PLASMODIOPHORALES
JOHN S. KARLING
Columbia Vnivernty
m
THE PLASMODIOPHORALES
Including a
Complete Host Index, Bibliography,
and a Description of Diseases
Caused by Species of this Order
BY
JOHN S. KARLING
Columbia Unh'ernitif
First Edition-
PUBLISHED BY THE AUTHOR
NEW YORK CITY
1942
COPYRIGHT, 1942, BY THE AUTHOR.
ALL RIGHTS RESERVED. THIS BOOK, OR PARTS
THEREOF, MAY NOT BE REPRODUCED IN ANY
FORM WITHOUT PERMISSION OF THE AUTHOR.
Dedicated to
R. A. HARPER
Oil tlie Occasion of the 80th
Anniversary of His Birtliday
PREFACE
This thkatisk is part of a serios of leoturcs prc-
sfiitcd to srailuatc and rosi-arcli students of mycol-
ogy at C'oluniliia I iiivcrsity on tlif di'vi'lopnicnt. ori-
gin, and pliyloju'iiy of the lower fuiifri. It liad been
originally planned to incorporati' tliis material in a
general treatment of the simiile. hiHagellate Ooniy-
eete-like fungi. I.agenidiales, and Cliytridiales, hut
inasnnieli as tlie Plasniodiopliorales at present a])-
pear to lie a fairly eolierent iiliylogenetie group, it
seems advisable to treat them separately. The Plas-
niodiophorales are an important and significant
group of organisms from the standpoints of [ilant
pathology and phylogeny of the lower fungi. As de-
structive parasites of crucifers and potatoes, some
species cause serious economic losses of basic food
crops. Phylogenetically. they possess certain devel-
opmental phases which are strikingly similar to those
of the Proteomyxa. Myxoniycetes. and simjile fungi
— similarities which suggest either a common origin
or parallelism in development.
Although the Plasmodiopliorales have been stud-
ied for more than a half century, no serious efl'ort to
summarize the accumulated data was made until
1<)33 when Cook monographed the group. Cook gave
a detailed description of the known genera and spe-
cies and also discussed their cytology and develop-
ment in relation to phylogeny. Unfortunately, this
otherwise worthy and excellent treatise is marred by
certain inconsistencies, based on the author's obser-
vations, which are confusing and misleading to be-
ginners in this field. Since that time, several new-
genera and species have been added to the group.
Particularly significant is the discovery of I.eding-
ham. Couch, et al.. and Barrett that the zoospores
are biflagellatc and heterocont and that thin-walled
evanescent zoosporangia are a characteristic devel-
opmental phase of the Plasmodiophorales. These
discoveries have greatly modified our concepts of the
group and make the present revision opportune,
worthwhile, and essential.
This book is intended primarily for graduate and
research students of mycology and the lower organ-
isms. Nevertheless, botanists and biologists in gen-
eral as well as protozoologists and phytopathologists
will doubtless find the summarized data, life cycle
diagrams, and descri]>tions of diseases of consider-
able value. As a treatise for research students, it nec-
essarily includes nnicli that is questionable and con-
troversial in nature and which ordinarily might be
omitted or discussed more briefly. -Some of the data
presented are of doubtful value and significance, in
the author's opinion, but they are nonetheless in-
cluded with as little bias as possible in order that
students may draw their own conclusions and inter-
pretations. Although the author agrees with Cook
and others that lihi-owi/ja, Sorolpidiiim, .-ind .liiiso-
mi/.rii are prob.-ibly synonyms of I.i</>iiiTa, these gen-
era are discussed separately as doubtful members.
Likewise, full treatment is given to the excluded
genera and s])ecies, thereby making these dat.i .ivail-
.■ible to research workers. The author's critical atti-
tude and seeming skejitieism toward existing data on
"akarvosis," extrusion of chromatin, sexuality, meio-
sis, and other critical developmental phases of this
group is not intended as a direct criticism of the
veracitv and accuracy of certain workers, but rather
to indicate how inconclusive present-day knowledge
and interjiretations are and thereby to stimulate
more intensive study of these phases. The Plasmodi-
ophorales are unfavorable for cytological study be-
cause of the minuteness of the nuclei. Likewise, the
intramatrical habitat of all species makes direct ob-
servation of gametic fusion, schizogony, etc., ex-
tremely diflicult in living material. It is therefore to
be expected that many data are conflicting and incon-
clusive.
Separate bibliographies are provided at the close
of each chapter to expedite reference to literature
on particular subjects, genera, and species. Since
many of the cited papers are general in nature and
relate to several genera, they have been listed several
times, which makes the bibliograjjhy somewhat re-
dundant. A host index is also provided with each spe-
cies. Due to war conditions abroad, it has been im-
possible to secure many of the publications relating
to club root and powdery scab, so that the host index
and bibliography of Plasmodiophora Brassicae and
Spoiiflospora suhterranea are unfortunately incom-
l)lete. In a bibliograjihy of this magnitude errors are
likely to occur, and the author will appreciate having
mistakes and omissions called to his attention. The
glossary is purposely brief and relates almost en-
tirely to terms used in the text.
Tlie writer has drawn freely from the illustrations
of authors in this country and abroad, to whom he is
very grateful. The list of contributors is too long for
individual mention, but full credit is given in the de-
scriptions of the drawings. The life cycle diagrams
presented in Chapters III and V have not been
copied directly from other authors' illustrations but
are based on their descriptions of the successive de-
velopmental phases. The author feels particularly
grateful to -Miss Amy L. Hepburn, Natural Science
Librarian of Columbia University, for her unstinted
help with the literature, without which this work
would have been impossible.
Columbia Vnivkbsitv
New York City
No\t:mbkr. 19U
CONTENTS
I'rct'iui' i
CHAI'iKH I
Introduction 1
(Tlossarv 2
Bibliography 3
CHAPTER II
Cvtologv 4
"I'l-oniitosis" -l
"Akdrvote" stage 10
Mciosis 12
Schizogony and Cleavage 14
CHAPTER III
Sexiialitv and Alternation of Generations 15
I'liisinodiophora 15
Tetramyxa 16
Sorosphaera 16
Sorodiscns 18
Spongospora 18
Ligriicra 18
Pnlijmi/.ra aiiiJ Ortoiiiij.ra 18
Bibliogra])hy 20
CHAPTER IV
Classification and Discnjjtion of Species 20
Key to genera 22
Plasmodiophora 22
Biological races 26
Reliition to bacteria 26
Relation to cancer 28
Bibliography .'J.'j
Excluded species '.H
Bibliography .■J6
Vll
5755H
PLASMODIOPHORALES
Tetramyxa 37
Octomyaxi 40
Sorosphaera 41
Sorodisciis 46
Membranosorus 52
Spongospora 54
Llgniera 58
Polymyxa 63
Doubtful genera 64
Rhizomyxa 64
Sorolpid'uim 66
Anisomyxa _ . . 68
Trematophlyctis 70
Pyrrhosorus 71
Excluded genera 72
Sporomyxa 74
Peltomyces 76
Cystospora 76
CHAPTER V
Phylogeny and relationships of the Plasmodiophorales 78
Historical 78
Relationships with the Myxomycetes 79
Relationships with the Chvtridiales 85
Relationships with Woronina 85
Relationships with the Proteomyxa and Protozoa 88
Bibliography 91
CHAPTER VI
•
Diseases caused by species of the Plasmodiophoraceae 93
Club root of crucifers 93
Losses due to disease 93
Discovery of disease 93
Symptoms 93
Cellular relations between host and pathogen 95
Entrance and spread of parasite 96
Dissemination of parasite in nature 96
Environmental factors 97
Hosts and degree of infection 99
Control of club root 104
Sanitary practices 104
Seed, seed bed, and seedling disinfection 105
Disinfection of fields 105
lONTKNTS
Liming ....
Hasio fortili/crs .
Soil drainage
Croj) rotation
Eradication of wild host
Resistant varieties of erucifers
Nature of suseeptibilitv and resistance .
Gcograpliical distril)iition of club root and bibliog
Powdery scab of potatoes
Significance of disease .
Predisposing factors
Symptoms
Cellular relations between host
Control
Sanitary practices
Seed tuber disinfection .
Soil disinfection .
Effects of fertilizers .
Resistant varieties
Distribution and bibliography
Species Index
Subject Index
Author Index
nd pathogen
raph
no
115
117
117
118
118
119
120
129
129
129
130
i:31
132
132
132
133
133
133
137
137
139
C'hapUr 1
Introduction
The Plasmodiophoralks iiicliulo one family of or-
ganisms wliicli are often referred to as parasitie
slime molds heeause tiiey arc i-liaraeterized by a
multiniuleate ulasmodial stauv as in the trne slime
molds and ))arasitize tilamentous fiingi, alu'ae. eryp-
togams. and liiirher plants. While this eomnion name
mav lie deseri|)tive. its use is unfortunate, since it
suggests a relationsliip witli the Myxomyeetes which
has not been definitely established. Most genera of
this order have rather complex life cycles which in-
clude zoosj)ores, amoebae, sjiorangiosori, zoosjio-
rangia. secondary zoospores, plasmodia, cystosori,
resting s))orcs, and probably isoniorjihic gametes.
Sporangiosori and tliin-walled evanescent zoospo-
rangia were first observed by Borzi in Rhizovii/jca
hypoi/ea as early as 188 t. and later by Neniec ('11.
'13) in Sorolpidiiim and Anis07ni/jra, but at that time
the relationship of these genera to the Plasmodi-
ojihoraccae was not clearly understood. Zoospo-
rangia were subsetjuently rediscovered by Cook
('26). Cook and Schwartz ('30). I.edingham ('33.
'3i. '3.5. '39). Fedorintscliik ('3.")), Coueli. et at.
('39) in Lignii-ra, Plasmodiophora, Poli/mi/.ra,
Sponr/ospora, and ()ctomi/xa and are now generally
believed to be a characteristic developmental phase
of the order as a whole. The zoosporangia are re-
garded by some workers as gametangia in which
meiosis precedes gametogenesis, but this has not been
conclusively ])roven.
The s])orangial phase is followed by the develop-
ment of a conijiaratively large multinucleate sporo-
genous Plasmodium in which meiosis is reported to
occur before or during cleavage into resting spores.
The latter may remain loose and free of each other
or unite in more or less compact cystosori. Upon
germination, tlie resting spores ))roduee uninucleate
amoebae or motile flagellate zoos|)ores. These cells
are regarded by many workers as isomorphic gam-
etes which fuse in pairs and thus initiate the diploid
generation, but so little is known about sexuality in
this order that nothing conclusive can be said as yet
about the sexual nature of these cells. Some my-
cologists contend that a true ])lasmodinm does not
exist in the Plasmodiophorales on the grounds that
the naked multinucleate tliallus is not formed by the
coalescence of numerous mutually attracted amoebae
in the manner described by Cienkowski ('63) for the
Myxomyeetes. In so doing, these mycologists disre-
gard the reports of Woronin ('77), Halsted ('93),
Nawaschin ('99), Evcleshvmer ('01). Massee ('08),
Osborn (']!), Kunkel ('15). Terby ('2t), Jones
('28). Home ('30). Cook and .Schwartz ('30). Milo-
vidov ('31 ). I.edingham ('39). and others that amoe-
bae as well as small plasmodia coalesce in Plasmodi-
ophora, Sponf/ospora, Pol i/nii/.ra, etc. \\ hether or not
these re])orts are accurate may be oi)en to question,
because they are not all based on observations of liv-
ing material. These data nevertheless exist in the
liter.-iturc and must be given serious <'onsideration.
I'urtherniore, the above-mentioned reasons for ex-
cluding the term ))lasmodiuin from the Plasmodi-
ophoraceae would also ])reclude its use in relation to
the .Myxomyeetes according to recent data on this
group. .lahn (11. '36), Skupienski ('28), Wilson and
Cadnian (28), Cadman ('31), and others have
shown that the ])lasmodium is initiated by fusion in
pairs (if isomorphic gametes and that the zygotes
may subsequently ingest unfused lia])loid amoebae
as food material. Thus, the conception of a Plas-
modium as Cienkowski interjjreted it has undergone
considerable modification and is now used jirinci-
l)ally as a deseri))tive term for the naked, multinu-
cleate, assimilative phase of the slime molds. In this
sense it may be equally well employed for the naked
multinucleate thallus of the Plasniodioiihorales.
Cook's use of the term myxamoeba for this stage is
unfortunate, misleading, and obviously unwar-
ranted. According to standard dictionaries .md glos-
saries, the term myxamoeba relates to the naked,
amoeboid, and usually uninucleate protoplasts
formed by the germinating resting spores of the
Myxomyeetes, and its introduction as a deseri])tive
name for the naked multinucleate plasmodial stage
of the Plasmodiophorales will lead to nothing but
confusion. Likewise, his use of the term "swarm
cells ' for the products of spore germination as a dis-
tinctive contrast to the name "zoos])ores " for the
flagellate cells formed in zoosporangia is not war-
ranted at present and should be avoided. I.edingham
and Barrett have clearly shown that the zoospores
are biflagellate and hcterocont regardless of whether
they are formed in zoosporangia or from resting
s])ores and that there are no structur.il distinctions
between the so-called swarm cells and zoosjiores. If
in the future it is found tliat the resting spores form
gametes and the s))orangia zoospores, or vice versa,
the two products may then be distinguished and
designated as gametes and zoospores, respectively.
.Mtliough most s|)ecies of this order, except P.
lirax.iicae and S. suhti-rratwa, a])pear to be compara-
tively rare in occurrence, they are nevertheless
world wide in distribution and have been re))orted
from North and .South .\merica. .\frica, Kurope,
Asia. Australia and several Atlantic and Pacific
islands. Three s])ecies occur in fungi, algae, and
cry))togams. while the remainder parasitize higher
|)lants. All s))ecies, exce)>t members of the genus JAfj-
n'tera, cause distortion of the host and marked
changes in its cells. These changes involve enlarge-
ment and divison of infected as well as of adjacent
PLASMODIOPHORALES
healtliy cells, with the result that conspicuous ex-
cresences and galls are usually formed. However,
only two species are economically important as para-
sites. Plasmodiophora Brassicae and Spongospora
subterranea are destructive pathogens of crucifers
and potatoes, respectively, and cause the diseases
commonly known as club root and powdery scab.
While these diseases had been recognized since
early times, their causative agents were not identified
until the latter part of the 19th century. The discov-
ery of P. Brassicae in hypertrophied roots of cruci-
fers by Woronin in 1 877 may be said to have initiated
the study of the Plasmodiophorales as a distinct
group of organisms. A second genus, Tetramiixa,
was found by Goebel in 1881, and in the same year
Zopf created a new family, Plasmodiophoraceae, in
the zoosporic Monadineae to include these genera.
Two additional genera, Spongospora and Soro-
sphaera were reported by Brunchorst and Schroeter
in 1886, but the relationship of the former genus was
not generally recognized until much later. Schroeter
ignored Zopf's classification and created a new or-
der, Phytomiixini, with one family, Phytomyxaceae,
to include these genera as well as the legume tubercle
organism which he redescribed as Phiitomijxa legii-
minosarum. Inasmuch as Schroeter's Phytomyxinae
was later ('97) incorporated in Engler and Prantl's
Die Natiirlichen Pflanzenfamilien, it was widely
recognized and accepted. Phiitomyxa as well as
Plasmodiophora Alni and P. Elaeagni were excluded
by Tubeuf and Smith ('97) and other pathologists in
their discussions of the parasitic slime molds, but
Schroeter's order and family names nonetheless con-
tinued to be used. In 1909 Maire and Tison made an
extensive review and study of these doubtful species
and showed again that P. legiiminosarum, P. Alni,
P. Elaeagni, Tylogonus Agavae, and Pseudocommis
J'iiis have little or nothing in common with the true
plasmodiophoraceous species. Since Phyiomi/.ra had
already been excluded, they pointed out that the
name Phytomyxaceae was no longer appropriate.
They accordingly adopted Zopf's Plasmodiopho-
raceae to include Plasmodiophora, Tetraviy.ra, and
Sorosphaera and listed Schroeter's Phytomyxinae
pro parte and Delage's Protomyxideae zoosporideae
as synonyms. Apparently unaware of ]\Iaire and Ti-
son's studies, some protozoologists nevertheless still
continue the use of Schroeter's Phytomyxinae or
some modification of this name.
In the meantime, Sporomyra and Peliomyces had
been added to the group, and following Maire and
Tison's first paper, Ligniera, MoUiardia, Sorodiscus,
Ostenfeldiclla, Cystospora, Tremaiophlyciis, Clath-
rosorus, Memhranosorus, Polymy.ra and Octomyxa
were successively discovered and included in the
Plasmodio])]ioraceae. However, many of these gen-
era have eitlier been merged or excluded entirely, so
that the order includes at present comparatively few
valid genera. The group as a whole was finally raised
to ordinal rank by Cook ('28, '33), following a sug-
gestion made by Schwartz in 191 K
Taxonomically, the Plasmodiophorales have been
bandied back and forth by protozoologists and my-
cologists for more than half a century, and few work-
ers are in agreement about tlie taxonomic position
and relationships of this order. Its members have
been included at various times in the Mycetozoa,
Monadineae, Proteomyxa, Rhizopoda, and Chytri-
diales. Some mycologists, particularly Gwynne-
V^aughan, Barnes, and Cook ('33), have maintained
that the Plasmodiophoraceae are not fungi and have
arisen along independent lines from more primitive
forms. However, the rediscovery within the last two
decades of zoosporangia in this order and the ob-
servations that biflagellate heterocont zoospores are
produced in such sporangia and also from resting
spores indicate a closer affinity with the simple fungi
than was formerlv believed to exist.
Glossary
Akaryote stage, a nuclear stage in which little or no
chromatin is visible in the nucleus.
Binuclearity hypothesis, the theory that the micro-
and macronuclei of infusoria contain the idio- and
• trophochromatin, respectively, and that the ordi-
nary nucleus of higher forms is accordingly a dual
"amphinucleus. '
Blepharoplast, the basal granule at the point of in-
sertion of each flagellum.
Capillitium, sterile filamentous, simple, branched, or
net-like tubes or fibers formed among spores in a
sporogenous body.
Chromidia, trophochromatin granules which are ex-
truded from tlie nucleus into the cytoplasm.
Chromidia hypothesis, the theory that the nuclei of
rhizopods and other similar organisms contain
idio- and trophochromatin. the latter of which is
extruded into the cytoplasm as chromidia and de-
generates or plays a dominant role in the differ-
entiation of specialized structures.
Chromidial stage, a nuclear stage during which the
trophoeliromatin is extruded into the cytoplasm.
Cruciform stage, equatorial ring stage of promitosis
in the Plasmodiophorales during which the nu-
cleole is elongate and forms a cross with the chro-
matin ring.
Cystosorus, a more or less compact aggregate of
cysts or resting spores.
Eucarpic, only a portion of the tliallus transformed
into a reproductive organ; remainder of thallus
vegetative.
Extramatrical, outside of host, matrix, or substra-
tum.
Double-anchor stage, anaphase stage of promitosis
in the Plasmodiophorales during which the arched
daughter chromatin bands and nucleoli are con-
nected by a chromatic strand and form a figure re-
sembling a double anchor.
Dumb-bell stage, more or less synonymous with
double-anchor stage of promitosis.
IXTKODUCTION
Flaiiitliim, a wlii))-likc protdpl.-isniic ora:;m of loco-
motion of zoospores, sw.inusporcs, and motile
iiametes.
(iaiiirtaiii/iiim, a ditlereiitiateci sac or vesicle which
produces gametes.
(iarlaiitl xtaf/r, a i>ropliasc stage of meiosis in wliicli
the chromatin is aggregated as garlands at the nu-
clear poles.
UrttTOcoiit. (flagella) of unequal length.
lltilocarpic. entire th.illus tr.insformed at maturity
into a re]irodiictive organ.
Ili/prrplasif, abnormal growth of tissue resulting
from undue cell division.
11 fiperirophii, abnormal enlargement of an organ.
II tipopla.li/, defective development due to insufficient
nourishment and consequent cessation of growth.
Ihtmoihallic, gameto])hytic or ha])loid thalli bi-
sexual.
Ileteroihallic, gametopliytic or liai)loid thalli uni-
sexual.
Ilnmophi/tic, sporophytic or diploid thalli bisexual.
Hctfrophi/tic, sporojiliytic or diploid thalli uni-
sexual.
Ilaplomoiioccioitx, haploid generation bisexual =
luimothallic.
Ilaplodioecious, ha])loid generation unisexual ^
lieterothallic.
Diplomonoeciotts, diploid generation bise.xual =
homophytic.
Diplodioecious, diploid generation unisexual =
heterophytic.
Ilaplosynoecious, haploid generation bisexual =
homothallic ^ haplomonoecious.
Ilaploheteroecioiis, haploid generation unisexual =:
lieterothallic = diplodioecious.
Diplosifnoecious, dililoid generation bisexual =
liomophytic = dijilomonoecious.
Diploheteroecioiis, diploid generation unisexual =
heterophytic ^ diplodioecious.
Ind'wchromatin, generative chromatin which is con-
cerned with reproduction.
Intramatrical, witiiin the host, matrix, or substra-
tum.
Isofjamy, fusion of structurally similar gametes.
Isokont, (flagella) of equal length.
Isomorphic, similar in shape and form but not in es-
sential structure.
Kari/ofjami/, fusion of gametic nuclei.
Meront, a uni- or multinucleate product of schizo-
gony.
Planocyte, a motile cell.
Plasmodiocarp, an irregular, sinuous, asymmetrical
fruiting body or si^orangium of the Myxogastres.
Plasmodium, a naked multinucleate protoplast cajia-
ble of amoeboid movement.
Plasmogamy, fusion of gametes, followed sooner or
later by karyogamy.
Promitosis, a pritnitive (?) type of intranuclear mi-
tosis in lower organisms wliich is characterized by
ill-defined cliromosomes and a large constricting,
dividing nudeole.
Protomilosis, .a variety of promitosis described by
.Viexiefl' in which no clearly defined equatorial
|)iate is formed. The perii)heral chromatin instead
is distributed in a diffuse f.ishion between the
polar halves of the divided karyosome.
Psriidoplasmodiiim, a false plasmodium or aggre-
g.ate of amoebae which retain their individuality;
ch.iracteristic of the Acrasieae and l,.iby rinthulae.
Psfiuhipodiitm, -.1 temjiorary i)roto))l.isniic extrusion
in .•imoebac and jilasmodia which may be retracted
or into wliich the whole mass may move.
Saturn stage, equatorial ring stage of ])romitosis in
the Plasmodiophorales during which the nudeole
lies in the center of a ring of chromatin.
Schizofiony , a jirocess of simjile or multi])!e division
of a schizont.
Schizont, a naked inultiiuicleate vegetative tliallus
which undergoes simple or multiple division.
Sorocarp, the fruiting structure of the Acrasieae.
Sorus, a group of sporangia or resting spores.
Sporangiosorus, a more or less compact sorus or ag-
gregate of sporangia.
Sporangium, a sac or vesicle which produces spores
endogenously.
Sporoci/st, a cyst which produces asexual spores.
Sporogonic, relating to spore formation.
Sporont, a thallus destined to form spores.
Synkaryon, the zygotic nucleus following karyo-
gamy.
Thallus, the vegetative body of algae and fungi,
without differentiation into root, stem, and leaf.
Transitional stage, a term used by Winge to describe
the transition in nuclear structure between pro-
mitosis and meiosis in the Plasmodiophoraceae;
synonymous to some degree with the so-called
akaryote stage.
Trophochromatin, somatic, vegetative chromatin
which is active in nutrition.
Zoocyst, a cyst in Monadineae which jiroduces amoe-
boid or flagellate cells.
'/.oosporangium, a s])orangium which produces zoo-
s])ores.
Zygote, the product of gametic fusion.
bibliography: introduction
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Bor/.i, A. 1884. Klii/.oinyxa, nuovo ficomicete. Messina.
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PLASMODIOPHORALES
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. 1934. Xature 133: ,534. 1935, Ibid. 135: 3994.
. 1939. Canad. Jour. Res. C, 17: 50.
Maire, H., and A. Tison. 1909. Ann. Mycol. 7: 22n.
Massee, G. 1908. Jour. Bd. Agric. London 15: 592.
Milovidov, P. F. 1931. Arch. Protistk. 73: 1.
Nawaschin, S. 1899. Flora 80: 404.
Xemec, B. 1911a. Ber. Deut. Bot. Gesell. 29: 48.
. 1911b. Bull. Int. Empr. Fran. Joseph Acad. Sci.
10: 09. 1913, Ibid. 18: 18.
Osborn, T. G. B. 1911. Ann. Bot. 2.o: 211, 327.
Schroeter, J. 1880. Cohn's Krypt. Fl. Schlesiens 3: 133.
. 1897. Engler und Prantl, Die Xat. Pflanzenf. 1,1:7.
Schwartz, E. J. 1914. Ann. Bot. 38: 227.
Skupienski, F. X. 1938. Acta Soc. Bot. Poloniae 5: 355.
Terby, J. 1934. Bull. Roy. Acad. Belg. 11:1.
Tubeuf, K. F., and W. G. Smith. 1897. Diseases of Plants.
London.
Wilson, M., and E. J. Cadman. 1938. Trans. Roy. Soc.
Edinburgh 55: .555.
Woronin, M. 1877. Arb. St. Petersburg Nat. Gesell. 8: 109.
Zopf, W. 1884. Die Pilzthiere oder Schleimpilze. Encyklop.
der Xaturwiss. 3: 139.
Chapter II
Cytology
"Promitosis"
Cytological studies of the Plasmodiophorales dur-
ing the pa.st four decades have centered primarily on
the type of nuclear division in the plasmodiuni, the
so-called "akaryote" stage, nieiosis, karyogamy,
schizogony, and cleavage. Nuclear division in the
Plasmodium has been described by most workers as
promitotic and fundamentally similar to that which
occurs in the Umax group of amoebae and other lower
organisms. So consistently has this type of division
been rei)orted that many students have regarded
promitosis as one of the most diagnostic characters
of the wliole order, and one which distinguishes the
Plasmodiophorales from all other fungi and higher
plants. Cook ('28) in particular has stressed this
character as follows: "The diagnostic feature which
characterizes the Plasmodiophorales is their two
methods of nuclear division, and failing to show evi-
dence that both promitosis and mitosis occur in the
life cycle, and that these two types are separated by
a stage iu which at any rate ])art of the chromatin is
extruded into the cytoplasm, no new fungus should
be included in this group." At the same time, other
workers have maintained that these divisions are
typically mitotic with well-defined chromosomes,
centrosomes, and astral rays. There is thus sharp
disagreement concerning karvokinesis in the Plas-
modium, and inasmuch as the presence of promitosis
has been regarded as an index of relationship to the
amoeba, a full discussion of the so-called vegetative
divisions in the Plasmodiophorales is essential to an
understanding of this order.
Nawaschin ('99) was the first to observe the char-
acteristic appearance of these divisions in Plasmodi-
ophora and to point out that they are different from
those which occur immediately before or during
spore formation. He nevertheless described the for-
mer mitoses as karyokinetic and regarded ('01) the
presence of the two types of division as an indication
of nuclear dimorphism — a view much in vogue among
the protozoologists of that time. Nawaschin's obser-
vation was confirmed by Prowazek ('02, '05), Maire
and Tison ('09), Blomfield and Schwartz ('10),
Schwartz ('10), Winge ('13) and Lutman ('13) for
other species and genera. Prowazek, particularly,
and later Blomfield and Schwartz, also stressed the
resemblance of the vegetative divisions to those
which had been described by protozoologists in cer-
tain coccidia and amoebae.
In the meantime, Nagler ('09) had proposed the
term promitosis for the type of nuclear division
found in Amoeba froschi, A. lacu.itrh, etc., which he
inter])reted to be a transition between amitosis and
mitosis. In these divisions neither chromosomes nor
well-defined spindles are formed, according to Nag-
ler. Division is intranuclear, and the large endo-
some or karyosome functions as a division center.
The latter elongates, and as it constricts the chro-
matin aggregates and forms a band across the equa-
tor of the nucleus. The karyosome then divides into
two bodies, and as these migrate toward the poles the
band of chromatin splits lengthwise. Each half ac-
companies a karyosome to the poles, and both are
there incorporated in the daughter nuclei. Subse-
quent workers, particularly Chatton ('10) and
Alexieff ('13) confirmed in broad outlines Nagler's
observations, but distinguished and defined other
similar and more advanced types of "primitive" mi-
tosis in amoebae. Since Nagler's time the term pro-
mitosis as a distinctive term has lost much of its ori-
ginal significance and has been employed rather gen-
erally for mitosis in lower organisms which are char-
acterized by an intranuclear spindle and chromatin
derived wholly or in part from a large karyosome.
In the process of division the latter is said to elongate
and divide and function as a nucleo-centrosome.
However, with tlie use of more refined and specific
fixatives and stains, many of the cases reported for-
CYTOI.OUY
mcrly as |)romitt)sis in protozoa, fimu;i. and aljiaf
have provin to lie tyi)ical mitosis.
NcvtTtlulfss. stmli-nts of tlit- I'lasmodiopliorales
ininu-diatcly rt-c-ognlzcd tin- similarity of Niiglfr's
jironiitotif divisions in Amoeba to tliosi- in tliis vt-jjo-
tativf Plasmodium, and in 1!)11 Main- and Tison
adopted Niiirlcr's tt-rni as descriptive of these Latter
divisions. Sulisecpient workers, ineliidiiiu: Cook (''Jii,
"28. '33), Cook and .Seliwart/, (,'-'!). ;}()). I.edingliam
('39). and Coueli <■( al. ('39) have used the term
protoniitosis. a variety of promitosis described by
Alexieff. Pavillard ('10). Wcrnham ('35). and oth-
ers have employed the term "cruciform" division.
Althousth they fijjured the same tyjie of division.
Neniec ('11. '13), l-'erdinandscn and Wins;e ('20),
and Milovidov ('31, '32. '33) avoided extensive use
of these terms, while Osliorn ('U) described the
ve!i:etati\c division in Spoiif/o.spora as amitotic. His
figures and deserijition of the jirocess are nonetheless
similar to those of previous and subsequent workers.
Favorski objected to the contention that promitosis
is specifically characteristic of primitive animals and
the lMasniodioi)horaceac and [lointed out that the
karyosome and eliromatin may behave in a similar
manner during mitosis in hisjlier ))lants. Terby ('32)
likewise condemned tlie use of promitosis for these
divisions in Plasmndiophura on the grounds that
chromosomes are present and the daugliter nucleoli
are formed anew from granules in the telophase nu-
clei and not by division of a mother nucleole. Home
('30) and Webb ('3.5) also contended that the vege-
tative divisions are tyjjically mitotic in Spongospora
and Suro.sphaera and thus contradicted all previous
workers who m.iintained that distinct chromosomes
are not )irescnt.
Two main view))oints have thus been ])resented by
these cytologists : one that the vegetative divisions
are premitotic and fundamentally similar to those in
certain amoebae: the other that they are typically
mitotic with well-defined cliromosomes. Prowazek,
Maire and Tison. .Schwartz, and Cook in ])articular
have cmi)hasizcd the former view, and their accounts
of the vegetative divisions may be taken as represen-
tative of those who held that these mitoses are quite
unlike anything present in other fungi and higher
plants. Terby, Home, and Webb may be looked upon
as re])resenting the other viewpoint. For the sake of
com))arison. drawings representative of both views
have been brought togetlier in Plate I and contrasted
in turn with those illustrating jjromitosis in certain
amoebae.
The resting nucleus of amoebae and i)l;ismodia of
the Plasmodioi)horaceae is quite small, so that its
structure is difficult to see and determine with cer-
tainty. Nawaschin described the chromatin in Plas-
mod iipliDra as a s])Oiigy. faintly-stainable reticulum
tliroughout the nucleus, while Prowazek figured the
nuch-i as having an alveolar achromatic structure
with several interspersed granules and a large cen-
tral nucleole lying in a clear zone. In other nuclei the
achromatic material was found to be radially ori-
ented on the nucleole (fig. 1). giving the nucleus a
wheel-like a))|)earance. Fn Hi>ri>iij>hafia .-ind 'I'l-tra-
iiu/.ra, Maire and Tison figured tiie rt'sting nucleus as
devoid of a chromatin reticulum (fig. 2) with the
nucleole lying in a \ acuole-like ele.ir sp.iee filled with
hyaloplasm, and numerous granules distributed on
the inner periphery of nuclear membrane. They
( '09) did not, however, regard these granules as true
I lirom.itin but instead as secretory chromidia derived
t'riiui the karyosome .-iiul destined to ))ass out into the
i\toplasm. In Spoiii/oxporu, on the other hand. Os-
liorn figured .1 wheel-like nucleus with numerous
chromatin granules distributed on radially oriented
liniu threads (fig. !•), but he likewise believed that
these granules had been derived from the karyosome.
Of the more recent workers. Cook, and Cook and
Schwartz have maintained that in Ligniera and Plax-
mod'iophora the chromatin is aggregated solely in a
layer around tiie inner i)eripliery of the nucleus
(fig. 5) with the result that the nucleole ai)i)ears to
lie in a clear vacuolate s))ace. but their observations
have not been confirmed. Cook's ('28) studies on
Lif/tiiera, however, were made from unsectioned ma-
terial stained in toto, which is obviously unfavorable
for study of nuclear details.
Although there is thus considerable difference of
opinion among these cytologists as to the structure of
the nucleus and the presence of a chromatin reticu-
lum, the "wheel" tyiie of resting nucleus neverthe-
less has been figured most often and shown to occur
in Plasmodiophora, Sponr/ospora, Soros pharra, Lif/-
niera, Sorodiscus, and Polifmyxa. Milovidov's ('32,
'33) observations on resting nuclei of P. Brassicae
stained by Feulgen's method are particularly jierti-
nent in this relation. In such prei5arations the karyo-
some. linin. and granules are colorless, and the only
visible structure is the faintly-stained luiclear mem-
brane. Milovidov, nonetheless, believed that small
chromatin bodies are present around the inner peri-
phery of the nucleus.
According to Nawascliin. the early ])rophases of
the vegetative divisions in Plasmodiophora may be
recognized by the emergence of distinct granules in
the nucleus (fig. (5) wliich have a markedly different
staining reaction from the karyosome and are not in
genetic connection with the latter. Their origin is
quite distinct from that of the karyosome, in Nawas-
chin's o))inion. These granules later unite and form
an equatorial ]jlate or band. Newaschin's observa-
tions were confirnied by Milovidov's ('32, '33)
studies which involved Feulgen's nuclear reaction
method. As the nuclei enter the )iro))hases. chromatin
granules and threads become visible in the nuclear
cavity, and these eventually form an equatori.d ring
(fig. .50). Prowazek ('0.5), on the other hand, de-
scribed the karyosome or "Inncnkorper" as enlarging
and difl'erentiating into a faint-staining achromatic
substance and a denser chromatic material (fig. 7).
The l.itter sul)stance then separates into a globular
luiclcole and a half moon-shaiied row of granules
(fig. 8), out of which the equatorial ring is formed
(fig. 9). Maire and Tison ('09), like Nawaschin,
noted the emergence of gramdes on the linin threads
PLASMODIOPHORALES
in Soiosphaera during tlie prophases of promitosis
(fig. 10, 11), but they contended tliat the granules
are derived from the karyosome and subsequently
aggregate around the latter as an equatorial ring.
Blomfield and Schwartz (10) and Osborn ('11)
have figured much the same type of prophases in S.
J'erouicae, L. Jitnci, and »S'. suhicrranea. I.utnian
likewise reported the presence of chromatin granules
in the prophases in Plaxmodiophora. "These gran-
ules had been previously concentrated as a hollow
sphere enclosing the tropochromatin of the central
body" (karyosome), and as the prophases progress
the granules of idiochromatin separate from the
karyosome and form a spireme, according to I.ut-
nian. In Sorodiscu.i Winge also reported a separation
of idiochromatin and tropochromatin (fig. 13) in
the karyosome in preparation for division, the former
giving rise to a thin equatorial plate and the latter
forming the nucleole. He believed that in the resting
nucleus the idiochromatin may "be partly resolved
in the tropochromatin. which later forms the chromo-
philous filaments radiating from the caryosome."
Cook ('26, '28) and Cook and Schwartz ('30) failed
to observe any marked prophase stages in Lir/niera
and Plasmodiophora but asserted that the peripheral
layer of chromatin which is present in the resting nu-
cleus condenses and becomes aggregated in a ring
around the karyosome (fig. 14). Shortly thereafter
the spindle fibers appear in the nuclear cavity and
form a fusiform intranuclear spindle (fig. 1.5) at
right angles to the chromatin ring, which in the mean-
time lias expanded and drawn away from the central
nucleole. Manj- of these cytologists have figured the
chromatin ring as a solid continuous band, but Maire
and Tison ('11) and Winge reported it to be com-
posed of numerous granules and chromosome-like
PLATE 1
Fifr. 1. Resting nucleus, P. Brassicae, showing wheel-like
structure. Prowazek, '0.5.
Fig. -2. Resting nucleus, T. parasitico , with karyosomic
granules at peri])hery. Maire and Tison, '11.
Fig. 3. Uninucleate amoeba, S. V eronicae , with centro-
some and astral rays. Maire and Tison, '09.
Fig. -1. Resting nucleus, iS. siibterraiiea, with wheel-like
structure. Osborn, '11.
Fig. 5. Resting nucleus, L. Juiici, with chromatin around
inner periphery of nucleus. Cook, '^8.
Fig. a. Early prophase, P. Brasxicae, showing numerous
chromatin granules. Nawaschin, '99.
Fig. 7. Early prophase, P. Briisslrne. showing separation
of idiocbromatin and tropbocliromatin in the karyosome.
Prowazek, I.e.
Figs. 8, 9. Differentiation of nucleole and chromatin ring.
P. Brasnicue. Prowazek, I.e.
Figs. 10, 11. Prophases, S. Vfroniciie, showing separation
of idiochromatin and its accumulatin on the linin. Maire
and Tison, '09.
Fig. 12. Early prophase nucleus, L. Juiici, with wheel-
like structure. Schwartz, '10.
Fig. 13. Separation of idio- and Irophochromatin in
karyosome during early prophase, S. Callitrichii). Winge,
'13.'
Fig. 14. Early prophase, L. Jiinci, showing formation of
chromatin ring around nucleole. Cook, 'J8.
Figs. 15, 10. "Saturn" stages of promitosis, L. Juiici.
Cook, I.e.
Figs. 17, 18. "Cruciform" stages with elongating nu-
cleoli, L. .IiincI and T. Tri</lorh!nix. Cook, I.e.; Maire and
Tison, '11.
Fig. 19. Splitting and sejiaration of chromatin ring, and
constriction of nucleole, L. .Tiniri. Cook, I.e.
Fig. 20. Later stage, L. .Jiiiici, showing division of nu-
cleole. Cook, I.e.
Fig. 21. "Double anchor" stage of promitosis, L. .Time!.
Cook, I.e.
Figs. 22, 23. Formation of daughter nuclei, L. .Tiiiiri.
Cook, I.e.
Fig. 34. Wheel type of resting nucleus, ./. iniinirohi.
Chatton, '10.
Fig. 2.'). Early prophase, ./. froschi. Nagler, '09.
Figs. 26, 27. Equatorial plate stages, ,1. lacustri'i. Nag-
ler, I.e.
Fig. 28. Same stage, A. inii,iicoIa. Chatton, I.e.
Fig. 29. Early anaphase, Vahlkiniipfia liiiiax. Calkins,
'33.
Fig. 30. Later anaphase, J. frnschi. Niigler, I.e.
Fig. 31. Similar stage, A. musicoUi. Chatton, I.e.
Fig. 32. Telophase, A. mu.iirola. Chatton, I.e.
Fig. 33. Reconstructed daughter nuclei, ./. froschi. Niig-
ler, I.e.
Fig. 34. Wheel type of resting nucleus, Spoiif/o.iporn siib-
terraiien, with nucleole, radiating linin threads, and chro-
matin granules. Home, '30.
Fig. 3.5. Resting nucleus, Soro.'!phaera Veronicae, with
eentrosomes and astral rays. Home, I.e.
Figs. 3(j, 37. Early prophase, S. Veronicae. Webb, '35.
Fig. 38. Same stage, P. Br<i.isicoe. Terby, '23.
Fig. 39. Spireme stage, >S'. xiibterroiiea. Home, I.e.
Figs. 40, 41. Late prophases, S. Veronicae, with four
elongate chromosomes. Webb, I.e.
Figs. 42, 43. Later stages, 8. Veronicae. Chromosomes
showing prophase split. Webb, i.e.
Fig. 44. Polar view of equatorial plate, S. Veronicae,
with four split, twisted chromosomes. Webb, I.e.
Fig. 45. Early equatorial plate, S. Veronicae, with four
Ll-shaped chromosomes. Webb, I.e.
Fig. 48. Equatorial plate or "Saturn-stage," S. Veroni-
cae, witb four chromosomes end to end in a ring around the
constricted nucleole. Webb, I.e.
Fig. 47. Similar stage, P. Brasnicae. with nucleole break-
ing up into globules. Terby, "32.
Fig. 48. "Saturn-stage," in S. nuhterranea with three of
the four chromosomes arranged in a ring. Home, I.e.
Fig. 49. Oblique view, N. Veronicae, of same stage. Webb,
I.e.
Fig. 50. Equatorial plate, P. Bra,<isicae. stained with
Feulgen's nuclear stain; nucleole colorless. Milovidov, '33.
Fig. 51. Metaphase, S. Veronicae, showing start of chro-
mosome separation. Webb, I.e.
Figs. 52-61. Successive anaphase and telophase stages,
S. Veronicae. Webb, I.e.
Figs. ()2, 63. Formation of daughter nucleoli f rimi gran-
ules in telophase nuclei, P. Bra.i.iicae. Terby, I.e.
Fig. 64. Daughter nuclei, ]'. Brasnicae, with remanent of
old nucleole between. Terby, I.e.
