectio aurea, 153

Sedum, 192, 255, 437

Seed size and plant size, 97

Segregation in somatic cells, 274

Selaginella, 12, 58, 171, 172, 175, 202,

248
Self-differentiation, 24, 73
Self-regulation, in development, 452

in regeneration, 231
Sempervivum, 395
Senescence, 38, 205, 211
Sequoia, 110, 159
Sex chromosomes in plants, 429
Sex determination, 430
Sex hormones in fungi, 400
Sex inheritance, XY type, 429
Sex-linked traits in plants, 429
Sex reversal by environmental factors,

317, 428
Shade leaves, 312

Shaking as substitute for light in develop-
ment, 346
Shoot apex, 59-75

chemical organization, 73

compared to organizer, 73

culture, 70, 73

ontogeny, 65

organized system, 74

role in differentiation, 70, 73

size and stelar development, 72,
222

totipotence, 70

in various ecological types, 65

in various plant groups, 65
Short-day plants, 315
Short-day shape of leaves, 315, 395
Sigmoid curve of growth, 13
Similitude principle, 359
Sinapis, 346
Siphonostele, 72
Sirenin, 400

Size, absolute, importance in develop-
ment, 359

in relation to form, 361
Sliding growth, 81, 83

Soap bubbles, division, 46

resemblance to cells, 44
Solanum, 261, 264, 268, 269
Solidago, 432
Somatic mutation, 273
Sophora, 263
Sorbose, 373
Sorocarp development in Acrasiaceae,

225
Sphacelaria, 233
Sphaerocarpos, 234, 426, 429
Sphagnum, 58, 191
Spinacia, 221
Spiral grain in wood, 166
Spirality, in cell wall, 165

as component of organization, 164

omnipresence, 165
Spirogyra, 38, 56, 119, 147, 150
Sporobolus, 131
Stellaria, 167, 177
Stentor, 455
Stereum, 233
Stichococcus, 311, 314
Stimulation and inhibition, balance be-
tween, 103
Stock in grafting, 258
Stock-scion interrelations, 262
Stomatal index, 325
Storied woods, cell length in, 37
Streckungswachstum, 31
Streptocarpus, 239, 253, 397
Sucrose, morphogenetic effects, 73, 371,

372
Sun leaves, 312
Surface-volume ratio, 38
Swaying, formative effects, 353
Symmetry, 147-180

axis, 147

bilateral, 169

as component of organization, 450

of crystals, 148

development, 178

in cellular systems, 179
in coenocytes, 178

dorsiventral, 147, 170-178

in flowers, 167

and form, 180

in inflorescences, 167

inorganic and organic, compared
148

pendular, 179

radial, 147, 149-169
lower plants, 150
meristems, 179
roots, 150
shoots, 150
Symphoricarpos, 279
Symplastic growth, 81
Syncephalastrum, 373

Subject Index

549

Synchitrium, 284

Synthetic growth substances, 374, 378,

391
Syringa, 73

Tagetes, 129
Taraxacum, 282
Teilungswachstum, 31
Temperature as morphogenetic factor,
337-344
and dormancy, 339
and mitosis, 40
various effects, 341
Tensile stress in development of pri-

mordia, 160
Tension, effect on tensile strength, 347-
350
formative effects, 351
at meristem, 186
Teratology, 277
Teratomata, 278
Tetrakaidecahedron, 53
Thermoperiodism and growth, 337
Thuja, 84, 171, 174, 214
Tilia, 282

Tilted grain in wood, 166
Tissue culture, 73, 75, 222, 296
entire organs, 297

organization of meristems in, 75, 298
single cells, 298
Tissue mixtures, 258-274
Tissue tension, in dead wood, 359
distribution, 358
effects, 358
Tolmiea, 251

Topiary and correlation, 99
Topophysis, 189, 212, 214

reversibility, 214
Torenia, 249, 253, 440
Totipotent structures, 102
Trace elements, 364
Tradescantia, 219, 237
Transpiration stream, as functional stim-
ulus, 333
as morphogenetic factor, 332
relation, to leaf area, 333
to vascular tissue, 333
Traumatin, 376, 403
Trichoblast, 131, 190
Trichosanthes, 51, 52
Trichosclereids, development, 191
Trillium, 40

Trisomies, genetic effects, 446
Tropaeolum, 60, 65, 72, 73, 109, 238,

309, 311, 419, 425, 427
Tropisms as morphogenetic phenomena,

345
Tuber-forming stimulus transmitted by
grafting, 262

Tumors, from incompatible crosses, 296

from tobacco hybrids, 295
Tunica in meristems, 62
Twin spots, causes, 274
2,4-Dichlorophenoxyacetic acid ( 2,4-D )
as herbicide, 407

Ultrasonics, effects, 354
Viva, 56
Urtica, 185
Ustilago, 280
Utricularia, 249

Valeriana, 185

Valonia, 132

Vaucheria, 233, 317, 399

Vegetative propagation, regeneration in,

244
Vernalization, 315, 339

chemical, 343

and day length, 340

effect, on flowering, 339

on vegetative characters, 341

and phasic development, 340

sensitive region in, 340
Viburnum, 313
Vicia, 29, 41, 76, 78, 103, 221, 279,

346
Vitamin C and cell size, 37
Vitamins in plant development, 373
Vitis, 38
Volvox, 149

Water as morphogenetic factor, 324-
336

in air and soil, effects, 329

experimental work on, 329

in "water" and "air" forms, 332
Water balance and heterophylly, 217
Whorls of cells, cause, 128, 289
Witches brooms, 280
Wound healing, 240
Wound hormones, 37, 376, 381, 402

bean test for, 403

chemical nature, 402

and cork formation, 402

nonspecificity, 402
Wound tissue, character, 289

Xanthisma, 184
Xanthium, 397, 398
Xeromorphy, 324

as adaptive character, 324

causes, 324

cell size in, 324

550

Subject Index

Xeromorphy, and drought resistance,
326
influence of immature leaves in, 327
and nitrogen deficiency, 329
Xerophytes, 324

Xylem and phloem, developmental rela-
tions, 84

Zalenski's law, 325

Zamia, 237, 250

Zea, 77

Zinc, role in development, 37]

Zinnia, 34, 261

Zonation in meristems, 64

Zygomorphic flowers, 176