Fig. 65. New formed nuclei, P. Brasaicae. with rema-
nents of old nucleoli in the cyt()]ilasm. Terby, I.e.
t YTOLOGY
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PLASMODIOPHORALES
bodies in Tetramy.ra (PI. 5, fig. 5) and Sorodisciis
(PI. 7, fig. 12), which lends support to tiie later
views of Terby, Home, and Webb that definite
chromosomes are present in the vegetative divisions.
The origin of the spindle has not been clearly dem-
onstrated in promitosis. Wiiether it originates frcmi
achromatic linin material, tropiiocliromatin, or in
relation to centrosomes and asters is not sufficiently
known. Nawaschin, Favorski, Osborn, Cook and
Schwartz, and Webb found no centrosomes and
asters during the vegetative divisions in Plasmodio-
phora, Lic/niera, and Sponc/ospora, but Prowazek,
Maire and Tison, Winge, Lutman, Nemec ('13),
Home, and Milovidov ('31) observed them in P/<i.v-
modiophora, Lif/niera, Tetrami/ja, Anisomyj:a (Lif/-
nieraf), Sorodisciis, and Sorospliaera (fig. 2, 10, 18,
3.5). Notliing is known concerning their presence or
absence in Membranosorus, Polymyjca. and Ocio-
myxa. Maire and Tison figured them in uninucleate
amoebae of S. Veronicae (fig. 3) and contended that
the centrosomes are derived from the karyosome and
may retain contact with this body by a slender chro-
matic strand. In P. Brassicae, however, instead of a
single body Miss Terby ('23) found a circle of five
to six granules around tlie poles of the nucleus from
which the aster-like filaments radiate.
In the early equatorial ring stage, the globular
nucleole may often be found in the center of the spin-
dle (fig. 15) surrounded by the peripheral ring of
chromatin, according to Cook and others, and be-
cause of its characteristic ajipearance this pliase has
been described as the "saturn" stage of promitosis.
The nucleole or karyosome then begins to elongate
and constrict in the center (fig. 16-18). In longitu-
dinal view the ring of chromatin and elongate nu-
cleole present the appearance of a cross, and this
phase is accordingly referred to as the "cruciform"
stage. The chromatin rings then split lengthwise, ac-
cording to most workers, and the two daughter rings
move apart witli the ends of the elongating nucleole
(fig. 19). The latter may divide completely in the
early anaphase (fig. 20), or the two ends may remain
attached for some time by a chromatic strand (fig.
21). The latter condition is usually described as the
"double anchor" or "dumb-bell" stage of promitosis.
The nucleole finally divides into two daughter nu-
cleoli, and the curved, lialf-moon-shaped bands of
chromatin curve around them (fig. 21, 22) until they
are enclosed in a more or less complete sphere, ac-
cording to Cook. In this manner the karyosome of
the daughter nuclei is built up of a peripheral layer
of chromatin and a central core of strictly nucleolar
material. In the meantime, the spindle fibers dis-
appear, while the nuclear membrane becomes drawn
out, curved and somewhat crescentrie. It then con-
stricts sharply in the equator and pinches in two.
according to Cook (fig. 22), forming the daughter
nuclei (fig. 23) which soon move apart and become
spherical.
Although variations in the jjrocess of promitosis
described above have been noted by some workers,
most of their views are in agreement about its fun-
damental outlines. However, P. M. .Tones' ('28) de-
scription of division in what he believed to be P.
Brassicae is quite different, contradictory, and as
Milovidov characterized it, whollv fantastic. "After
the nucleus has become very large, the karyosome
moves to one side, and then escapes from the nucleus.
The karyosome, during this movement, assumes a
dumb-bell sliape and starts dividing by promitosis.
When the karyosome has completely left the nucleus,
it undergoes rapid division, by mitosis, until the Plas-
modium becomes filled with little nuclei. These nu-
clei increase in size to form a multinuclear Plasmo-
dium. The Plasmodium stops feeding and assumes a
frothy appearance. The nuclei becomes vacuolated,
chromidia are distributed around tlie vacuoles, and
collect into new vacuoles, to form new nuclei . . . . "
It is to be particularly noted that the majority of
the early cytologists interpreted the karyosome in
terms of the duality concept of the cliromatin. They
believed that the chromatin which forms the equato-
rial ring and the division nucleole are derived from
the karyosome. This body is accordingly dual in
structure and consists of idio- and trophochromatin
which separates in the prophases, the latter forming
the dividing nucleole and the former the chromatin
ring. Maire and Tison described the division of the
tropochromatin as amitotic and that of the idiochro-
matin as indirect or mitotic. According to them, the
karyosome at rest is comparable with the nuclei of
Trypanosoma nociieae or Amoeba limaj:; during di-
vision it corresponds to the karyosome of Cari/otro-
pha mcsnilii, to tiie macronucleus of the Infusoria, to
the true chromidia of Goldschmidt, and to some ex-
tent to the nucleocentrosome of Euf/lena.
The type of division illustrated in figures 1 to 31 is
obviously very similar to promitosis, in the strict
sense, which has been described in certain species of
amoebae. In order to compare the processes more
concretely, drawings by Nagler, Ciiatton, and Cal-
kins of successive promitotic stages in such species
have been brought together in figures 21 to 33. Both
the wheel-like (fig. 24) and "vacuolate" resting nu-
cleus (fig. 25) with large, conspicuous karyosomes
have been reported in Amoeba and these are strik-
ingly similar to the nuclei shown in figures 1, 2, l,
and 31 of tlie Plasmodiophorales. Division is like-
wise intranuclear. No sharply defined spindle and
chromosomes are formed, but instead the chromatin
aggregates into a more or less continuous band across
the equator (fig. 26—28). As the karyosome elon-
gates, constricts, and divides, tlie cliromatin band
splits lengthwise (fig. 29), and the daughter halves
migrate toward the opposite poles of the nucleus (fig.
30, 3 1 ) where they are incorporated with the daugli-
ter karyosome (fig. 32). As the nuclear membrane
disappears in the equator (fig. 32), new membranes
are develo])ed around the karyosome. and the daugli-
ter nuclei (fig. 33) are thus formed.
To this extent the similarities are very striking —
so much so, in fact, that as one reads the accounts
of some students of the Plasmodiophorales it be-
comes obvious that their observations have been in-
( YTOI.OCiY
fluoiu-fd liy tlio ('••irlior di-sc-riiitions iif Niijilcr. C'li;it-
toii, Ah'xicff. I'tc cif promitosis in .Initichn. IIow-
i-vt-r. oiu- in.-irkrd (lifftTfiU'C i.s iipiiart-nt. In tiic I'las-
niodiopliorali's tlii' kjirvosonu' (lot's not apiu-.ir to
fiiiu'tion as a nucli-o-i-ontrosomc durinjc division. In
sevt-ral jriiura of this ordiT cU-arly-detint'd crntro
sonu's and astral rays have Ucvn rci)ortfd. strui'turts
wliicli arc latkina- i!i tlic mitoses shown in fiiiurts 2 !■
to ."i.'t. \\ Inthir or not the division spindle orii;inates
in relation to the eentrosonies in the i'lasnio(iio|)ho-
rales is still uneertain. The most strikinj; ditlerenee.
however, between the two types of division in these
two a:rou|)s. aeeordins; to Terhy. Home, and Webb,
is the jiresenee of sharply-defined ehromosomes in
the i)rophases and the equatorial ring stages. This
differenee will beeome more a])i).irent in the discus-
sion which follows.
Turnini; now to the observati(nis of Terhy, Home,
and Webb, these workers contended tii.it the failure
of previous investigators to find ciiromosomes in the
vegetative divisions was due to insufficient study of
the propliases where the chromosomes originate. In
Spotuiospora and Sorospharra, Home found wheel-
like resting nuclei (fig. 3t) with large karyosomes.
radially oriented achromatic strands, and numerous
chromatin granules, but he did not regard this as a
constant and static structure of resting nuclei. Ac-
cording to him. the structure may change during the
various developmental phases. In Sorosphaera he
found consiiieuous centrosomes and astral rays dur-
ing the i5roi)hases (tig. 3.5). but such structures were
never observed by U'cbb. possibly because the latter
eniploved a strictly nuclear stain. By using a modifi-
cation of Newt(Mi's gentian violet-iodine method,
Webb was able to detect small chromatin granules
connected by fine threads throughout the resting nu-
cleus. The first visible evidence of division is an in-
crease in the staining capacity of the chromatin gran-
ules (fig. 36) which soon becomes alined on the
threads (fig. 37). according to Webb. These threads
contract as they move away from the ))eri))hery and
form slender chromosomes (fig. 1-0) directly, with-
out ))revious deveIoi)ment of a coiled spir<nie stage.
Home likewise observed a thickening of chromatic
rods projecting from the nuclcolc as the first indica-
tion of |)ro))liase. Later an irregular chromatic net-
work emerges which goes into a tyi)ieal coiled spi-
reme (fig. 39) from which the chromosomes even-
tu.allv emerge. Hornc found mimerous ))ost-s))iremc
configurations with only two or three \'-sha))ed chro-
mosome, but he nevertheless believed that the ha))-
loid number in Spone/ospora is four. Miss Terby
also found mimerous rods and threads in the pro-
phase nuclei of P. Brasxicae (fig. 38) from which
the chromosomes are subsequently formed. Milo-
vidov. on the other hand, was unabh' to recognize
chromosomes in material stained Viy l-'eulgen method.
Returning to Webb's account of Sorosphaera, the
four chromosomes contract further in the prophases
and become V- and U-.shaped (fig. H. Vh). and soon
thereafter s)>lit ends become visible (fig. t2). indi-
cating a splitting of the chromosomes in jirejiaration
for division. Uj) to this time the nueleole reni.iiiis
more or less globui.ir. but it soon begins to elongate
in the direction of the poles. The chromosomes then
become arranged end to end in .-in irregular, liroken
ring in the equator of the nucleus (fig. 13). \ jiol.ir
view of such a stage is shown in figure H- with the
s))lit .and twisted chromosomes lying near the i)cripli-
ery of the nuclear menibrane. Following this stage,
ihev contract and thicken, so th.-it the longitudinal
split is no longer \ isible (tig. Ki). The ehroniosomes.
nonetheless, retain their iiuiividu.ility . according to
Home's and Webb's dr.-iwings. .'is is shown by the
breaks in the equatorial ring (fig. K>. IS, li)). This
ring stage persists for a comparatively long time
and is the one most frequently observed in the vege-
tative divisions.
,\eeording to Home's and Webb's figures, the
elongate nueleole may become slightly constricted at
this stage in preparation for division (tig. Vd. IS).
.Miss Terby ('"^3). however, found that the nucleolar
changes vary considerably in P. Brassicar. Instead
of constricting and dividing more or less equally, it
may fragment into two or more unequal parts (fig.
Vl) or move intact as a single body to one of the
poles. Oftentimes, jiarts of it remain stranded be-
tween the daughter nuclei (fig. GK 65) as in higher
plants.
The metaphase split reapjiears first in the median
region of the chromosomes (fig. 51 ) at the conclusion
of the equatorial ring stage and travels outward to
the ends, which suggested to Webb that the spin-
dle fiber attachment is median. As the chromosome
halves separate, two daughter rings are formed (fig.
52) which migrate toward the opposite poles (fig.
33-57) until they reach the ends of the elongate
nueleole (fig. 56, 58. 59). According to Webb, the
nueleole in Sorosphaera does not constrict as a rule
until telophase (fig. 57-59). The two parts finally
separate and become surrounded by daughter ehro-
mosomes (fig. 60) at the poles of the nucleus. The
nuclear membrane then constricts and divides in
much the same manner as the nueleole .and thus forms
the daughter nuclei (fig. 61). The ciiromosomes ad-
iiere to the nueleole at first, but later sejiarate from
it. Miss Terby. however, maintained that the nucleoli
are formed anew at each telophase in P. Brassicae.
.\fter the daughter nuclei have been formed, the
chromatin mass gives ofl' material which unites to
form the daughter nucleoli (fig. 62. 63). .As to the
origin of the daughter nuclear areas. Miss Terby
('23) reported that they begin in the projihases as
two hyaline vesicles on the jiolar sides of tiie nu-
eleole. As the latter elongates, divides, and the two
segments separate, the vesicles ])recede them to the
|)olcs of the nucleus. The vesicles then pass through
the nuclear membrane at the ))oles and expand, and
shortly thereafter the d.aughter nuclcol.ar segments
and chromatin enter .uid are thus incor|)or;ited in the
vesicles. The boundaries of the vesicles become the
nuclear membranes and thus constitute the limits
of the daughter nuclei. In a later paper, however.
Miss Terby ('32j modified this account and rejiorted
10
PLASMODIOP MORALES
that the polar vesicles contract to small globular
areas surrounded by granules from which astral rays
radiate, as noted elsewhere. Thus the vesicles them-
selves do not become the nuclei, but tlie daughter nu-
clei are formed in the areas occupied by the vesicle
before contracting.
The type of division described by these three
workers is distinctly mitotic and, except for the be-
havior of the nucleole, according to Home's and
Webb's figures, is fundamentally similar to nuclear
division in the higher plants. Miss Terby, as noted
before, held that the nucleole also undergoes the
same changes as in the higher plants, so that there is
no difference in this respect either. On the other
hand, the divisions figured by Home and Webb are
also similar to tlie promitoses illustrated in figures 1
to 23. The chief difference is the presence of chromo-
somes. It is not improbable, as Webb contended, that
the earlier workers overlooked the early prophases
and the origin of the chromosomes and that their
fixation and staining technique did not differentiate
chromosomes in the equatorial ring. As noted else-
where, the nuclei of the Plasmodiophorales are quite
small, and their structure is difficult to interpret. The
use of more specific and refined technique in inten-
sive study of the early prophases and equatorial ring
stages may thus possibly eliminate the present con-
troversy on the nature of the vegetative divisions.
In tliis relation it is to be noted tliat typical mito-
sis without large nucleoli has been reported in the
vegetative zoosporangial stage of Ligniera, Plasmo-
diophora, Polf/mt/J-a, and Ociom_i/xa by Cook ('26,
'28), Cook and Schwartz ("30), Ledingham ('39),
and Miss Whiffen ('39). In these as well as other
genera the zoospores from germinating resting
spores develop into plasmodia which eventually
cleave into uninucleate segments — the rudiments of
zoosporangia. These segments develop walls, and
their nuclei divide twice to several times in a strictly
mitotic manner in preparation for zoospore forma-
tion. Cook and Schwartz reported that up to tlie time
of cleavage into zoosporangial segments the nuclei
in the plasmodia of Ligniera and Plasmodiophora di-
vide promitotically, but in Polymyxa I^edingham re-
ported that division in the thalli which form zoospo-
rangia is mitotic from the start. Miss Whiffen also
found that the divisions in the zoosporangia of Octo-
miiia are mitotic. These authors thus reported a
regular alternation of mitosis and promitosis. The
zoosporangial stage is characterized by mitosis, then
follows a phase of premitotic division in the early de-
velo))ment of the sporogenous plasmodium which is
terminated by the so-called transitional stage, and
finally two meiotic divisions. Inasmuch as the divi-
sions in the zoosi)orangia are mitotic and very simi-
lar to the two divisions at sporogenesis. Cook ('26,
'28, '33) and Fedorintschik ('3.5) concluded that
they are meiotic in Ligniera and Plasmodiophora,
respectively. In P. Brassicae, however. Cook and
Schwartz described them as merely mitotic. In an
attempt to explain the alternation of meiosis and pro-
mitosis in this species, they proposed the theory that
promitosis is characteristic only of diploid nuclei, a
theory which is contradicted by their own observa-
tion that the first meiotic division of the diploid nu-
cleus in spore formation is indirect and not pro-
mitotic. Furthermore, if Cook's ('28, '33) previous
report is correct that the primary nucleus of the in-
cipient zoosporangia in Ligniera is diploid (and un-
dergoes meiosis), it should accordingly divide pro-
mitotically. However, he described and figured such
nuclei as dividing mitotically.
The report of typical mitotic divisions during zoo-
spore formation, promitosis in the developmental
stages of the sporogenous plasmodium, and the re-
occurrence of mitosis during the reduction divisions
nevertheless raises numerous questions on the signifi-
cance of this alternation (if it actually does occur),
and it is thus obvious that future studies of karyo-
kinesis in the Plasmodiophorales must be closely
correlated with the various developmental phases.
"Akaryote Stage"
The period of vegetative divisions in the develop-
ment of the sporogenous plasmodium is reported to
be followed shortly by the so-called "enucleate."
"akaryote," "chromidial" or "transitional" stage.
According to most workers, this phase is charac-
terized by a reduction in size and disappearance of
the karyosome, comparatively empty, vacuole-like
nuclei, and the presence of numerous deeply-stain-
able bodies or chromidia in the cytoplasm around the
nuclei. Nawaschin first observed this stage in Plas-
modiophora in 1899. and since that time it has been
reported by most subsequent students for the other
genera of this order. In the opinion of many cytolo-
gists it is thus as constant and diagnostic a character
of the Plasmodiophorales as promitosis.
Stages in the development of the akaryote stage
are shown in Plates 2 to 13, which illustrate the life
cycles of all the plasmodiophoraceous genera, and
will not be illustrated separately at this point. After
the vegetative divisions have been completed, the
karyosome decreases in size as the somatic or tro-
phochromatin is extruded into the cytoplasm in the
form of secretory chromidia, according to Prowazek
('05), Maire and Tison ('09), and others. Maire and
Tison regarded this extrusion as a cleansing process
by which the generative chromatin is separated from
the nutritive chromatin in preparation for the sporo-
gonic divisions which follow. As a result of this ex-
trusion, the nuclei, when stained with haematoxylin.
appear comparatively empty and devoid of stainable
material and frequently have the appearance of vac-
uoles in a cytoplasm filled with deeply-stained chro-
midia.
According to Blomfield and Schwartz, Schwartz,
and Osborn, extrusion of chromatin in Sorosphaera,
Liqniera, and Spongospora takes place along the
linin threads until the chromatin reticulum and
karyosome have disappeared. These workers be-
lieved that the nuclear membranes also disappear
during this stage. In L. Jiinci, Schwartz described
the process as follows: "the nuclear membrane dis-
t YT()I.<)(iY
11
appc.-irs. ;in(l tlic k.'irvosdiiic (liiuinislios in size ;iikJ
finally disappoars also, so that wt- have a number of
vacuoles more or l<ss eireular in outline situated in
the spherieal mass of plasma." Osliorn likewise de-
serilied the disappearance of tlie nuclear membrane
in Spoil (/(IS pora and the formation dc iidfd of new
nuclei. F. M. Jones ('28) also maintained that the
nuclei disajjpear completely in P. Brassicae and that
the new nuclei are formed by the agfjre^ation and
fusion of chrouiidia within small vacuoles. Cook (''i(i,
"28) described a complete extrusion of chromatin
from the nuclei of L. Jiiiici, but later he and
Schwartz reported that in P. Brassicae a .small
amount of chromatin may remain within the nuclei.
They, nevertheless, refuted the reports of previous
workers that the nuclear membrane disappears.
However, in SoTodiscus radicicolus. Cook later ('31 )
rejiorted that all of the chromatin is extruded during
the akarvote stage .-iiid later re-enters ( I ) the nucleus
in preparation for meiosis. Winge, on the other hand,
found no marked chromatin extrusion and akarvote
condition in S. Callitrichis and referred to the
changes which the nuclei undergo in preparation for
meiosis as the transitional stage, a term later adopted
by Home and Webb. In Spongospora, Home also
noted tliat the nuclear membrane remains clear and
distinct throughout this stage and the nuclei have a
well-defined chromatin reticulum, chromidia. and a
faintly-stainablc nucleole. Similar stages were found
bv Miss Terby ('21-) who denied the existence of an
akarvote stage in P. Brassicae. By using Newton's
gentian violet iodine stain on Sorosphaera, Webb
also found the normal interphase chromatin reticu-
lum and a large faintly-stainable nucleole present
in the nuclei during the transitional stage. His ob-
servations were later confirmed in part by I.eding-
ham's study of I'oli/mi/j-a. The latter worker ob-
served a well-difined reticulum in nuclei stained by
Newton's method, whereas in preparations stained
with iron-alum haematoxylin the nuclei appeared to
be devoid of chromatin. The latter four workers ac-
cordingly refuted previous cytologists on the pres-
ence of marked akarvote stage at the conclusion of
the vegetative divisions.
With the excejjtion of Terby. Home, Milovidov.
Webb, and Ledingham. most workers have described
a definite reorganization of nuclei following the so-
called akarvote stage. As noted before. Schwartz,
Osborn. and .Jones contended that the generative nu-
clei arise de novo on new sites in the eyto])lasm from
extruded chromatin, while Blomfield and Schwartz
were uncertain about their origin in Sorosphaera. All
other workers, however, held that the nuclear mem-
branes persist and that the nuclei undergo certain
characteristic changes. During this process centro-
somes and astral rays become quite consj)icuous in
the cyto|)lasm. but it is not certain whether they arise
de novo and divide or originate from the karyosome,
as Maire and Tison contended. Whereas several
workers denied the ))resence of these structures dur-
ing the vegetative divisions, most of them agreed that
centrosomes and astral rays are conspicuous features
of the reconstructed nuclei .and si)orogenous divi-
sions. However, Blomfield, Schwartz, and Cook .a))-
p.areiitly never found these structures in any of the
developmental stages of Li(/iiiera, Sorosphaera, and
Plasniodiaphora, since none of their figures show
centrosomes and asters. Concomitant with the devel-
opment of these cyt()))lasmie structures, chromatic
strands, granules, and other configurations appear
in the nuclei, which are generally regarded as i)ro-
|)hases of meiosis and will be discussed in greater de-
t.iil below.
It is al)parent from this discussion that the ob-
servations of the early cytologists of the Flasmodio-
|)lii)r.ilcs were gre.itly iuHueneed by the chromidia
iiypothesis of Cioldsehmidt. Seiiaudin. Poiiott'. .md
other protozoologists of that jieriod. Its infiuence
is also evident in the more recent contributions of
P. M. Jones and to a large extent in the papers by
Cook and Schwartz. Lack of space does not allow a
detailed account of the chromidia hyjjothesis here.
Suttiee it to note that in .Ictinosphaeriiim, Arcella,
.irachnula, Eiitamoeha, and numerous other rhizo-
poda R. Hertwig, Sehaudin, Popoff, Dobell, and
others reported a gradual disajipearance of the nu-
cleus as chromidia are extruded into the cytoplasm
and the subsequent formation of new nuclei in repro-
ductive cells from chromidial granules. These obser-
vations among others were the foundation of (Jold-
schmidt's theory and eventually led to the "binu-
clearity hypothesis" of Sehaudin. Prowazek. Maire
and Tison. Blomfield and Schwartz, and others in-
terjjreted the akarvote and reconstruction stages of
the Plasmodiophorales in terms of this chromidia
hypothesis, while Schwartz, Osborn, and Jones ap-
pear to have adopted this theory completely as an
explanation of the changes undergone by the nuclei
during these phases.
The chromidia hypothesis has been largely dis-
credited in the last three decades by researches in-
volving the use of mitochondrial fixatives. Feulgen's
nuclear stain, and other more specific fixatives and
staining techniques. In Arcella and Clami/dophrt/s,
for instance, the nuclei do not disintegrate as was
jireviously claimed, according to ,lollos, but instead
are masked during certain stages by a chromidial
network which can be dissolved away in trypsin and
pepsin, leaving the nuclei sharp and clear. That this
network is not com])osed of chromatin derived pos-
sibly from the nucleus is evident by its negative re-
action to Feulgen's stain. Likewise, in most of the
earlier reported cases of chromidia extrusion and
growth, the so-called chromidia have been found to
relate to chondriosomes, ergastic, reserve, and de-
generative products of metabolism, etc. In .Ictino-
sphaeriiim, classic exam])le of chromidia extrusion,
Rmnjantzew re))orted that the chromidia ajjpear to
be composed of a carbohydrate held in a mechanical
or perhaps adsorbtive imion with a protein. In Dif-
fliif/ia they a])pear to be com))osed of glycogen, ac-
cording to Zuelzer, while in Kimeria they are made
up of volutin or metachromatin which have a strong
affinity for basic dves. Additional cases of this na-
PLASMODIOPHORALES
ture may be cited to show that what had previously
been regarded as chromatin extruded from the nu-
cleus is now known to be chondriosomes, reserve, and
degenerative products of metabolism. Belar ('26)
thus characterized the present status of the chro-
midia theory as follows: "Die Lehre vom Chroma-
tindualismus steht und fallt mit einer unkritischen
P'assung des Cliromatinbegriffs, sie is das posthume
Produkt einer naiven Interpretation der histologis-
chen Fiirbung." In light of tliese more recent data
from the field of protozoology, Prowazek's, Claire
and Tison's, Blorafield and Schwartz's, Schwartz's,
Osborn's, Cook's, and Jones' interpretations of chro-
matin extrusion, chromidia, and the origin of the
generative nuclei in the Plasmodiophorales need re-
vision.
Milovidov attempted to do so in a restudy of the
akaryote and nuclear reconstruction stages in Plas-
modiophora with the aid of mitochondrial fixatives
and Feulgen's nuclear stain. From these studies he
concluded that the so-called chromidia in the cyto-
plasm are nothing more than chondriosomal residue,
excretions, or secretions. He found that shortly be-
fore spore formation the plasmodium becomes quite
vacuolate and tliat chondriosomes and other bodies
may frequently lie within such vacuoles. This ap-
l^earance, according to him, is the basis for Schwartz,
Osborn, and Jones' claim that new nuclei arise de
novo in vacuole-like areas from extruded chromatin
granules. With Feulgen's stain such granules show
no positive chromatin reaction. As to the presence of
a marked akaryote stage with nuclei partly or com-
pletely devoid of chromatin, Milovidov discredited
previous workers and maintained that it does not
exist as a distinct developmental phase of the Plas-
modiophorales. He contended that the plasmodium
does not fix and stain uniformly throughout all of its
developmental phases, so that fixatives and stains
wliich give good preparations of one phase are un-
suitable for anotlier stage. In none of the properly
fixed and stained plasmodia did he find empty, vac-
uole-like nuclei. Instead, when so-called enucleate-
and akaryote-like stages described by previous work-
ers were stained by F"eulgen's method, the nuclei
were found to have numerous chromatic granules,
strands, and spireme-like threads, all characteristic
of meiotic projjhases. Milovidov thus concluded that
the akaryote and nuclear reconstruction stages of
earlier cytologists relate in part to artifact, as Miss
Terby had earlier pointed out, misinterpreted mei-
otic prophases and telophases, poorly fixed and
stained resting nuclei of vegetative plasmodia, and
abnormal nuclei of degenerating schizonts and plas-
modia. His contentions are supported to a great ex-
tent by the failure of Maire and Tison, Winge,
Terby, Home, Webb, and Ledingham to find marked
akaryote stages in Trtrami/j-a, Sorodixciis, Pla.smo-
diophora, Spoiif/oxpora, Soiosphaera, and Polymy.ra,
respectively.
Meiosis
It is now ratlier generally believed that meiosis oc-
curs during the last two divisions before or during
cleavage into resting spores, and tliese divisions arc
respectively referred to as hetero- and homeotypic.
Nawaschin first noted these divisions in Plasmodio-
phora but reported only one mitosis before spore for-
mation. Prowazek ('05) found two mitoses, and since
that time two divisions have been universally re-
ported. Claire and Tison ('09) were the first to count
the chromosomes during these divisions in Soro-
sphaera, and because tlie number appeared to be
lialved in the first divisions they accordingly con-
cluded that these divisions are reductional. Tlieir
interpretation has been accepted by most subse-
quent workers. Exceptions to this view, neverthe-
less, may be found in the literature. Prowazek ('05)
reported that reduction in Plasmodiophora occurs
during maturation of the resting spores following
autogamy or a previous fusion of cleavage segments
or incipient spores. Winge contended that a numeral
reduction of chromosomes takes place in the second
instead of the first sporogonic division in Sorodisciis.
More recently Cook ('26, '28, '33) and Fedorintschik
('35) reported a second reduction division in the zoo-
sporangia or gametangia of Ligniera and Plasmodio-
phora in addition to the one which occurs at sporo-
genesis. According to Cook ('33, p. 221). the two
reductions in Ligniera are necessitated by a double
fusion, one between "swarm cells" and tlic other
between zoospores. F'edorintschik reported only one
fusion in P. Brassicae. However, neither of these
workers counted the cliromosomes during the first
two divisions in the zoosporangia, and their conten-
tion that these divisions are meiotic is based solely
on the similarity in appearance of the latter to the
reduction divisions at sporogenesis. In Tetrami/xa
Elaeagni, Yendo and Takase ('32) reported tliat the
sporonts are haploid. which presupposes a reduction
before the plasmodium cleaves into spore mother
cells or sporonts.
As noted before, most cytologists reported that
the vegetative meiotic divisions are separated by a
marked akaryote stage, but Terby, Home, Webb,
Ledingham, and particularly Milovidov failed to
confirm these reports. Thus, the latest data from
carefully fixed and stained material suggest tliat the
akaryote stage of the early workers relates in part
to an achromatic phase of the nucleus and partly to
the meiotic ])rophases. Prowazek's ('05) figures 17
to 22, for example, show chromatin reticula, loops,
garlands, spireme threads, and eight chromosome-
like bodies which are very characteristic of the mei-
otic prophases of later workers.
Following the more or less achromatic transitional
phase, tlic nucleole and chromatin filaments of Soro-
sphaera, Plasmodiophora, and Spongospora, accord-
ing to Maire and Tison ('09), Terby ('24) and
Home, become more basophyllic and clearly visible
in tlie nucleus. At tlie same time sharply defined cen-
trosomes and asters apjjcar at tlie poles. The chro-
matin then aggregates at tlie poles into two more or
less dense masses, which may remain connected by
fine chromatic filaments. This is the so-called "gar-
land stage" of meiosis. Home found that each polar
( YTOl.OCY
18
nuiss is <'()iii))i)s((l (if fiiiir ilistiiu't clironiosoiius in
.S'/i()Hf/(».\7»()ro. Sonuwiiat siniil.ir c-irly clianuis wen-
riportcd \<\ M.iirc .uul Tisoii (11) and \\ iimc tor
Tftramtidti, W'injrc for Sorixliscitx (Fl. 7. (ij;. Ml, 2;i,
21), Wingc and W't'lib for Soro.iphnrra (Pi. (5,
fig. 29, 30), Terliv (21) for /'. lirassicai-, and Cook
('31) for S. radicicolus. Winge fonnd tliat tlu- two
polar niassts may he arranged in tlu' form of gar-
lands with I'oiinci'ttd filanu-nts. an arrangtuu-nt jirc-
vioiisly reported by Frowazek for /'. Hrax.iicar, and
snl)se<iiiently by Terby (I.e.) and Cook (I.e.). The
nueleole may gradnally disaiJjiear dnring this st.ige
or beeome tjattened and aggregated with the eliro-
inatin ma.ssc.s and filaments at one .side of the nuelen.s.
Tlii.s nnelear eonfigiiration is strikingly similar to
the eollapsed .synizetie (zygotene) stage in higher
plants. In the Flasmodiophorales. however, it is gen-
erally referred to as synapsis and has been so far
rei)orted as sueh in PlasniotUophora (Terby, Cook
.and Sehwartz. .Milo\ idov), Spdiif/ospora (Osborn,
Home), SoTOsphaera (Maire and Tison, Webb), and
Sorodisciis (?) (Winge). In Spoiu/ospora, Home
found two contraction stages and designated the sec-
ond one as .synapsis. Each loop in the second contrac-
tion stage is converted directly into a heteroty|)ic
chromosome. Cook ('28) found no meiotic jirophases
in L. Jiinci, and in P. Brassicae he and .Schwartz re-
])orted and figured only one stage wliieh might be
interpreted as such. The chromatin was arranged
in a thick thread with several globular nucleole-
like bodies distributed along its length. Cook and
.Schwartz regarded this stage as com))arable to syn-
apsis, but it bears little or no resemblance to the
synajitie stage figured by other workers.
Before or during the contracted stage, the nueleole
disappears, while the chromatin threads loosen up
and take on the appearance of elongate chromo-
somes. According to Webb, in Sornsphaera the chro-
matin at this stage consists of beaded threads spread
over the |)eri))hery and has the ajipearanee of a nor-
mal ))aehytene. Tlie threads occasionally appear
double, and after further contraction four chromo-
somes become visible (PI. 6. fig. SJ). This stage
corresponds to diplotene in higher plants, according
to Webb. Then follows diakinesis (PI. (5. fig. 3.5).
during which four well-defined bivalents are visible.
In /'. Brnssicae, Cook and .Schwartz failed to find
comi)arable stages and merely reported that the
chromatin thread segments into chromosomes as the
nucle.ir membrane disa])i)ears. Miss Terby (^t), on
tlie other hand, found well-defined stre))sitene. early
and late diakinetic stages (PI. 3. fig. ()8-71) with
four bivalent chromosomes in P. lirassicae, which
indicates that Cook and Schwartz overlooked these
|)liases. \ diakinetic stage with thick broadly
\'-sha|ied ;ind ring diromosonies was also observed
by Home in SpDiKjospora.
.Shortly after diakinesis the nuclear membrane dis-
appears, and tlie chromosomes become oriented in
the equator of a well-defined divi.sion sjjindle with
centrosomes and asters. .•\!1 other workers reported
that the nuclear membrane disajjpears during meta-
phase. but in Plniiiunlidpliiira and Spoiiijospora,
Prowazek ,inil Ilorni' figured it as persisting until
tlu' telophases. The origin of the nuiotic spindle has
luit been sohcd, but \\ ilib lielie\cd tli.at it grows in-
ward from the Jioles to the equator. According to
most cytologists the heterotyi>ic ehronu)somes are
closely associated on the equatorial ])late and in
metai)hase and often appear as an irregular band or
row of connected globules, so that the ))rofile and
))ol;ir views ;ire not very ciiaracteristic of hetero-
ty|)ie divisions. In Spiitifidxpora, however. Home
figured the chromosomes .-is short .-md thick with con-
s|)icu()us intervening ga))s in the t(i\iatorial jilate,
wliieli makes it possible to recognize and count the
individual members. At this stage tliey may often
show four blunt ends, which indicates their tetrad
nature, according to Home.
With the excei)tion of Winge, most cytologists
held that the homologues separate at metapliase of
the first division and move to the ))oles where they
are incorporated in the daughter nuclei. In Soro-
xphnera, ^A'ebb found the late ana))hase and telo-
phase chromosomes to be double, which suggests that
the equatorial split for the homeotypic division oc-
curs quite early. Cook ('28) failed to see nuclear
membranes in the late telo)ihases of L. Jitnci and
thus concluded that they are no* formed between the
first and second divisions. All previous and subse-
quent workers, however, have shown that a well-
defined membrane develops around the telo))hase
groups of chromosomes and that daughter nucleoli
are subsequently formed. Interkinesis is usually
short in duration. In P. Brassicae Miss Terby ('2f)
reported that the telophase nuclei go directly into
the prophases of the next division, but in Spongo-
spora wheel-like resting nuclei and distinct pro-
))hases may intervene between the two divisions.
The second division is likewise mitotic or indi-
rect but considerably smaller in size than the first
one. Palling to count the chromosomes. Cook and
Schwartz regarded this size difference as ))roof that
these two divisions are res])eetively hetero- .ind ho-
meotypic. a criterion which is obviously of no critical
\alue in this respect. Osborn. Milovidow \\'ernham,
Whitf'en. and others also made the s.ime assuiu))tion
without counting the chromosomes. On the other
hand, Maire and Tison, Winge. Terby. Home,
Yendo and Takase. and Webb based their contention
on a numerical reduction in chronuisome nmnber dur-
ing these divisions. Whetlier or not their chromosome
counts are accurate remains, however, to be shown
from more intensive study of these divisions.
The chromosomes of the PIasm(>dio|)hor.iles are
quite small and are not always clearly defined on the
equatorial plate, so that it is difficult to make accu-
rate counts. Xevertheless. numerous attempts have
been made, as is shown in table 1 .
The numbers are low multi|)les of 2, with 8 )ire-
dominating as the di])loid inniiber. In .S. V iron'icae
Maire and Tison reported Hi .and 8 chromosomes, but
Webb later found only 8 and i. \\'inge. as noted be-
fore, described the first division as vegetative or so-
11
PLASMODIOPHORALES
Table 1. Chromosome numbers in the Plusmodiophorales.
Species Author
Sorosphaera Veronicae Maire and Tison, '09
S. Veronicae Webb, "35
Tetramyxa -parasitica Maire and Tison, '11
T. Elaeac/ni Yendo and Takase, '32
Sorodisciis Callitrichis Winge, '13
S. rudicicohis Cook, '31
S. Heternntherae Wernham, '35
Plasmodiiiphora Brassicae Maire and Tison, '09
P. Brassicae Lutman, "13
P. Brassicae Terby, 'H 4
P. Brassicae Nawaschin, '34 ?
P. Brassicae Tones, ^-2S ?
Spongospora subterranea Osborn, '11 ?
S. subterranea Home, '30 4
Number
3'
sy
8
16
4
8
i
8
6
12
4
■;
o
4
»
4-
6
?
8
^
8
6-8
8
8(?)
8
matic and recorded 16 individual cliromosomes asso-
ciated in eight pairs on the equatorial plate, which
separated and were distributed to the daughter nu-
clei. In the second division this number was halved
to four. Winge's confusion as to the nature of the
respective divisions has led to tlie belief that the
chromosome numbers in S. Callitrichis are 16 and 8.
but it is evident from Winge's report that 4 should be
recorded as the reduced number. In P. Brassicae four
workers have recorded 8 as the diploid number, and
curiously enough this is the number of bodies figured
earlier by Prowazek ('05) in the transitional phase.
In Spongospora subterranea, Osborn figured polar
views of the second division with 7 chromosomes,
which corresponds closely to the number later re-
corded by Home for the first division. It is not im-
probable, however, that Osborn's figure relates to the
first meiotic division.
Schizogony and Cleavage
Vegetative multiplication of young plasmodia by
division, segmentation or fragmentation has been re-
ported for all genera of the Plasmodiophorales ex-
cept Memhranosorus and Octomifxa. In Ligniera it is
said to be lacking entirely or reduced to the forma-
tion of a few daughter segments, while in T. Triglo-
chinis and P. graminis true "multiple division" has
been re])orted. Nawaschin did not observe segmenta-
tion in Plasmodiophora, but he believed that its oc-
currence is the only plausible explanation of the fre-
quent presence of numerous uni- and multinucleate
amoebae and plasmodia in a single host cell. Since
that time most cytologists have reported its occur-
rence, although none of them, with the ])ossible ex-
ception of I.edingham, actually observed it in liv-
ing material. Like Nawaschin, they found several
amoebae and plasmodia in the same cell and assumed
that the former were the products of fragmentation.
Maire and Tison ('10) found similar stages in Soro-
sphaera but interpreted them as fusion stages of
amoebae and young plasmodia in the formation of
the s))orogenous plasmodium. Brasil, however, sug-
gested that these stages relate instead to fragmenta-
tion or scliizogony — a suggestion which Maire and
Tison adopted. These workers thus introduced the
protozoologists' term "schizogony" as descriptive of
the vegetative fragmentation of the plasmodium, and
since that time it has been rather widely adopted.
Pavillard ('10), however, contended that schizogony
in Sorosphaera, as described by Maire and Tison,
resembles plasmotomy instead of true schizogony as
in Trichosphaerium sieholdii (Doflein, '09, '27) and
Hepatazoon anis (Wenj'on, '26), for example. He
thus restricted the term schizogony to the "multiple
division" of Doflein, while Maire and Tison ('11)
interpreted it in the broad sense of most protozoolo-
gists to include the plasmotomy of Doflein as well as
all other methods of simple and multiple divisions.
Schizogony in the Plasmodiophorales is reported
to occur most frequently during the 8- and 16-nucle-
ate stages of the plasmodia or schizonts. A few uni-
and multinucleate meronts may be formed as in Lig-
niera, or the whole plasmodium may undergo mul-
tiple division as in T. Triglochinis and P. graminis.
The latter type of complete fragmentation appears
to be limited as far as present-day knowledge goes.
Most cases so far reported involve primarily the con-
striction and cutting off of peripheral uni- and multi-
nucleate segments. No cases have yet been described
in which all or most of the nuclei migrate to the
periphery of the schizont and become enveloped in
cytoplasmic buds, which are subsequently pinched
off, leaving a central mass of degenerating cytoplasm
and nuclei, as in Hepatasoon anis, for example. The
mechanics of schizogony are unknown, because the
process has not been extensively observed in living
material. In Polymiioca graminis, Ledingham merely
reported that the pseudopodia are retracted and the
protoplasm becomes denser before the thallus splits
up into meronts.
In cases in which only a few meronts arc formed
the remaining portion of the schizont may mature
directly into a sporogenous plasmodium or sporont.
The delimited meronts grow in size and become mul-
tinucleate and may in turn function as schizonts.
Otherwise, they develop into sporonts. The destiny
of the various portions depends to some extent on
the length and activity of the vegetative period. Inas-
Sl'.M Al.nv AM) AI.TKIIXATIO.N OF GKNK.IIATIOXS
15
iniu'li as solii/.ojiiiny will hv disciisscil fiirtlicr in tlit'
ilcMTiption lit" imli\ iiliial spii-ifs in Chapter IN', fur-
tluT discussion of the proc'css nt-od not l>c jircscntiil
IllTC.
Cytokinesis or division of tin- plasmodiuin or spo-
ront into resting spores takes place by cleavajie. and
as far as is now known may be closely associated in
|)oint of time with the two meiotie divisions. In Soro-
xpharra I'l-ronicaf, aceordinj; to Main- and Tison
(OS)), cleavaiie begins in tlie late ))rophases of the
first division (PI. (i. fig. 33). and by tiie time of the
cqu.itorial plate stage, spore mother cells have been
completely delimited (fig. 37). These cells divide
into two uninucleate segments (fig. 38) in which the
second division then takes place (fig. U). At the
completion of this mitosis these segments in turn di-
vide into the definite spore rudiments (fig. f2). In
tills sjiecies at least cytokinesis may follow each
mitosis. A similar sequence has been re))orted liy
Wingc for Sorodi.icus (PI. 7. fig. 26-30), although
the stages do not appear as sharjily defined. Figure
27. however, suggests that the sequence varies and
that the first division may be complete before cleav-
age begins. .Similar variations have been reported for
Pla.smod'iophora also. Lutman ('13) and Milovidov
('31 ) found that the first meiotie division is usually
comiilete by the time the initial segments are delim-
ited. The latter may be uni-. bi-, or multinucleate,
and after the second meiotie division has been com-
l)leted (PI. 4, fig. 80. 81) they cleave into uninucle-
ate spore segments (fig. 82. 83). Cook ('28). Cook
and .Schwartz ('30), however, reported that cleavage
in Liqiiiera and Pla.smod'iophora does not begin until
both divisions have been completed. I-edinghani's
))hotomicrographs suggest the same sequence of
events in Poli/mt/xa. In Tetrami/.ra the peripheral
Plasmodium first cleaves (PI. 5, fig. 8) into uninucle-
ate segments or sporonts (fig. 9-12). Two meiotie
divisions occur in these segments, and these mitoses
are usually over (fig. 13-17) by the time cleavage
into definite spores is complete. In Octomi/j-a large
uninucleate segments are delimited in which the two
meiotie divisions occur, and following the completion
of the second divisions, which are quadri])ol.ir, the
segments cleave into sjiorcs. a<-eording to \\'liirt'en.
\'ery little is known about cytokinesis in the other
genera. The time relations of clc.iv;ige to the succes-
sive meiotie divisiiins doubtless varies in diliercnt
species and probably in the same species, so tli.at
under varying conditions it may occur during as well
as after meiosis.
.Marked changes take place in the cytolilasm jirior
to cleavage. In /'. /yrn.v.v/cac, according to Nawaschin
('99). Lutman. and .Milovid<iv, the cytoplasm be-
comes highly vacuolate (PI. 1. fig. 78) and thus fills
the host cell more or less completely. In Poli/mi/.ia,
however, Ledingham reported that the cytoplasm be-
comes less vacuolate, smaller in volume, and denser,
while numerous oil globules emerge and increase the
refringency of the plasmodium. According to Lut-
man, the denser cytoplasm collects around the nuclei
in /'. Brassicae, while the vacuoles fuse and cut the
jjlasmodium u]) into uninucleate segments. He con-
tended that the process of spore formation in the
Plasniodiophorales is quite difl'erent from that de-
scribed by Harper (00) for certain myxomycetes,
but his figure 3'1 (PI. -i, fig. 79) nevertheless shows
a well-defined cleavage furrow progressing between
the nuclei. Milovidov's ('31) text-figure 3 likewise
shows that large segments are first delimited by fur-
rows, and these in turn cleave into uninucleate
spores. Progressive cleavage by furrows is also sug-
gested by figure 99, Plate 4 of P. Diplantherae, fig-
ure 33, Plate 6 of S. J'eronicae, figures 3 and 10,
Plate 7 of Sorodiscus karlingii, etc. Contrary to
Lutnian's belief, cleavage in the Plasniodiophorales
appears to take ])lace by progressive furrowing as
in the myxomycetes. Furthermore it does not appear
to be simultaneous as Woronin, Nawaschin, and
Maire and Tison reported.
Other cytological details such as cellular relations
between host and pathogen are discussed in Chapters
IV and VI in connection with the descriptions of in-
dividual species and the diseases which they cause.
Cluipter III
Sexuality and Alternation of Generations
Very little is known about sexual reproduction in
the Plasmodiophorales, yet most workers have as-
sumed that it occurs. .So far, actual fusion of gametes
in living material has been observed only in Spoiu/o-
spora suhterranea. The evidence of sexuality in the
group as a whole is tlierefore largely indirect. It is
based on isolated observations of paired amoebae
and zoos))ores. binucleate amoebae, the a])l)earance
of paired .-ind fusing nuclei in the plasmodium, and
j)rimarily on the reported occurrence of meiosis at
s))orogenesis. which presup|)0ses a nuclear fusion at
sonic stage of development. Inasmuch as there is con-
siderable dilTerence of opinion about the time. ])lacc,
and nature of plasmogamy and karyogamy in differ-
ent genera as well as in the same sjiecies. the data on
sexuality for each genus will be considered sepa-
rately.
In Plasmod'wphora, Nawaschin ('99) reported
the union of several amoebae in the formation of
the jilasmodium, but lie did not regard these fusions
as having anv sexual significance. Later, Miss Terby
('21), Milovidov ('31), and several other workers
expressed the same view concerning the develojiment
of the sporogenous iilasmodium. Prowazek ('0.5),
however, contended that the incipient spore seg-
ments or "sporogametes" fuse in pairs following
cleavage (PI. 1, fig. 89), after which the zygote or
binucleate spore begins to encyst (fig. 90, 91). One
16
PLASMODIOPHORALES
of the so-called gametic nuclei then divides (fig. 92),
during which division it undergoes a chromatin re-
duction and forms a variable number of reduction
bodies ( !). ]Meiosis is followed almost at once by
karyogamy. Apparently all but two nuclei degen-
erate (fig. 93), and the two remaining ones fuse to
form a synkaryon (fig. 9i). Prowazek's account of
reduction is not very clear, and his drawings of the
process do not clarify the accompanying description.
It is accordingly difficult to determine from his con-
fusing account the duration of the respective diploid
and haploid generations in Plnsmodiophora. Accord-
ing to him, the diploid phase is api)arently quite
short (text-fig. 1).
Prowazek's account was refuted by ]\Iaire and
Tison ('09) who failed to find any evidence of plas-
mogamy and karyogamy following cleavage. They
nevertheless believed that sexual fusions occur in
Plasmodiophora and postulated that it might take
place between two amoebae from germinating spores.
Pavillard ('10) rejected this view and considered it
more plausible that karyogamy occurs in the Plasmo-
dium shortly before meiosis. presumably following
a coalescence of amoebae. His theory, however, re-
lates to the Plasmodiophoraceae as a whole rather
than to Plasmodiophora specifically. Winge con-
curred with Maire and Tison's view and assumed
that the motile cells from resting spores copulate in
pairs to form small myxoplasma which penetrate the
host and develop into plasmodia. The diploid phase
persists until the second sporogonic division where
reduction occurs, according to Winge (text-fig. 2).
This text-figure is also representative of his view
concerning alternation of generations in all genera
of the Plasmodiophorales. Lutman, Chupp, and
Milovidov ('31) were uncertain about the time and
place of plasmogamy and karyogamy, but believed
that they must occur at some stage on the grounds
that a reduction in chromosome number takes place
during the first sporogonic division (PL 3, fig, 63-
73). Miss Terby ('21') postulated that fusion occurs
outside of the host cell between pairs of zoospores, a
view which Nawaschin had accepted by 192i.
P. M. Jones ('28) described and figured the for-
mation of two types of gametes from germinating
spores in culture. In some cases a large pyriform uni-
flagellate gamete is formed in germination, while in
others the content of the spore emerges, grows, and
then divides into as many as 20 minute gametes.
Both types of gametes may fuse in pairs and form
zygotes, but sometimes a large number of micro-
gametes which have not completely separated re-
unite to form a plasmodium. .Tones furthermore re-
ported that during the chromidial stage a whole Plas-
modium may break up into gametes which subse-
quently fuse in pairs, as is shown in text-figure 3.
However, his account of the life cycle of P. Brassicae
is so unorthodox and confused that most later work-
ers have seriously questioned the accuracy of his ob-
servations. As noted elsewhere. Cook and Schwartz
('30) maintained that the small flagellate cells pro-
duced in zoosporangia are gametes which fuse in
pairs either in the root hairs of the host or after
migrating into the cortex. They regarded these small
zoospores as comparable to the minute gametes re-
ported by .Jones. Cook and Schwartz, however, never
observed actual fusion, and their hypothesis is based
entirely on the observation of zoospores lying side
by side in pairs and the subsequent occurrence of
binucleate amoebae. Obviously, neither of these phe-
nomena are conclusive proof of fusion. According to
these workers, the zygote thus formed develops into
the sporogenous plasmodium, and reduction occurs
during the first sporogonic division. As is shown in
text-figure -t, the diploid generation thus embraces
only the zygote and sporogenous ])lasmodium. Cook
and Schwartz were uncertain whether the gametes
come from tlie same or from different gametangia. If
sex is genotypically segregated at meiosis, the rest-
ing spores, zoospores, haploid plasmodia, gametan-
gia, and gametes are of two types, as is indicated in
text-figure 5. Fedorintschik confirmed Cook and
Schwartz's report of fusion of gametes from zoo-
sporangia or gametangia but believed that it occurs
later, following a period of vegetative budding
within the host. As noted before, he also believed that
two reductions occur in P. Brassicae — one during the
first division of the sporangium nucleus and another
at sporogenesis. Fedorintschik may have been in-
fluenced by a previous report by Cook of two simi-
lar reductions in Lif/iiiera. If two reductions occur,
obviously there must be two nuclear fusions, but
Fedorintschik reported only one. No additional or
more convincing evidence of sexuality in Plasmodio-
phora has since been presented as far as the author
is aware, and the question thus remains in this un-
certain state. It will doubtless remain thus until in-
tensive monospore studies have been made.
In Telramyxa, Cook ('33) reported that "swarm
cells" fuse in pairs at their anterior ends as they
migrate from cell to cell and thus form amoeboid
zygotes in which karyogamy soon occurs. These ob-
servations were apparently made from slides of fixed
material furnished by Prof. O. V. Darbishire and do
not relate to fresh material. No other data on sex-
uality in this genus exist so far as the author is
aware. According to Cook, T. parasitica has a dis-
tinct alternation of haploid and diploid generations,
as is illustrated in text-figure 6.
Nothing definite is known about sexuality in Soro-
sphaera. Cook ('33, p. 198) stated that amoebae
from resting spores fuse in pairs and form amoeboid
zygotes, but this statement is not based on observa-
tion. No one lias yet reported actual observation of
gametic fusion. However, inasmuch as reduction is
said to occur at s))orogcnesis, most workers have
nevertheless assumed that plasmogamy and karyog-
amy take place at some stage of develoi)mtnt. Webb
found no evidence of plasmogamy but rejiorted that
the chromosome number is doubled during the transi-
tional phase. He thus concluded that karyogamy oc-
curs at this stage, as Home had ])reviously described
for Spongospora. According to \\'ebb, the diplophase
of Sorosphaera is very short and includes only the
SKXIAMTV AND A 1. TKllN ATIO.N OK tiKNKHATIONS
17
y^
m
w
•■<»■
•%
I
\kp
\m
*)^'
^^■•
«S^';fe-.
''-^
iCft
...-^
/IXSM0G4W)'
/
o.-J^.-
H4PLO/0
^
\
^.
• • •
DIPLOID
i
• ■ • • • ■ •* • V ■ ,^
V",,~
"V
if"
..^'
•oKi
TEXT- FIG 1 LFE CYCLE OF P BRASSICAE. accokdinc to
PROWAZEK. 1905
TEXT-FIG 2 LIFE CYCLE OF P BRASSICAE. accohoihO to
WINGE. 1913.
uKmcAtere fusion
/ zrcoTE /woeauLA maturc
YOUNG smne autupe spots.
AMOEBA DH/IDING
VKUOLATE AtlOEBA
>ew NUCLEI fhom
O*>0MIDIA
P/fCTfiLASUIC BUO nDmNG OUT,
OflOMIDIA IN OLD PORT/ON
NUCLEI BREAKING
UP INTO OtfOMIDIA
NUCLEAR BUD DIVIDING.
OfKMIDIA IN LCWEP END
NUCLEAR BUDDING
tew NUCLEAR BUO
TEXT-FIG 3 LIFE CrCLE OF P BRASSICAE. according to JONES. 1928.
18
PLASMODIOPHORALES
maturation stages of the plasmodium and sporogen-
esis, while in Cook's opinion it extends from the time
of gametic fusion through scliizogony and "akaryo-
sis" to sporogenesis, as is shown in text-figure 7.
The data relative to sexual reproduction are even
more scanty in Sorodiscus. Winge assumed, as he had
for all members of the Plasmodiophoraceae, that
gametes from germinating spores copulate in pairs
and thus initiate the diploid phase of S. Calliirichis,
but he never actually observed fusion. Likewise,
plasmogaray and karyogamy have not been seen in
S. karlingii. In S. radicicolus, however. Cook ('31)
figured and described fusion of amoebae in pairs
within the host cell (PL 7. fig. 6). The two gametes
here figured are unequal in size, but Cook did not say
wliether or not this species is heterogamous. His
study was made on fixed material sent from South
Africa, and figure 6 shows the only case of pairing
observed in sudi material. This may possibly repre-
sent only a chance association of amoeba without
sexual significance. Obviously, additional data are
needed before definite conclusions can be drawn
about sexuality in Sorodiscus. Cook ('33), never-
theless, believed that fusion of gametes occurs in
S. radicicolus and that this species has a well-defined
alternation of diploid and haploid generations as is
shown in text-figure 8.
In Spongospora suhterranea, Massee, Kunkel, and
Osborn reported that the sporogenous plasmodium is
formed by coalescence of numerous amoebae, but
they were uncertain about the origin and sex of the
latter. Home was of the opinion that the amoebae
are of opposite sex and that in this respect the plas-
modium is similar to that of Diciyostelium muco-
roides reported by Skupienski ('18). According to
Osborn, coalescence is followed by the akaryote
stage during which the nuclei disappear. New nuclei
are reconstructed de novo, and these subsequently
associate in pairs (PI. 10, fig. 28). Karyogamy soon
follows as the nuclear membranes break down at the
points of contact (fig. 29). Nuclei which do not pair
degenerate the manner described by .Tahn for Cera-
tiomi/ja. Home confirmed Osborn's report of kary-
ogamy before meiosis but maintained that it occurs
during instead of after the transitional or akaryote
stage. He did not observe paired and fusing nuclei
but based his conclusion on the discovery that the
chromosome number following the transitional stage
is twice that in amoebae and young plasmodia. Ac-
cording to Osborn and Home, the diploid phase of
S. suhterranea is quite short in duration and includes
only the sporogenous plasmodium, as is shown in
text-figure 9. Osborn's, and to some extent Home's,
observations and reports of karyogamy shortly be-
fore sporogenesis in Spongospora are strikingly
similar to the earlier accounts of the nuclear fusion
in the myxomycetes. In Ceratiomyxa, Arci/ria, and
Trichia,0\he ('07) , Kranzlin ('07), and .lahn ('07,
'08) described nuclear pairing and fusion in the plas-
modium shortly before resting spores are delimited,
but these accounts have subsequently been refuted.
Cook ('33), on the other Iiand, reported that the
zoospores from germinating resting spores pair at
the anterior end, retract their flagella, and fuse (PI.
10, fig. 20-22). Plasmogamy is followed shortly by
nuclear pairing and fusion (fig. 22). The zygote may
become flagellate again, and later, apparently, in-
fects the host. Its nuclei divide promitotically, ac-
cording to Cook, and at the 6- or 8-nucleate stage the
zygote undergoes schizogony. Whether or not the
meronts later coalesce and thus form the sporogenous
Plasmodium is not apparent from this account. Led-
ingham ('35) also observed germination of resting
spores and formation of biflagellate zoospores, but
he found no evidence of gametic fusion. A few binu-
cleate zoospores with four flagella were present in
Ledingham's cultures (PI. 10, fig. 9), but he was
not certain whether these were the product of fusion
or incomplete cleavage. Thus, Cook's report of isog-
amy has not been substantiated. He nevertheless be-
lieved that the diploid generation of this species em-
braces the zygote, schizonts, meronts, and plasmodia,
while the haploid phase is limited to the cystosori,
resting spores, and gametes, as is shown in text-fig-
ure 10. The zoosporangia and zoospores found by
Ledingham are apparently a means of rapid vegeta-
tive multiplication and doubtless relate to the hap-
loid phase, as is indicated in this diagram. Barrett
found fusion stages between zoospores or gametes
derived from zoosporangia in S. Cotulae, but these
relate only to fixed and stained preparations.
In Ligniera, Maire and Tison, and other workers,
assumed that plasmogamy and karyogamy take place
at some stage of development, because the nuclei ap-
pear to undergo reduction at sporogenesis. Cook
('26, '33), however, reported a double fusion and
reduction in L. Junci. The zoospores from resting
spores fuse in pairs at the anterior end and give rise
to diploid ])lasmodia. As noted before, these cleave
into uninucleate segments, which develop walls and
become incipient zoosporangia. The first nuclear di-
vision in these sporangia is meiotie, and the zoo-
spores or gametes subsequently produced are hap-
loid. These fuse in pairs and form the diploid sporo-
genous Plasmodium in which meiosis later occurs at
sporogenesis. Ligniera Junci thus has two diploid
phases each of which is separated by a haploid ])hase,
according to Cook, as is illustrated in text-figure 11.
Cook neither observed plasmogamy and karyogamy
nor counted the chromosomes at meiosis, so that he
had no direct evidence for his assumption. It is not
improbable that the zoosporangia and zoospores are
merely means of vegetative multiplication without
sexual significance and relate to the haploid genera-
tion, provided an alternation does occur, in much t!;e
same manner as is indicated in text-figure 10 of S.
suhterranea.
No direct evidence of gametes, gametic fusion and
karyogamy have been observed in Memhranosorus,
Poli/?ni/^-a, Octomyjra, and the doubtful genera, 7?/;;'-
somi/xa, Anisomij.ra, and Sorolpidium. Ledingham
found a few tetraflagellate binucleate zoospores in
Poh/mi/.ra, but he was not certain whether these were
SK.VrAl.lTV AND A I.TKH \ ATH).\ OF (iKX K» ATIDN S
19
rvt^noH sKAc
fc: *» '
/Q
HAPLOID
o s\
\ ^
e><s£
I
ll
.,0*
ZOOSP^^
/
'S»J
§ ".
.v<
DIPLOID
%?:^^s
HAPLOID
7EXT-FIG4 LFECyCLEOFPBRASSICAE. accohdihg to COOK AND
sormPTZ. 1930
TEXT-FIG 5 LIFE CYCLE OF P BRASSICAE. SUGGESTED BY-
COOK AND SCHWARTZ S STUDIES. 1930.
SfCft
'._
;T'
L^^>
1
''^^'^^^^^
HAPuyo
:<^^:.
®\
v.
DIPUD/D
.-. ^w^ .
© ® ©©■■
'^J ® © S) o'
'"■S-^iMvTJ PLtSMD^
:A
■"^h;'
S!^^
^
X
p£5'
i-rC
r:"-^:>-
/
HAPLOID
%m
\
<'%
DIPUDID
aiMKC
V12\
1^
^
.t^
TEXT-FIG 6 LFE CrCLE OF TETRAMYXA. xcononc to
COOK. 1933
TEXT-FIG 7 LIFE CYCLE OF SOROSPHAERA. /cccwing to
COOK. 1933.
20
PLASMODIOPHORALES
the products of gametic union or incomplete cleav-
age. Tetraflagellate zoospores were likewise found
bv Couch et al. in Octomi/j-a, but no fusions were ob-
served. However, in this genus as well as in Mem-
hranosorus Whitten and ^^'ernham each reported re-
duction at sporogenesis. which presupposes karyog-
amy at some state of development. Miss Whilfen be-
lieved that karyogamy occurs during the akaryote
stage of O. Achli/ae.
It is obvious from this review that the data on sex-
uality in the Plasmodiophorales are quite limited. In
S. stibierranea, tlie only species in which gametic
fusion has actually been observed, the respective
gametes are reported to be alike and show no struc-
tural, mobile, and physiological differences. In this
species at least sexual reproduction appears to be
isogamous. Whether it is homo- or heterothallic is
not known, since no studies involving monospore cul-
tures have yet been made. Therefore, any discussion
at present of sex determination, haplosynoecism,
haploheteroecism, antithetic alternation of gameto-
and sporophytic generations, etc., in the Plasmodio-
phorales must be speculative and, in light of the
meager present-day knowledge, largely futile.
bibliography: cytology and se.xiality
Alexieff, A. 1913. Arch. Protistk. 39: 344.
Belar, K. 1936. Ergeb. Foitschr. Zool. 6: 335.
Blomficld, ,T. E., and E. J. Schwartz. 1910. Ann. Bot. 34:
3.5.
Calkins, G. X. 1933. Blolojry of the protozoa. Philadelphia.
Chatton, E. 1910. Arcli. zool. Exp. 5 ser. 5: 339, 36T.
Cook, W. R. I. 1936. Trans. Brit. Mycol. Soc. 11: 196.
. 1938a. New Phytol. 37: 330, 398.
• . 1938b. Ann. Bot. 43: 347.
. 1931. Ann. .Mycol. 39: 331.
. 1933. Arch. Proti.stk. SO: 179.
, and E. J. Schwartz. 1939. Ann. Bot. 43: 81.
, and . 1930. Philos. Trans. Roy. Soc. London
318 B: 383.
Couch, J. X., J. Leitner, and A. Whiffen. 1939. Jour. Elisha
Mitchell Sci. Soc. 55: 399.
Doflein, E. 1916. Lehrbuch der Protozoenkunde 4th ed.
Jena.
Favorsky, W. 1910. Mem. Soc. Nat. Kieff 30: 149.
Ferdinandsen, E., and O. Winge. 1930. Ann. Bot. 34: 467.
Fedorintschik, N. S. 1935. Summ. Sci. wk. Inst. pi. protect.
Leningrad 1935:69.
Harper, R. A. 1900. Bot. Gaz. 30: 317.
. 1914. .\mer. Jour. Bot. 1: 137.
Home, A. S. 1911. Rept. Brit. Assoc. Adv. Sci., Ports-
mouth, p. 573.
. 1930. Ann. Bot. 44: 199.
Jahn, E. 1907. Ber. Deut. Bot. Gesell. 35: 23. 1908, Ibid.
36a : 343.
Jones, P. M. 1938. Arch. Protistk. 63: 313.
Kninzlin, H. 1907. Ibid. 9: 170.
Ledingham, G. A. 1939. Canad. Jour. Res. C, 17: 38.
Levine, I., and M. Levine. 1933. Jour. Cancer Res. 7: 163,
171.
Lutman, B. F. 1913. Vermont Agr. Exp. Sta. Bull. 175.
Maire, R., and A. Tison. 1909. Ann. Mycol. 7: 22%.
, and . 1910. Bull. Soc. I.inn. Normandie 6 ser.
3:57.
, and
-. 1911. Ann. Mycol. 9:336.
Milovidov, P. F. 1931. Arch. Protistk. 73: 1.
. 1933. C. R. Soc. Biol. 109: 170.
. 1933. Arch. Protistk. 81 : 138.
Niigler, K. 1909. //)W. 15: 1.
Nawaschin, S. 1899. Flora 86: 404.
. 1901. Kiev Lap. Ohsch. Jest. 17: 1: XXXVI.
. 1934. C. R. Acad. Sci. Russie 1934: 173.
N'emcc, B. 1911. Bull. Inter. Empr. Fran. Joseph Acad. Sci.
16: 69. 1913, /hi'rf. 18: 18.
Olive, E. W. 1907a. Trans. Wise. Acad. Sci., Arts and Let-
ters 15:7,53.
. 1907b. Sci. n. s. 35: 366.
0.sborn, T. G. B. 1911a. Rept. Brit. A.s.sn. .\dv. Sci. Ports-
mouth, p. 573.
. 191 lb. Ann. Bot. 35: 371, 337.
Palm, B. T.. and M. Burk. 1933. Arch. Protistk. 79: 363.
Pavillard, J. 1910. Prog. Rei. Bot. 3: 475.
Prowazek, S. 1903. Osterr. Bot. Zeitschr. 53: 313.
. 1905. Arb. Kais. Gesundheit 2-2: 396.
Schwartz, E. J. 1910. Ann. Bot. 34: 511.
Skupien-ski, F. X. 1918. C. R. Acad. Sci. Paris 167: 960.
Terby, J. 1933. Mem. Roy. Acad. Belg. 7: 1.
'—. 1934. Bull. Roy. Acad. Belg. 5 ser. 10: 519.
. 1933. Mem. Roy. Acad. Belg. 11: 1.
Webb, P. C. R. 1935. Ann. Bot. 49: 41.
Wenyon, C. M. 1936. Protozoology 1 : 66.
Wernham, C. C. 1935. .Mycologia 37: 363.
Whiffen, Alma. 1939. Jour. Elisha Mitchell Sci. Soc. 55: 343.
Winge, (). 1913. Ark. f. Bot. 13, no. 9: 1.
Wissenlingh, C. 1898. Jabrb. Wiss. Bot. 31: 619.
Vendo, V., and K. Takase. 1933. Bull. Sericult and Silk
Inc. Japan 4, no. 3: 4.
Chapter IV
Classification and Description of Species
The Plasmodiophorales include one family, Plas-
modioplioraceae, and approximately eight genera
and twenty-three species. Numerous other genera
and sjiecies have been added at various times, but
these liave either been merged with existing genera
or excluded entirely as invalid. A natural classifica-
tion is well nigh inijjossible at present because so lit-
tle is known about tiie critical diagnostic characters
of most siJCcies. Furtliermore, the genera are not
shar])ly defined and, as Palm and Burke ('33) have so
well em])hasized, tend to merge and overlap, so that
in certain members generic distinctions are difficult
to recognize. The oldest and most frequently used
criterion of classification is the grouping assumed
by the resting spores at maturity. This criterion was
introduced by Schroeter in 1 897, who separated the
genera on the basis of whether the spores are free or
united in clusters and cystosori. Schroeter also em-
])Iiasized the presence or absence of a soral mem-
lirane as a distinctive character of Tetrami/.ra and
SE.Xl'AI.lTV AND Al.TKHN ATION (IF (iKNKHATUJNS
21
HAPLOID
Dinao
^^v^
< '•[
N,
XIOav
HAPLOID
*KtfiyCir£ STAGE
,^*^;:
■ « ♦ * A
TEXT-FIG e LFE CYCLE OF SOROO/SCUS RADtQCOLUS.
ACCOKono TO COOK, I93L
TEXT-FIC.9 LIFE CYCLE OF SPONGOSPORA SUBTERRANEA,
ACCORDINO TO OSBORN, 1911.
PLASUoawr
•^
ZOOSP0/>/IMJIAL
STAB£
HAPLOID
DIPLOID
■^ ■■^. ^•
r.®^
,, ^
<^^'-'^B^../:^f%
AKwixm sTJce
PLASMOGAUr
TEXT-FIC 10 LIFE CYCLE OF 5. SUBTERRANEA, accowing to
COOK. 1933
TEXT-FIC. II LIFE CYCLE OF LIGNIERA JUNO. AccoKomc n
COOK, 1933
22
PL ASMODIOP MORALES
Sorosphaern. Although mycologists and protozoolo-
gists have clearly recognized the inadequacy of these
criteria, they have nevertlieless continued to use tliem
as the basis of classification. More recently. Cook
('33) has used the presence of zoosporangia and zoo-
spores as another basic distinction. However, since
zoosporangia have been subsequently found in nu-
merous genera, the mere presence of sucli structures
is no longer generically distinctive. Likewise, liis em-
pliasis on tlie presence or absence of a membrane
around the cystosori as a diagnostic character is open
to question, since there is considerable doubt about
the occurrence of soral membranes in any of the
genera. Palm and Burke, in particular, Iiave severely
criticized tlie present-day system of classification
and characterized it as artificial. From tlieir obser-
vations on the wide variations exiiibited by cystosori
of S. 1 eronicae , tliey concluded that Spongoxpora,
Lif/niera, Sorodiscus, Ostenfeldiella, Clathrosoriis,
and Memhranosorus should be regarded as synonyms
of Sorosphaera. On the basis of similarity of life
cycles and general structure, they further advised
the merging of all known genera except C ystospora
into one large genus, presumably Plasmodiophora.
The author is in complete agreement with these
workers on the low taxonomic value and inadequacy
of present-day generic distinctions. However, Palm
and Burke's suggestion of reducing the number of
genera or merging them does not solve the difficulties
of classification in this group. As Ledingham ('39)
pointed out, it merely shifts the generic indistinc-
tions to tlie species.
Further taxonomic distinctions ajjpear to be
emerging from the discovery of zoosporangia in old
and new genera. When these developmental stages
have been fully investigated, the relationship of the
various genera will doubtless become clearer, and it
may then be possible to separate or merge them with
greater accuracy. In the meantime, Schroeter's sys-
tem of classification serves as a working basis, and
although an unsatisfactory expedient, it may be used
to advantage. In the key wliich follows, size, number,
and sha])e of zoosporangia are used to some extent in
diagnosis, but these characters are of doubtful gen-
eric value. Some of the genera — i.e., Memhranosorus
and Lif/niera — listed here are obviously questionable
and sliould ])erhaps be merged with Sorodiscus and
Sorosphaera, but until more is known about the fam-
ily as a whole, it may be worth while to treat tliem
separately.
PLASMODIOPHORACEAE
Zopf, 188-i. Die Pilzthiere oder Schleimpilze
Thallus a naked. ])lasmodial, multinucleate proto-
plast capable of amoeboid movement and undergoing
sciiizogony into uni- or multinucleate meronts, wliicli
in turn may function as schizonts. Sporogenous thal-
lus cleaving into uninucleate spores at maturity.
Resting spores loose and free or united in small clus-
ters and cystosori ; usually producing one zoospore
or amoeba in germination. Zoospores anteriorlj' bi-
flagellate and heterocont. Zoosporangia formed di-
rectly from zoospores or cleavage segments of young
Plasmodia ; free or united in sporangiosori ; produc-
ing a few to numerous zoospores which are similar to
those formed from resting spores.
Key to Genera
I. Resting spores not united, free and loose. Zoosporangia
few or numerous, small, and producing few zoo-
spores 1. PLASMODIOPHORA, p. 22.
II. Restin); spores united in small clusters or more or less
compact cystosori
A. Spores usually in tetrads or dyads. Zoosporangia un-
known 2. TETRAMYXA, p. 37.
I?. Spores usually in octads. Zoosi)orangia numerous,
small, oval, and spherical with or without exit
papillae 3. OCTOMYXA, p. 40.
C. Cystosorus predominantly spherical to ellipsoidal and
hollow; often variable in size and shape. Zoospo-
rangia small 4. SOROSPHAERA, p. 41.
D. Cystosorus predominantly disc-shaped, two-layered
and flattened; often variable in size and shape.
Zoosporangia unknown
5. SORODISCUS, p. 46.
E. Cystosorus oval, spherical, and s])onge-like, lacking a
central cavity but traversed by prominent canals
and fissures. Zoosporangia numerous or few, small,
oval and spherical, or large and irregular
6. SPONGOSPORA, p. 54.
F. Cystosorus indefinite in size and shape
1. Zoosporangia small, oval and spherical; producing
few zoospores 7. LIGNIERA, p. 58.
3. Zoosporangia usually large, elongate, lobed and
irregular with prominent exit tubes
8. POLYMYXA, p. 63.
PLASMODIOPHORA
Woronin, 1877. Arb. St. Petersburg Nat. Gesell.
8:169.
Osti'iiffliUeUa Ferdinandsen and Winge, 1914. Ann.
Bot. 28: 64.
(plates 2. 3. 4.)
Resting spores lying free in host cell, not united
in cystosori, variable in size and shape, usually pro-
ducing one zoospore in germination. Zoospores an-
teriorly biflagellate and heterocont, becoming inter-
mittently amoeboid, infecting the host as an amoeba
( ?), dividing and budding (.''), and eventually form-
ing multinucleate plasmodia, which cleave into uni-
nucleate segments. Cleavage segments developing
into small zoosporangia which produce few zoo-
spores. Secondary zoospores reinfecting host and
forming additional ])lasmodia. Sporogenous ))lasmo-
dium partly or com])letely filling host cell, moving
slowly in amoeboid fashion within the host cell and
in migrating from cell to cell ; occasionally luider-
going schizogony into uni- and multinucleate me-
ronts; rarely encysting; cleaving into resting spores
at maturity.
PLASMOniOIMlOKA
23
Pta.imodiopliora iiirhulcs at prisciit live sjucics,
of wliicli only one, /'. lirassicae, is fairly well known.
Most of tlu' otluT spci'ics arc so little known that
tlu'ir validity as nu-nilnTs of tlu' genus has ht-i-n seri-
ously questioned. They nevertheless (jossi-ss the eoni-
nion ability of eaiisiiii; eonspieuous galls and malfor-
mations of the host tissues. Numerous other organ-
isms with )>lasmodial stages have been inehided in
the genus from time to time, but eareful reinvestiga-
tion has shown them to be invalid. Pla.imodiophora
is distinguished from the other genera of the family
by the laek of a distinet eystosorus. The resting
spores are not united or attaeiied to form a sorus of
definite size and sliajx' but lie loose in the host eell.
as is shown in figures 88 and 100. When the host eell
disintegrates, the spores are liberated into the soil
where they may germinate at onee, as in P. Brassi-
cae, or remain viable up to seven or eight years
(Jorstad, '23), So little is known about the other
species of Plasmodiophora that present day discus-
sions of the genus must necessarily be based princi-
pally on /'. lirassicae. .\lthough this species has been
intensively studied for more than .50 years, there
is still considerable disagreement and controversy
about its critical developmental stages, and doubt-
less much remains to be discovered.
The resting spores of P. Brassicae normally give
rise to a single zoos])ore in germination (fig, 13-17),
but it is not imj)rob.ible that more than one may be
produced by the occasional large, bi- and multinu-
cleate resting spores. Some workers, including Pol-
lacei (12) and Honig ('31), have seriously ques-
tioned the production of zoospores in this species.
Honig, in particular, maintained that only non-flag-
ellate amoebae are formed in germination (fig. 16—
18). .\lso, most investigators have figured and de-
scribed the zoospores as anteriorly uniflagillate, but
Ledingham ('St) clearly demonstrated that they are
biflagellate and heterocont (fig. 22, 23). They have
also been described in tile literature as varying from
oval, pyriform, and fusiform to spherical in shape
(fig, 19-23). After emerging from the sjiore case
tliey may swim 'apidly away or become intermit-
tently amoeboid v ;. 19. 20), during which the ante-
rior end may double back and forth and thus jerk
the sjiore body along.
.\ccording to most students, the zoospores come
to rest on the host and enter as amoebae through the
root hairs and e))idermal cells, where they soon cause
local hypertroi)hy (fig. 28, 29), A few workers, how-
ever, have questioned these observations. Kunkel
('18) found nothing but thalli of Olpidium Brassicae
in the root hairs of the host sjieeies which he studied
and like F.ivorski (10) concluded that the ])revious
reports on the occurrence of /'. Brassicae in such host
cells were erroneous. However, subsequent investi-
gators, including Cook and .Schwartz ('30). Honig
('31), Rochlin ('33). and Fedorintschik ('lio) have
clearly shown infection of root hairs. Honig ajipears
to have been the first to observe, describe, and figure
actual penetration of the parasite into root h.iirs (fig.
27). He maintained that the ))r<)toplasts derived
from geruiin.iting resting sjiores are true .iiiioebae
without Hagella, a contention which has been re-
futed by subsequent observers. Honig found small
amoebae .as well as giant ones meas\iring l-2(i jx by
2l'-3(>/( abundant around root hairs and observed
tii.it both tyi)es may readily enter the host eell. In
so doing they become closely .iiiplicd to the root h.iir,
and soon thereafter a hole appe.irs in the wall at the
region of attachment, through which they then enter.
The hole closes u]> immediately afterwards, so that
it is no longer visible after the parasite has entered,
Honig also observed that amoebae may live sapro-
|)hytieally for weeks in the soil and increase mark-
edly in size (fig. 3.")).
It is not imiirobable. ;is Hoelilin's ('33) study
suggests, that under certain enviroiiment.il condi-
tions and particularly when s])ores germinate in eon-
tact with the host cell, flagella are not formed, and
the jiarasite enters the host almost at once in the
amoeboid state. Rochlin found that the resting spores
become attached to the root hairs and e))idermal cells
of the root and cap and cause localized swelling of
the eell wall (fig. 21-26). These regions become
gelatinized and show no cellulose reactions when
tested with chloro-iodide of zinc, indicating that a
chemical change has taken place. .Small jjlastic,
spherical protoplasts which presumably emerge
from the attached sjiores, pass through these swollen
and gelatinized regions (fig. 26) and enter the host
cell.'
The amoebae and young ))lasmodia in the host cell
may bud and divide repeatedly (fig. 30), according
to Gay lord (Ol), Chupp (17), Kunkel, Fedorints-
chik and others, and thus multiply in number. They
may also encyst and develop fairly thick hyaline
walls (fig. 44—46) under unfavorable conditions. As
the ))lasmodia grow in size and their nuclei multi))lv,
they penetrate the walls of the adjacent cells and
thus migrate from cell to cell (fig. 31-33), accord-
ing to W'oronin ('78), Lutman ('13), Chupp ('17),
Kunkel, Honig, Rochlin, Larson ('34), and Fedo-
rintschik ('3.5). As to the method of cell wall jiene-
tration, Rochlin noted that the plasmodium may be-
come closely a))plied to a region of the wall and
through lysic action cause localized swelling and
gelatinization (fig. 7) of the latter. Passages in the
walls are thus formed through which the plasmodium
enters. Kunkel believed that only young and small
Plasmodia free of oil bodies and other priidiicts are
cai)able of migration. Cook .-iiid Schwartz ('30) were
uncertain on this jihasc of develoi)ment and some-
what vague in their description of it. In one )iart of
their paper (p. 287) they stated that the amoebae
"have the ])ower of ]>enetr;iting the walls of the host
cells and in this way can tr.ivil through the cortical
tissues of the host, " but they thought it im))robable
()). 297) that the plasmodia are able to do so. I'inally
(|). 301 ) they expressed the belief that oidy gametes
from sporangia have the ability of ))assing from cell
to cell, .ind after gametic fusion the zygote is dis-
tributed onlv bv division of infected host cells.
24
PLASM ODIOPHOR ALES
Cook and Schwartz, nonethek-ss, discovered a
hitherto unknown stage in tlie life cycle of P. Brassi-
cae. The amoebae derived from flaoellate zoospores
penetrate root hairs, grow in size, and by regular
mitosis become multinucleate plasmodia which soon
cleave into uninucleate portions. These segments
round up. develop thin hyaline walls, and become in-
cipient zoosporangia (Hg. 37). In view of this dis-
covery, it seems probable that the small cleaving
Plasmodia which Cliupp described and figured (p.
•i36, fig. 104H) as stages in resting spore formation
in root hairs relate to the development of zoosjioran-
gia. The nuclei of the zoosporangia (fig. 38) divide
mitotically two or three times, after which the proto-
plasm cleaves into uninucleate segments (fig. 39—
42). forming thus four to eight pyriform zoospores
(fig. 43). These are smaller than those derived from
resting spores, according to Cook and Schwartz,
who regarded tliem as gametes. As the walls of the
sporangia collapse the zoospores emerge, fuse in
pairs, either in root hairs or after migrating into the
cortex, and form zygotes which grow into diploid
sporogenous plasmodia, as has been described in
Ciiapter III.
Fedorintschik confirmed Cook and Schwartz's dis-
covery of zoosporangia. He reported that individual
amoebae in root hairs develop directly into large
plasmodia containing up to 100 or more nuclei. These
plasmodia cleave into uninucleate segments which
develop walls and become rudimentary zoosporan-
gia. The first division of their nucleus is meioiic,
and then follow a second and sometimes a third
mitosis, after which the protoplasm cleaves into four
to eight zoospores. A single amoebae in a root hair
may, according to Fedorintschik's observations, ulti-
mately result in the formation of 400 to 800 zoo-
spores. These zoospores become amoeboid and mi-
grate into the cortical tissues and multiply rapidly
by budding. After the content of the host cell is ex-
hausted, they fuse, presumably in pairs (?), and
later develop into plasmodia. Fedorintschik believed
this fusion constitutes the sexual phase of P. Brassi-
cae, and thus confirmed Cook and Schwartz's earlier
report of sexual reproduction in this genus. In light
of Ledingham's ('3.5, '39), Couch, Leitner, and
Whiffen's ('39) studies on Sponc/ospora, Poli/mi/.ra,
and Octoviifxa, however, it seems more probable that
these so-called gametes are only secondary zoospores
which reinfect the host and give rise to an additional
amoebae and plasmodia in much the same manner as
is indicated in text-figure 10 of Spongospora.
Several workers have reported that tlie Plasmo-
dium of P. Brassicae may undergo schizogony and
give rise to a few or several meronts, whereby the
parasite is rapidly multiplied. Nawaschin ('99) did
not actually observe the ))roeess, but he believed that
the large number of small thalli in a host cell could
be explained only on the assumption that they had
arisen by division of a preexisting thallus. He
thought that the extended pseudopodia of the Plas-
modium were cut off as buds, a belief which was later
supported by I.utmau and by Henckel ('23). Subse-
quently, Maire and Tison ('C9). Chupp, Kunkel,
Jones ('28), and Cook ('33) also reported schizog-
ony of the Plasmodium of P. Brassicae. It must be
noted, however, that many of the early described
cases of schizogony in the superficial host cells may
possibly relate to the development of zoosporangia.
As is shown in figure 36, the meronts may be uni- or
multinucleate, and it is not improbable that after a
period of growth they in turn may function as schi-
zonts and form secondary meronts.
With the exception of Cook and Schwartz and
Fedorintschik who reported that the sporogenous
Plasmodium is formed by the fusion of two gametes,
many investigators who studied this phase of devel-
opment were of the opinion that the plasmodium
arises by the union of several vegetative amoebae or
small Plasmodia. Woronin was uncertain whether it
originates from a single amoebae or by the fusion of
several, although he thought the latter method more
plausible. Eycleshymer ('01) observed that if a
slide with zoospores and amoebae is kept in a moist
chamber, larger ])lasmodia appear, which he assumed
had arisen by fusion of amoebae. Honig, however,
maintained that the amoebae observed by Evcles-
hynier do not relate to P. Brassicae. Halsted ('93)
also believed that amoebae coalesce to form large
Plasmodia. Nawaschin ('99) tliought that the schi-
zonts and meronts remain more or less independent in
the host cell until shortly before sporogenesis, when
the}' flow together and form a large plasmodium.
He admitted also that single amoebae may grow in-
dependently into large plasmodia. Gaylord. Ericks-
son ('13), Esmarch ('24), Prowazek, and Terby
('24) supported Nawaschin's belief on the union of
amoebae, but INIaire and Tison ('09) refuted this
contention. They pointed out that although meronts
and schizonts may appear to be fused, they are none-
theless separate and distinct. They based their view
primarily on the lack of synchronism in nuclear di-
vision in the closely associated amoebae and plas-
modia in the same host cell. Lutman, Chupp, and
Kunkel were uncertain about the union of amoebae,
but Lutman noted that the nuclei in a plasmodium do
not all divide simultaneously, which suggests that
they may have been derived from several amoebae
of different ages. Later, Jones ('28a, '28b) also re-
ported fusion of amoebae and ])lasmodia in cultures
of P. Brassicae, but there is considerable doubt about
the validity of the organism he had in culture. In ad-
dition to describing the origin of the plasmodium
from a zygote. Cook and Schwartz reported that in
the early stages of development several amoebae and
later small plasmodia may fuse vegetatively to form
the incipient sporogenous plasmodium. Since that
time Milovidov ('31) also reported vegetative fusion
of several amoebae.
The plasmodium of /'. Brassicae is capable of slow
amoeboid movement, and this mobility apparentlv
enables it to move from cell to cell. Rochlin reported
that the plasmodium first sends out a hyaloplasmic
thread (Geissel) in the direction of movement, and
shortly thereafter tlie more ajranular mass begins to
I'l.ASMODIIU'lldH S
25
niovo. In vouiim: ))l.isiiuHii:i tlio psiiulo|)(i(ls .ire nl.i-
tivflv loni: .•iiul tt iiuous. but a> tin- i)l;iMii(i(liuin lu.i-
tiircs. tlu-v lu'coiuc Itss oxti-iisivc and more rouniloil
at till- ptri))li(r_v. I'ignri- 31 shows a mature Plasmo-
dium with several dense, opaque, iiseuihiixidial lobes
at the anterior end. The posterior end in eontrast is
quite vacuolate, thin, and relatively hyaline. 'I'lu
amoebae .-ind younji jdasmodia are hyaline, somewhat
transparent, viseous and slimy, and eomparativily
free of oil dro))lets and other bodies, but as the i)l;is-
modium inere.ises in size, the i)rotoplasm becomes
denser, more opacpu'. .md very rieh in oil jjlobuies.
Infected hypertrophied host cells are often rich in
starch grains, and according to Woronin. Xawaschin
("99). Prowa/.ek ('05). and Lutman. these grains
may frequently be found in the folds of the Plasmo-
dium. N.iwasehin. I'avorsky ('10), and Henckel
('23) did not believe tiiat amoebae and ))lasmodia
are capable of engulfing solid )iarticles, and Nawas-
cliin |)ointed out that starch grains, such as those
shown in figure 7 !■, are often caught between fusing
merouts and thus come to lie within the plasmodiuni.
Woronin, Eyeleshymer, and Lutman inferred that
the i)lasniodium feeds on these grains, because by
the time sporogenesis begins they have almost en-
tirelv disai)peared, although a few may occasionally
be found later scattered among the sjjores. Although
Honig did not observe the plasmodiuni engulfing
solid particles, lie nevertheless described it as nour-
ishing itself sai)roi)liytically outside of the host for
several weeks. In addition to oil globules, starch
grains, and other bodies, chondriosomes are quite
abundant in the i)lasmodia (fig. 48). according to
Von wilier ('18) and Milovidov ('31). They also
occur abundantly in the resting spores (fig. 86) and
amoebae.
L'nder unfavorable environmental conditions plas-
modia and segments of the same in P. Brassicae may
encyst and develop thick walls, according to Prowa-
zek. Cook and .Schwartz, and Milovidov (fig. 46. 47).
Prowazek ('05) and .Milovidov regarded these cysts
as ))athological and involution forms. Cook and
Schwartz described the ])lasmodium as becoming en-
veIoi)ed by a distinct wall and then segmenting into
several portions which in turn develojied thick walls
(fig. 47). With the return of favorable conditions
the walls disa))pear, and the plasmodium continues
to function normally. Encysted ))lasniodia have also
been described in /'. Fici-repeniis by Andreucci
('26). The cysts in this species are globular. 9.15-
73 n in diameter, with sculi)tured. thick w.-ills, and in
germination give rise again to plasniodia. The sig-
nificance of these cysts as a phase in the life cycle of
Plasmodiophora is not clearly understood, but they
are doubtles comparable with the sclerotia of the
niyxomycetes.
The majority of resting spores are iniimuliatc,
but occasional globose and irregular ones (fig. 87)
have been reported by Prow.azek. Milovidov. and
others. Milovidov. in jtarticular. has figured numer-
ous tetra-. tri-. and binucleate spores. The binueleate
and nndtinucleate condition mav have resulted from
the f;iilurc of large cleavage scgMuiits to (li\ ide .-iftcr
flu- comi)letion of the second nuclear division. On the
other hand, it is not altogether improb.-ible th.it it
may have arisen ;is the result of ;i third mitosis in
the inci))icut s))orc seguuMits in the maimer described
by Maire and Tison and Home in Soro.sphacra I't-ro-
iiirar and Sponrjospora siihicrranea, respectively.
I.utman ('13) and Tcrby ('2f) also figured biuuele-
.itc spores (fig. 95) and believed they had arisen as
tiu> result of division in the spore. After the spores
h.ive been formed they may remain stuck together for
.1 short time by the slimy intercellular substance left
from the jjlasmodiuui. Howc\er. they soon develo)j
hyaline walls, dehydrate, and sejiarate. .\t no stage
are they cnvelol)ed by a common membrane or form
a cystosorus of definite structure, size, and shape.
According to the rejiorts in the literature the resting
spores may vary up to and more than 200 per cent in
size. The early investigators found the siiores to be
quite small, but measurements by subsequent work-
ers have shown them to be considerably larger.
Woronin ('78) rejiorted them to be 1.6 /x in diam-
eter; Lowenthal ('05), 4 ;u ; Molliard ("09), 1.8-
2.2 /x: Chupp ('17) and Appel ('28), 1.9-4.3 /i, and
2.5-6.9 (u for the irregular ones; Esmarch ('24),
1-2 /J,; Pape ("25) and Honigmann ('26). 2.8-3.3 ix;
Wellman ('30), 1.7 /x; Cook and Schwartz ('30),
2-3 /x, and 4.6X6 /x for the oval ones; and Honig
("31), 3.9 jx. The last-named worker made extensive
measurements from nimierous hosts grown in differ-
ent types of soil and under varying climatic condi-
tions and found that the spores did not differ more
than 0.5 /x in diameter. According to Wissenlingh
('98) the spore wall consists of chitin and shows no
cellulose reaction when tested.
The account given above is generally considered to
be the usual developmental cycle of P. Brassicae.
Henckel and P. M. .lones ('28b). on the other hand,
have reported life cycles for this species which vary
markedly from the orthodox type. In his study of
club root of radishes Henckel described the resting
spores as "aplanoamoebae" which by a jirocess of
gelatinization or softening give rise to "Umax amoe-
bae." These multi))ly outside of the host by budding,
and when this jirocess is eomijleted, the numerous
daughter amoebae enter the host and form a ))lasmo-
dium. At no stage iu the life cycle are zoos))ores or
flagellate gametes develojied. according to Henckel.
In connection with his account it may be noted that
Favorsky also figured and described spore germi-
nation in rotten tumors as a process of gelatiniza-
tion and softening of the s])ore wall, whereby large
/('ma.r-like amoebae are formed. P. .M. .lones re))orted
that he had isolated eight |)ure cultures of /'. Brassi-
cae from cabbage roots and ui.iintained them in ta]i
water under lal)oratory conditions for two months.
These cultures caused galls on turnips when used
as an inoculum and were subsequently recovered in
culture from the diseased roots. .Vccording to .Tones
(text-fig. 3). the following successive stages occur
within the host: gametes, zygotes, preplasmodia,
Plasmodia, cysts and spores ; while in culture outside
26
PLASMODIOPHORALES
of the host, gametes, zygotes, cysts, amoebae, pre-
plasmodia, and buds are formed. If conditions are
favorable, however, P. Brassicae does not develop
all of these phases. Jones' account has never been
confirmed, and most subsequent investigators have
doubted tlie accuracy of his observations. In light of
present-day knowledge about P. Brassicae it seems
likely that he may have been dealing with develop-
mental pliases of more than one organism. Milovidov
and Honig contended that some of the stages figured
bv Jones relate to Olpidiiim Brassicae and Asiero-
cystis radicis.
P. BRASSICAE Woronin, I.e., pis. 1-6. 1878. Jahrb. Wiss.
Bot. 11: .548. Pis. :39-34.
Resting spores globose, spherical 1.6-4.3 /x. aver-
age 3.9 jx, oval, ellipsoidal, 4.6X<3jU., sometimes
constricted, elongate and irregular, 2. .5-6. 9 /i, with
smooth, relatively thin, hyaline walls. Zoospores
pyriform, splierical, 2. .5-3.5 /it, swimming rapidly
and becoming intermittently amoeboid. Sporangial
Plasmodia variable in size. Zoosporangia few or nu-
merous, small, oval, spherical, 6-6.5 /^. angular and
elongate with thin hyaline walls : producing 4 to 8
zoospores which are liberated by the collapse of the
sporangium wall. Sporogenous plasmodia 100-200 /x
in diameter, hyaline to pale-grey in color, amoeboid;
encysting occasionally, undergoing schizogony into
uni- and multinucleate meronts.
Parasitic in the roots of wild and cultivated cruci-
fers in temperate climates throughout the world,
causing spindle-shaped, globose and irregular swell-
ings, or galls and occasionally dark sunken spots and
lesions.
A complete list of hosts, degree of infection, geo-
graphical distribution, and bibliography of P. Bras-
sicae are given in Chapter VI.
Biological Races of Plasmodiophora Brassicae
Marked differences in degree of infection have
been found in various species and varieties of wild
and cultivated crucifers, and this has led to the belief
that P. Brassicae may include several biological
races or strains which are more or less virulent and
specific for certain hosts. Appel and Werth ('10),
Ericksson ('13), Hostermann (according to Honig.
'31), and Gleisberg ('23) suggested the existence of
such races, and numerous attempts have been made
to demonstrate their jiresence. Between 1924 and
1929 Honig made six experiments involving a large
number of cruciferous liosts from which he ('31) re-
ported positive results. A strain of P. Brassicae from
kohlrabi was found to be readily transmissible to
kohlrabi, cauliflower, rape, turnips, and Cammelina
sativa, but could be transmitted only with difficulty
to radishes. A cauliflower strain was also discovered
which proved to be similar to the one on kohlrabi, but
strains from Savov cabbage and radish were found
to be distinct. Motte ('33, '35) and MacLeod ('31)
believed that they liad obtained evidence of biologi-
cal specializ.-ition, but later after making tests of
spores from 50 different sources, the latter worker
found no evidence to confirm this belief. Motte ('33)
found that the form from charlock grew especially
well on turnips. Gibbs ('31) likewise tested various
inocula for evidence of specialization, but all of his
results were negative. In 1939 J. C. Walker observed
a high degree of resistance to club root in swedes in
Wisconsin, which was contrary to results obtained
elsewliere, and thought that this difference indicated
a variation in pathogenicity of the causal organism.
He accordingly secured spores from widely sepa-
rated regions of the United States and tested their
virulence on swedes, but found little difference in
pathogenicity.' The data in the literature on the ex-
istence of biological strains are therefore conflicting,
and most investigators, witli the exception of Honig
and ^Nlotte. liave doubted tlie presence of such strains
in P. Brassicae.
1 However, in a paper presented before the Dallas,
Texas, meeting of the American Phytopathological So-
ciety, December, 1941 (Phytopath. S2: 18). Walker gave
additional data on physiological specialization in P. iJro.v-
.licae. Purple Top Milan turnip remahied completely free
of club root when grown in heavily infested soil in Wis-
consin, but when planted in naturally infected soil in Eng-
land, about -'0 per cent of the plants were diseased. On the
other hand, an English variety. White Stone, which showed
87 ))er cent infection in an English test, failed to develop
clubbed roots in inoculation tests with a representative
American isolate of P. Brassicne. Walker accordingly con-
sidered this evidence as proof of the existence of physio-
logical races.
Bacteria in Relation to P. Brassicae
The association of bacteria with P. Brassicae in
roots of diseased crucifers was noted by Eycleshy-
mer in 1894 and confirmed by Pinoy ('05). E. F.
Smith ('11). and other early workers. From his pre-
PLATES 2, 3, 4
Pldsmndiofihorn Brassicae
Fig. 1. Infected cabbage roots with spindle-shaped swell-
ings. Woronin, '78.
Fig. -2. Beginning of club formation on roots of cabbage
inoculated experimentally. Woronin, I.e.
Fig. 3. Heavily infected turni]) root. Woronin, I.e.
Fig. 4. Cross section of infected cabbage root. Note two
compact groups of infected cells on lower right side, the
so-called "krankheitsherde." Woronin, I.e.
Fig. 5. Nuclear division in an enlarged infected host cell.
Lutman. '13.
Fig. (i. Division of infected cell. Lutman. I.e.
Fig. 7. Enlarged cells of cabbage with mature plasmodia
showing the swelling and dissolution of intervening cell
walls. Hochlin, "33.
Fig. 8. Normal host nucleus. Lutman, I.e.
Fig. f)-\2. Enlargement, distortion, and degeneration of
liost nuclei in infected cells. Lutman, I.e.
Fig. 13. Germination of resting spore. Chuiip, '17.
Fig. 14, 15. Same. Woronin, I.e.
Fig. l(i-18. Germination of resting spore, and amoebae.
Honig, '31.
Fig. 19, Jl. .Amoeboid, anteriorly uniflagellate zoospores.
Woronin, I.e.
Fig. JO. Fixed and stained zoospore with anterior blepho-
rophist. Cook and Schwartz, '30.
IM.ASMDDIOlMlOltA
27
I'LATl'l •>
28
PL ASMODIOP MORALES
vious studies (02, '03) on bacteria in relation to tlie
niyxoniycetes. Pinoy (05, 07) concluded that bac-
teria were essential to the development of P. Brassi-
cae and described the relationsliij) between them as
true symbiosis, a viewpoint which Vouk (13) later
supported. Pinoy reported that the spores of the
fungus will germinate only in the presence of these
bacteria, and as the zoospores or amoebae enter the
host they are accompanied by cocci which continue
to live in constant association with the parasite
throughout its entire life cycle. Chupp (17) re-
peated Pinoy's experiments to some degree and
found that bacteria are absent in small, young swell-
ings and do not appear until the galls have become
quite large and old. Furthermore, instead of cocci,
he found the most prevalent form to be a motile, rod-
shajjcd bacillus which forms yellowish, ojjalescent
colonies on nutrient media. Chupp concluded from
his experiments that bacteria do not enter the host
with the amoebae and that the disease must attain a
certain advanced stage before the bacteria can enter.
According to him, they are not essential to the devel-
opment of P. Brassicae, but as Sorauer (08) had
previously jjointed out, they may act in decomposing
the host cell wall and thus liberating the spores.
Naumov ('2.5) likewise failed to find bacteria in
young galls, while Fedotowa (30) reported that bac-
teria may be present within one and a half to five
months after infection. He found that P. Brassicae
spores may be easily freed of bacteria by immersing
them for five minutes in a .001 per cent corrosive
sublimate solution. From diseased roots he isolated
one bacillus and two coccus forms which when in-
jected into roots in pure culture produced no signs
of hy])ertrophy or injury, Fedotowa tlnis showed
that bacteria are in no way necessary to spore ger-
mination, entrance of the amoebae, or to the nutrition
of the Plasmodium.
Plasniodiophora Brassicae and Cellular Inclu-
sion of Cancer Cells, Small Pox, and Rabies
At the close of the last century when animal path-
ologists were actively engaged in trying to prove the
parasitic nature of the inclusions found in carcinoma
Fifr. -2-2, i3. Anteriorly biflagellate, heterocont zoospores.
Leclinpliam, '34.
FifT. 2i. Restinjr spores attached to root hair tip, small
spherical myxamoeba within the cell and two myxamoi-ba
entering through a swollen gelatinized region of the wall.
Rochlin, '33.
Fig. :?.5. Three parasites lying in a swollen gelatinized re-
gion of tlie root liair wall. Rochlin, I.e.
Fig. 2G. Entry of the parasite through the epidermal cell
wall of the root of B. arvensis. Note other swollen and dis-
organized regions where additional parasites have entered.
Rochlin, I.e.
Fig. 27. Entry of an amoeba in root hair. Honig, I.e.
Fig. 38. Swollen root hair of cabbage with a living myx-
amoeba. Woronin, I.e.
Fig. 39. Uninucleate myxamoeba in root hair wliich is
locally swollen. Cliupp, I.e.
Fig. 30. Division of a myxamoeba by fission. Chupp, I.e.
Fig. 31. Early stage in cell wall penetration by a young
Plasmodium. Kunkel, '18.
Fig. 33. Later stage. Kunkel, I.e.
Fig. 33. Young plasmodium passing through cell wall.
Kunkel, I.e.
Fig. 34. Large living amoeboid plasmodium moving
within liost cell. Note pseudopods at the anterior and vacu-
oles in the posterior end. Woronin, I.e.
Fig. 3.5. Large saprophytic amoebae or ])lasmodia out-
side of host. Honig, I.e.
Fig. 3(). Root hair filled with meronts, possibly incijiient
zoosporangia. Chupp, I.e.
Fig. 37. Empty and developing zoosporangia in a root
hair wliieli have been formed from a plasmodium. Cook and
Schwartz, I.e.
Fig. 38. Uninucleate segment of plasmodium which will
develop into a zoosporangium. Cook and Schwartz, I.e.
Fig. 39. First mitosis (meiotie?) in incipient zoosporan-
gium. Cook and Schwartz, I.e.
Fig. 40. Binucleate stage of same. Cook and Schwartz,
I.e.
Fig. 41. Zoosporangium with four ineijiient zoospores.
Cook and Schwartz, I.e.
Fig. 43. Same with three fully formed zoospores. Cook
and Schwartz, I.e.
Fig. 43. Nonflagellate zoospores from zoosporangium.
Cook and Schwartz, I.e.
Fig. 44—46. Encysted myxamoeba and young plasmodia.
Milovidov, "31.
Fig. 47. Large segmented jilasniodium, the segments of
which have encysted. Cook and Schwartz, I.e.
Fig. 48. Binucleate plasmodium with numerous cbondrio-
somes. Milovidov, I.e.
Fig. 49. Resting nuclei of large plasmodium. Cook and
Schwartz, I.e.
Fig. 50. Same in young plasmodium. Nawaschin, "99.
Fig. 51. Same in amoebae with centrosomes and astral
rays. Milovidov, I.e.
Fig. 53. Early prophase of "promitosis" with chromatin
in the form of numerous granules. Nawaschin, I.e.
Fig. 53. Equatorial plate stage of "promitosis" with di-
vided nucleole. Nawaschin, I.e.
Fig. 54. Same stage. Cook and Schwartz, I.e.
Fig. 55, 56. "Double anchor" stage of "promitosis." Na-
waschin, I.e.
Fig. 57, 58. Late anaphase and telophase of "promitosis."
Nawaschin, I.e.
Fig. 59-61. Successive stages In development of the
"akaryote" stage. Cook and Schwartz, I.e.
Fig. 63. Akaryote stage. Cook and -Schwartz, I.e.
Fig. 03. Siiireme stage of the first sporogonic (meiotie?)
mitosis. Lutman, I.e.
Fig. 64, 65. Synapsis and i)ossibly diakinesis, respec-
tively. Milovidov, I.e.
Fig. 66. Early prophase of meiosis. Terby, '34.
Fig. 67. Synapsis. Terby, I.e.
Fig. 68. Strepsitene. Terby, I.e.
Fig. 69, 70. Diakinesis. Terby, I.e.
Fig. 71. Polar view of equatorial plate stage showing
eight chromosomes. Terl)v, I.e.
Fig. 73. Profile view of equatorial plate stage, first divi-
sion. Lutman, I.e.
Fig. 73. Polar view of same showing eight large chro-
matic bodies. Lutman, I.e.
ri.A.S.MDUlOl'IlOllA
PLATE 3
29
iiv-^'^>^
65 V-'-'
66
62
63
67
68
IMiisiiiodiojiliorii
69' 70 71
^64 £^.
f o
72 73
30
PLASMODIOPHOHALES
cells, numerous parallelisms were drawn between
cancer and club root of crucifers. The superficial re-
semblance of the tumors on cruciferous roots to can-
cerous outgrowths in animals as well as the similarity
of the amoeboid stages c P. Brassicae to the cellu-
lar inclusions (Plimmer bodies, etc.) in cancer cells
led some workers to the belief that fungi, particu-
larly tlie myxomycetes and Plasmodiophora, may be
associated with, or the cause of cancer in animals.
Numerous experiments were accordingly performed
in which infected cruciferous tissues were implanted
in various kinds of animals. While these studies
failed to throw light on tlie cause of cancer, they
nonetheless focused attention on club root from the
purely pathological viewpoint and are of consider-
able liistorical interest.
In 1898 and 1899 Behla pointed out the similarity
of club root and potato wart to cancer and discussed
the possible relation of Plasmodiophora and Sijn-
chytrhnn to this disease in animals. After having in-
fected animals with these fungi and noted the simi-
larity of their developmental stages to certain inclu-
sions in carcinoma cells, he concluded in 1903 that
cancer is caused by a chytridiaceous organism. In
1900 and 1903 Podwyssotzki reported that he had
succeeded in producing tumors in guinea pigs and
dogs by subcutaneous and intraperitoneal implanta-
tions of infected crucifer tissues. These tumors were
about the size of a walnut and resembled large-celled
sarcoma, endothelioma, or granuloma. They were
mesodermic in origin and had arisen through pro-
nounced hypertropiiy and repeated division of the
connective tissue cells and endothelium of the peri-
vascular fissures. Leucocyte infiltration was quite
evident at first but disappeared after 8 to 12 days.
Podwyssotzki found furtlier that P. Brassicae pro-
duced many other changes in animal cells which
were similar to those induced in cells of crucifers.
Further attempts to draw analogies between the
inclusions of cancerous cells and those produced by
P. Brassicae in animal cells were made by Feinberg
('02) and Gaylord ('04). The latter succeeded in
infecting animals locally with P. Brassicae, and
from his observations on tlie tumors produced he
pointed out in detail the parallel cellular symptoms
of club root and cancer. Gaylord concluded that can-
cer is caused by an amoeboid organism the develop-
mental stages of wiiich are very similar to P. Brassi-
cae. In 190.5, however, I.owenthal refuted all pre-
vious reports that the club root organism produces
typical cancerous tumors in animals. He implanted
infected crucifer tissues in the stomach, liver, and
kidney of dogs and in the skin of white rats, but
failed to get tumors or any other specific reactions in
the animals. In the same year Prowazek (0.5) made
an extensive comparison of P. Brassicae and the in-
clusions of carcinoma cells, particularly the Plimmer
bodies, and concluded that except for superficial
similarities they have very little in common funda-
mentally, ^lore recently Levine and I.evine ('22)
have made a comparison of the tumors of P. Bras-
Fiir. 74. Simultaneous nuclear division (meiotic?) in a
large, somewhat vacuolate plasmodium. Note large starch
grains lying in clear regions. Xawaschin, I.e.
Fig. 75. First meiotic division with centrosome-like bod-
ies and astral rays apart from nuclei in the cytoplasm.
Terby, I.e.
Fig. 7(). Second meiotic division showing four chromo-
somes. Terby, I.e.
Fig. 77. Second meiotic division showing centrosome-like
bodies. Terby, I.e.
Fig. 78. Vacuolate stage of plasmodium prior to cleav-
age. Lutman, I.e.
Fig. 79. Cleavage furrow at edge of plasmodium. Lut-
man, I.e.
Fig. 80. Nuclear division in a large cleavage segment.
Milovidov, I.e.
Fig. 81, 8-2, 83. Mitosis and cell division in smaller cleav-
age segments. Lutman, I.e.
Fig. 84. Fully formed resting spores witli chromatin
around inner periplierv of nucleus. Cook and Schwartz,
I.e.
Fig. 8.5. Mature resting spore with fat droplets. Lutman,
I.e.
Fig. 86. Resting spores with chondriosomes. Milovidov,
I.e.
Fig. 87. Variations In size and shape of resting spores.
Milovidov, I.e.
Fig. 88. Fusion of incipient resting spores. Prowazek,
'0,5.
Fig. 89. Binucleate resting spore. Prowazek, I.e.
Fig. 90. Division of one gametic nucleus. Prowazek, I.e.
Fig. 91, 9-3. Formation of "reduction bodies." Prowazek,
I.e.
Fig. 93. Karyogamv. Prowazek, I.e.
Fig. 94. Centrosome separating from nuclear membrane
to become the blephoroplast. Terby, I.e.
Fig. 95. Resting spore with blephoroplast. Terby, I.e.
Fig. 96. Binucleate resting spore. Terby, I.e.
Fig. 97. Host cell filled with resting spores. Woronin, I.e.
P. J>iphnifherae
Fig. 98. Infected plant of Diplanthera U'rif/htii with
hvpertrophled bead-like intcrnodes. Ferdinandsen and
Winge, "14.
Fig. 99. Cleaving plasmodium which fills enlarged host
cell and envelops host nucleus. Drawn from photograph.
Ferdinandsen and Winge, I.e.
Fig. 100. Host cell filled with resting spores. Drawn from
photograph. Cook, '33.
Fig. 101. Normal and collapsed resting spores. Drawn
from photograph. Ferdinandsen and Winge, I.e.
/'. Flcl-rej)(ntis
Fig. 102. Gall on branch of FIciis repen.-:. Drawn from
l)hotograph. Cook, I.e.
P. II(ilujihil<(e
Fig. 103. Hypertro])hied petiole of IlalophUii ovnVis.
Ferdinandsen and Winge, '13.
Fig. 104, 105. Normal and collapsed resting spores.
Ferdinandsen and Winge, I.e.
P. Iiirtaifldtit
Fig. 106. Plasmodium t-nvcloping enlarged host mu'leus.
Feldmann, '40.
Fig. 107. Cleavage into resting spores. Feldman, I.e.
Fig. 108. Resting spores. Feldman, I.e.
ri. ASMOniOIMIOHA
81
I'LATK 4
--^s::^-,'*w „u
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I'la>mo(li()i>liora
32
PLASMODIOPHORALES
sicae on crucifers and the malignant neoplasia in
animal cancer.
Analogies have also been drawn between tlie club
root organism and the cellular inclusions formed in
vaccination against small pox. Gorini ('01) suc-
ceeded in producing a slow but marked proliferation
of the cornea epithelium in dogs by implanting in-
fected cabbage tissues and found that tlie intracellu-
lar effects were very similar to those caused in vac-
cination. Certain phases of P. Brassicae under these
conditions resembled the Ci/torcf/tes bodies associ-
ated with small pox. Pollacci ('12) pointed out some
of the striking resemblances between the early devel-
opmental stages of P. Brassicae and tlie Negri bodies
of rabies in dogs and believed that there might be a
connection between these two cellular structures.
P. DIPLANTHERAE (Ferdinandsen and Winge) Cook,
193-'. Hong Kong Nat. Suppl. 1:34.
Oxtf'iifcUUella Diplantherne Ferdinandsen and Winge,
19U. I.e., pi. 45. Fig. 1-4.
Resting spores globose, spherical, 4-4. .5 /j,. with
fairly thick, brown, smooth walls; germination un-
known. Zoospores and evanescent zoosporangia un-
known. Plasmodium filling host cell, 125-200^ in
diam. ; schizogony doubtful; cleaving directly into
uninucleate resting spores during sporogenesis.
Parasitic in Diplanthera icrif/htii, St. Croix, West
Indies, causing large galls on tlie stems in the re-
gion of the internodes.
This imperfectly known species was found in 1913
by Ostenfeld who turned over his material to Ferdi-
nandsen and Winge for further study. From this
scanty and poorly fixed material they created a new-
genus, Osienfeldiella, for the species at hand. Cook
subsequently examined their prepared slides and
concluded that the fungus is a species of Plasmodio-
phora. Because its plasmodia cleave directly into
resting spores which are not united in cystosori but
lie loose and separate in the host cell as in Plasmo-
diophora, there is no reason, on the basis of present-
day knowledge, for keeping this species in a separate
genus. Cook's disposition of it is accordingly fol-
lowed here.
Ptasmodiophora Diplantherae attacks only the in-
ternodes and causes them to enlarge, so that the stem
has the appearance "of a string of pearls." as is
shown in figure 98. The parasite is restricted to the
inner cortex where it leads to marked enlargement of
the infected cells. Normal cells measure approxi-
mately 35 /i in diameter, while infected ones vary
from 12.5 to 200 (u. In the early stages of infection
the young liost cells apparently retain their ability
to divide, and it is not improbable that the young
parasites may be dispersed by division of the host
cell. The plasmodium seems to envelop the host nu-
cleus (fig. 99), and witli the start of the sporogonic
phase tlie nucleus begins to degenerate. The pres-
sure exerted by the enlarging cells causes tangential
stretcliing of tlie outer cortical elements, and in cases
of unilateral infection the central cylinder becomes
laterallv displaced. Since the parasite is localized in
the inner cortex, infected stems can readily continue
to grow and elongate.
Whether schizogony or any other division of the
parasite within the host occurs in this species is un-
certain. So far none has been observed. Ferdinand-
sen and Winge nevertheless concluded that the young
amoebae divide after each mitosis, because only uni-
nucleate stages are to be found in the meristematic
areas of the stem.
P. HALOPHILAE Ferdinandsen and Winge, 1913.
Centralbl. Bakt. Parasitenk. II, 37: 167. Fig. a-c.
Resting spores yellowish in mass, hyaline when
single, globose, 5 /a, with fairly thin smooth walls.
Plasmodia one to several in a cell, variable in size
and shape, subglobose. elongate, 30-60 /x long. All
else unknown.
Parasitic in the petioles of Halophila oralis on the
island of Noesa Kembangan near the southern shore
of Java, causing conspicuous pea-shaped galls.
The diagnosis of this species is based on a study
of dried material which Ostenfeld found in a collec-
tion of H. oralis in the Botanical Museum of Huana.
He believed that the hypertrophied petioles (fig.
103) were parasitized by a species of Plasmodi-
ophora but made no study of the organism. The dried
material was subsequently sent to Ferdinandsen and
Winge who diagnosed the parasite as a new species.
It has never since been collected, nor is anything
more known about its structure and development.
The species which Feldman ('36) found on peti-
oles of Halophila BaiUonis in CJuadeloupe, West
Indies, may possibly be identical or closely related to
P. Halophilae. Feldman merely noted its occurrence
witliout describing or identifying the parasite.
P. FICI-REPENTIS Andreuoci, 1926. Arch. But. 2: -26.
Resting spores spherical. 1.5.5 /x. with thin, hyaline
walls; producing pyriform uniflagellate (?) zoo-
spores in germination ; flagellum 2.7 jx in length.
Thin-walled evanescent zoosporangia unknown.
Amoebae and young plasmodia from zoospores varia-
ble in shape and size. 6 X 24 ju,, aggregating and
fusing into larger plasmodia. which later cleave into
irregular segments and finally into spores; some-
times encysting to form hyaline, globular, 9.15-73 /x
cysts with granular and sculptured thick walls : cysts
producing plasmodia in germination.
Parasitic on the large and small branches of Ficiis
repens in Italy, causing Avoody, brownish-gray,
globular, irregular and coral-like tumors up to 5 cm.
in diameter (fig. 102).
This species differs from 7'. Brassicae ])rimarily
bv its smaller resting spores and the fact tiiat it at-
tacks aerial organs rather than the roots of its host.
It has been recorded but once, and Andreucci unfor-
tunately did not illustrate it. However, Cook ('33)
examined dried galls, which were unsuitable for cyto-
logical study, and described tliis species as a doubt-
ful member of the genus.
l'l..\SMllllll)l'lll)Il.\
88
P. BICAUDATA l-Vldmiin, ISUd. Hull. So.-. Hist. Nut.
AfriiiiK- Noril M : ITH. Fip. 1. -'.
Kcstiiig spores ovoid ami sli<tl\tl_v .spiiullc-.sliapcd,
3-3..) fi \ 7 fi. tliin-wallod and brijilit yellow with
a firu- attenuated bristle at one or luitli ends; fjernii-
nation unknown. I'l.isniodia larjre. Hllinu; liost eell
eonipletely. Zoospor,iiii;ia. zoos])ores. and .unoebae
unknmvn.
I'arasitie on /.nxtrra nanii in Mauritania, Iri-neii
West Africa, causini; marked swellinu; and sliortcn-
ing of tlie internodes.
Feldman's study and diagnosis of /'. hicaudata
were made on material preserved in aleoliol sent by
Mur.it from Tanoudert. Mauretania. and many of
the developmental stages are thus unknown. Like
other members of Vlasmodophora, this s))eeie.s has
a marked etfeet on its host. Infected internodes may
be two to three times tlie diameter of healthy ones.
so that atfected stalks have a characteristic nionilioid
appearance whicli is even more striking and accentu-
ated than that of D. xcrightii parasitized by P. Di-
planthcrac. This hy])ertrophy appears to be due en-
tirely to eell enlargement, since division of infected
an(i adj.uent he.iltliy cells has not been observed.
The enl.irged cells of infected internodes are undif-
ferentiated and meristematic. so that the galls pro-
duced by the parasite are typically kataplasmic.
The parasite is confined to the cortical and epi-
dermal cells and does not infect the vascular bun-
dles. In infected stalks, however, the latter tissue
may be twice its normal diameter, due perhaps to
reduction in longitudinal growtli. Infected cortical
cells may be two to six times their usual size and
completely filled with the plasmodium or spores.
They apparently do not divide after infection.
although Feldman did not study the early develop-
mental stages of the disease. He nevertheless found
a few binucleate infected cells, which suggests that
mitosis is not completely inhibited. The jilasmodium
may envelop the host nucleus (fig. 10(i) which is
thereby stimulated to enlarge and becomes six to ten
times as large as those of liealthy cells. The nu-
cleole likewise enlarges, while the chromatic mate-
rial becomes more basophj-llic and also vacuolate.
The nucleus may persist until after the sjiores are
mature, and in greatly enlarged cells with rii)e spores
it may be 3.5 to iO n in diameter, enucleolate, and
looks like a partially empty vesicle containing a small
amount of chromatic debris.
bibliogk.mmiy: pl.asmodiopiior.\
.^ppel, (). 19JK. Handli. Pflanzenkr. 2. Herlln.
.and K. WVrth. 1910. Mitt. Kpl. Hiol. .\nst. I.aiul.-u.
Fnr>tw. 10: 17(i.
Hehla. K. 189K. Ontralhl. Hakt. Parasitk. 2i: HJ9.
. 1899. /..itschr. Hy;:. 3J: i:«.
. 1903. Die I'flan/.eiiparasltare L'rsadic des Krel)ses
und die Krebspriipliylaxe. Berlin.
Cliupp. C. 1917. Cornell I'nlv. .\gr. Kxp. .Sta. Bull. IWT.
Cook. W. K. I. 19i6. Trans. Brit. .Mycol. Soc. 11: 19(i.
. 19.>8a. Bull. Soc. .Mycol, France 44: 10,i.
. 19:;8b. .Ann. Bot. 4J: 347.
. 19;!3. .\reli. I'rotisdv. Ml: 179.
, und K. J. Schwartz. 19;{(). I'liil. I r.iiis. Uny. Scic.
Ser. B. .MS: -'H;1.
Courh, .1. N'., ,1. I.eitner. and .\. WliitTrn. l!i:i!i. .lour. Klislia
Miteliell Scl. Soc. .Vi: S99.
I'.rickssoii. ,1. 19IS. Die Pflanzcnkr. l.aiuhv. KiilturpM.iiize.
I.fii>zitr.
Esmurch, F. 19-'4. Die Kranke I'flanze 1: 169.
KycleshyiiHT, A. C. 191)1. .lour. Mycol. 7: 79.
Fiivorsky, \V. 1910. Mem. Soc. N'iif. Kieflf. M): 149.
Frdotott-a. T. 19:J0. I'liytiipatli. /eitsclir. I: 19.V
Fr<loriiitscliik, N. S. IH;U. Sinniii. Sci. \\k. Inst. I'l. I'lntcct.
l.riiiii;rrad 19;{."): lj9-7(>.
F.inlKTf:, I.. 190.'. Her. Deut. Bot. (Jes. 19:533.
Fildniann, .1, 19:i(). Bull. Bot. .Soc. France S3: Ons.
Caylord, 1904. /eitsclir. Krehsf. 1: 93.
Ciihbs, ,J. G. 1931. New Zealand .lour. .\)rr. 4.': I, 193.
Gleisberjr, W. 19:33. Nachrbl. Deut. I'tianzenscli'd. 4:10.
Corini. D. C. 1901. Centralbl. Bakt. Parasitk. abt. I. 39: .589.
Ilalsted, B. D. 1H93. New Jersey .Apr. Exp. Sta. Kept.
1893: 33 J.
Henckel. X. G. 19.'3. Bull. Inst. Hecli. Biol. P.rnie, fasc. 2.
Hoiiifr. F. 1931. CJartenbauwiss. 5; 11(>.
Houifrniann. 19:2(». Pflanzenbau. Halbnischr. f. Saatwesen
Anbau u, Pflege d. Kulturjiflanz. 2: 29U.
Home. A. S. 1911. Jour. H.iy. Hort. Soc. 37: 303.
. 1930. Ann. Bot. 44: 199.
Jones, P. M. 19-'Sa. Arch. Protistk. 62: 313.
. 19.'8b. Bot. tiaz. 81 : 441).
Jorstad, I. 19-'3. Norsk. Havetid. 39: 126.
Kunkel, L. O. 1918. Jour. Agr. Ke.s. 14: .543.
I.arsen, H. H. 1934. Ihirl. 49: (>07.
I.edinfrham. G. A. 1934. Nature 133: 534. 193.5. IhhI. 135:
3994.
. 1939. Canadian Jour. Res. C, 17: 38.
I.evine, I., and M. Lcvine. 19:2:?. .lour. Cancer Ros. 7: 163.
Ihl<l. 7: 171.
I.owenthal, W. 1905. /.eitsclir. Krobsf. 3: 41).
I.utman, B. F. 1913. Vermont .\gr. Exp. Sta. Bull. 175.
.Maire, R., and A. Tison. 1909. ,\nn. Mycol. 7: 226.
.MacLeod, D. J. 1931. Rept. of Dom. Bot. for 1930. Div.
Bot. Canad. Dept. Agr. 1931: 181.
.Milovidov, P. F. 1931. Arch. Protistk. 73: 1.
.Molliard, .M. 1909. Bull. Soe. Bot. France .>(>: .'3.
.Motte, M. H. 19.33. Jour. d'Afrr. Prat. 97: 177. 1935, IhM.
99: 93.
Naumov, N. A. 19.V.. .Morbi Plant. 14: 49.
Nawaschin, S. 1899. Flora 8(i: t04.
. 1901, Kiev, Zap. Obseb. Jest. 17: 3(J.
, 19;?4, C. R. .\cad. Sci. Russie 19J4: 173.
Pape, H. 193.5. Pflanzenbau -': 173.
Pinoy, E. 1903. Bull. .Soc. .Mycol. France IS: 388.
. 1903. C. R. Acad. Sci. Paris 137: 580.
. 1905. C. R. Soc. Biol. 58: 1010.
. 1907. Ann, Inst. Pasteur 31 : (iSfi.
Podwyssozki, W. 1900. Centr.ilbl. Bakt. Parasitk. abt. I,
37: 97.
. 1903. Zeitsebr. klin. .Med. 47: 199.
Pollacci, G. 1913. ,\tti Inst. Bot. Univ. Pavia. 3 ser. 15: 391.
Prowazek, S. 1905. .\rb. Kais. Gesund. 22: 39(i.
Rocblin, E. 1933. Pbytopatb. Zeitsebr. 5: 381.
.Smith. E. F. 1911. Bacteria in relation to pl.mt disease 3:
l(i9.
Sorauer, P. 1908. Ilandb. Pflanzrnkr. Berlin.
Terby, J. 1933. .Mem. Roy. .\ead. Belg. 7: 138.
. 1934a, Bull. Roy. Sr>c. Bot. Bel);i(|ue 5(i: 48.
. 1934b. Bull. Roy. Acad. Belp. 5 ser. 10: 519.
. 1933. .Mem. Roy. Acad. Belp. 1 1 : 1-30.
31
PLASMODIOPHORALES
Van Wissenlingh, C. 1898. Jalirb. Wiss. Bnt. 31: 619.
Vonwiller, P. 1918. Arcli. Protistk. 38: 279.
Vouk, V. 1913. Die Naturw. 1: 81.
Walker. J. C. 1939. Jour. Agr. Res. .59: 815.
Wellman, F. L. 1930. U. S. Dept. .\pr. Tech. Bull. 781.
Winge, O. 1913. Ark. Bot. 1-2, no. 9: 1.
EXCLUDED SPECIES
P. ALNI ( Wor.) Moeller, 1885. Ber. Deut. Bot. Ges. 3: 10:3.
Figs. 1-4. 1890. Ibid., 8: .'15.
In 1866 Woronin found an organism in galls on
the root.s of Alniis gliifinosa which he named Schin:ia
Alni and believed to be a hyphomycetou.s fungus.
Gravis discussed its identity in 1879. and in 188.5
Moeller placed it in Plasmod'wphora where it was
subsequently retained by Schroeter ('86, '97). Since
that time its identity and relationship have been tlie
subject of extended controversy. In 1886 Brunchorst
made an intensive study of the galls of Alnus spe-
cies and found no evidence of a plasmodium. Instead,
he found a mycelioid fungus with numerous sporan-
gia wliich he named Frankia .iiibtilis and believed to
be related to the Mucorales or Saprolegniales. This
led Moeller ('90) to restudy the causal organism,
after which he retracted his former view and con-
firmed Woronin's and Brunchorst's observations on
the presence of a mycelium in the host cells. Frank
confirmed these observations in 1891, but lie was un-
certain as to the nature of Frankia subtUis. While he
pointed out that it might well be a form of Lepio-
thrix, he was nonetheless inclined to the view that
it is a mycorrhizal fungus. In 1900, according to
Maire and Tison ('09, p. 242), Chodat studied the
organism in question and asserted that it is a species
of Plasmodiophora. Two years later, after an inten-
sive study of the tubercles on AIniis roots, Schibata
came to tlie conclusion that no hyphomvcetous fun-
gus was present and tliat tlie galls are caused by an
organism with bacterium-like filaments which even-
tually become bacteroid and deformed. In 1901
Bjorkenheim figured and described fungus hyphae
in the galls, but three years later Keissler reported
the organism again as Plasmodiophora Alni.
Finally, in 1909, Maire and Tison undertook a
cytological study of tlie tubercles and confirmed the
observations of Shibata. They found an abundance
of partially digested mycelial filaments, the ends of
which became vesicular and later segmented into a
large number of irregular chromatic bodies. Maire
and Tison changed the name of the organism to
FrankieUa Alni, but since that time Keissler and
I.ohwag ('37) have reported it again as Plasmodio-
phora Alni on Alnus species in China.
P. ELAEAGNI Schroeter, 1889. Cohn's Krypt. Fl. Schle-
siens 3: 134. 1897, Engler u. PrantI, Nat. Pflanzenf.
1:7.
Schroeter gave this name to an organism wliich
he believed to be the cause of galls on the roots of
Elacafintis angtistifolia. It seems that he was not
aware that Brunchorst ('86) had already found the
same organism on F. anr/nstifolia, F. argi-niea, F.
pitnc/ens, and Hippophae rhamnoides and named it
Frankia subtilis. Claire and Tison ('09) also ob-
served similar galls on the //. rhamnoides, and since
they found the causal organism to be of the same
tvpe as F. Alni, they renamed it FrankieUa Flacagni.
It has subsequently been reiJorted as Plasmodio-
phora Flaeac/?ii hy J aap ('07) and Sydow ('21) from
Switzerland and New Zealand.
P. VITIS Viala and Sauvageau, 189;2. C. R. Acad. Sci.
Paris 114: 1.558; Jour, de Bot. 6:355, pi. 13.
This species was described by Viala and Sauva-
geau as causing the "brunissure " disease of grape
leaves in Europe and the U. S. A. The disease had
previously been observed by several workers, and in
1891 Pastre gave an account of its external symp-
toms. It was subsequently reported in England
(Anony., '93; Cooke, '93; Massee, '93), Italy
(Briosi, '94; Briosi and Cavara, '94; Cuboni, '94;
Solla, '01), Germany (Moritz and Busse, '94; Beh-
rens, '99), Algeria (Debray, '94a, '94b). Holland
(Bos, '95), and France (Frilleiux, '95; Roze, '99).
Cooke believed that the clubbing of vine roots also
was due to this organism.
The presence or absence of a causal organism in
this disease as well as its identity and relationship
have been the subject of much debate. In 1894 De-
bray pointed out that the organism was more closely
related to Ceratium than to Plasmodiophora, and in
the following year he established a new genus, Pseu-
docommis, to include it. In 1895 Massee reported
that the plasniodia and amoebae figured by ^'iala and
Sauvageau were nothing but vacuolated tannin vesi-
cles and the reticulate primordial utricle of the host
cell. Behrens likewise questioned the presence of a
causal organism in this disease, but in the same j'ear
Roze reported that P. litis occurs widely and is
almost a universal parasite. Ducomet ('03, '07) con-
firmed Massee's view that "brunissure " is the result
of certain environmental and physiological condi-
tions. Maire and Tison (09) also reported that no
organism was present in the diseased tissues which
they examined, and they thus concluded that the so-
called plasniodia were products of cell degeneration.
P. CALIFORNICAE Viala and Sauvageau, 1893. C. R.
Acad. Sci. Paris 115:67-69.
Viala and Sauvageau believed this s])ecies to be
the cause of a vine disease in California, and it was
subsequently reported as such by Casali and Fer-
raris ('00) in Italy. Massee ('95) pointed out that
the disease is physiological and that the rejiorted
amoebae and plasniodia are nothing more than tan-
nin vesicles and reticulated host jirotoplasm. Ravaz
KXl I.rUKl) Sl'KHES
35
('()(>) also r»-|)ortf(l that /'. Calif iiruiae is not an or-
K.-iiiisin Init only (Icjicntratfd cliloroiiliyll. and in
IJ>0!l .Main- and Tison conliniud the (indinys of Imtli
of tlu'sc in\ (stiirators.
P. ORCHIDIS MasMO. l!>!)j. Ami. Bot. !): 170, IJl-U'i),
1>1. 1.").
L'ndir this nanu- Ma.ssec reported an organism
whieli lie believed to be tlie cause of spot diseases of
orehid leaves. Later in the same year after more in-
tensive stndy he retracted this view and sliowed that
what he had previously believed to be s))ores were
nothing more than tannin vesicles.
P. TOMATI .\l)l»y. IWI."). .lour. Hurt. M-A ser. 30:.%a.
.Vbliey st.ited in a letter to the .lourii;il of Horti-
culture tiiat this organism is probably the cause of a
disease of tomatoes, but as far as the present writer
is aware he never gave a description of the parasite.
Massee ('9.5, p. 427) believed that Abbey's disease
is not due to a ))arasitic organism but to certain rapid
changes in environmental conditions.
P. HUMULI Kirk. lS()(i. Utpt. Dept. Agric. New Zealand
11: 337.
On the roots of hops in New Zealand Kirk found
galls which were similar to those produced by P.
Brassicae on crueifcrs. and without seeing the causa-
tive agent, he assumed the disease to be caused by a
species of Plasmod'tophora to which he gave the name
P. huniuli. In 1922 Nicholls reported a disease of
hojis in Tasmania which showed the "take all " symp-
toms, and he assumed it to be caused by the same
organism without examining the tissues microscopi-
eally. Later, in his correspondence with Miss Mc-
Lennan ('31. p. 12) he stated that he had found a
mvxoniycete which he took to be P. humiili. In study-
ing the "take all" disease of hops more intensively
in Tasmania, McLennan concluded that it may be
caused by a virus. In some of the diseased plants,
however, she found a })lasniodial organism which
was later isolated and grown in pure culture and
turned out to be a proteomyxean species. Leptomyxa
reticulata var. hiimuli. .She also examined preserved
material of diseased hops labelled 1'. humiili which
belonged to the Department of .\griculture, Mel-
bourne, but found no evidence of a myxomycete. Miss
McLennan accordingly concluded that tiie tumors
described by Kirk were crown galls caused liy Pseii-
dnmonas tumrfacicns and that P. huniuli is no longer
valid.
P. VASCULARUM Matz, lO.'O. .Jour. Dcyit. Afrric. Porto
Kifo J: I.), fi(:s. 7-9.
Liiniifra rn»rulnrum M. T. Cook, Ifl.'B. Ihiil. 13: l!t. Pis.
3-6.
Soroiiphaera vimculiirum M. T. Cook. 1937. Ihiil. :31:S1.
Pis. 5-7.
This species was described by Mat/. ('20, '21,
'22) as causing the dry top rot of sugar cane, Sac-
fhanim officinal i, in Porto Hieo. and in lilSl it wa.s
re))orted on the s.ime liost in \'ene/,uel;i by Chardon
.ind Toro. .M . '1'. Cook triiusfcrred the org.-inisin to
the genus Lii/nicra because it does not cause hyper-
trophy of the host. Later ('32), W. R. I. Cook m.adc
an intensive study of the organism from material
sent by M. T. Cook and found that the disease was
caused by two protozoan ))arasitcs to which he gave
the names Amocbo.iporus t'asculariini .uid ./. Sac-
charinum. M. T. Cook later ('37) tr.insfcrrcd it to
the genus Snro.s'pliarra.
P. TABACl Jones, 19-'(>. I?ot. Gaz. xl: Uli, pis. 31-37. Kig.
1. -'.
/'. lulu, cum .Tones, Ifl.'fi. Pliytopatb. Ifi: fi7.
In tobacco. |)otato and tomato plants ati'ected with
mosaic-like symptoms and leaf roll, Jones found a
plasmodiaceous organism which he believed to be a
species of Plasmodiophora. Infected cells become
necrotic and adjacent ones hyperplastic, and all tis-
sues except bast fibers and xylem are invaded by
))lasmodia which pass from cell. .lones found only
Plasmodia in the host plants, but when these are
cultured in Knop's solution, they give rise to amoebae
and uniflagellate organisms, both of which may or
may not encyst. The amoebae which eontiiuie to de-
velop discharge ehromidia from the nucleus into the
cytoplasm, and these chromidial bodies soon aggre-
gate to form daughter nuclei, thereby making the
enlarged amoebae multinucleate. Such amoebae give
rise to motile uniflagellate isogametes which fuse
shortly, forming a uniflagellate zygote. The zygote
then divides into two zoospores which in turn form
amoebae.
The flagellate cells and amoebae which encyst pro-
duce amoebae on germination, and these fuse to form
the Plasmodium. According to .Tones, hundreds of
amoebae may flow together in this manner and make
a huge Plasmodium which creeps along ra})idly like
a giant amoeba ingesting food in its path. S])orogen-
esis in this species is unlike that of any known mem-
ber of the Plasmodioi)horaceae. As the ])lasmodium
moves along, oval and s|)lierieal sjiorcs are delimited
in rows and left behind. The nuclei of these spores
soon enlarge, discharge chromidi.i. and eventually
disappear, while the ehromidia in the cytoi)lasm ag-
gregate and form daughter nuclei. Walls develop
around these nuclei, and in this fashion 3 to 15
endogenous spores are formed. Plasmodiophiira ta-
haci has a very complex life history, according to
.Tones, but he was not certain as to the sequence of
stages. Since he also found cert.-iin flagellate and
amoeboid stages which could not be fitted into any
known life cycle, it is not ini])robable that he may
have had more than one organism at hand. Miss Mc-
Lennan ('31) believed that the plasmodial stage
may relate to a proteomvxean-like organism of the
Lcpfnmi/ja reticulata type. In IStSI Cook expressed
a similar opinion in st.iting that P. iahaci is prob-
ably a species of amoeba which had temporarily en-
tered the tobacco leaf, but in 1933 he suggested that
36
PLASMODIOPHORALES
the stages which Jones found in mosaic diseased
plants may relate to excitation and degeneration
products of the kind described by Kunkel, Goldstein,
Holmes. Sheffield, and others." At any rate P. tabaci
has but little in common with other known members
of genus, and the author agrees with Cook that
there is little if any justification at present for in-
cluding it in the Plasmodiophoraceae.
Since he was able to produce mosaic-like symp-
toms in plants by inoculation with cultures, .Tones
believed his organism relates to the cause of tobacco
mosaic. Later in the same year, however, he. Link,
and Taliaferro ('2G) found that the organism could
be cultivated from healthy as well as diseased plants.
Furthermore, upon inoculation, mosaic-like symp-
toms appeared only when the amoebae and Plas-
modia came from diseased plants. They accordingly
concluded that P. tabaci is not the cause of mosaic
but may be a carrier of the causative agent.
In 1937 .Tones retracted his previous views about
P. tabaci and redescribed it as the soil amoeba. Nae-
gleria gruberi, wliich he claimed is not an amoeba
proper but a stage in the life cycle of a myxomycete.
He excluded it from the Plasmodiophorales on the
grounds that: (1) several amoebae fuse and form a
large multinucleate plasmodium; (2) the nuclei di-
vide promitotically as in an amoeba; (3) the plasmo-
dium forms an aggregate of separate resting spores ;
and (i) it does not parasitize jilants. He furthermore
reported that N. gruberi may be an alternate host for
the mosaic producing organism in tobacco. .Tones'
above-cited reasons for excluding this organism from
Plasmodiophora are obviously no more critical than
those presented previously for including it in this
genus. The additional data which he has presented
do not clarify its taxonomic jiosition or relationsliip.
P. SOLANI Brehmer and Biirner, 1930. Arb. Biol. Reich-
sanst. f. Land-u. Forstwirtsch. 18: 1-S4, pi. 1, fifr. 1-32.
Brehmer and Earner gave this name to an oval.
4.3.5-.5..5 /i X 2.9 fi, amorphous, pale yellowish-green
organism with a distinct refringent sheath which
they found in older portions and parenchymatous tis-
sues of potato stems sliowing leaf roll, mosaic, and
other degenerative symptoms. The thallus divides
into as many as eight daughter cells, and tliese in
turn give rise to vesicles or spores which are subse-
quently liberated by the breakdown of the daughter
cells. The spores produce a filamentous zoospore, 5 jx
in length and a fraction of a micron in diameter.
Brehmer and Barner found all of these stages in fil-
tered juices of diseased plants as well as in plants to
which virus symptoms had been communicated by
grafting and concluded tlierefrom that P. Solaiii is
the cause of potato virus. These authors pointed out
the similarities of tlieir organism to .Tones' parasite
Calkinsi and the so-called "X" bodies of various in-
1 Kunkel, L. O. 1921. Hawaiian Sugar Planters' Assoc.
Bot. Ser. 3: 108.
Goldstein. B. 192T. Bull. Torrev Bot. Club 54: 285.
Holmes. F. O. 1938. Bot. Gaz. 86: 50.
Sheffield, F. M. I>. 1931. Ann. Appl. Biol. 18: 471.
vestigators and considered it to be either an inde-
pendent amoeboid entity capable of spore formation
or a Plasmodium living in symbiotic relationshi))
with the plastids. They regarded it as a member of a
hitherto unknown group of the Archimycetes allied
to the Plasmodiophoraceae. It has subsequently been
reported by Moesz ('38) on potatoes in Hungary.
There is little in the life cycle of this organism, as
described by Brehmer and Barner, which indicates
relationship to Plasmodiophora, and it is accordingly
excluded from the genus.
P. THEAE Fitzpatrick, 1930. The lower fungi-Phycomy-
cetes. New York.
See Sorosphaera Theae Speschnew.
bibliography: e.\cluded species
Anony. 1893. Card. Chron. 74: 217.
Behrens, .1. 1899. Weinb. u. Weinh. no. 33.
Bjiirkenheim, C. G. 1904. Zeitscli. Pflanzenkr. 14: 1 «l.
Bos. R. 1895. Zeitschr. Pflanzenkr. 5: 286.
Briosi, G. 1894. Boll. Notiz. Agr. 16: 5-22.
, and F. Cavara. 1894. Essiccati, delineati e descritti.
Fasc. X.
Brunchorst. 1886. Untersuch. Bot. Inst. Tiibingen 2: 151.
Casali. C, and T. Ferraris. 1900. Giorn. Vitic. Entolog. 8:
10.
Chardon, C. E., and R. A. Toro. 1934. Monogr. Univ. Porto
Rico, Phys. Biol. Sci. ser. B, no. 2: 75.
Cook, M. T. l'929a. Phytopatli. 19: 91.
. 1929b. Ann. Rept. Insular Exp. Sta. Dept. Agr.
Labor. Porto Rioo 1927/'28. 1929: 59.
Cook, W. R. I. 1931. Ann. Protist. 3: 197.
. 1932: Jour. Dept. Agr. Porto Rico 10: 407.
Cooke, M. C. 1893. Gard. Chron. 13: 711.
Cuboni, G. 1894. Boll. Notiz. .-Vgr. 16: 378.
Debray, F. 1894a. C. R. Acad. Sci. Paris 119: 110.
'. 1894b. Rev. Vitioult. nos. 35, 38.
. 1895. C. R. Acad. Sci. Paris 120: 943.
Ducomet, V. 1903. C. R. Assn. Franc, avanc. Sci. 32 sess.
Anglers 2nd pt. pp. 697-707.
. 1907. Ann. lecole d'Agric. Rennes 1: 1-284. 1908,
Ihkl 3: 1-70.
Frank, B. 1891. Ber. Dent. Bot. Ge.sell. 9: 244.
Gravis, A. 1879. Bull. Roy. Soc. Bot. Belgique 18: 50.
Jaap, O. 1907. Ann. Mycol. 5: 246.
Jones, P. M. 1928. Arch. Protistk. 62: 307.
. 1937. Amer. Nat. 71: 488.
Keissler, K. 1907. Ann. Mycol. 5: 220.
, and H. Lohwag. 1937. Fungi Symb. Sinicae 2: 2.
Link, G. K., P. M. Jones, and W. H. Taliaferro. 1926. Bot.
Gaz. 81: 403.
Maire, R., and A. Tison. 1909. Ann. Mycol. 7: 242.
Massee, G. 1893. Gard. Chron. 14: 282.
Matz, J. 1921. Esta. Exp. Insular Porto Rico 8: 63.
. 1922. Jour. Dept. Agr. Porto Rico 6: 28.
McLennan, E. I. 1931. Australian Jour. Exp. Biol. Med.
Sci. 8:9.
Moesz, G. 1938. Ann. Hist. Nat. Mus. Hungary 31: ,58.
Moritz, J., and W. Busse. 1894. Zeitschr. Pflanzenkr. 4: 257.
Nicholls, H. M. 1922. Ann. Rept. Govt. Microbiol. Dept.
Agr. Stock, Tasmania 1920-21 and 1921-22.
Prillieux, E. 1895. Maladie des Plantes Agric. 1: 47.
Ravaz. 1906. Rajip. Caise Rech. Paris 1906: 173.
TETU.\MV\A
Ho/.<-. M. K. IS!)!I. Hull. S(K-. Myoil. Fraiu-o lo: S7.
Shibiitii, K. im:. .Iiihrl). wiss. Hot. :{7: (i«.
S|ioschiu'w, N. N. 1!'07. nil- ril/.|iariisilcn <li"s 'rtcstrauclios.
K.'riin.
Sollii. 1901. /.cit.schr. I'rtiiiiz.-nkr. II: J.'.S.
Sydiiw, H. 19.H. .\mi. Mvcol. .'.': .'9:1.
Wiiroiiin. .M. I.S(i(;. Mnn. .\c.iil. Sci. St. IVtirsliiirL' T sir. 10,
no. (i: i:{.
TETRAMYXA
Gocbel, 1S«4', Floni G7 : 317
(l-L.^TK 5. FIG. 1-26)
Molllardia Main- and Tison. 1911. Ann. Mypol. 9: :.?3G.
Resting spores u.sii.illy in titrads hut often scpa-
ratinj; and lyinj; sinijly. or in iliads and triads ; vari-
ou.sly .sliapi'd. srivinj; rise to a sinu;li' nonflajiellate ( ?)
and anioelioid cell in aerniiiiation. Plasmodia usually
small, liocomini; |)arict.il in tlu- host cill at maturity
and clravinii into uninucleate spore-mother cells or
sporonts which usually divide twice to form tetrads
of resting spores. Zoosporangia and zoospores un-
known.
Tctrami/da is the second ))lasniodioj)horaceous
genus to he recognized as such, and although it has
heen known for many years, our knowledge of its
critical develo|)niental stages is meager. It includes
at present two species and possihly a third one, which
is so imperfectly known that its inclusion in Teira-
mi/xa is very problematical. While this genus ap-
pears to be comparatively rare in occurence, it is
widely distributed and has been reported frotn Fin-
land. Germany, (ireat Britain. France, Morocco.
Ja))an. and California. L . .S. A. Further studies may
show it to be world wide in distribution.
No zoosporangia or zoospores have been observed
in Tetramifxa, and the resting spores are reported to
give rise to amoeboid, nonflagellate cells. More care-
ful and intensive studies under optimum develop-
mental condition, however, may show that these cells
are biflagcllate and heterocont .ind that zoosporangia
also are developed.
T. PARASITICA Chh-1i<-1. I.e. PI. 10. Hissliifrer, 1888.
Meddel. .Sue. Fauna et Flora Fenn. 14: .53. PI. 1-10.
Maire and Tison, 1911. .\nn. .Mycol. 9: 2-2H. PI. 10.
ThfC'iphorn Riipplae Setchell, 193i. Mycologia Hi: H:i.
PI. 18. Fig. 3, i.
Resting spores spherical, 3. .5-7 /x. and angular.
with smooth hyaline walls, giving rise to nonflagel-
late (?) amoeboid cells upon germination. Plasmodia
usually several in a cell, small. 1.5— 30 /x. or almost
filling host cell.
Parasitic in the stalks of Uiipjna ro.stfllata, Zaniii-
clidlia poli/cnrpa, and /. paluxtrm in Finland and
(iermany ( Hissingir and Cioeliels. I.e.) ; Ruppia sp.
and Z. palii.stri.s in Cireat Britain (Boyd. '97;
Schwartz. 11: Haddon. '22) ; li. rostrllata in France
(Maire and Tison. '10, '1 1). Potamocfelon panormi-
tanus in Morocco (Maire. '17: Maire and Werner,
'37). and Ruppia maritima var. roxtrata in C'jilifor-
nia. U. S. A. (Setchell, I.e.). causing sni.ill or large,
ui» to 1.5 mm. in di.ini., greenish .-ind Later whitish —
brown g;ills on the st.ilks. peduneh-s. .ind lu.irgins of
the leaves.
The galls (fig. 1 ) are primarily due to increased
cell multi})lication. The infected and adjacent cells
do not increase much in size, but are stimulated by
the parasite to divide ra))idly. This is ))artieularly
true of the infected cells, and by such means the me-
ronts or ))orti()ns of the ])lasinodiuni are j>assively
distributed to the res|)ective d.iughter cells (fig. !•).
This ap|)ears to be the ))rimary me.-ms of dispersal of
the parasite within the host tissue, although Cook be-
lieved that the amoebae are capable of migrating
from cell to cell. The relation between host and
l)athogcn is very intimate, according to ISIaire and
Tison. and no antagonism is exhibited. The cyto-
plasm of both often ap|)e.irs to be confluent, and it is
frequently impossible to determine the boundaries
between them. Although the nuclei of the host cells
may be enveloped by the jdasmodium (fig. 2). they
do not become enlarged and deformed or divide ami-
totically as in Triglochin palustre parasitized by T.
Triglochinis. When young, the infected cells contain
a fairly large amount of starch, but this usually dis-
ajjpears after the sporulation of the Jiarasite. The
nucleus remains intact for some time later, but even-
tually degenerates.
Cook ('33) re])orted that this s])ecies had been col-
lected by Boyd and Haddon in Scotland and F'.ng-
land and that a diseased specimen of R. rosteUata in
the Father Reader Herbarium, University of Bristol,
had been collected as early as 1885 in Hampshire.
Maire and Tison (11) found T. parasitica in abun-
dance on R. rostellaia, which grew in close associa-
tion with Z. palu.siris var. pedicellata. The latter host
was not infected. Claire and Tison accordingly ex-
pressed doubt about Hissinger's report of the j)ara-
site's occurrence on L. polycarpa, because many au-
thors regard this species as only a form of Z. pa'its-
tris.
T. TRIGLOCHINIS .Molliard. 1909. l?iill. -Soc. Hot.
France .56: i4.
Mntli„ril!fi Trii/lorhinis (.\I,ill.) Main- and Tison. 1911.
.Ann. .Mycol. 9: J.W. Pi. 1.', fig. +7 ()3; PI. 13. fig. G5-()7.
Resting s])ores, zoos|)ores. and zoosjiorangia un-
known. Plasmodia small, usually numerous in a host
cell: undergoing niulti|)le division into several oval,
elongate, sickle-slia))ed uninucleate meronts which
grow in size, and during the two- to eight-nucleate
stage function in turn as schizonts. .\11 else unknown.
Parasite on the stems, flowering stalks, stamens,
ovaries, but rarely on the leaves of Triqlochin paliis-
fra and 7'. maiifiniim in France (Molliard. Maire
.iiul Tison. I.e. ) and 7'. maritiinim in Kngland (Cook.
'33). causing small fusiform, ov.al .-ind irregular
galls.
No resting spores have been observed in this s])e-
cies. so that its relationship to the other members
of the Plasmodiophoraceae is obscure. Because of
the lack of resting spores, Maire and Tison regarded
38
PLASMODIOPHOHALES
it as representative of a new genus, but as Cook
pointed out. there are no good reasons for introduc-
ing a new genus until more is known about the life
history of this species. It is accordingly retained
provisionally in Tetramyia. Maire and Tisons cyto-
logical study, nonetheless, indicates its similarity to
T. parasitica in the type of vegetative nuclear divi-
sion and the presence of centrosomes and astral rays.
The effects of this species on the host are striking.
According to Molliard. the parenchyma cells of the
stem and flowering stalk are greatly hypertrophied
and divide irregularly, while development of the
sclerenchyma is inhibited Likewise the flowers in an
infected region are sterilized. The infected cells may
enlarge to four times their normal diameter, while
their nuclei become enormous and deformed (fig.
20 j. The nucleoli also increase markedly in size and
become deeply basophyllic. At the same time nu-
merous deep-staining, chromosome-like chromatic
bodies develop in the nuclear cavity. Furthermore,
infected cells may often become multinucleate (fig.
19) as the result of amitosis. according to Maire and
Tison. The nuclei of adjacent cells may also become
enlarged and deformed. The presence of the parasite
further stimulates starch formation in the cells sur-
rounding infected regions.
T. ELAEAGNI Yendo and Takase. 1933. BulL Sericult
Silk — Ind. Japan 4, no. 3: 5.
Plasmodium inter- and intracellular, segmenting
into uninucleate spore mother cells which divide
twice to form tetrads of resting spores. Amoebae
formed from germinating resting spores. .Sporangia
and zoospores unknown.
In the roots of Elaeaf/nui multiflora in Japan.
This species causes tubercles or nodules which in
exceptional cases may attain the size of a man's fist
on old trees. The parasite occurs most abundantly in
the cortex and causes marked hypertrophy of the in-
fected cells as well as enlargement and distortion of
the nuclei. Yendo and Takase found that the percent-
age of nitrogen in the nodules was almost twice that
of the normal cortex, and for this reason they be-
lieved that there is a definite symbiotic relationship
between host and parasite.
So little is known about this species that its valid-
itv as a member of the Plasmodiophoraceae is very
doubtful. Yendo and Takase reported that the Plas-
modium spreads over the host cells and fills the in-
tercellular spaces. Furthermore, the resting spores
are said to be capable of forming fine, curled, non-
septate, branched germ tubes or filaments instead of
amoebae. The formation of germ tubes suggests that
Yendo and Takase may have had spores of another
fungus at hand.
ADDITIOXAL BIBLIOGRAPHY: TETEA.MVXA
Cook. W. R. I. \9%2. Honp Kong Nat. Suppl. no. 1: 38.
■ -. 1933. .\rch. Protistk. 80: :?16.
Maire, R., and \. Tison. 1910. C. R. .\cad. Sci. Paris 50:
1768.
.Schwartz. E. J. 1911. .\nn. Bot. 35: 79+.
Winge, O. 1913. .\rk. f. Bot. 13, no. 9: 36.
PLATE O
Tetramyxa para»itiea
Fig. 1. Galls on stems of Rvppia rottelhita. Goebel, I.e.;
Maire and Tison, '11.
Fig. 3. Multinucleate plasmodium surrounding host nu-
cleus. Maire and Tison, I.e.
Fig. 3. Plasmodium consisting of two multinucleate me-
ronts which appear to be fusing: nuclei dividing in one and
at rest in the other. Maire and Tison. I.e.
Fig. i. Division of infected cell by which the meronts
have been passively divided and distributed. Maire and
Tison, I.e.
Fig. 5. Equatorial ring stage of "promitosis'' in which
distinct chromosomes are evident. Maire and Tison, I.e.
Fig. 6. .\naphases of same. Maire and Tison, I.e.
Fig. 7. Plasmodium becoming parietal and cleaving into
uninucleate spore-mother cells or sporonts. Centrosomes
and astral rays present at poles of some nuclei. Maire and
Tison. I.e.
Fig. 8. 9. Prophases of meiosis in sporonts. Maire and
Tison, I.e.
Fig. 10. Equatorial plate stage of first meiotic division.
Maire and Tison, I.e.
Fig. 11. Binucleate sporont with conspicuous astral rays.
Maire and Tison, I.e.
Fig. 13. Equatorial plate stage of second meiotic divi-
sion. Maire and Tison, I.e.
Fig. 13. Cleavage into tetrads.
Fig. 14. Tetrad of resting spores.
Fig. 15. Enlarged host cell with resting spores isolated
and single, in linear series, in diads. triads and tetrads.
Large resting spores binucleate. Maire and Tison, I.e.
Fig. 16. Four resting spores in linear series. Goebel, I.e.
Tetramyxa Tri{/lochinit
Fig. 17. Galls on Triglochin palu»tre caused by T. Tri-
glochinh. Maire and Tison, I.e.
Fig. 18. Enlarged host cell with spherical multinucleate
and fusiform uninucleate meronts. Maire and Tison, I.e.
Fig. 19. Enlarged host cell with uninucleate meronts in
vacuoles. Host cell tetranucleate: nuclei with numerous
densely chromatic bodies. Maire and Tison. I.e.
Fig. 30. \n enlarged, deformed host nucleus. Maire and
Tison, Lc.
Fig. 31. Uninucleate fusiform meronts. Maire and Tison,
I.e.
Fig. 22-2i. Equatorial plate, anaphase and telophase
stages of "promitosis."
Fig. io, 36. Bi- and multinucleate thalli. Maire and
Tison, I.e.
Oetomyra Arhlyae
Fig. 37. Habit sketch of Achlya glomerata showing
effects of parasite on the hvphae. Couch, et al.. '39.
Fig. 38. Early infection stage showing large parasite nu-
cleus in host cell.
Fig. 29. Binucleate thallus surrounded by host proto-
plasm: nuclei dividing "promitotically."
Fig. 30. Large plasmodium in a vacuolate area of hyphal
tip.
Fig. 31. Sporangiosorus of nearly mature zoosporangia.
Fig. 33. Zoosporangia with emerging zoospores.
Fig. 33. 34. Biflagellate heteroeont zoospores.
Fig. 35. Zoospore killed in osmic acid fumes and stained
with gentian violet. Drawn from photomicrograph.
Fig. 36. Large tetraflagellate zoospore.
Fig. 37. Sorus of resting spores.
Fig. 38-40. Groups of resting spores.
TETRAMYXA
89
ri.ATK 5
Tetranivxa, Octomvxa
40
PLASMODIOPHORALES
OCTOMYXA
Couch, Leitner, and Whiffen, 1939. Jour. Eli.sha
Mitchell Sci. Soc. 55: 400. Whiffen, 1939.
Ibid. p. 243.
(PL.^TE .5, FIG. 27—10)
Re.sting spore.s usually adhering in groups of
eight, sometimes in groups of six to nine; forming
zoospores whicli infect the host and develo]) into
vegetative plasmodia. Such plasmodia cleaving into
sporangiosori composed of numerous small zoospo-
rangia, which are sometimes conjoined by narrow
isthmuses ; exit papillae lacking on some zoosporan-
gia. Zoospores anteriorly bifiagellate and hetero-
cont. Sporogenous plasmodia cleaving into small
segments which in turn divide into eight uninucleate
spores.
This monotypic genus is characterized by resting
spores wliich are grouped usually in clusters of eight
(fig. 38). As in other genera, the zoospores enter the
host hyphae directly and completely without leav-
ing a spore case on the outside. Infection may occur
at any place along the hyphae, but hypertrophy of
the host occurs only at or near the tip (fig. 27). The
young, naked parasite is surrounded by the host pro-
toplasm (fig. 28-29) and soon develops into a multi-
nucleate Plasmodium. As the latter develops, the
hyphal tip swells and attains its maximum size be-
fore the parasite is completely mature. As a result.
the Plasmodium lies in a vacuolate region (fig. 30)
of the swelling, surrounded by radiating strands of
host protoplasm along which small particles may be
seen moving toward the parasite. The latter thus
lives within and in intimate contact with the host
protoplasm, and in the early stages of development
the two protoplasts are indistinguishable. The plas-
modium usually develops from a single zoospore, but
Couch et al. believed several small plasmodia may
fuse to form a large one.
The mature plasmodium, however formed, may
give rise to sporangesori or cytosori, but the latter
do not usually appear until the cultures are several
days old. The zoosporangia (fig. 31) are delimited
as globose or ovoid masses which soon develop thin,
hyaline walls. Sometimes cleavage may be incom-
plete, so that several sporangia are joined by nar-
row isthmuses. As the sporangia mature, exit papil-
lae are formed on those adjacent to the host wall and
on some in the center of the group or sorus. As a re-
sult, the zoospores may be discharged (fig. 32) di-
rectly to the outside or within the host cell. They
emerge from the zoosporangia singly and slowly, and
after moving about sluggishly for a few seconds at
the mouth of the exit papillae swim away. The two
unequal flagella are attached at or near the anterior
end, and during motility the shorter one extends for-
ward while the longer i)rojects backward. Occa-
sional zoospores witli four flagella occur (fig. 36),
which ajjpear to be the result of incomplete or un-
equal cleavage instead of fusion.
The plasmodia which give rise to the resting
spores arc indistinguishable from the zoosporangial
Plasmodia until after cleavage begins. Miss Whiffen
('39) reported that the two are to be distinguisiied
cytologically by the fact that the nuclei of the rest-
ing spore plasmodia pass through the so-called akar-
yote stage and undergo reduction division. However,
she has not yet counted the chromosomes present
during the two meiotic divisions. The sporogenous
Plasmodia cleave into a number of comparatively
large masses, as in Tetrami/.ra, and these in turn
usually divide into eight uninucleate segments which
soon encyst in groups of two tetrads of resting
spores. This grouping, however, may frequently
vary from six to nine. Four normal-sized spores and
two larger ones may sometimes occur, while nine and
seven may be found in other groups. After a short
dormant period, the resting spores germinate, each
one giving rise to a single zoospore. The structure.
type of flagella, and method of swimming of these
zoospores are unknown.
O. ACHLYAE Couch, et al, I.e., PI. +7, 48.
Resting spores spherical, 2. 1—3.2 /x, with smooth,
slightly thickened walls. Zoosporangia spherical,
ovoid, sometimes flattened by mutual pressure, 6-16
IX in diameter, hyaline and thin-walled; single exit
jjapilla on sporangia adjacent to host wall and in the
center of gall; deeper lying sporangia often dis-
charging zoospores through the peripheral sporan-
gia. Zoosjjores 6-11 in a sporangium, discharged di-
rectly to the outside and also within the host wall ;
oval; flagella attaciied to or near the anterior end,
the shorter one extending forward and the larger one
backward during swimming.
Parasitic in Achli/a r/lomcrata in North Carolina,
U. S. A., causing marked enlargement of the hyphal
tips.
This species appears to be an obligate parasite of
A. glomeraia. Couch, et al., attempted to transfer it
to Saprolegnia feraj', S. mef/asperma, .J. imperfecta,
A. flageUata, A. colorata, A. racemosa, A. deBary-
ana, Aphaiiomyces stellatus, Apodachlya brachi/-
nema, A. minima, and AUomyces arbii.^ciila, but all
results were negative. So far, this is the only known
species of the Plasmodiophoraceae parasitic in a
fungus.
The life cycle of 0. Achli/ae seems to be almost
identical with that of JVoronina poli/cijstis as far as
both species are known at present, and it is not im-
probable that the two may prove to be related. Ac-
cording to Couch, et al., 0. Achylae differs from W.
polycy.<!ti.s by the fact that it usually causes spherical
swellings and does not lead to septation of the host
hy])hae. Furthermore, its cystosori are hyaline in-
stead of brown, and the resting spores are usually
grouped in clusters of eight rather than in spherical,
oval, elongate, and irregular masses. The first dif-
ference cited above is not very significant, since the
shape of the swellings is not a very fundamental di-
agnostic character. What seems more significant is
that the sporangia and resting spores of W. poly-
cy.iti.i- give a definite cellulose reaction, while those
of O. .ichiilae do not.
SOUOSIMIAKHA
41
SOROSPHAERA
Solirocter, .1. 1S()(>. Colm's Kivpt. Fl. von Sililo-
sicns .■{ : l."{.").
( E'l.ATK ()")
Cystosori one to several in .1 ii II. pri (louiiii.intly nt'
the slia|)0 of hollow sjiheres or ellipsoids, luit often
extremely variable in size anil shape; presenee of
oonimon eiiveloj)lng membrane doubtful. Resting
spores oval, ellii)soidal. j)vriforni, pyramidal and
urn-sliapeil with yellowish-brown to brown, thin,
smooth or \errueose walls; with or without .ipie.il
eollar; produeinj;: a siniilf bitlaiiellate, heteroeont
zoos])ore in gerniin.-ition. Kv;nieseent thin-w.illed
zoosporansjia sm.ill. I'l.isniodia one to several in a
eell. large or small: sehi/.otjony present ( ?) or lack-
injr; produeinji a sinj;le cystosorus.
This genus includes at present only two species
which have been reported in moist and damj) locali-
ties in Europe. England, and the U. S. A. Of these
two, iS. r eronicac appears to be more common and
has been frequently studied cytologically. Nonethe-
less, many of its critical develo])niental stages are
still im)>erfeetly known, and there has been consid-
erable controversy relative to many of its cytologieal
details. Germination of the resting spores had not
been observed until very recently. Blomficid and
.Scliwartz ('10) re|)orted the jjresence of amoebae in
a sterile infusion of 1 erunica leaves which had been
inoculated with i)ortions of dead tumors. Since this
infusion was thus no longer sterile and soon became
invaded with bacteria, molds and other organisms
from the tumors, the uninucleate amoebae which they
found after fourteen days in the bottom of the test
tube may not relate to S. J'eronicae at all. In S. radi-
cali.s. Cook and .Schwartz likewise failed to observe
germination, but among diseased root hairs they
found anteriorly uniflagellate zoospores which they
assumed relate to their s))eeies. However, they did
not follow the development of these zoosjiores into
mature thalli. On the other hand. Barrett foinid that
the zoospores from sporangia are distinctly bitlagel-
late and heteroeont. He also succeeded in germinat-
ing the resting spores, but has not yet determined
the number of flagella on such zoos))ores. I.edingham
('3S). p. 1-3) found that zoos|)ores from resting s))ores
of .S'. t'eronicae also are biflagellate and heteroeont.
Cook ('33) stated that the resting s))ores form a sin-
gle amoeba or zoospore, but it is quite probable that
the multinucleate spores rejiorted by Maire and
Tison (fig. 49-.5I) may give rise to several zoo-
spores.
-Vs the primary uninucleate amoebae of .S'. I'l-ro-
nica (tig. 9) increase in size within the host cell, their
nucleus divides, and multinucleate |)lasmodia are
soon formed (fig. 11-1.5, 22). Hy the time the eight-
nucleated stage has been reached, the plasmodia may
function as schizonts and split off uni- and multi-
nucleate meronts (fig. 23. 2 J), according to Maire
and Tison, The multinucleate meronts may in turn
undergo schizogony into uninucleate segments be-
fore further mitoses occur. The unimicleate meronts
are ciiuiv.ilent to the primary amocb.ii' and ni.iy thus
begin the eyi'le .mew. while the scliizont from which
they are derived ])asses into the s))orogonie jihase of
(levelojimcnt, in the opinion of .Maire and Tison.
It is to be noted, however, th.-it these workers have
ncxcr observed the actu.-il s))litting oft' of meronts,
.ind their re])orts on the presenee of schizogony are
based only on the .ipiiea ranee of constricted plas-
modia (fig. 2.i. 2 1-) .-md the grc.-it abuiulance of uni-
luiele.ite amoeb.ie in infected cells. The Latter may
well be the result of nuiltiple infection, while stages
such as are shown in figures 23 and 21' may possibly
rei)resent, as Maire and Tison earlier interpreted
them, fusions of uni- and bimicleatc amoebae with
nuiltinucleate |)lasniodia. \\'hile the author readily
admits the possibility of schizogony, he does not con-
sider the evidence so far ))reseiited as sufficiently re-
liable to have conclusively settled the jtroblem. In
this connection it is significant to note that schizog-
ony has not been recorded in species, such as S. radi-
cal'is, where the process if present could be readily
observed in living material.
Tl'.e vegetative phase is terminated by the so-
called transitional stage after which follow cleavage
and meiosis, as has been described in Chajiters \\
and III. The plastic cleavage segments or incipient
resting spores become associated in a globular mass
(fig. H) and resemble myxamoebae in a pseudoplas-
modium. By mutual readjustment they soon move to
the periphery (fig. II) and thus form a hollow
s])here or ellipsoid. At this early stage the center of
the mass is filled with a viscuous fluid, doubtless a
residue of the plasmodium which is not used up in
cleavage. Whether or not this substance rejiresents
extraneous waste material which is dumped into a
central vacuole in the dediiferentiation of the proto-
))lasm ])reparatory to sporogenesis as in various pro-
teomyxean species is not certain. Maire and Tison
stated that it has an osmotic coerticient and exerts
centrifugal pressure on the s))ores whereby they are
|)ushed to the periphery of the mass.
.Shortly after their arri\al there, the individual
s])orcs develop delicate walls wliic'h thicken and turn
brown with maturity and often become verrucose. No
evidence of cellulose or i)ectin M-as found in these
walls by Maire and Tison. By mutual compression
the spores usually become iientagon.-illy and hex-
agoiially |)yramidal in shaiie with convex external
and slightly concave intern.-il surfjices. According to
^\'inge. a eollar is formed .at the ;i))ex or external
surface (fig. 18), but this structure has not been re-
corded by other workers. Occasional bi- and trinu-
cleate spores occur (fig, ■19-.51). which may have
arisen by incomplete cleavage or by subsequent di-
vision of the spore nucleus (fig. .50).
It is to be partieul.irly noted that in none of the
figures and descriptions of Blomficid and .Schwartz
or Maire and Tison which illustrate the aggregation
of incipient resting spores and their transformation
into cystosori is there evidence of a distinct, common
eiivelo))ing membrane around the sorus. Likewise, it
42
PLASMODIOPHORALES
is lacking in Rostrup's, Winge's, and Palm and
Burk's figures of cystosori. Cook's ("33, PI. 6, fig. 9)
own photographs of S. J'eronicae fail to show a dis-
tinct membrane. Nonetheless, he has often contended
that it is present and has used ('33) the presence of
this structure as one of the distinguishing generic
characters of Sorosphaera as well as Sorodisciis. In
the original diagnosis of the genus. Schroeter de-
scribed the cystosori as being surrounded by a com-
mon cuticle, and this may be partly responsible for
Nemec's ('H) and Cook's contention as to the pres-
ence of a membrane. Webb described it as being
formed after the spores had developed their individ-
ual walls, but he gave no figures of its development.
Winge ('13, p. 30) denied its existence, while Blom-
field and Schwartz as well as Maire and Tison, who
have so far made the most extensive study of the
genus, said nothing about it. It is quite probable
that the adjacent lateral walls of the spores become
more or less fused by mutual pressure as they de-
velop, and this prevents the spores from separating
readily at maturity. The best cytological data in the
literature to date do not, therefore, support Cook's
view on the presence of a membrane, and the use of
this structure as a diagnostic generic character is at
present open to serious question.
The cvstosori of S. J'eronicae are predominantly
hollow spheres and ellipsoids, but numerous varia-
tions in shape have been noted by Maire and Tison,
Trotter, Webb, and others. Palm and Burk in par-
ticular found them to be unusually variable in galls
on r. americana collected in Colorado, U. S. A. In
this material they found the cystosori to be three
principal shapes: hollow spheres, flattened ellip-
soids, and irregular sponge-like masses, and between
these types all degrees of variations and intergrada-
tions were observed. As is shown in figures .52 to 57,
the Sorosphaera- or hollow-sphere type predomi-
nated, but two-layered flattened discs as in Soro-
disciis (fig. 53, 54), spongy masses with narrow or
wide channels as in Spongospora (fig. 55, 56), and
irregular masses of indeterminate shape as in Lig-
niera (fig. 57) were not uncommon. Likewise within
the same sorus, spores with smooth and verrucose
walls were present (fig. 53, 55, 57). Palm and Burk
accordingly concluded that the shape of the cysto-
sorus and the relative arrangement of the spores are
governed largely by environmental conditions and
that the size and shape of the host cell are determin-
ing factors. They furthermore concluded that since
sori typical of those of Spotu/ospora, Sorodisciis,
Ligniera, Osienfeldiella, Claihrosoriis, and Mem-
hranosoriis may all be found in S. J'eronicae, these
genera should be regarded as synonyms of Soro-
sphaera. Fitzpatriek ('30) believed that Ligniera
also should be incorporated in Sorospftaera on the
grounds that the only difference between the two is
that the former causes no hypertrophy of the host.
In 1907 Speschnew (p. 22, PI. 2, fig. 7-12) de-
scribed a species on tea leaves in the Caucasus which
he named Sorospliaera tlieae. Two years later, how-
ever, Ducommet ('09) reported that no organism is
present in the leaves and that the so-called spores
are only tannin deposits in the cells. Fitzpatriek re-
ferred to this species as PlasmodiopJiora Theae.
S. VERONICAE Schroeter, I.e.
Tiihirciiiia f'erouicae Schroeter. 1877. Beitr. Biol. Pflanz.
;? : 383.
Sorusporiiim Veronicae Winter. 188-t. Die Pilze Deutsch-
lands, Oesterreich und der Schweiz 1 : 103.
Cystosori bright brown, one to several in a cell,
variable in size and siiape, predominantly in the
form of hollow spheres, ]8-42(a, occasionally elon-
gate, flat and disc-shaped, irregular and indeter-
minate, compact or loose and spongy with numerous
ramifying channels, composed of from four to 61
spores. Resting spores ovoid, pyramidal, urn-shaped
1-5 IX X 8-9 fx., with brown, smooth or verrucose
outer walls, often surmounted by an apical collar.
Zoospores biflagellate and heteroeont. Plasmodia one
to several in a cell, 20-30 /i, schizogony doubtful;
producing a single cystosorus. Zoosporangia un-
known.
Parasitic in J'eronica hederaefolia, J', cliamae-
drifs, and /'. triphifUos in Germany (Schroeter, '77,
'86, '97 ; Winter, I.e. ; Diedieke, '11; Grevillius, '13) ;
/'. saj-atilis, J', officinalis, J', hederaefolia, J', scii-
tellata, J'. Beccahiinga, J'. Anagallis, J', aqiiatica,
J'. serpi/Uifolia, and /'. Chaemaedri/s in Finland,
Norway and Sweden (Lagerheim: see Winge, '13;
Palm, '08) ; J\ hederaefolio in Sehleswig-Holstein
and Denmark (Hennings, '91 ; Rostrup, '94) ; T.
Chamaedri^s in France (Maire and Tison, '08, '09,
'10, '11; Maire, '10); /'. Chamaedrys in England
(Blomfield and Schwartz, '10; Cook and Schwartz,
'29) ; r. arvensis and J', hederaefolia in Italy (Trot-
ter, '04, '16); r. americana and J', arvensis in the
U. S. A. (Palm and Burk, '33; Donald, '34), caus-
ing tumors up to 5 mm. in diameter on the stems,
petioles, and midrib of leaves.
This species was first described by Schroeter in
1877 as a member of the Ustilaginales under the
name Tuhercinia J'eronicae, and in 1884 ^^'inter
transferred it to the genus Sorosporium. In 1886,
however, Schroeter created the genus Sorosphaera
for it and transferred it to his newly established
Phytomyxinae. Rostrup found it in Denmark in
1894 and replaced it in the Ustilaginales, and ac-
cording to Winge, Lagerheim found it in Norway
and Sweden on a large number of J'eronica species,
and as early as 1901, "and knew the correct system-
atic position of Sorosphaera." Trotter discovered it
in Italy in 1904, and while he questioned its inclusion
among the smuts, he also doubted that it is a mem-
ber of the Mycetozoa. The subsequent studies of
Maire and Tison and Blomfield and Schwartz clearly
showed that it belongs in the Plasmodiophoraeeae in
close relation to P. Brassicae.
The tumors caused by S. J'eronicae vary from pin-
head size to 5 cm. in diameter and are usually com-
])osed of a mass of healthy and infected undifferen-
tiated cells among which are intersjiersed a few spi-
ral and annular vessels. The galls are the result of
SOUOSPIIAKRA
13
both cell limit ipliiaf ion and itll cnlarmciiicnt witli
tin- lattiT proi-css playiiiii tlif (loniinaiit role in tin-
lati-r stages of divclol)nunt. Since the (larasite has
a ])redilcetion for the provascular strands in tlic
aj)ieal nieristem. the tumors may involve the entire
stem in instances of severe infection. In such eases
the priuiordia of the stems and leaves are reduced
to a mass of cells in which |)ith. cortex, etc., are indis-
tingiiish.-ihle. In less extensive infections only small
portions of the stem hceome involved, and the normal
growth of the plant is not seriously artectcd. .\ccord-
ing to Lagerheim. the development of the vascular
ring is suppressed in the region of infection, while
in the outer cortex the collenchyma is still present.
The rem.iining cortical cells become tangentially
oriented in growth and greatly enlarged. The ejiider-
mal cells become isodiametric. and the gu.ird cells of
the stomata are often considerably enlarged, with
the pore itself abnormally wide.
.\lthough infection has not been observed. S. J'e-
ron'icae appears to make its initial entrance in the
apical meristem. because the youngest plasmodia and
smallest galls occur in or near the apex. Blomtield
and .Schwartz succeeded in jiroducing tumors on Ve-
ronica seedlings by si)raying them with water con-
taining crushed cystosori and found single, isolated
infected cells close to the growing point. The amoe-
bae of the parasite are apparently unable to pass
through the walls into adjacent cells. According to
Blomtield and .Schwartz, and Cook ("33). they are
passively distributed by the repeated division of in-
fected provascular cells. If the young plasmodia un-
dergo schizogony, as Maire and Tison reported, the
number of amoebae is greatly increased, and by re-
peated division of infected cells, large diseased areas
are soon formed. In the early stages of the disease the
presence of the [larasite apparently does not inhibit
cytokinesis of the host cells, but later on after they
have become enlarged the latter lose the ability to di-
vide. The enormously enlarged nuclei, however, un-
dergo several mitoses with the result that the infected
cells become multinucleate (fig. 3). Division of the
host nuclei is greatest at the close of the vegetative
stage of the parasite, but with the onset of the sporo-
gonie ])hase mitosis ceases. At this stage the host nu-
clei become distorted (fig. .5), more densely stainable,
(fig. i). and eventually disintegrate (fig. Vt). By the
time the cystosori are mature, only atroi)hied and de-
generated nuclei are to be found, according to Bloni-
field and Schwartz. On the otlier hand. .Maire and
Tison rei)orted that the nuclei as well as ))]astids and
starch grains may jM-rsist long after the sori have ma-
tured.
In the early stages of infection only slight en-
largement of the host cells occurs, but as the plas-
modia increase in size, marked expansion takes place.
In exceptional eases infected cells may enlarge to 20
times their normal diameter. Sorosphaera J'eronicae
accordingly not only causes enormous cell enlarge-
ment but also prevents cell diflferentiation. .\djacent
healthy cells as well as stomatal guard cells may also
be stinuilated to enlarge by the presence of the para-
site. .\s is shown in figure 2. there ,ai)))ears to be no
visible .■intagonisni between tlie proto])l;ism of the
host and pathogen. The I.itter lies embedded in the
host eytoiilasm and in the young stages may be
closely associated with the host nucleus. Infected
cells may contain numerous jilastids and starch
grains, but these are not so abundant as in the adja-
cent healthy cells. According to I.agerheim. ei)idcr-
mal cells in the infected regions .ire richer in crystals
th.in tiiose in healthy j)ortions of the stem.
Slugs frequently feed on the galls, and it is be-
lie\ed th.it they play a signifie.int role in spreading
the disease. Most tumors soon soften and decay, lib-
erating the cystosori into the soil, where the resting
sjiores germinate. When new plants push up through
the soil, their ajjices a])l)arently become infected.
Sorosphaera J'eronicae has never been found jiara-
sitizing the roots.
Nematodes also may cause galls on Veronica which
arc strikingly like those ))roduced by .V. J'eronicae
and may easily be mistaken for them. I''or this rea-
son Cook ('33) regarded with susijieion the rejjorts
of I.agerheim and Winge of the presence of the para-
site in a large number of J'eronicae species in Nor-
way and Sweden.
S. RADICALIS Cook. 1933. .\reh. Protistk. 80: .'01. PI. T,
fig. 10, 11.
S. nuliriile Cook and Sclnvart/.. lfl-'9. .\iiii. Hot. 43: 86.
PI. 2.
Cystosori single and Jiartly filling host cell, hol-
low, rarely spherical, 20 yu,, usually oval, ellipsoidal
.and elongate, 1(5-20 fj. X 20-.57 /u,, bright yellowish-
brown ; including up to 500 spores. Resting spores
oval, 3 X ^ /i. with thin yellowish-brown, smooth
walls ; producing one zoos])ore in germination. Zoo-
spores oval and sl)lierical, 2-3 /x. with an anterior
flagellum (.'') l—ti/x long. Evanescent zoosjjorangia
unknown. Plasmodia single and partly filling host
cell. 20-60 /J. ill diameter, producing one cystosorus ;
schizogony lacking (.').
Parasitic in the root hairs only of Poa fluiians
MoniVia caerulea, Catabrosa aquaiica, and other
grasses in England, causing localized enlargement
of the infected cells.
This species is distinguishable from .S'. J'eronicae
jirimarilv by its oval, ellipsoidal and elongate cysto-
sori which are also much larger ;iiid com])Osed of a
greater number of small resting sjiores. In .addition,
its nuclei are considerably smaller. While .V. radicalis
may occur in the same vicinity with and infect some
of the hosts of Lifjniera J unci as well as L. verrucosa
and L. piloriim. Cook and Schwartz maintained that
it is ()uite distinct. However, it is to be noted here
that these Lifjniera s|)ecies may also occur in locallv
' In recent correspondence with the aiitliiir. Prof. .J. T.
Barrett, College of .Agriciiltnre, Califdrnifi rniversity, re-
ported that he had fonnil what lie helieves to he S. ridlirnlis
in roots of I'oa annua on the eoUejie rani]>iis. In addition to
cystosori and resting spores, he ohserved thin-walled spo-
ranjria which produce hifhifrellate, hettrocont zcM)spores.
Harrett thus confirms I.edingham's previous n-)iort of sudi
/,oo,..pores in Sftro.splifiern.
44
PLASMODIOPHORALES
swollen root hairs and occasionally form almost
spherical, oval and elongate hollow cystosori.
Sorosphaera radicalis lias been found only in root
hairs and does not attack the other tissues of the root.
Hence no external symptoms of the disease are visi-
ble on the host plant except a slight reddening of the
stem and leaf bases. When the infected root hairs
decay, the cystosori are liberated into the soil. In-
fection by zoospores api)arently occurs during the
early developmental stages of the root hairs.
.Although Cook and Schwartz failed to count the
chromosomes, they nonetheless believed that meiosis
occurs during the first of the two last divisions pre-
ceding sporogenesis. No evidence of gametic fusion
has been observed.
Cook and Schwartz reported that at the conclusion
of promitosis "a wall is now secreted around the
Plasmodium, and the whole mass passes into a spor-
ing stage." If this statement and observation are
true, it is obvious that .S'. radicalis differs radically
in this respect from all other known species of the
Plasmodiophorales.
PLATE 6
Sorosphaera Veroiiicae
Fig. 1. Vcroiiira chamaedrys with galls caused by S.
t'eronicae. Winge, '13.
Fig. -2. Hypertrophied host cell with six plasmodia. Note
relative sizes of healtliy and infected cells. Blomfield and
Schwartz, '10.
Fig. 3. Hypertrophied ho.st cell with five plasmodia. Four
host nuclei in telophases of division. Blomfield and
Schwartz, I.e.
Fig. i. Nucleus of parasitized cell witli numerous nu-
cleoli. Blomfield and Schwartz, I.e.
Fig. 5. Lobed and distorted nucleus of an infected cell.
Maire and Tison, "09.
Fig. 6. Old host cell with four cystosori; protoplasm
almost completely gone. Blomfield and Schwartz, I.e.
S. rfi(UcaUs
Fig. 7. Hypertrophied root hair with cystosorus in sur-
face view. Cook and Schwartz, '29.
Fig. 8. Median longitudinal section of an ellipsoidal
cystosorus. Cook and Schwartz, I.e.
S. f'erontcae
Fig. 9. Uninucleate stage of thallus. Maire and Tison, I.e.
Fig. 10. Resting nucleus of young parasite. Blomfield
and Schwartz, I.e.
Fig. 11. Beginning of promitosis of a 4-nucleate Plas-
modium with centro.somes and astral rays. Maire and
Tison, i.e.
Fig. 12. "Saturn stage"' of promitosis. Maire and Tison,
I.e.
Fig. 13. Early anaphases. Maire and Tison, I.e.
Fig. 14. "Double-anchor" stage of promitosis. Maire and
Tison, I.e.
Fig. 1.5. I.ate anaphases with centrosomes and asters.
Maire and Tison, I.e.
Fig. Hi. I.ate prophase of vegetative nuclei in Plasmo-
dium with four chromosomes. Webb, '3.5.
Fig. 17. Later stage sliowing four split chromosomes.
Webb, I.e.
Fig. 18. Four chromosomes arranged in a ring around
constricting nucleole. Webl), I.e.
Fig. 19. Metajjhase; daughter chromosomes beginning to
separate. Webb, I.e.
Fig. 20. Early anaphase. Two rings of four chromosomes
each moving apart. Webl), I.e.
Fig. 21. Later ana])liase. Webb, I.e.
Fig. 22. Telophases of jiromitosis. Maire and Tison, I.e.
Fig. 23, 2i. Schizogony of jilasmodium ; uni- and binucle-
ate segments respectively being split off. Maire and Tison,
I.e.
Fig. 25. Beginning of akaryote stage; chromatin passing
out into cytoplasm. Blomfield and Schwartz, I.e.
Fig. 26. Akaryote stage; nuclei clear and vacuole-like.
Blomfield and Schwartz, I.e.
Fig. 27. Reconstructed nuclei following akaryote stage.
Blomfield and Schwartz, I.e.
Fig. 28. Later stage showing reappearance of nucleoli
and chromatin. Maire and Tison, I.e.
Fig. 29. So-called "garland" stage of reconstructed nu-
clei. Maire and Tison, I.e.
Fig. 30. Same stage highly magnified. Winge, I.e.
Fig. 31,32. Synezesis (?). Maire and Tison, I.e.
Fig. 33. Beginning of cleavage into spore mother cells;
appearance of nuclei suggestive of diakinesis. Maire and
Tison, I.e.
Fig. 34. Early diakinesis. Webb, I.e.
Fig. 35. Diakinesis with four pairs of homologous chro-
mosomes. Webb, I.e.
Fig. 36. Equatorial plate stage of heterotypic division
during sporogenesis. Cleavage into spore mother cell com-
plete. Maire and Tison, I.e.
Fig. 37. Same stage. Winge, I.e.
Fig. 38. Late anaphases of meiotic division; first division
of spore mother cells beginning. Maire and Tison, I.e.
Fig. 39. First division of spore mother cells complete.
.Maire and Tison, I.e.
Fig. 40. Late prophase nucleus of second or homeotypic
division with four chromosomes. Webb, I.e.
Fig. 41. Equatorial plate stage of second division during
sporogenesis. Maire and Tison, I.e.
Fig. 42. Second cell division into incipient resting spores.
Fig. 43. Incipient resting spores aggregating into a
globular mass; initial stage in formation of cystosorus.
Maire and Tison, I.e.
Fig. 44. Later stage in cystosorus development; spores
arranged at periphery with a viscous substance in the cen-
ter. Maire and Tison, I.e.
Fig. 45. Young cystosorus in median section with well-
defined walls around spores; remants of viscous substance
in center. Maire and Tison, I.e.
Fig. 46. Cystosorus in median section. Blomfield and
.Scbwartz, I.e.
Fig. 47. Portion of a cystosorus in surface view. Blom-
field and Schwartz, I.e.
Fig. 48. Urn-shaped resting s])ore witb apical collar.
Winge, I.e.
Fig. 49. Binucleate resting spore. Maire and Tison, I.e.
Fig. 50. Division of nuclei in binucleate resting spore.
.Maire and Tison, I.e.
Fig. 51. Trinucleate resting spore. Maire and Tison, I.e.
sonosiMiAKiiA
45
PLATE 6
V^^
® ^
AM i I ^ XW i7 4,W
■■■■ » ^11^''' ^* ■ ^ti^' '^;y
• -i- ,25 26
33
40
--A^'i
C2
#«%
%.#
41
46
- 43
48 49"
Sorosplidcra
m--.
.^^.^'
32
pa
44
50
39
46
PLASMODIOPHORALES
PLATE 6— Continued
Sorosphaera Veronicae
Fig. 52-57. Variations of the cvstosori of iS. Veronicae.
Palm and Burk, "33.
Fig. 53. Typical hollow Sorfinphaera-tike cvstosori with
smooth and verrucosa spores.
Fig. 54. Flattened Sorodhcus-lihe cystosorus.
Fig. 55. Spongy Span gospora-Whe cystosorus.
Fig. 56. Loose, spongy Clathrnsonix-hke cystosorus.
Fig. 57. Irregular LU/nierri- and globular Sorosphaera-
like cvstosori.
Smith, A. L., and J. Ramsbottom. 1917. Trans. Brit. Mycol.
Soc. ti: 231.
Spescbnew, X. X. 1907. Die Pilzparasiten des Teestrauches,
p. -22. Berlin.
Trotter, A. 1904. Ann. Mycol. 2: 536.
. 1916. Marcellia 15: 58.
Webb, P. C. R. 1935. Ann. Bot. 49: 41.
Winge, O. 1913. Ark. f. Bot. 12, no. 9: 4.
ADDITIONAL BIBLIOGRAPHY: SOROSPHAERA
Blomficld, J. E., and E. J. Schwartz. 1910. Ann. Bot. 24: 35.
Diedicke, H. 1911. Mitt. Thiir. bot. Ver. n. f. 28: 83.
Donald, L. 1934. Phytopath. 24: 843.
Ducomet, V. 1909. Ann. I'eeole X'at. d'Agric. Rennes 2: 1.
Grevillius, A. Y. 1913. Abh. Ver. Nat. Erfors. Niederrheins
1: 165.
Henning, P. 1891. Schrift. Xat. Ver. Schleswig-Holstein 9:
235.
Ledingham, G. A. 1939. Canadian Jour. Res. C 17: 43.
Maire, R. 1909. Ann. Mycol. 7: 226.
. 1910. Bull. Soc. Linn. Xormandie 6 ser. 2: 57.
. 1911. Ann. Mycol. 9: 226.
, and A. Tison.1908. C. R. Acad. Sci. Paris 147: 1410.
Palm, B. T. 1908. Svensk. Bot. Tids. 2: 48.
, and M. Burk. 1933. Arch. Protistk. 79: 263.
Rostrup, E. 1894. Bot. Tidsskr. 19: 201.
Schwartz, E. J. 1914. Ann. Bot. 28: 229.
SORODISCUS
Lagerheini and Winge, 1913. Ark. f. Bot. 12: 23
(plates 7, 8)
Cvstosori usually flat, oval, disc-shaped and com-
posed of two layers of spores pressed closely to-
gether ; often variable in size and shape, rarely hol-
low spheres, occasionally an elongate and irregular
linear series of spores or reduced to tetrads, triads,
diads and rarely monads ; soral membrane doubtful
or lacking. Resting sjiores polygonal, angular and
urn-shaped or oval and almost hemispherical with
hyaline smooth or spiny outer walls ; apical collar
and cap present or lacking; remaining attached to-
gether or separating at maturity; producing one or
SOHOIIISI IS
n
possibly nioro tli;iii oiio zoospore in ■;crinin;iti<in. Zoo-
sporangia unknown. I'lasnuuiia ono to several in a
coll. large or small; sehizogony laekinji or doubtful
in some species.
Siinnliscim inehuies at present three or jiossibly
four species (see MrinhraiiosDriix in this eoniieetiou )
which h;ivc been reporteil from Russia. Norway.
Sweden, .South Africa and the United States. They
occur under fairly moist and aqu.atic coiuiitions. (i.-ir-
asitize algae and hiiilier i)lants. and cause marked
hypertrophy of the host in the form of galls or
tumors which may be uni- or nuilticellular. Since
most of these species have been studied only from
fixed and st.-iined material many of the critical
dcvclopnuiit.il stages are (loorly known, and the va-
rious claims concerning the ])rcsence of sexviality.
karyogamy. meiosis. alternation of haploid aiul dip-
loid generations, etc.. arc obviously based on inade-
quate cytological data.
Furthermore, the outstanding character of the
genus, namely, oval and almost circular, flat and disc-
sha)>ed cystosori composed of two closely jiressed
layers of resting s])ores. has been seriously ques-
tioned. In the type species, iS'. Callitrichis, the cysto-
sori m;iy sometimes be hollow spheres, while in S.
karliiifiii they may vary from hemisi)herical multi-
nucleate monads, diads. triads, tetrad, flat discs, and
elongate linear series of spores to almost hollow
spheres (PI. 8, fig. 11-21). In all of the s])ecies.
however, the majority of cystosori are flattened and
disc-like. M'hile A\'inge ('13) regarded Sorodixciis as
a distinct genus he nonetheless pointed out that its
similarity to Soros phaera is so great "tiiat it would
seem most reasonable to unite them into one genus."
Later, however, in a communication to Cook ('31.
p, 318) he said "that the spore masses are so char-
acteristic in Snrodi.scu.1 that it would be wrong to put
it in the s;ime genus as Soro.iphai'ra." Palm and
Burk (33). on the other hand, regarded Sorodisciis
as a syiu)nyni of the latter genus.
Schizogonv has not been observed in Sorodi-icus,
although Winge believed that the widespread distri-
bution of amoebae in the galls formed by -S'. Calli-
trichis suggests its occurrence. Whether or not a
common enveloping membrane is jircsent around the
cystosori in all species is uncertain at i)resent. Fur-
thermori-, little is known about the origin and devel-
o|)mcnt of this membrane in the s]>eeies in which it
has been reported to occur. In S. Callitrichis, accord-
ing to Winge. the resting "spore-wall divides into
two layers of which the outer one merges into that
of the neighboring spores (fig. 31. 32) so that it
gives one the inij)rcssion of the spores being de-
posited in a common substance." According to this
statement no distinct and separate wall is formed,
and tlie s))ores are merely adherent by the outer
layer of their walls. Figure 33, however, shows an
enveloping membrane. Cook considered Winge's in-
terpretation incorrect and stated that in S. radici-
colus a distinct wall is laid down around the cysto-
sori. He did not. however, present any evidence
about its origin — whether it consists of the original
liouuding mcmbr.inc of the plasmodium ])riscut at
the time of clcav.-igc or is dc])ositcd subsecpiently by
the m.ituring resting sjjorcs. Furthermore, his fig-
ures 23 and 21 of mature spore cakes do not show a
separate common w.all .-iround the sjjores. In S. kar-
lliif/ii no evidence of an enveloping membrane has
vet been observed (fig. 11-21). 'I"hc )iresence of
such a membrane in the genus as a whole is thus still
open to serious question, and if ))rcscnt its origin and
method of development arc certainly in need of in-
tensive cytological study.
^^'inge and Cook differed also in their observations
relative to sporogenesis and the stage at which meio-
sis occurs. In -S'. Callitrichis numerous binucleate
segments or s|)ore mother cells are formed by ])ro-
gressive cleavage of the plasmodium (fig. 27). and
these segments (fig. 28 and 29) then divide once to
form groups of s|)ores in twos (fig. 30), according to
Winge. These groups of incipient resting s])ores soon
aggregate together, deposit two-layered walls (fig.
28, 29). and thus form the characteristic cytosori
(fig. 33). In iV. radicicolus, however, according to
Cook ('33. p. 207). the j)rimary cleavage segments or
sjiore mother cells (fig. 20) divide twice to form four
instead of two inci])ient resting spores. Cook did not
show clearly how these united to form the cystosorus
and an enveloping wall. It may be that the two
species actually differ in this respect, but further
study is necessary to determine this point. If Winge's
and Cook's accounts are correct Sorodiscus shows
marked similarity to Sorosphaera by the ])resence of
s])orc mother cells which divide into diads and tet-
rads and subsequently aggregate into sori.
S. CALLITRICHIS I.aperheim and Winpe, I.e.. p. 33.
PI. 1, fig. 9, 1(1; PI. -'; PI. 3. fi;:. 43-63.
Cystosori up to 10 in a cell, usually circular, flat
and "disc-shaped. 30-1-5/. X 10-6.5 )x X 12-11/1,
rarely spherical and hollow; composed of U|) to 200
resting spores usually arranged in two layers and
closely pressed together ; outer layer of spore walls
continuous {!). Resting spores urn-shaped in longi-
tudinal section and hexagonal in cross section, t- .5 /n
X 6-7 //. with smooth hyaline walls surmounted at
the al>ex by a collar; germination unknown. Zoospo-
rangia and zoosjjores unknown. Plasmodia one to
several in a cell, large. 10-00 /x in diam., each form-
ing one cystosorus; schizogony doubtful or lacking;
cleaving at maturity into binucleate segments or
sjjorc mother cells which divide once (?) into two
resting s])ores.
P.irasitic in Callitriche icrnaVis in Norway ( I.a-
gerheim and Winge, I.e.) and C. autiimnalis in Russia
( KareltsehikotT and Ros.inoff. '70) and Sweden
(Ostenfeld). causing globular galls uj) to 3X''' mm.
on the primary and secondary axes.
This species was first recorded in 1870 by Ka-
reltschikoff and RosanofT who mistook the cystosori
for cystoliths and com))ared them with those present
in the L'rticaeeae. although Rosaimrt was of the
o|)inion that they might be rcmnauts of a parasitic
mycelium. According to Winge, Lagerheim collected
48
PLASMODIOPHORALES
this species on C. vernalis in Norway in 1893 and
1900. and altlioua;li lie fixed, sectioned and studied his
material lie ])uhlished notliing but passed the mate-
rial on to \^'inge. In 1907 Rosenfeld (Anonymous,
08) discovered the fungus on C. autumnalis in
Sweden, and since that time it has not been reported.
Sorodiscus CaUitrichis has a marked effect on the
host. All parts of the stem except the outermost corti-
cal tissues and ejjidermis are attacked, and the vascu-
lar bundles become displaced and lie scattered about
in the tumors or are completely destroyed. Infected
cells may often enlarge to 10 times their normal di-
ameter, but whether or not they and adjacent healthy
ones are stimulated to divide by the fungus is un-
known. It is not improbable, however, that the galls
are due to both cell enlargement and cell multiplica-
tion. The nucleus of the host cell apparently en-
larges also and forms several conspicuous nucleoli.
So far nothing is known about the site and method
of infection.
S. RADICICOLUS Cook, 1931. Ann. Mveol. 29: 321. Pis.
1,2.
Cystosori one to several in a cell, usually flat and
disc-shaped; composed of up to 50 resting spores
usually arranged in two layers and closely pressed
together; enveloped in a delicate membrane which
later disintegrates and frees the individual spores.
Resting spores oval, rectangular and jiolygonal in
section, 3.8-4..2 ix X 3.2-3.6 fj., with smooth walls,
the outer layer of which may be extended to form
blunt spines ; separating at maturity and giving rise
to zoospores in germination. Zoospores oval pvri-
form. 2. .5-3. .5 jj., soon becoming amoeboid. Zoospo-
rangia unknown. Plasmodia one to several in a cell,
small 15-30 /t in diameter: schizogony doubtful or
lacking; each producing a single cystosorus ; at ma-
turity cleaving into uninucleate segments or spore
mother cells which divide twice into four resting
spores.
Parasitic in tlie roots of Giinandrops'is penla-
phi/lla near Pretoria, South Africa, causing con-
voluted, coral-like galls, 3-15 mm. in diameter.
Cook's study of this species was based entirely on
prepared slides and fixed material sent by Dr. E. M.
Doidge from South Africa. It has accordingly never
been examined in the living state. Many of the criti-
cal developmental stages such as resting spore ger-
mination, fusion of gametes, schizogony, alternation
PLATE 7
Sorodiiciis
(Fig. 1, 3, 9-15, 23-33 after Winge, '13. Remaining figures
after Cook, '31. Fig. 8 drawn from portion of a plioto-
graph.)
Fig. 1. Callltilche viriudis with lunnerous galls caused
by .'^. Callitrichii-:
Fig. 2. Enlarged gall.
Fig. 3. Diagrammatic sketch of cross secticm througli the
root and gall of Gjinandrojinis pentaphyUa showing the
progressive developmental stages of parasite from the root
to the opposite side of tumor. S. radiciroliis.
Fig. 4. Anteriorly flagellate zoospore or gamete. .S. rad'i-
cicolus.
Fig. 5. Amoeboid stage of same. S. radicieoliis.
Fig. 6. Fusion of gametes. S. radicicoliis.
Fig. 7. Young binucleate Plasmodium after first division
of zygote nucleus. .S. rndicicoliis.
Fig. 8. Large multinucleate plasmodium. S. toi/iVico/h.*.
Fig. 9. Resting nucleus of plasmodium. S. CaVitrirhis.
Fig. 10. Prophase, showing differentiation of "tropho"
and "idioehromatin." S. ('iillltrlchh.
Fig. 11. Equatorial plate stage of "iiromitosis" (?). S.
C'allitrichin.
Fig. 12. Similar stage from a young plasmodium showing
chromatin aggregated into chromosome-like bodies. S. Citl-
iitrichin.
Fig. 13. Anaphase with conspicuous astral rays. S. Calll-
trirhis.
Fig. 14. Late telophase showing differentiation of
"tropo-" and "idioehromatin." S. Cdllilrichi.i.
Fig. 1.5. Daughter nuclei with well-marked centrosome-
like bodies and astral rays. .'?. CaUitrichis.
Fig. IB. Beginning of cliiomatin discharge into cyto-
plasm from nucleus during chromidial stage. /S. radici-
foluif.
Fig. 17. Later stage showing karyosome broken u]) into
granules which lie at the inner peri))hery of nucleus. iS.
rndicicoliis.
Fig. 18. Final akaryotc stage with all stainable chro-
matin discharged from nucleus. S. rridicicoliis.
Fig. 19. Prophase of meiosis, the so-called "garland
stage." S. radicicoliis.
Fig. 20. Equatorial plate stage of meiosis with four chro-
mosomes. Plasmodium segmenting into spore mother cells.
.S'. radicicoliis.
Fig. 21. Binucleate spore mother cell >S'. racliciciihis.
Fig. -2-2. Second meiotic division with two chromosomes.
S. ratlicicohis.
Fig. 23-24. So-called "garland" stages in S. Callitrichi.i.
Fig. 35. Equatorial plate stage of the first (homeotypic)
division. S. CaUitrichis.
Fig. 2(). Equatorial plate stages of meiosis. Plasmodium
cleaving into segments. S. CaUitrichis.
Fig. 27. Paired daughter nuclei in cleaving plasmodium.
S. CaUitrichis.
Fig. 28, 29. Binueleate segment of plasmodium. S'. CaUi-
trichis.
Fig. 30. Four incipient resting spores resulting from
cleavage of two binucleate segments. Nuclei quite large.
•S'. Callit richis.
Fig. 31. Mature spores with two-layered walls, the outer
layer merging with that of neighboring spores. S. CaUi-
trichis.
Fig. 32. Young spores with outer and inner walls. .S'. Cal-
lit richis.
Fig. 33. Side view of cystosorus of S. CaUitrichis show-
ing common enveloping membrane.
Fig. 34. Young spore with incompletely formed walls.
»?. radicicoliis.
Fig. 3.5. Surface view of small cystosorus. S. radicicoliis.
Fig. 3(i. Spiny resting spores. S. radicicoliis.
Fig. 37. Thick-walled resting spore broken away from
cystosorus. S. radicicolus.
SOHODISt TS
H)
ri.ATK 7
Sorodiscus
50
'LASMODIOP MORALES
of haploid and diploid generations, ete., are thus in
need of further investigation.
The method of infection has not been observed,
but Cook believed that the amoeboid zoospores or
amoebae are capable of passing through the walls
from cell to cell and even to the outside of the host
where they may infect other roots. As is shown in
figure 3 at least two generations of the parasite may
occur in large galls during the course of one season,
but the host plants are not seriously affected by the
presence of the galls and fungus. The central cylin-
der of the roots apparently is not attacked, and the
galls seem to originate in the cortex, although Cook
was not at all clear about their origin. Infected cells
do not enlarge greatly, but their nuclei eventually
become disorganized and degenerate. The presence
of the fungus may possibly stimulate cytokinesis or
at least does not ])revent division of infected and ad-
jacent healthy cells. The galls are therefore doubt-
less due to both cell enlargement and cell multiplica-
tion.
S. KARLINGII Cook, 1933, I.e. p. 207. Karling, 1938. Am.
.Tour. Hot. 1.5: 485. PI. 3;?, fig. 1-9.
Cystosori numerous, up to 400 in a cell, quite va-
riable in size and shape, often oval, elongate and
disc-shaped, 15-30 /x X 15-70 /x, occasionally almost
spherical, 10-35 /x in diameter, irregular, or reduced
to tetrads, triads, diads and rarely monads; consist-
ing of from 1 to 200 spores; enveloping membrane
unknown. Resting spores polygonal and angular,
•t-9 ;«., when pressed together in large sori, spherical,
oval and ellipsoidal when single or in small groups,
5-23 /J. in diameter, uni- or multinucleate with hya-
line smooth walls and surmounted by one and oc-
casionally two fairly thick caps; germination un-
known. Plasmodia one to several in a cell, multi-
nucleate, and uj) to 90 /j, in diameter; schizogony
unknown. Zoosporangia and zoospores unknown.
Parasitic in Chara coniraria and C. delicatiila in
New York City, causing marked hypertrophy of the
infected cells.
This is the only known species which parasitizes
algae. Because of the great variation in the size and
shape of its cystosori and the lack of a common sur-
rounding membrane, it is a doubtful member of
Sorodiscus, and until more is known about its life
cycle it is retained only provisionally in this genus.
Its effect on the host is quite marked and extensive,
and all cells appear to be equally susceptible. Hyper-
trophied stipules, leaflets, spicules, internodal and
cortical cells have frequently been found. As is
shown in figures 1 and 2 infected cells may swell to
many times their normal diameter and have the ap-
pearance of s))herical. oval and elongate green blis-
ters.
The presence of the plasmodia has no visible effect
at first on the streaming of the host jjrotoijlasm and
are continually carried along ])assively with the host
nuclei and cytoplasm. Individual hypertrophied cor-
tical cells have been removed from the leaves and
kept alive in hanging drops for ten days, during
which period the plasmodia, host nuclei and cj'to-
plasm rotated continually. The streaming begins to
slow down in about 12 days and ceases entirely
within 20 days, after which the cell soon dies. As is
shown in figure 3 the host nuclei and cytoplasm ap-
pear normal during the actively streaming period,
and in spite of the extension which it has undergone
the cell wall remains normal in thickness. Later, the
host protoplasm is reduced to a thin layer. The jires-
ence of the parasite mav also often lead to the for-
mation of an abundance of storage starch grains in
the plastids.
The cystosori, which were previously ('28) called
sporangesori by the author, are quite variable in size
and shape, and those consisting of a few large multi-
nucleate and several small uni-nucleate spores (fig.
15, 21) have possibly arisen by unequal and incom-
plete cleavage of the plasmodium. The unusually
large multinucleate spores (fig. 19) are probably
the result of the encystment of the entire plasmodia
which failed to segment. Since such spores are multi-
nucleate, it is not improbable that they form several
zoospore in germination.
ADDITIONAL BIBLIOGRAPHY: SORODISCl'S
Anonymous. 1908. Bot. Tidsskr. -28: XXVII.
Cook, W. R. I. 1933. Arch. Protistk. 80: 303.
KareltscliikoiT, S., and S. Rosanoff. 1870. Mem. Soc. Sci.
Nat. Cherbourg. 3nd ser. 5: 12i.
Palm, B. T., and M. Burk. 1933. Arch. Protistk. 79: 371.
Schwartz, E. .J. 1914. Ann. Bot. 38: 330.
PLATE 8
Sornclisrus karliiigil
(All figures after Karling)
Fig. 1. Hypertrophied internodal cell of C. fhlicnfiiln
which has burst the sheath of cortical cells.
Fig. 3. An extreme case of parasitism of the cortical cells
of C. contraria.
Fig. 3. Longitudinal section of an enlarged cortical cell
witli twenty-six cystosori and seven plasmodia surrounded
by the host protoplasm. The six host nuclei appear normal.
Fig. 4-6'. Uni-, bi- and tetranucleate stages of the jiara-
site.
Fig. 7. A multinucleate vacuolate plasmodium in surface
view.
Fig. 8. Similar plasmodium in edge view.
Fig. 9. Large irregular plasmodium.
Fig. 10. Cleavage of plasmodium to form cystosorus.
Fig. 11. Surface view of a large flattened cystosorus con-
sisting of approximately 300 spores.
Fig. 13. An almost spherical cystosorus.
Fig. 13. Flattened cystosorus in end view.
Fig. 14. Tetrad of resting spores.
Fig. 15, 1(). Further variations in size and shape of cysto-
sori.
Fig. 17, 18. Small resting spores in side and surface views
showing the apical caps.
Fig. 19. Large isolated multinucleate spore.
Fig. 30, 31. Cystosori consisting of two and three spores.
SOKOUISllS
51
PT.ATK 8
"^S^^
10
Sorodiscus karlingi
PLASMODIOPHORALES
The genus Membranosonts has been regarded as a
synonym of Sorodiscus, but inasmuch as its inclusion
in this genus as well as in Sorosphaera is highly
questionable at present it seems advisable for the
time being to discuss it separately.
MEMBRANOSORUS
Ostcnfeld and Petersen, 1930. Zeitschr. f. Bot.
23:17.
(PL.\TE 9)
Cystosori one or more in a cell, variable in size
and shai)e ; frequently a hollow, single-layered struc-
ture wliich covers the inner periphery of the host
cell and conforms to the latter's size and shape ; often
oval, disc-like and single-layered, rarely double-
layered, occasionally composed of an irregular mass
of loosely attached spores or a row of spores ar-
ranged in a linear series. Resting spores slightly
variable in size and shape ; germination unknown.
Plasmodia one or more in a cell, variable in size and
shape; often in the form of a parietal layer around
the host protoplasm; schizogony unknown. Zoospo-
rangia and zoospores unknown.
In light of present-day knowledge Memhrano-
sorus is obviously a doubtful genus which should
perhaps be discarded entirely, but until more is
known about the Plasmodiophoraceae as a wliole its
inclusion in any of the other genera is open to serious
question. Wernham's observations have shown that
the outstanding character described by Ostenfeld
and Petersen, namely, hollow single-layered cysto-
sori which line the inner periphery of the host cell
and conform to the latter's size and shape, is too va-
riable (fig. n-18) to be of significant diagnostic
value. The incorporation of Memhranosorus in Soro-
sphaera or Sorodiscus is equally questionable if the
present-day concepts of these genera are to be main-
tained, because only occasionally are cystosori in
the form of hollow spheres or double-layered discs
developed. By the extreme variability of its cystosori
this genus resembles perhaps more closely Lif/niera
and Poli/mi/xa. Ostenfeld and Petersen regarded it
as closelv related to Sorosphaera and Tetrami/.ia,
while Wernham implied tliat it should be incorpo-
rated with Sorodiscus. Palm and Burk regarded
it as a synonym of Sorosphaera. Cook api)arently
overlooked its existence entirely in his monograph of
the Plasmodiophorales.
M. HETERANTHERAE Ostenfeld and Petersen, I.e.,
fi)i. 1-6.
Sornili.iciig Hi'teranlherae, Wernham, 1935. Mycologia
3T:-212. PI. IT, 18, ftp. 1,2.
Resting spores always aggregated in multiitles of
four. Globose, ovoid, angular. S.5-5 /x in diameter,
hyaline and buff-brown, with smooth. 0.6-1.0 // thick
walls : apical ring, collar or operculum lacking. Plas-
modia oval, ellipsoidal. 8 ft in diameter, or disc-like,
flat and often ribbon-shaped. 28-70 /n in length, and
encircling the host protoplasm.
Parasitic on Heieranthera dubia in Ontario and
Quebec, Canada; Vermont and New York. U. S. A..
causing marked hyjjertrophy of adventitious and
true roots.
Whether or not the species described by Osten-
feld and Petersen, and Wernham. respectively, are
identical is not absolutely certain, but since they
have the same habitat and distribution, cause the
same symptoms, infect the same tissues of identical
hosts, and agree closely as to spore size and shape,
they are listed herewitli as synonymous. The chief
differences so far relate to spore color and variations
in the size and shape of the cystosori. Since Osten-
feld's and Petersen's material was very scanty they
may have missed most of the variations later ob-
served by Wernham. Likewise, although Wernham
never found a single-layered cystosorus completely
lining a host cell, his figure 2 shows that the type of
sorus described by Ostenfeld and Petersen was often
api)roximated in his material. Tliere is accordingly
good evidence that they may have had the same spe-
cies at hand.
Nothing is known about tlie method by which this
parasite gets into the roots, but entrance appears to
PL.\TE 9
Membridio.iorus Heterantheroe
(Fig. 1-3, 6, 19 and 20 after Ostenfeld and Petersen; re-
mainder after Wernham; fig. 5 and IS drawn from
photographs.)
Fig. 1. Portion of infected stem of //. fliibia with 10
swollen and 5 normal roots.
Fie. 2. Early infection stage with small granular para-
site attached to host nucleus.
Fig. 3. Young bi- and trinucleate parasites in daughter
host cells.
Fig. 4. Young parasite with three nuclei.
Fig. .5. Large parietal plasmodium which almost com-
pletely envelopes host protoplasm.
Fig. (i. Large multinucleate plasmodium enveloping the
host nucleus.
Fig. 7. Plasmodium with nuclei dividing promitotically.
Fig. 8. Plasmodium in which nuclei are about to undergo
reduction division.
Fig. 9. Plasmodium with nuclei which have just under-
gone reduction division.
Fig. 10. Second meiotic divisions. Plasmodium cleaving
into resting spores.
Fig. 11. Cystosorus of young thin-walled resting spores.
Fig. 12. Flat, almost circular cystorus composed of a sin-
gle layer of resting spores.
Fig. 13. Similar cystosorus with one resting spore pro-
jecting beneath.
Fig. U. Flat, two-layered cystosorus.
Fig. 15. Cystosorus with resting spores In a row.
Fig. 16 and 17. Irregular cystosori with loosely attached
resting spores.
Fig. 18. Single-layered cystosorus incompletely lining
Inner periphery of host cell.
Fig. 19. Similar cystosorus completely lining inner pe-
riphery of the host cell.
Fig. 20. Surface view of similar cystosorus.
MKMBHA.NOSOIUS
53
ri.ATE 9
Meinbranosorus
54
PLASMODIOPHORALES
be effected at or near the tip. Cells of the periblem
are more frequently attacked, and the fungus occurs
most abundantly in a region approximately 0.5 cm.
back of the root tip. The cells of the central cylmder
apparently are never infected. According to Osten-
feld and "Petersen, the fungus first appears as a
small plastic granular body close by or attached to
the host nucleus (fig. 2), and as it grows in size and
becomes multinucleate it may envelop the host nu-
cleus and cytoplasm (fig. 3. 5. 6). There is thus a
close association of the protoplasts of host and
pathogen, and in Ostenfeld and Petersen's drawmgs
it is difficult to distinguish between them. The para-
site causes the infected cells to enlarge somewhat but
apparently does not stimulate cell division. Figure 3,
however, "suggests that infected cells may divide,
whereby the' parasites are passively distributed to
the daughter cells.
The mature plasmodia vary greatly in size, and
the large extensive ones may often line the inner
periphery of the host cell (fig. 5) as in Tetramiixa.
According to Wernham, cruciform nuclear divisions
occur (fig. 7) during the vegetative phase of the
Plasmodium, and the nuclei undergo meiosis in the
first of the two divisions prior to cleavage into rest-
ing spores. Although he stated that he had observed
numerous meiotic stages and counted four to six
pairs of chromosomes, his figures (fig. 8, 9, 10) show
nothing of the process.
SPONGOSPORA
Brunchorst, 1887. Bergens Mus. Aarsberet.
1886: 225.
Clathrosorus Ferdinandsen and Winge, 1920. Ann.
Bot. 31.: 168.
(plate 10)
Resting spores usually arranged in hollow or
irregularly-channeled spongy, globose balls or cysto-
sori! Resting spores loosely or fairly closely packed
together, spherical, oval, pentagonal, hexagonal in
op'tical section with hyaline, yellowish to yellowish-
green, smooth, thin or fairly thick walls ; each spore
producing a single ( ?) zoospore; such zoospores giv-
ing rise to either plasmodia or zoosporangia. Plas-
modia usually large, irregular, amoeboid and multi-
nucleate ; partly or completely filling the host-cell ;
forming one or more spore balls. Zoosporangia sin-
gle or in clusters, variously-shaped. Zoospores from
resting spores and zoosporangia similar, small, bi-
flagellate and heterocont; flagella attached at or
near anterior end.
Sponqospora includes at present three species, one
of whicii is poorly known and doubtful. The type spe-
cies, .S'. siibterraneaMs been repeatedly studied mor-
phologically and cytologically. but there is still con-
siderable disagreement concerning some of the criti-
cal stages of its life history. As noted in Chapter III.
these controversies have centered primarily around
the stages at which plasmogamy and karyogamy
occur, and the manner by which the parasite invades
and spreads in the host tissue. Johnson ('07) de-
scribed the resting spores as one- to eight-nucleate
and giving rise to a corresponding number of zoo-
spores in germination, but subsequent workers in-
cluding Massee ('08), Kunkel ('15), Cook ('33)
PLATE 10
Spongospora sitbterranea
(Fig. 7-9, 11 and 23 drawn from photographs)
Fig. 1. Potato with shallow powdery scab lesions.
Fig. 3. Malformed potato with deep cankerous lesions
and excrescences.
Fig. 3. Powdery scab galls on roots of potato.
Fig. i. Enlarged host cell with eight spongy spore balls
or cvstosori. Osborn, "11.
Fig. 5. Section through a mature cystosorus. Osborn, I.e.
Fig. 6. Uninucleate resting spores. Osborn, I.e.
Fig. 7, 8. Zoospores from germinated resting spores.
Ledingham, '35.
Fig. 9. Tetrafiagellate zoospore. Ledingham, I.e.
Fig. 10. Dividing amoeba. Massee, '08.
Fig. 11. Irregular ^oosporangium. Ledingham, I.e.
Fig. 1:2. Uninucleate amoebae surrounded by host cyto-
plasm. Osborn, I.e.
Fig. 13. Host cell with three amoebae and numerous
starch grains. Osborn, I.e. ,. , ., ^ ,
Fig. U. Dividing host cells with passively distributed
amoebae. Osborn. I.e.
Fig. 15. Hypertrophied cells of S. xcarso-n-iczii which
have divided": amoebae aggregated around host nuclei.
Melhus, et al. "16.
Fig. 16. Group of infected enlarged tomato cells; typi-
cal "Krankheitsherde." Melhus, et iil. l-c.
Fig. 17. Infecting plasmodium pushing down between
host cells. Kunkel, "15.
Fig. 18. Plasmodium entering host cell and enveloping
nucleus. Kunkel, I.e.
Fig 19 Coalescence of amoebae to form plasmodium;
host nucleus enlarged, irregular, and densely chromatic.
Osborn, I.e.
Fig. 20. Plasmogamy of two amoebae derived from ger-
minated resting spores. Cook, '33.
Fig. 21. Karyogamy. Cook, I.e.
Fig. 22. Zygote. Cook, I.e.
Fig. 23. S'aprophytic plasmodium (?) grown on nutrient
agar. Kunkel, I.e.
Fig. 24, 25. Vegetative nuclei degenerating and extrud-
ing chromidia into cytoplasm. Osborn, I.e.
Fig. 26. Akaryote and chromidial stage. Osborn, I.e.
Fig. 27. Reconstructed nuclei emerging on new sites. Os-
born, I.e. , _ 1 f ■
Fig. 28, 29. Reconstructed nuclei pairing and fusing.
Osborn. I.e.
Fig. 30. Late stage in karyogamy. Osborn, I.e.
Fig. 31. Diploid nuclei. Osborn, I.e.
Fig. 32. I>ate prophase of meiosis with eight chromo-
somes. Home, '30.
Fig. 33. Contraction stage and beginning ot pairing ot
homologous chromosomes. Home, I.e.
Fig. 31. Dlakinesis. Home, I.e.
Fig. 35. Metaphase, first division, showing three of the
chromosome pairs. Home, I.e.
Fig. 36. Equatorial plate, second division, showing seven
chromosomes. Osborn, I.e.
Fig. 37. Anaphase, second division, and cleavage. Os-
born, I.e.
SPONIiOSl'OllA
55
Pl.A'i"K 10
20 21 2Z ^ " \
Spongospora
S^.
56
PLASMODIOPHORALES
PLATE 10~Continned
Spongospora Campanulae
Spoil (jospora Ciimpnnulae
Fig. 38. Campanula rapiinculoules with numerous jfalls
and nodules on roots. Ferdinandsen and Winge, "JO.
Fig. 39. Young parasite with nuclei dividing "promitoti-
cally." F. and W., I.e.
Fig. 40. Multinucleate Plasmodium. F. and W., I.e.
Fig. 41. Plasmodium enveloping host nucleus. F. and W.,
I.e.
Fig. i-2. Irregular cystosorus. F. and W., I.e.
Fig. 43. Section through a cystosorus. F. and W., I.e.
Fig. 44. Section through two resting spores showing
finely punctate warty walls. F. and W., I.e.
and Ledingliam ('35) observed only one zoospore.
Furthermore, all earlier investigators figured and
described the zocspores as uniflagellate, but Led-
ingliam demonstrated conclusively that they are bi-
flagellate and heterocont (fig. 7, 8). Whether the
flagella are attached at or near the anterior end is
not definitely known. Massee, Kunkel, Osborne
('11 ) and Home ('30) held that the plasmodium is
formed by the fusion of several amoebae (fig. 19).
but they were not certain whether such amoebae arise
by division of a single amoeba within the infected
host cell or are the result of infection bv several
amoebae. Cook ('33), on the other hand, contended
that the plasmodium is initiated by the fusion of
gametes in pairs (fig. 20-22).
There is also difference of opinion about infection
and spread of parasite in the host tissue. Massee and
Cook in particular held that the amoebae have the
ability to penetrate the host cell walls and thus pass
from cell to cell, spreading the infection. Osborne
and Home, in contrast, maintained that the amoebae
are incapable of boring through the walls and are
distributed passively and fortuitously by division of
the infected cell (fig. 14). Kunkel, however, reported
that the primary infection of young tubers as well as
secondary infection of tissues around old sori occurs
by invasion of the plasmodium. The latter passes
through and between the epidermal cells, and once
beneath the epidermis it spreades out in all directions
(fig. 17). Johnson ('09) believed that the plasmo-
dium may migrate from the diseased parent tubers
into the stem and stolons of the young plants, and
eventually infect the young tubers. Massee thought
that the plasmodium might encyst during the cold
winter season and renew its activities when the
tubers began to sprout. \\'ild ('29) considered the
Sl'ONGOSPORA
57
Icnticils. instead of the imlirokoii ciJidtTinis, to he
flif i)riiu-i|)al .-imihu' of initial infection, with sonu"
luni'lration tliroiigli wounds.
.\feordin<t to Kunki'l. tlif resting spores jienninate
readily on initrient agar and form plasniodia in enl-
ture. By weekly transfers, sneli jilasinodi;! may be
kept in an active growing condition on synthetic me-
dia for a long time, and under these conditions they
are strikingly similar in api)ear;ince, sha])c. he-
havior, and locomotion to the ])l;ismodia of the
Myxomycetes (fig. 23). Wlien subjected to drouglit
they encyst or sclerotize, and if transferred to fresh
media the plasniodia may often break up into
smaller masses which move away and form stalked
fruiting structures like those of Dictiinxti-liiim
and Poliixphoncli/lium. The erect, single or branched
sporojihores bear sori of rod-shaped spores like
Dicti/oxtcliiim, and in germination give rise to
niyxamoebae which later aggregate to form pseudo-
plasmodiu. These in turn form sporophores again.
Kunkel's observations have not been confirmed, and
since species of the Acrasiales occur in soils with
S poll f/os pore it is not improbable that he may have
introduced coiit.-iminants of this type in his cultures.
It is to be particiilarli) noted, however, that the Plas-
modium which he |)lu)togra)ilHd looks like a true
myxomycctous plasmodium. .Since it has none of the
characteristics of an acrasiaceous pseudoplasmodium
in wliich the individual niyxamoebae retain their in-
dividuality as cells, it is difficult to conceive how
Kunkel got Dicti/osffliiim- and Poli/xphonili/Iiiim-
like sorocarjis from a |)lasmodium of the ty|)e shown
in figure 23. His photographs and descri])tions sug-
gest that he may have had more tiian one type of
Plasmodium at hand. The possibility that .S'. spoiif/o-
spora may form large plasniodia on nutrient agar
remains thus to be proven by pure culture studies.
S. SUBTERRANEA (Wall.) Lafrfrlieim, 1891. .Tourn.
Mycol. 7: 104.
Eri/yihfi »n1>tirraiii<i Wallmth. IH-l.'a. Mnnaea Ifi: 3.3^!.
\»MK Beitr. zur. Bot. 1: IIH.
Prnlotniires Tuliir-Sotinii .Martius. \Hi2a. Die Kartoffel-
e|)i(lemie der Irfzten .lahre order die .Stockfiiule und
Hiiude drr KartofTeln, .Miinchen. IHl.'l), C. R. Acad.
.Sci. Paris IJ:3U.
Hhhd.iiKiriiim Stiliiiii Hahenhorst. 184.S. .Arcli. Pharin.
83: 300. 1844, Kryjit. Fl. Dputs<li. Oisttrr.. uiid der
Schweiz I.
Tiilierrinia grahHn Berkeley, 18Hi. .lour. Hurt. .Scic. I.(in-
don 1: 33. PI. 4. fip. 30-31.
Soronporhim Krnhieti Waldheim, 1877. .Xpcriii .System.
des L'stilag. Paris, p. 33.
Spon<i<»i><)rti Solan! Brunchorst, I.e.
.S. srnltieg Massee, 1908. Jour. Bd. \^t\v. Knjriand 1.5:
.594. Fip. 1-1:?.
.S. siihltrrnnm ri(tllriri>hi Blattny, 19.3.5. Hee. Inst. Kecli.
.\(rr(in. Rep. tclieeosl. 137: ii.
S. .iiilitirriniiii liihi rirohi Blattny. I.e.
Resting spore clusters or balls oval, elongate, ir-
regular, 19-8.5 p. in diameter, somewhat spongy with
numerous irregular channels. Resting spores loosely
l)acked together, angular, polygonal, spherical, 3..5-
i.a i-i, with smooth, thin, yellow to yellowish-green
walls. Plasniodi.i uiiusu;illy large, u)) to 70 /( or more
in length, amoeboid, irregul.ir ; giving rise to one or
more sjiore w.alls. Zoospor.-ingia single or in clusters,
U)) to a dozen or more in a cell, si)herical, oval, elon-
gate, lobed and irregular, hyaline and thin-walled ;
ojicuing by the rupture of a small pajiilla which
bursts through the host cell wall emitting the zoo-
spores. Zoospores from resting sjiores and zoospo-
rangi.i oval. si)hcric;il, 2. .5-3. .5 /t, with two unequal
Hagella.
P.irasitic on Sdlaiium tiihi'rosum, S. rcarscczcicsii,
S. haematododuin, S. mamusum, S. marc/inatum, S.
ciliatum, S. commersomi, S. nigrum, and Li/copersi-
coii esciilenitim, causing scabby lesions and cankers
on the tubers, and galls on the roots and steins. A
further account of the distribution and hosts of this
species is given in Chapter W.
Spoiigospora xuhtcrranca causes the disease of
potatoes commonly known as powdery or corky scab.
While it is chiefly a parsite of the potato, it may also
infect close relatives of this host. In extensive inocu-
lation experiments Melhus, et al. ('16), found that
it will infect all but one of the hosts listed above but
not S. nigrum, S. mauritianum, S. duplo.iumatori ,
S. Lohelii, S. heteracanthum, S. srafnrthianum, S.
lanciniatum, S. iorviim, and Solatium sj). Ferdinand-
sen ('23), however, reported that it is transmissible
to iS. nigrum in Denmark. Weber ('22) and I.eding-
ham ('35) also found it on tomatoes in Denmark and
Canada, respectively. It has also been reported by
Rybakova and Nedoshivinia ('36) on Ullucus tii-
bero.sus of the Chenoiiodiaceae in Russia. Truscott
('Si) found a Spongoxpora-like organism in the roots
of strawberries in Canada, but he was not certain
about its identity. Blattny's distinction of two forms
of S. suhterranea on the roots and tubers, respec-
tively, does not seem justified. The two forms may
be transferred readily from one organ to another
and do not differ greatly in size and color of their
s])ore balls. Blattny, nevertheless, believed that the
root form may be inycorrliizal instead of l)arasitic.
Rybakova and Nedoshivinia also described an aber-
rant form near Moscow which differs from the nor-
mal type by the occurrence of its spore balls out-
side of the host cells. These balls are faintly brown
instead of yellowish-green in color, jilicate or ir-
regularlv crumpled on the surface, and m.iy be
aggregated in a common mass. They vary in size
from 20-2.5 /x by 13-19 /x .and show no cellular struc-
ture. Khrobrykh ('38) ex|)erimented with various
forms of .v. mihtrrraura from different jiotato va-
rieties of different geographical origin and con-
cluded that these forms are not biotypes or geo-
gra))hical races but ecotypes dependent on the host
variety, height, and size of the |nistules. In this con-
nection it may also be noted that .Sharpies ('23) de-
scribed a disease of the ))etioles ;ind le;if stalks of
the cocoanut |);ilin in Mal.-iya which appeared to be
associated with a species of Spongospora, but he was
not certain about the identity of the causal organism.
It probably does not relate to Spongospora at all.
58
PLASM ODIOPH OR ALES
Spoiigospora suhterranea was the first species of
the Plasmodiophoraceae to be reported in the litera-
ture, but it was not recognized as a member of this
family until about fifty years later. It was first re-
ported, in part by Wallroth in 18-t2, but he had
apparently found it tiie year before as is indicated in
Bartling's (18H) discussion. As is sliown in the
synonomy above, it was rediscovered a number of
times shortly afterwards in connection with otlier
fungi in scabby lesions of potatoes, and included in
various genera. It was not until 1886, however, that
Brunchorst first recognized it as a species of the
Plasmodiophoraceae. For a considerable number of
years a long controversy raged about its identity
and synonj'my, which has been fully reviewed by
Lagerheim, Massee, Pethybridge and Cook, and
need not be discussed further here.
S. CAMPANULAE (Ferdinandsen and Winge) Cook,
1933. Arcli. Protistk. 80: 2lo.
Clathrosorus Camija indue Ferdinandsen and Winge, Lc.
PI. 21.
Spore clusters or balls irregular, rounded or elon-
gate, 25-.50 /jL in diameter with large irregular chan-
nels. Spores spherical, 4-5.5 /jl, oval, irregular, trun-
cate, with fairly thick and slightly verrucose walls.
Plasmodia solitary in the host cell and only partly
filling it. multinucleate, irregular, 30-50 fi in diam-
eter, when mature ; segmenting into resting spores
which remain attached in a fairly loose spore ball.
Zoosporangia and zoospores unknown.
Parasitic on the roots of Campanula rapiinculoides
in Denmark, causing numerous single or confluent,
tubercle-like galls.
This species has been reported but once. Whether
it belongs in Sponc/ospora, as Cook believed, or rep-
resents a new genus is obviously questionable in light
of present-day knowledge, but since its spore clus-
ters are reported to be loose, irregular, round or
elongate balls (fig. 38), it may be conveniently in-
cluded here for the time being. It occurs in the cortex
of the roots (fig. 38), and although the central cylin-
der mav be distorted, it is never parasitized. The
infected cells are only slightly if at all enlarged (fig.
40-12) and do not divide, but the presence of the
parasite nonetheless stimulates adjacent healthy
cells to divide. The galls are thus almost entirely the
result of cell multi])lication. The nucleus of the host
cell is often enveloped by the parasite (fig. 10), but
it does not become greatly enlarged.
According to Ferdinandsen and Winge, meiosis
occurs during the last two nuclear divisions in the
Plasmodium preceding sjiore ball formation. They
did not, however, count the number of chromosomes
nor observe plasmogamy and karyogamy, .so that
their conclusions are not based on adequate observa-
tions.
Another species of Sponc/ospora was recently re-
ported and described by ,1. T. Barrett in a brief
paper presented before a joint meeting of the Ameri-
can Mycological and Phytopathologieal Societies at
Philadelphia, Pennsylvania, December 30. 1910. Dr.
Barrett has not completed his study of this species,
but he has graciously allowed me to include a few
notes on the essential features of its life cycle. This
species parasitizes Cotula australis in California and
causes cons])icuous galls or nodules on its roots.
Barrett accordingly named it .S'. Cotidae. In germina-
tion each resting spore produces a single zoospore
with two unequal flagella as in <S'. suhterranea. The
zoospores infect the host and eventually give rise to
zoosporangia which in turn form motile cells of the
same type and character as the zoospores produced
by the resting spores. Barrett found fusion stages of
the zoospores or gametes from the sporangia in fixed
and stained material, but he has not yet observed
plasmogamy in living material. Whether or not the
sporogenous plasmodium is thus zygotic in origin is
uncertain at present. The spore balls or cystosori
and resting spores, nevertheless, usually follow the
sporangial stage and thus complete the cycle of de-
velopment.
ADDITIONAL BIBLIOGRAPHY: SPONGOSPORA
Bartling, E. 1841. Versammelung. Deut. Nat. u. Aerzte zu
Braunschweig im September 1841. Vieweg und Sohn,
184:3.
Ferdinandsen, C. 19-'3. Tidsskr. f. Landokonomi. 19J3.
Home, A. S. 1930. Ann. But. 44: 199.
.lohnson, T. 1907. Econ. Proc. Roy. Dublin Soc. 1: 345.
. 1909. Sci. Proc. Roy. Dublin Si>c. n. s. 12: 165.
Khrohrykb, \. D. 1938. Summ. Sci. Res. Inst. pi. protect.
for' 193()- 1938: -21.
Kunkel, I.. O. 1915. Jour. Agr. Res. 4: ^65.
I.edingham, G. A. 1935. Nature 135: 394.
Massee, G. 1908. Jour. Bd. Agrio. England 15: 594.
Melhus, I. E., J. Rosenbaum, and E. S. Schultz, 1916. Jour.
Agr. Res. 7: -'13.
Osborn, T. G. B. 1911. Ann. Bot. 25:211, 337.
Rybakova, S., and H. Nedosliivina. 1936. White Russ.
Acad. Sci. Inst. Biol. Sci. Minsk 1936: 57.
Sharpies, A. 1933. Malayan Agric. Jour. 11: 367.
Truscott, J. H. L. 1934. Canad. Jour. Res. 11: 1.
Weber, A. 1933. Tomatsygdonime. Copenhagen.
Wild, N. 1939. Phytopath. Zeitschr. 1: 367.
LIGNIERA
Maire and Tison, 1911. C. R. Acad. Sci. Paris
152: 206.
(plate 1 1)
Resting spores not consistently aggregated in cys-
tosori of characteristic shajie and structure ; vari-
ously-shaped with relatively thin hyaline or colored,
smooth or verrucose walls. Plasmodium relatively
small, ])artly or comi)letely filling tlie host cell; seg-
menting into either zoos))orangia or one or more
cystosori; schizogony reduced or lacking (?). Zoo-
sporangia numerous in a cell and usually grouped to-
gether, small and variously-shaped ; opening by a
rupture of the wall. Zoosj)ores from sporangia ]iyri-
forni. Germination of resting spores doubtful or un-
known at ])resent.
I.KiXIKllA
59
Tliis jji-iuis was cstaMislKd l)_v Main- aiul 'rismi
for all i)lasiiio<lio|)liorjicfinis species cliaraeteri/.cd
by loosely and variously ajijirejiated restintr spores.
little or no seliizujiony of the iilasiuodiuiii. (■oni])lete
develo)>nu'nt within a sinirle host eell. and whieli
eause no hyiiertropliy of the iiost. As sueh. it is a
very questionahle i;eiuis and should iierhajis lie dis-
carded, since noiu- of its charai'ters are very distinc-
tive and diajjnostic. In the first |)lacc the shape and
character of the restinji spore clusters or cystosori
are too variable to be of nnich {generic value. Sec-
ondly, none of the si)ccies has yet been studied in-
tensivclv and sutHciently well to determine whether
or not sehizoiiony is well developed, redui'cd. or
lackinsr entirely. I'urthcrniore. it is not certain tli;it
the l);irasite completes its entire life cycle within one
host cell. Fin.illy. the Jircscnce or absence of host
hypertrophy is not a structural or eytological char-
acter of tlie jiarasite itself, but relates to the reac-
tions of host and ])athogen. Even if this latter charac-
ter were tenable, it would not be diagnostic for the
group as a whole, because I>. plloriim, according to
Fron and (iaillat. causes marked local enlargement
of the root hairs of Poa annua. t)n the basis of ])res-
ent-day knowledge. Lif/niera al)pears thus to be
scarcely more than a convenient dumping ground
for species which cause little or no hypertrophy.
Further intensive studies, however, may reveal a
more fundamental basis of distinction.
The pyriform uninucleate zoosi)ores of Lif/niera
have been described by Cook as anteriorly uniHagel-
late (fig. 1). but more careful study will doubtless
show them to be biflagellate and heterocont as in
Plasmodiophora, Pol_i/mi/da, Sponr/ospora, and Ocfo-
mi/xa/ After penetrating root hairs and epidermal
cells, they may become flagellate and actively motile
again in the host ]iroto])lasm (tig. 2B). according to
Cook. The flagellum soon disap|)ears. however, and
the parasite becomes amoeboid in sha)3c and motion
(fig. 3). Nuclear divisions occur as the amoebae in-
crease in size (fig. K 8. 9). until a multinucleate
Plasmodium is formed. One or more amoebae and
Plasmodia may be present in a host cell, but so far
no conclusive evidence has been presented to show-
that they coalesce to form a larger structure. As
noted before Cook ('33) re))orted that the zoospores
are isogametes which fuse in i)airs to form zygotes.
but his evidence of plasmogamy or karyogamy is not
very conclusive.
Host cells usually contain only one plasmodium.
which fills them almost eomjiletcly (fig. 12). Very
little is known about the feeding habits of the intra-
matrical plasmodia. They alijiarcntly absorb the host
cvtoijlasra. envelop the nucleus, and lead to the dis-
appearance of the starch grains, so that the infected
regions of the roots ap])ear quite pale in color.
Maire and Tison ('11). however, reported th.it the
Plasmodium is cal)able of engulfing large food pnr-
• This is suppestrd by Rarretfs discovery of biflajrcllate
heterocont zoospores in Khhiinuij-a hiipoijea whieli is re-
garded as a combination of Liijniern sp., and another fun-
gus species.
tides, .-iiid figured ;! yiiuiig p.'irasite with live en-
gulled algal cells (fig. .5).
Whether or not schizogony incurs in Lii/nii'ra is
still questionable. Schwartz ('10) reported that the
young plurinuele.ite iil.ismodi.-i of /.. Jiinci function
.■IS schizonts. siilitting off smaller uni- or multiiiuele-
;ite daughter segments. .M.iire and 'I'ison (lib), on
the other hand, believed that schizogony may be
l.iekiiig entirely or is reduci<l to the formation of two
or three iiieronts (fig. 10). Suiiseqiunt workers also
have doubted its occurrence or cl;iimed that, if pres-
ent at all. it takes place only in the young develoj)-
ment.il stages.
With the doubtful exception of /,. plloriim (fig, 2.5.
2(). 38). species of Li(/)ticra ha\e no noticeable effect
oil the host tissues, according to most accounts in the
liter.iture. No galls are ))roduced, and the infested
cells arc not markedly enlarged or stinuil.ited to di-
vide. Schwartz (H), however, reported that para-
sitized cells of Poa annua are often considerably
elongated, due either to the failure of transverse wall
dev(lo])ment or the absorbtion of such walls by the
parasite. Subsequent workers, however, have not
confirmed these observations. The relation between
the ))rotoi)lasts of the host and ])athogen ap|)ears to
be very intimate, and no marked antagonism is ex-
liibited, according to the figures and descriptions in
the literature. Schwartz reported that tlie amoebae
are strongly attracted to the host nucleus and mi-
grate toward it as soon as they have entered the eell
(fig. 0. 7) like in .S'. subterranea. The amoebae shown
in these figures, however, look like nuclei of the
parasite, which suggests that the host nucleus in
these instances miglit )iossibly be envelojied by a
multinucleate plasmodium. Complete envelopment
of the host nucleus and a mixing of the two proto-
plasts has also been shown in root hairs of J uncus
articulatus (Schwartz. '10, fig. .5). Figure 37 shows
a host nucleus inside a mature eystosorus. The nu-
cleus of infected cells shows little or no enlargement,
and no conspicuous signs of degeneration are evi-
dent until the parasite is almost mature. Maire and
Tison's figures (11. 37) suggest that as degenera-
tion progresses the nucleus becomes more chromatic
and densely stainable.
According to Cook ('2G, '28) the mature ))lasmo-
diuni may form either zoos]>orangia or cystosori. In
the former event uninucleate segments (fig. 20) are
delimited by ])rogressive cleavage, and their nucleus
divides twice and occasionally three times. Cook
claimed that the first division is heterotypic and the
second homeotypic, liut his evidence is not at all con-
clusive (see Chap, III). In resting spore develo])-
ment uninucleate amoebae may sometimes undergo
two nuclear divisions (fig. 22) and form tetrads of
resting spores, according to M;iire and Tison (1 lb).
It is not inijirobable. howe\er. that their figures m.iy
relate instead to sjioriingia and zoospore develo))-
ment. In larger ))lasmodia. the reconstructed nuclei
following the so-called "akaryote" stage also divide
twice. Following these divisions the jilasmodium
cleaves into uninueleate segments, which round u)).
60
PLASMODIOPHORALES
become invested with a wall (fig. 31), and mature
into resting spores. These spores usually remain at-
tached to each other and form cystosori of variable
sizes and shapes (fig. 28-40) in accordance usually
with the size of the plasmodium and tlie shape of the
host cell.
L. JUNCI (Schwartz) Maire and Tison, I.e.
Sornsphuera Jiiiici Schwartz, 1910. Ann. Bot. 24: 513.
PI. 10.
S. (/raminh Schwartz, 1911. Ibid. 25: 791. PI. (il.
L. graminh (Schwartz) Winge, 1913. Ark. f. Bot. \-2,
no. 9: 15.
L. rridicdlii Maire and Tison, I.e.; 1911. Ann. Mycol. 9:
333. PI. 11, fip. 34-38.
L. Bellidis Schwartz, 1914. Ann. Bot. 38: 333. PI. 13, fig.
7-8.
L. Menthae Schwartz, I.e. PI. 13, fig. 1-6.
L. AlisnuiUs Schwartz, I.e., p. 333.
Resting spores rarely in tetrads, sometimes end to
end in a linear series ; more often in irregular masses,
solid or hollow, flat, globose or ellipsoidal, cylindri-
cal and elongate cystosori. Resting spores spherical
oval, angular and polyhedral when compressed to-
gether, 4-7 /i in diameter, with relatively thin hya-
line smooth walls; apparently giving rise to zoo-
spores which infect the host cell. Plasmodium partly
or completely filling the host cell ; segmenting into
either zoosporangia or one or more masses of rest-
ing spores, schizogony questionable or reduced. Zoo-
sporangia oval, subglobose, spherical, angular and
polyhedral, 15-20/x, in diameter, with thin hyaline
smooth walls; method of dehiscence unknown. Zoo-
spores from sporangia 4 to 8 in number, pyriform,
3. 5X^-5 jn.
Parasitic in the root hairs and roots of Junciis arti-
ciilatus, J. obiusiflorus, J. biifoniiis, J. lamprocar-
piis, Poa annua, Bellis perennis, Mentha piilegium,
Alisma Plantago, CallHriche stagiialis, Votomgeion
natans, Polyc/onum H i/dropiper. Iris pseudocorus,
Ranunculus circinatus, R. aquatilis, Plantago ma-
jor, Cerastium vidgatum, Veronica Beccahunga,
and Chri/santhemum leucanthemum in England
(Schwartz, '10, 'II, "14; Cook, '26, '27, '28. '33) ;
Callitriche stagnalis and Poa annua in France
(Maire and Tison, I.e., 'lib); Alisma Plantago in
New York, U. S. A. (Karling, '34).
Cook ('26) made extensive cross inoculation ex-
periments involving 16.5 individuals of different spe-
cies, 151 of which became infected with L. Junci
after four months. These plants included the hosts
of Schwartz's L. graminis, L. Bellidis, L. Menthae,
and L. Alismantis, and since Cook found no essen-
tial differences between these Ligniera species and
L. Junci, he concluded that they are identical. The
species which he found in Callitriche stagnalis was
likewise capable of infecting the same hosts ; and for
this reason he ('33) later concluded that L. radicalis
described by Maire and Tison in C. stagnalis in
France is also identical to L. Junci. The resting
spores of L. radicalis, however, are only 4- .5 /x in
diameter, while those of L. Junci range from .5 to
7 /x. This difference is not very great and may not
PLATE 1 1
Liffniera
Fig. 1. Zoospore highly magnified (Z/. .Tunc!: Cook, '38).
Fig. 3a. Zoospore outside of root hair; 3b, after entering
host cell (Cook, "36).
Fig. 3, 4. Developmental stages of amoebae and young
Plasmodium (L. (/ramini.i; Schwartz, '11).
Fig. 5. Young thallus with five engulfed alga! cells (L.
radicalis ; Maire and Tison, '11).
Fig. 6. Two amoebae approaching a central host nucleus
(L. fframinin; Schwartz, "11).
Fig. 7. Amoebae clustered around host nucleus {L. (/ra-
mini.'i Schwartz, I.e.).
Fig. 8. Young amoeboid plasmodium (L. (/rfiminis;
Schwartz, I.e.).
Fig. 9. Young plasmodium in root hair; nuclei with large
karyosome and abundant chromatin {L. .Junci; Cook, '3fi).
Fig. 10. Possibly schizogony of plasmodium {L. radi-
calis; Maire and Tison, I.e.).
Fig. 11. "Promitosis" of vegetative nuclei (L. (/rdminis;
Schwartz, I.e.).
Fig. 13. Single large plasmodium in a host cell. Nuclei
entering akaryote stage (L. fframini.i: Schwartz, I.e.).
Fig. 13. Akaryote stage; nuclei appear as clear spaces
{L. graminis; Schwartz, I.e.).
Fig. 14. Akaryote state; cytoplasm with numerous chro-
matic granules ; host nucleus densely chromatic in base of
cell (L. radicalis; Maire and Tison, I.e.).
Fig. 15-18. Successive stages of extrusion of chromatin
from the nucleus (L. .fund: Cook, "33).
Fig. 19. Prophase of heterotypic division (?) in a recon-
structed nucleus {L. .Junci: Cook, "38).
Fig. 30. Cleavage of plasmodium into zoosporangia; the
two large mitotic figures in upper left segments are equa-
torial plate stages of the first heterotypic division (?);
the remainder relate to homeotypic division (?) (L. .Junci;
Cook, "36).
Fig. 31. Cleavage into zoospores {L. .Junci; Cook, "38).
Fig. -23. Second mitoses prior to resting spore formation
{L. radicalis; Maire and Tison, I.e.). May possibly relate to
sporangia and zoospore development like in figure 30.
Fig. 33. Zoosporangia {L. Junci: Cook, '38).
Fig. 34. Empty zoosporangia {L. .Junci; Cook, '38).
Fig. 35. Plasmodium in swollen root hair tip {L. pilo-
rutn : Fron and Gaillat, I.e.).
Fig. 37. Cluster of empty resting spores in swollen root
hair tip (L. graminis: Schwartz, I.e.).
Fig. 38, 39. Small groups of resting spores (L. Minthae;
Schwartz, "14).
Fig. 30, 31. Types of resting spore clusters (i. graminis;
Schwartz, '11).
Fig. 33. Single resting spore {L. .Junci: Cook, "38).
Fig. 33. Resting spore ball filling host cell {L. Jsoetes;
Palm, '18).
Fig. 34. Cross section of a similar hollow resting spore
ball {L. Isoetes: Palm, I.e.).
Fig. 35. Loose chain of resting spores (L. Isoetes: Palm,
I.e.).
Fig. 3(i. Longitudinal section of hollow cylindrical rest-
ing spore cluster (L. radicalis: Maire and Tison, I.e.).
Fig. 37. Cluster of resting spores with host nucleus inside
(L. radicalis: Maire and Tison, I.e.).
Fig. 38. Resting spore clusters of L. piloruni in swollen
base and tip of root hair (Fron and Gaillat, I.e.).
Fig. 39, 40. Types of resting spore clusters (L. verru-
cosa; Maire and Tison, I.e.).
I.KiNIKltA
61
PLATE 11
Ligniera
62
PLASMOmOPHORALES
be sufficient reason for separating the two species.
Light appears to be the dominant factor in infection.
No infection occurs in roots exposed to light even
when other environmental conditions are optimum,
according to Cook ('27).
In this connection it may be noted that Hildebrand
('34', PI. I, fig. 5) observed cystosori of indefinite
size and shape in diseased rootlets of strawberries
in Canada. Whether or not these resting spores re-
late to Lif/niera or another genus is uncertain at
present, since Hildebrand made no further study of
the organism in question.
L. PILORUM Fion and Gaillat, 193.5. Bull. Soc. Mycol.
France H : ,390. PI. 10.
Resting spores aggregated into globose and ir-
regular clusters or cystosori, or lying end to end in
a linear series ; oval, spherical, 4—6 /t, or angular
and polyhedral when compressed together, with thin
Iiyaline smooth walls. Plasmodium filling the en-
larged base or tip of the host cell ; schizogony ques-
tionable ; Plasmodium apparently segmenting into
either zoosporangia or resting spores. Zoosporangia
(?) oval, spherical, angular and compressed, 4— 6 /x
(.'') with tliin, smootli hyaline walls, opening by the
rujjture of a thin localized area. Zoospores small,
pyriform, up to 1 /x (?) in diameter; flagellum of
same length as spore body.
Parasitic in the root hairs of Poa annua in France,
causing marked local hypertrophy ( ?).
Fron and Gaillat's drawings and descriptions of
the developmental stages of this species are very
brief and inadequate, and it is not clear whether the
zoos]Jores arise from germinating resting spores or
zoosporangia like those described by Cook ('26) for
L. Jnnci. The latter view seems more plausible be-
cause figures 7 and 8 by Fron and Gaillat show what
appears to be several zoospore initials within a single
unit of the aggregate; whereas the resting spores of
most plasmodiophoraceous species are now rather
generally believed to form but one zoospore apiece.
If Fron and Gaillat's measurements are correct, this
species is characterized by unusually small zoo-
spores. Cook ('26, '33) regarded L. piloriim as syn-
onymous with L. Jiinci, because it also occurs in Poa
annua and agrees with the latter in life cycle and
resting spore size. The chief differences are zoospore
size and the fact that L. pilorum causes hy])ertrophy
of the host cell, according to Fron and Gaillat. Cook
maintained that such hypertrophy is not due to the
stimulus of the parasite but that L. pilorum may
fortuitously infect root hairs which are already
swollen. In further support of his belief that the two
species are identical, he Jjointed out that L. Junci
occasionally attacks swollen hairs also. Schwartz
('11) likewise observed that normally swollen root
hairs (fig. 27) may sometimes become infected witli
L. Junci. It seems almost too accidental, however,
that all the infected root hairs shown in IVon and
Gaillat's (fig. 1) are greatly enlarged at the ti)).
Nevertheless, it is not entirely improbable that L.
Junci and L. pilorum are identical, but until more is
known about the latter siiecies and host range, its
identity and validity will remain questionable.
L. VERRUCOSA Maire and Tison, I.e. 1911, Ann.
Mycol. 9: -'35. PI. 11, fig. 39-41; pi. 12, fig. 43-46.
Resting spores occasionally aggregated in a linear
series, more often in globular, ellipsoidal solid,
rarely flattened, and disc-shaped, or hollow balls ;
resting spores oval, spherical, 4— .5 /x in diameter,
angular and polyhedral when compressed, with
fairly thin, hyaline verrucose walls. A})parently giv-
ing to rise to zoospores in germination, which infect
the host. Plasmodium partly or completely filling the
host cell ; giving rise to one or more cystosori ; schi-
zogony reduced or lacking entirely. Zoosporangia
and zoospores unknown.
Parasitic in the root hairs and roots of Veronica
arvensis (Maire and Tison, I.e.), Beta vulgaris,
Chenopodium album, Bromus sp., and Fcstuca sp. in
France (Guyot, '27), without causing hypertrophy
of the host tissue.
This species is imperfectly known at present, and
many of its critical stages remain to be studied. As is
sometimes true of the previous species, the shape and
structure of the cystosori de])end to a large degree
on the character of the host cell. ^^Mlen the cystosori
occur in elongate narrow root hairs, they may consist
of a linear series of resting spores, but if they de-
velop in the cortical parenchyma cells, they usually
have the form of more or less solid, globose and ellip-
soidal balls.
Guyot regarded this species as a variety of L.
Junci, because the characters of his specimens of L.
verrucosa seemed to merge imperceptibly with those
of L. Junci. Cook ('33), after examining material
submitted by Guyot. and Claire and Tison found no
difficulty in distinguishing L. Junci and L. verrucosa.
However, the warts on Guyot's specimens were
found to be much less pronounced than those on
Maire and Tison's material. Palm and Burk did not
regard the presence of warts as a specific character,
since in a single species of Sorosphaera on T'eronica
americana they found both smooth and warty spores
with all degrees of gradation between the two types.
Hence, they regarded L. verrucosa as identical to L.
radicalis or L. Junci. The development of smooth and
warty spores in a single species is not at all uncom-
mon among fungi, and Palm and Burk were probably
right in their conclusions. !More intensive study of the
develojjment, variations, and host range of L. verru-
cosa is. however, essential.
L. ISOETES Palm, 1918. Svenska Bot. Tidsskr. 12:328.
Fig. 1-3.
Resting spores sometimes in more or less loosely
aggregated clusters, more often in hollow balls which
fill the host cell and conform with the latter's shape.
Resting spores oval, almost spherical, angular and
l)olyhedral when compressed, .5X6—8 fx, with thin,
smooth brownish-colored walls. Plasmodia jjartly or
POLYMYXA
G3
oomiiK'tcIy tilliiii; tin- host cell. ZoDspiiriiiisiia ;m(]
zoospores unknown.
I';ir;isitii' in tlic Ic.iMs and roots of Isoftts lacii-i-
tris in Swi'ilin (^I'alni. l.o. ) and Ni'W .Icrsi-y. U.S.A.
(Karling. "Si), (■.•luslns; larjrf. dark spots in tin- iiost
tissuo but no hypcrtropliy.
This spi'firs is so littK- known at jnxscnt that its
identity is very doulitful. As Cook pointed out, it may
well he identieal to L. Jiinci, but some of the rest-
injl si)ore elusters tifiured by Palm are strikini;ly
like those of speeies of Soroxphncra and Mrriihraiid-
soru.i. The jiresent writer's observations on this s))e-
cies in 1931- were very limited, and sinee then he has
not added any further data on its structure ,ind de-
velopment.
L. VASCULARUM (Matz) M. T. Cook (\'9) does not
appear to In- a valid species. See PlimmndUtjihom vtm-
ritUivum.
.\DDiTiox.AL bibliography: Lic/iiicm
Cook, \V. H. J. 19.'(>. Trans. Brit. Myool. Soc. 11 ; 19(>. 19.^,
I hill. 12: 2SJ.
. 19iSa. lUiU. Soi-. Mycol. France U: 1().>.
. 19.'81>. Ann. Hot. i2: 347.
-. 19:}-'a. Hoiijr Koiifr Nat. Suppl. No. 1 : 2i).
. 19:l.'l). .lour. Dei)t. .\pr. Porto Rico 1(>: +09.
, 19:«. tllaniorau County Hist. Nat. Hist. 1: ;.'13.
. 19:U. Watson's .Microscope Record — : 'i, 9.
Guyot, .\. I.. 19.'7. Rev. path. Ent. Afrr. It: 17(>.
Hiidehrand, A. A. 19;U. Canadian .lour. Res. 11: 2i.
KarlinfT, .T. S. 1934. Torreya 34: 13.
Palm, H. T., and .M. Hurk". 1933. Arcli. Protistk 79: 363,
Smith, .\. I.., and .1. Ranisliottom. 1917. Trans. Brit. Mycol.
Soc. (>: -'31.
POLYMYXA
Lcdinglmm, llKiS, Phvtopath, 23: 20.
(I'LATF. 12, FICS. 1-22)
Cvstosori or restinjj spore clusters indefinite in
size and .shajjc, without a common membrane ; formed
by cleavage of a naked multinucleate plasinodium.
Resting spores few or numerous, variable in shape,
Zoos)>orangia conjoined in a more or less linear
series : formed by tin- se))t.ition of an elongate, lobed,
irregul.-ir and tubular thallus, which may extend
through one or more host cells: exit tubes one or
more, variable in length, and septate. Zoospores from
resting spores and zoosporangia biflagellate and
heterocont.
Poliimjisa is a monotypic genus, and like Sponc/o-
spora, Lifiiiirra, Plasmodiophora, etc., includes zoo-
sporangial and naked ))lasni<)dial stages in its life
cycle. The zoos))ores a))parently jienetrate the host
cell wall directly (fig. (i, 7) aiul lie in the host ])roto-
plasm as small globose bodies. As is shown in figure
8, they soon begin to increase in size and elongate,
and as growth continues they become lobed (fig. 9,
10), branched, irregular, and tubular, and sometimes
extend through the host walls into adj.icent cells. In
this manner l.irgi- septate thalli .are deM-loped which
;ire couipletely surrounded from the begiiniiug by ;i
thin hyaline w.ill .lud closely resend)lc the thalli of
Srplol pidiiim, I.nifcniiliiim, M iizociji'ium, etc. The
segments of the th.alli beeonu' zoosjMjrangia (fig. 1 1 )
.-iiul dcvcloj) one or more septate exit tubes of vari-
able length. The protopl;ism then undergoes cleav-
;ige into zoosjiores which exhibit considerable move-
ment within the /.oospor.angia before emerging.
When mature, they emerge fully formed in succes-
si(Ui from the exit tubes, become amoeboid for a few
nu)uients, and swim away.
The zoospores are ))yriform and ov.ite in slia))e,
usually uninucleate, and ])Ossess a long and short
flagellum attached to the nucleus near the anterior
end of the spore body (fig. 1-t). A few binuclcate
zoospores with four flagella have been found, but
I.edinghain v\'as not certain whether they were the
result of unequal cleavage or fusion of two biflagel-
late s))ores. During active swimming the flagella may
extend out in front, but the zoospores are usually
propelled from behind, according to Ledinghani.
They rotate on their axes or roll over in swimming,
and their motility appears to be somewhat slower
than that of most chytrid zoospores. After an active
swimming stage of about two to three hours, the
flagella disappear, and the zoospores become amoe-
boid again (fig. o). In this state they move about by
pseudopodia, and may often engulf small food par-
ticles or objects. These amoeboid zoosjiores may
penetrate and reinfect host cells, but it is not certain
from Ledingham's account whether tliey give rise to
another crop of zoosjiorangia or develop into large
multiinicleate plasmodia. A))parently they ]iossess
both ))otentialities.
The thallus from which the resting sjiore cluster
is formed begins in the host cell as a naked uninu-
cleate amoeba (fig. 12), and at no time does it jiossess
a membrane or wall. As it increases in size, repeated
nuclear divisions occur, and a multinucleate Plas-
modium is soon formed. Its shajjc changes constantly
as it moves about in the host cell. It may frequently
be long and tenuous, extending the full length of the
host cell, or form a crescentric mass around the host
nucleus with long thread-like, r.idiating pseudo])odia.
These pseudo))odia are later retracted as the jjroto-
))lasin becomes denser, and the plasmodium may then
segment into a number of portions or meronts (fig.
18) which often lie in rows or closely ))aeked grou))s
in the tr.ichcal and cortical cells. Occasionally fusion
of several separate ))l.asuu)dia may occur in the same
host cell (fig. II-). but I.edingham was not certain
whether these were th.alli of ojiposite sex or merely
meronts derived by division of a common schizont.
He was unable to count the chromosomes in the nu-
clear divisions preceding resting s))ore formation
and accordingly found no evidence of meiosis at this
stage.
In the early stages of growth the ))lasuu>dium is
very vacuolate, but as devcloiiment |)roceeds the
vacuoles decrease in size. As a result the thallus be-
comes more granular and refringent in texture and
6*
PLASMODIOPHORALES
appearance. Very shortly thereafter progressive
cleavage (fig. 15) begins and delimits the individual
resting spores which remain in continuity as clusters
(fig. 16). The resting spores are usually uninucleate,
and in germination each gives rise to one zoospore
(fig. 21 ) which is similar in size, shape and structure
to those formed in the zoosporangia.
Polymyxa is strikingly similar to Ligniera in size
and shape of its cystosori, size, shape and arrange-
ment of resting spores, and by its failure to cause
hypertrophy of the host. It differs primarily by the
shape and size of its zoosporangia, but this differ-
ence may be only specific instead of generic. The
lack of schizogony in Polymyxa, which Ledingham
cited as an additional difference, may not prove to be
of great significance, since its presence in Ligniera
also is still quite doubtful.
P. GRAMINIS Ledingham, I.e.; 1939. Canadian Jour.
Res. C, 17:50. PI. 1-3.
Resting spores spherical, polygonal, 4-7 /tt ; con-
tents hyaline and ref ringent ; inner wall hyaline,
outer wall smooth, yellowish-brown. Zoosporangia
lobed. oval, uteriform and irregular; exit tubes of
variable length. Zoospores broadly spindle-shaped,
ovate, pyriform, I— .5 jj. in diameter; flagella 16—20 jx
and 4— .5 /x long respectively ; zoospores emerging
fully formed and swimming directly away ; rolling
over and over while in motion, intermittently amoe-
boid. Plasmodium variable in size and shape, often
filling host cell, amoeboid in shape and motion.
Parasitic in the roots of Triiicum aestiz'iivi, T.
durum, Hordeum vulgare, and Secale cereale in
Canada.
Ledingham found similar resting spores in roots
of species of Agropyron, Scolochloa, Rumex, and
Impatiens, but since no sporangia were present, he
was uncertain about the relation of this fungus to
P. graminis. He reported further that species of
Juncus and Poa in which Ligniera parasites occur
failed to become infected when grown witli parasit-
ized wheat roots. He accordingly regarded P. grami-
nis as an obligate parasite. Truscott ('34) also re-
ported what he believed to be P. graminis in roots of
strawberries in Canada.
DOUBTFUL GENERA
Under tliis title are presented four genera about
which there has been much disagreement and con-
troversy. Rhi-omyxa, Sorolpidium, and Anisomyxa
occur in the roots of higher plants, do not cause hy-
pertrophy, and form cvstosori of indefinite size and
shape. In these characters they resemble Ligniera
and are regarded by most recent investigators as
synonyms of this genus. Trematophlyctis, however,
parasitizes leaves and petioles and causes marked
hyixrtrojjhy. There is very little evidence in Patouil-
lard's account to warrant inclusion of this genus in
the Plasmodiophoraceae, but inasmuch as Palm sub-
sequently reported it to be "an undoubted member of
this family" a brief description of its life cycle is
herewith presented. The present writer is in agree-
ment with Maire and Tison's, Ciuyot's, Cook's, and
Barrett's interpretation of Rhisomyxa, Sorolpidium
and Anisomyxa, but further intensive study may pos-
sibly reveal distinct generic differences. For this rea-
son thev are described and figured separately, so that
research students may judge independently the evi-
dence of identity and relationships of these genera.
RHIZOMYXA
Borzi, 1884. Rhizomyxa, nuova ficomicete, Mes-
sina.
(plate 12, fig. 23-30)
Plasmodia partly or completely filling host cell,
variable in size and shape ; forming at maturity
either single large zoosporangia or sporangiosori
composed of small zoosporangia. or cystosori ( ?).
Cvstosori and resting spores poorly known or doubt-
ful.
R. HYPOGEAE Borzi, I.e., pi. 1, 3.
Sporangiosori one or more in a cell, spherical,
ovoid, irregular, elongate, sometimes made up of lin-
PLATE 12
Pnlymy.ra graminis
(All figures, except 30 and -21, after Ledingham; fig. (i, 7,
8, 17, 19 and il drawn from photographs.)
Fig. 1-3. Biflagellate heterocont uninucleate zoospores.
Fig. 4. Large binucleate tetraflagellate zoospore.
Fig. j. Living, amoeboid zoospores.
Fig. 6. Zoospore on surface of root hair.
Fig. 7. Zoospores after entrance Into root hair.
Fig. 8. Stained zoospore inside of cortical cell shortly
after penetration.
Fig. 9-11. Stages in development of zoosporangial thalli.
Fig. 12. Mature zoosporangia with exit tubes passing
through adjacent cells.
Fig. 13. Naked myxamoeba during period of active
growth.
Fig. 14. Segments or meronts formed by division of Plas-
modia.
Fig. 15. Same cell as in fig. 13 after meronts have coa-
lesced to form a large plasmodium.
Fig. K). Plasmodium just I'.rior to cleavage into incipient
cystosori.
Fig. 17. Cleavage of plasmodium into cvstosori.
Fig. \S-2\. Variations of cystosori. (Fig. .'0 and 2\
drawn from material presented by Ledingham.)
Fig. 22. Zoospore from resting sjiore stained in Into.
Hhh(>myx<t hypogeae
(.\11 figures after Borzi)
Fig. 23. Zoospore.
Fig. 2\, 2o. Germination and infection stages.
Fig. 2ti. Plasmodia within liost cells.
Fig. 2", 2S. Sporangiosori and sporangia.
Fig. 29. Emergence of zoospores.
Fig. 30. Zoospores from sporangia.
DorUTFCI. (iKXKUA
TLATK 12
C.j
Polymyxa, Rhizomyxa
66
PLASMODIOPHORALES
ear rows of sporangia. Large single zoosporangia
spherical, oval and elongate, produeing up to 21' zoo-
spores ; zoosporangia in sporangiosorus usually
small, spherical and ovoid. 5-6 /x in diameter with
thin, hyaline, smooth walls and a short exit pupilla;
forming usually 1—2 zoospores which emerge fully
formed and swim direeth' away. Zoospores pyriform,
egg-shaped and small; flagellum 10—1.5 /x. Cystosori
( .'') of indefinite size and shape, 20—60 /x, in diameter.
Resting spores oval and spherical, 8 /x; germination
unknown.
Parasitic in the cortical cells of young roots and in
root hairs of Agrostis alba, Aira Cupaniana, Briza
viaxlma. Poa annua, Setaria glomerafa, Stellaria
media, Silene coloraia, Capsella bursa pastoris, Bis-
cutella lyrata. Delphinium longipes, Lotus ornitho-
podioides, Medicago tribuloides, Trifolium resupina-
tum, .Inagallis ari'ensis, Borrago officinalis, Dinaria
reftejca, Barisia Trijcago, hamium amplexicaule,
Fedia cornucopiae. Campanula dichoioma, Calen-
dula arvensis, and Erigeron canadensis in Italy
(Borzi, I.e.) ; Triglochin palustre, Juncus Gerardi
and Ranunculus sceleratus in Germany (Fischer,
'92) ; in numerous species of grasses in Belgium (De
Wildeman, '93) ; and Stellaria media in the U.S.A.
(Barrett, '35), without causing hypertrophy of the
host cells.
The above diagnoses differ somewhat from those
given by Borzi. since it is now generally agreed that
the antheridia and oogonia which he described relate
to another organism. The plasmodia (fig. 26), spo-
rangiosori, (fig. 27, 28) and zoospores (fig. 23, 36),
however, doubtless relate to a species of the Plas-
modiophoraceae. The identity and relationship of R.
hypogeae have been the subject of lengthy discussion
and speculation since the time of its discovery in
ISS-t. Borzi was uncertain of its taxonomic position,
but in 1892 Fischer pointed out that it is probably a
combination of two or more fungi, Olpidium- and
Oipidiop.iis-\ike species and a Jf'oronina-like fungus.
Because of the ])resence of sporangiosori and cyto-
sori, he placed it next to IVoronina in the Syncliy-
triaceae. A year later de Wildeman found it in the
roots of various grasses in Belgium and from a study
of the plasmodia and sporangiosori came to the same
conclusions as Fischer concerning its identity and re-
lationship. Schroeter ('97), however, emphasized
the heterogamous type of sexual reproduction de-
scribed by Borzi and included 7?. hypogeae in the
I.agenidiaceae. In 1911 INIaire and Tison pointed out
the similarities between certain of its stages and
those of their new genus Ligniera, and suggested that
R. hypogeae is ])robably a combination of L. verru-
cosa and another fungus. This viewpoint was sub-
sequently supported by Guyot ('27), and Cook ('33).
Minden (11) excluded the sexual phase as relating
probably to a species of Myzocytium, included the
remaining stages of Borzi's fungus in the Synchy-
triaceae, and pointed out that it is very similar to
Worouina except for its anteriorly iniiHagellate zoo-
sjiores. Fitzpatrick ('30) believed that the large zoo-
sporangia relate to Olpidium. In more recent years
Barrett has thrown further light on the identity of
Borzi's fungus. He found a species of Ligniera in
roots of Stellaria media which was frequently asso-
ciated with antheridia, oogonia and oospores of the
type described by Borzi. The zoosporangia of what
he called Ligniera sp., are comparatively large and
isolated with fairly broad exit tubes and form ante-
riorly biflagellate zoospores as in Plasmodiophora,
Polymyxa, Octomy.ra, etc. Antheridia and oogonia
may occur in association with Ligniera or are iso-
lated in separate roots, and Barrett thus concluded
that the two are unrelated. In his opinion Borzi's
fungus is a combination of Ligniera and a species of
the Lagenidiales ( Ancylistales). Barrett's observa-
tion is particularly noteworthy in that it is the first
record of biflagellate zoospores in the genus Lig-
niera. The early suggestion of Maire and Tison that
R. hypogeae is in part a species of Ligniera thus ap-
pears to be confirmed by the observations of Barrett.
It is further supported by the fact that this fungus
does not cause hypertrophy of its host cells and oc-
curs in some of the hosts which harbor other species
of this genus. Whether or not it is identical to L.
iwrrucosa as Maire and Tison, and Cook suggest,
however, is not certain at present, since well-defined
cystosori and resting spores have not yet been de-
scribed.
SOROLPIDIUM
Xemec, 1911. Ber. Dcut. Bot. Gcs. 29: -18. 1911b,
Bull. Int. Enip. Fran. Joseph Acad. Sci.
16: 69.
(plate 13, FIG. 1-25)
Cystosori one or more in a cell, indefinite in size
and shape; flat and almost round, oval, elongate,
angular and lamellate ; consisting of few to many
resting spores arranged in linear series, in single or
double, flattened layers, or irregular masses. Resting
spores variable in size and shape, usually polygonal
or hexagonal at first but becoming knobby and some-
what stellate at maturity ; usually producing several
zoospores in germination. Plasmodia one to several
in a cell, variable in size and shajie, often lying in
the central vacuole or surrounding the latter as a
broad band or plate ; ])roducing either zoosporangia
or cystosori ; schizogony unknown. Zoosporangia one
or more in a cell, spherical, oval, and elongate ; pro-
ducing few to many zoospores which emerge through
an irregular opening in the sporangium wall. Zoo-
spores oval, obpyriform, uniflagellate (.''), size un-
known.
S. BETAE Nemec, I.e., pi. 1, 2, text-figures 1-6. Ibid.
lH:-2i.
Resting spores 1.2X5 fi- — 1.6X'5-2 fi. For further
details see the generic diagnosis above.
Parasitic in the roots of Beta vulgaris^ in Czecho-
• Cook (";36) reported that Xemee found the parasite in
B. mnritimri, which is obviously a mistake.
DOlDTFn, (iKNEHA
Slovakia (Xcnicc, I.e.). tlie U. S. .\. (Rawliiigs. '25),
and France ( .') (Cuyot. '27) witliout (•.nisiiiK liyper-
trojiliy of tlie invaded tissues.
Si>rolpitliinii liftar lias lieen tlie sulijeet of eon-
siderable diseussion sinee tlie time of its discovery liy
N'eniee. He described it as a species of the Cliytri-
diaccae with close iirtiiiities with tlie l'lasniodi(i])lio-
raceae, hut hecause of the jircsenee of lar«e. tliiii-
walled 7.oosi)oraiigia he did not l)elie\ e it siiould he
included in this family. Since similar zoosjiorangia
have subsequently been found in several genera of
the l*l;isniodiophoraceae. this obji-etion is no longer
significant. The large, thick-walled, stell.-ite resting
cysts surrounded by a thin envelope which Neniec
figured are now generally recognized as relating to
Olpidium, and outside of these cysts there is nothing
in the life cycle of Sorolpidium, as described by
Nemec. which excludes it from the Plasmodiopho-
raceae. The presence of large holocarpie zoospo-
rangia and multinucleate resting spores which pro-
duce several zoospores is in line with more recent
discoveries in other genera of this family. Saccardo
('26) likewise included .S'. Brtae among the Chytri-
diales. Winge ('13), however, asserted that it is
closely related to Pi/rrho.soriis and the Plasmodio-
phorficeae. Subsequent workers, on the other hand,
have questioned the identity of Sorolpidium as a dis-
tinct genus of this family and contended that it re-
lates to Lif/niera. Cook ('2(3) regarded it as a combi-
nation of Lif/niera and Asteroci/sii.s, a view which
Giiyot sui)])orted in 1927. The latter worker suc-
ceeded in inoculating roots of Beta vulgaris with L.
verrucosa and Asteroci/stis radicis, and concluded
that Nemec's fungus is merely an accidental associa-
tion of these two species in the same host tissues.
Cook ("32, '33) later incorporated Sorolpidium in
Lif/niera and classed S. Betae (pro parte) as a syn-
onym of L. J unci. In the sha])e of its cystosori and
the fact that it docs not cause hypertrophy of the
host tissues .V. Betae is very similar to species of
Lif/niera. Should it prove to be a species of this genus
its identity to L. Junci and L. verrucosa will none-
theless remain somewhat questionable, because
Nemec unfortunately did not give any measurements
of the sjjorangia and zoospores.
The life cycle of .S'. Betae is similar to that of other
])lasmodio])horaceous si)ecies. The earliest recogniz-
able stage consists of a uninucleate oval or spherical.
highly vacuolate thallus (fig. 1) which us\ially lies in
the primordial utricle of the host cell. This thallus is
probably the result of zoospore infection, although
Nemec was uncertain whether the zoos|)ore enter di-
rectly or first become amoeboid. Within the host the
thallus grows in size (fig. 2. 3. K and 5), becomes
multinucleate and i)lasmodium-like. The division of
the nuclei (fig. 3) during this developmental phase
appears to be "promitotie,"' according to Nemec's
figures, and no sharply-defined chromosomes are
formed. One or more plasmodia (fig. I. o) may occur
within a single host cell and are usually embedded in
' Cook {'J>i) stated that N'eniee did not figure "promito-
sis," but he obviously overlooked figure 3.
the host ))rotopIasm or occupy Ihc icntrjil vacuole.
They may be spherical. o\al, clongati', or take the
shape of the cell which they occupy. Sometimes, the
))lasmodium may form .i broad band or ))latc around
the vacuole (fig. 5).
.\t maturity the ))lasuu)(iiuui develops .i rrlati\ely
thin, enveloping nienibranc and may be transformed
directly into a /.oos|)orangiuni. In tiiis respect Sorol-
pidium differs from I'lasmodiophora, Lii/iiiera, and
Octom/ixa, where the plasmodium is reported to
cleave into a number of uninucleate segments which
develop into zoosjiorangia. This difference suggests
perliaps that the zoosjiorangia (fig. (i, 7) which
Nemec described may relate to a species of Olpidium
(.isteroci/stis) with large stell.ite resting sjjores. It
is to be noted in this connection, however, that the
sporangia of Olpidium usually form more or less
elongate exit tubes, which are lacking in Nemec's
■S'. Betae. On the other hand, Nemec may have over-
looked the cleavage stage of the plasmodium which
results in the formation of several zoos))orangia. His
text-figure .5 suggests this possibility. At any rate,
the protoplasm of the zoos))orangium cleaves into un-
inucleate segments (fig. 6, 7) which become zoo-
spores and emerge through an irregular opening in
the sporangium wall. The zoospores from such spo-
rangia are usually uninucleate, oval or pyriform
(fig. 8) and unifiagellate {?). Unfortunately Nemec
did not say whether they were anteriorly or pos-
teriorly flagellate, which would have settled conclu-
sively their identity as well as that of the large zoo-
sporangia shown in figures 6 and 7. If these zoo-
spores relate to a plasmodiophoraceous sjiecies they
will doubtless prove to be anteriorly bifiagcllate and
heteroeont.
In other mature plasmodia which occur in almost
emjity host cells. Nemec found that the nuclei lacked
nucleoli and were comparatively jjoor in chromatic
material (fig. 9). Peripheral chromosomes later ap-
peared (fig. 10). and the nuclei divided in regular
mitotic fashion (fig. 11-15). The appearance of
these nuclei and their manner of division are very
similar to what has been described in most of the
other genera, and suggests that figures 9 to 1.5 relate
to the so-called "akaryote" stage and ])ro))hases of
meiosis preceding sporogcnesis. Some of the nuclei
in figure 10 have six chromosomes. The same num-
bers are present in figures 11 and 15. but whether or
not this is the basic number in Sorolpidium is uncer-
tain. Nemec described a second mitosis in such plas-
modia in which the chromosomes are larger, elongate,
and rod-shalied. but it is difficult to reconcile his con-
clusions about this division with ))revious and subse-
quent descri])tions of the hoineoty|)ic mitosis in other
genera.
These jilasmodia. nonetheless, devcloji a thin en-
veloping membrane and cleave into uninucleate seg-
ments (fig. 16), which form fairly thick walls and
become resting spores. The envelo))ing membrane
soon disappears, but the resting s|)ores remain at-
tached and thus form cystosori of various sizes and
shapes (fig. 17-21). They may consist of a linear
68
PL ASMODIOP MORALES
row of resting spores (fig. 19), double rows (fig. 18,
24), or flat, rounded or irregular masses (fig. 17, 20,
21 ). When first formed the resting spores are usually
polygonal (fig. 17), but later they become more glo-
bose. As the}' mature they become knobby and some-
what stellate (fig. 18, 19, 20, 22, 23) with intercel-
lular spaces between them. Single isolated resting
spores may be formed occasionally (fig. 23), and
among the normal-sized spores in a cystosorus un-
usually large ones may sometimes occur as is shown
in figure 17. In these respects S. Betae shows the
same variations as other genera.
Since the resting spores function as sporangia in
germination, Nemec called these aggregates spo-
rangesori. In germination the resting spores increase
in volume and become more rounded in outline (fig.
17), their nuclei divide, and the protoplasm cleaves
into uninucleate segments which round up (fig. 22)
and become zoospores. An opening in the spore wall
is soon formed through which the zoospores emerge
(fig. 21). The number of zoospores formed varies
with the size of the resting spores. Nothing is known
about the size of these zoospores, but they are prob-
ably similar to those formed in the large zoospo-
rangia. Nemec found no evidence of gametes and
sexual fusion in S. Betae.
Like sjjecies of Lic/niera, S. Betae causes no hy-
pertrophy or other malformations of the invaded tis-
sues. In fact, parasitized rhizodermal cells may re-
main alive longer than non-infected cells, according
to Nemec. The presence of the parasite, however,
causes an accumulation of cytoplasm in infected cells
and enlargement of the host nucleus (fig. 1, 5). The
latter mav often become irregular and develop an
unusually large nucleole. As the plasmodia mature
the host protoplasm is reduced to a thin parietal
layer and eventually disintegrates. The entrance of
the zoospore through the cell wall often leads to a
marked reaction. As is shown in figure 25 the en-
trance hole becomes plugged up and a conspicuous
thickening around this plug is formed on the inner
peri])hery of the wall.
ANISOMYXA
Nemec, 1913. Bull. Int. Empr. Fran. Joseph
Acad. Sci. 18: 18.
(plate 13, FIG. 26-1.5)
Plasmodia usually solitary, partly or almost com-
pletely filling host cell and conforming with the lat-
ter's size and shape ; schizogony unknown : cleaving
into groups (sporangiosori) of small and large zoo-
sporangia. Sporangiosori usually solitary, rarely
more than one in a cell ; indefinite in size and shape ;
spring and winter sporangiosori composed of small
and large zoosporangia respectively. Zoosporangia
variable in size, exit papillae or tubes lacking; pro-
ducing four or more uniflagellate ( .'') zoospores. Cy-
stosori made up of relatively thick-walled resting-
spores ; germination unknown.
It is not certain from Nemec's account whether or
not cystosori composed of thick-walled resting spores
are formed in this genus. He reported that the Plas-
modium divides into aggregates or sori of polygonal,
hexagonal and oval cells which are quite variable in
size. In spring and summer, sori of small and uni-
form cells are formed (fig. 41), while those produced
in the winter are made up of much larger cells (fig.
43, 44). In both types of sori, however, the cells are
uninucleate at first but later become multinucleate.
Because they have tiiin walls and produce several
PLATE 13
Soi'olpktium Betae
(All figures after Nemec)
Fig. 1. Cell of Beta vulf/aris with two uninucleate para-
sites.
Fig. i. Binucleate stage of S. Betae.
Fig. 3. Four-nucleate stage; nuclei dividing "promitoti-
cally" (?).
Fig. 4. Host cell with four plasmodia.
Fig. 5. A large band-shaped Plasmodium surrounding
the central vacuole.
Fig. 6, 7. Large and small zoosporangia with zoospores.
Fig. 8. Zoospores from sporangia.
Fig. 9. Plasmodium in which the nuclei lack large nu-
cleoli (achromatic stage?).
Fig. 10. Later stage; nuclei with parietal chromosomes.
Fig. 11-1.5. Division stages of such nuclei with six well-
defined chromosomes.
Fig. 16. Plasmodium cleaving into resting spores.
Fig. 17. Young cystosorus (?) with polygonal resting
spores.
Fig. 18-2-2. Cystosori of various sizes and shapes.
Fig. 19, 20, 22. Cystosori of mature knobby, stellate rest-
ing spores.
Fig. 22. Resting spores with zoospores.
Fig. 23. Single, isolated stellate resting spore.
Fig. 34. Cystosorus of empty germinated resting spores.
Fig. 25. Swollen cell wall at point of entry of zoospore.
Anisomy.va Plantaffinh
(All figures after Nemec)
Fig. 26. Uniflagellate zoospore.
Fig. 27. Biflagellate (?) zoospore.
Fig. 28. Small uninucleate thallus.
Fig. 29. Binucleate thallus with resting nuclei.
Fig. 30. Same with both nuclei dividing "promitoti-
cally" (?).
Fig. 31. Tetranucleate thallus with centrosomes and
astral rays.
Fig. 32. Equatorial plate stage of "promitosis" with
cap-like centrosomes at poles.
Fig. 33. Achromatic or "akaryote" (?) stage of nuclei.
Fig. 34-36. Prophase of meiosis (?).
Fig. 39. Mature multinucleate plasmodium with some of
the nuclei associated in pairs.
Fig. 40. Zoosporangia cleaving into zoospores.
Fig. 41. Spring sporangiosorus composed of small zoo-
sporangia.
Fig. i2. Sporangiosorus composed of sporangia arranged
in a linear series.
Fig. 43, 44. Sporangiosori of large multinucleate spo-
rangia.
Fig. 45. Cell with cyst-like sporangia.
nOfTlTFfl. r.^XEPA
69
PLATE 13
&
k
26
28
29
S>^
/fi^''^S:^
30
33
Sorolpidium, Aiiisoinvxa
70
PLASM ODIOPHORALES
zoospores Nemec regarded tliem as zoosporangia
and like in SorolpidUim named the aggregates spo-
rangiosori. It is not improbable, however, that some
of these sori may be cystosori of relatively thin-
walled resting spores, since in describing the cytol-
ogy of Anisomi/xa Nemec reported several nuclear
changes and appearances (fig. 11-15) which sug-
gest the meiotie prophases which precede sporogen-
esis.
Although his account of Anisomyxa is fragmen-
tary and not altogether clear, it is evident that
Nemec was dealing with a species of the Plasmodio-
phoraceae. Wliether or not it represents a new and
distinct geims, however, remains to be seen from fu-
ture studies. Nemec regarded Anisomi/jra as closelj'
related to Rhisomifxa and possibly intermediate be-
tween the Plasmodiophoraceae and S_vnchytriaceae.
Fitzpatriek ('30) discussed it as a doubtful genus,
while Cook ('32, '33) merged it with Ligniera and
listed A. Plantaginis {pro parte) as synonymous
with L. J unci. The latter worker had previously
('26, '27) found L. Junci in roots of Plantago major,
which doubtless influenced his belief that A. I'lanta-
gi7iis is a combination of L. Junci and a chytrid.
A. PLANTAGINIS Nemec. I.e., p. -21. pi. 1, -2. Text-figures
1-.).
Spring and winter sporangiosori variable in size
and shape ; irregular, elongate, and oval ; consist-
ing of a few to numerous sporangia. Zoosporangia
usually remaining attached together in a sorus ; poly-
gonal, hexagonal, oval or almost spherical with thin,
smooth walls ; spring zoosporangia approximately
4.5X6 /i, producing 4 zoospores; winter sporangia
10.5X15 /^) forming numerous zoospores. Zoospores
oval, 1.5X1-8 /i, spherical, 1.5 /j. in diameter.
Parasitic in the roots of Plantago lanceolata in
Czechoslovakia, without causing hypertrophy of the
invaded tissues.
The zoospores of A. Plantaginis are very small
and oval to spherical in shape (fig. 26). Nemec re-
ported them as uniflagellate, but he did not state if
the flagellum is anteriorly or posteriorly inserted.
It is to be noted here that he figured one zoospore
(fig. 27) which appears to be biflagellate. It is ac-
cordingly quite probable that when this species is
studied more intensively the zoospores will prove to
be anteriorly biflagellate and heterocont. Nemec pos-
tulated that zoospores of two sizes might be pro-
duced, because he found cleavage segments of un-
equal sizes in several zoosporangia.
Penetration of the parasite into the host cell has
not been observed. Nemec found small oval uninu-
cleate thalli in several host cells (fig. 28, 42) which
appear to have come from zoosporangia. Such tlialli
apparently grow in size as their nuclei divide and
eventually become multinucleate plasmodia (fig. 31,
39). The nuclear divisions (fig. 30, 32) in the devel-
oping Plasmodium resemble the so-called "promito-
sis" ty|je and are described by Nemec as vegetative
mitosfs in which eentrosomcs and astral ravs are
usually quite conspicuous (fig. 31, 32). Following
completion of the vegetative divisions the nuclei lose
their chromatin, and the nucleole is reduced to a
small globule (fig. 33). The cytoplasm, on the other
hand, becomes filled with small deeply stainable
granules. This stage is followed shortly by another in
which dense chromatic granules, rods, and bands
appear at one side of the nuclei (fig. 36, 37) and sug-
gest synaptic phases of meiosis. These stages initiate
the reproductive divisions, according to Nemec.
However, figures 33 to 38 are strikingly like the
"akaryote" phase and prophase stages of meiosis
which in other genera have been interpreted as ini-
tiating sporogenesis. It is not clear from Nemec's ac-
count whether these stages precede the formation of
spring or winter sori.
The mature plasmodium does not become envel-
oped by a wall like in Sorolpidium but cleaves di-
rectly into sporangia which remain aggregated and
form sori. The zoosporangia are polygonal (fig. 41)
at first but later become oval and spherical (fig. 40).
In the small spring sporangia, two nuclear divisions
of the mitotic tj'pe occur, and the protoplasm cleaves
into four segments which become zoospores (fig. 40).
In the larger winter sporangia numerous mitoses
occur, producing multinucleate zoosporangia (fig.
42—44) which give rise to numerous zoospores (fig.
21, 22). No exit papillae or tubes were observed by
Nemec and nothing is known about the emergence of
the zoospores from the sporangia.
Nemec found no evidence of sexual fusions in
Anisomi/.ra, but he pointed out that tlie nuclei in the
mature plasmodium (fig. 39) are often associated in
pairs, implying perhaps that karj'ogamy may take
place. This suggestion is further implied by his fig-
ures of synaptic (fig. 36. 37) and diakinetic (fig.
38) division stages. In addition to the two types
of sporangiosori Nemec also found several large,
sporangium-like oval cysts (fig. 45), 14.5- 20;it X
20-26 fi. which he believed might possibh' be cysto-
sori. Whether or not these are large isolated resting
spores of A. Plantaginis is not certain.
TREMATOPHLYCTIS
Pcatouillard, 1918. Bull. Soc. Mycol. France 34:
86, fig. A-G.
(plate 14. fig. 1-6)
Patouillard established this genus to include a spe-
cies, T. Tjcptodesmiae, which parasitizes petioles and
leaves of Leptoc/esmia congesta in Madagascar. His
diagnosis was based on dried material eollected by
V^iguier in 1912, and there is very little evidence in
his brief description to warrant inclusion of this spe-
cies in the Plasmodioplioraceae at the present time.
The infected leaves and petioles become thick, fleshy
(fig. 1,2), and reddish in color, and later numerous
round or irregular, 0.5 to 3 unn. high, solitary or ag-
gregated, open, aceium-likc pustules filled with yel-
low spores appear in the infected areas.
norirnii. (iKNi'.iiA
Tlio farli('>t kiunvn di'vcloiinifntal stajjos of '/'.
Lrpldilrsniitir consists of an tlliptical. rouiiil. or
irrojjiilar plasinoiliuin (?) which fills tlic hypcrtro-
phied host cell (fifc. !•)• Its protoplasm is honio-
pciK'ous, brownish, and slightly granular and not
enveloped by a distinct membrane With maturity
the protoplasm becomes more siramilar, and the en-
tire thallus segments into spores, which are at first
polygonal but later become oval and si)herical, 12-
1(5^. and develop smooth hyaline walls (fig. 5).
When mature they have a yellowish tint, and as the
sorus breaks open to the outside of the host it as-
sumes the structure and appearance of a cup-like
pustule tilled with pulvereseent spores (fig. 2). Ger-
mination of these sjiores has not been observed.
P;itouillard's figures and description of the sorus.
spore formation, and the appearance of the pustules
suggest that T. Lcptodtumiae may possibly be a spe-
cies of Si/iichi/triiim of the .S. decipifiis type which
forms open Jjustules. His figures of a naked plas-
modial stage and comparatively thiek-walled spores,
however, militates against this view, but in dried
herb.arium material it is obviously difficult to deter-
mine tlie ])resence or absence of an enveloping mem-
brane. .Saceardo ('31 ) listed T. Lepiodc.im'iae among
the IMasmodioi)horaceae. but Cook ('33) excluded
it. Palm (see Palm and Burke. '33) collected mate-
rial of a species closely related, if not identical, to
Tremaiophli/ctis on an unnamed host in southern
Madagascar, and his statement that it is an "un-
doubted member of this family" carries the implica-
tion tli.it be believed Patouillard's genus might be
valid. Lnfortunatcly Palm has jjublislicd nothing
addition.il on this fungus, and the status of Tremaio-
phli/cti.i will remain doubtful until more is known
about its life cycle.
In relation to these doubtful genera a discussion
of Pi/rrhosoriis .fuel may be logically presented at
this ))oint. although in so doing the author does not
imi)ly that it should be included in the Plasmodio-
])horaceae as this family is now recognized. This
genus was created by ,Juel ('01) for an orange-
colored species. P. marinus, which he discovered in
a red alga, Ci/stoclonium piirpiirascens, in Sweden.
Since he found it only in dead branches .luel con-
cluded that it is a .saprophyte, but Winge ('13) be-
lieved that during some of the developmental stages
reported by ,Iuel the organism may be ]);irasitic. P.'/r-
rhosoru.s- mariniix has never since been observed, but
because it includes several ])lasmodi()i)hor.iceous-like
stages in its life cycb- it merits consideration in any
discussion of the Plasmodiophorales. .luel was uncer-
tain about its taxonomic position, relationship, and
phvlogeny but jiointed out and discussed the charac-
ters it lias in common with Jf'oronina, Iihi:nmi/xa,
Trtramjixa, Pnifomi/sa, and other genera of lower
organisms. He particularly stressed the similarity of
its tvjjc of sjiorogenesis to that of Trtrnmi/.ra.
The life cycle of /'. marinus is as follows: In the
early developmental stages it consists of small globu-
lar thallus lying within the host cell (PI. 11-. fig. 8).
Such thalli may often be associated in pairs (fig. 9)
or groups, and .luel aeeordiiigly considered it ))os-
sible tiiat they may l.-itcr co.ilisee and form a large
pl;ismodium. The iminucleate thallus grows in size
as its nucleus enlarges (tig. 10) and app.arently di-
vides. Mitoses in the iilasmodium have not been ob-
served, and .hiel was uncertain as to the manner of
origin of the multinucleate stages. A later stage is
shown in figure 1 1 of a plasmodium with four large
nuclei. The developing plasiiiodia a|)pareiitly Iiavc
the .ability to dissolve intervening cell w.ills ( fig. 1 1 )
■and m.iy eventually occujiy several cells. Although
they may be distinctly amoeboid in shajie with nu-
merous blunt, pscudopod-like extensions and vacu-
oles (fig. 12, 13) it is not certain from Juel's account
that they move about and migrate from cell to cell
as in Pla.smodiophora, etc. No evidence of schizog-
ony was observed by .luel. but \\'inge interjireted
some of the uninucleate stages as ))robable meronts.
The mature plasmodium is multinucleate, vacuo-
late, and usually irregular in shape (fig. 12-1 t), and
just before sporulating forms an enveloping mem-
brane like Sorolpidiiim. Plasmodia which are exten-
sively drawn out and occupy several host cells may
accordingly ap))car lobed, irregular and tubular (fig.
18) after the wall has formed. Following this stage
the i)roto])lasm divides into uninucleate segments.
In this process no distinct cleavage furrows have
been observed. The jilasmodium appears to become
highly vacuolate (fig. If) during this process, and
the cytoplasm accumulates around the nuclei and
forms stellate i)roto])lasmie islands which resemble
somewhat the sporonts of Teirami/ja. These seg-
ments soon become almost spherical or spindle-
shajjcd (fig. If), and .luel thought that the latter
type of cells arc formed in ])lasmodia which are
highly vacuolate and scarce in cytoplasm. In addi-
tion to these two kinds of segments, irregular elon-
gate, oval and smaller ones may be formed, appar-
ently as the result of unequal cleavage, which finally
degenerate.
The si)herieal. 8 u. in diameter, and siiindle-shaped
segments are uninucleate, naked, and never develo))
a distinct wall. They aggregate to form a definite
sorus (fig. 1.5) and each cell soon divides into oetads
of s))ores as in Octomi/.ra, which led .luel to call them
spore-mother cells. In this jirocess of spore forma-
tion the nuclei divide mitotically (fig. 21-2f) and
each mitosis is followed by cell division. Definite
chromosomes (2 to .5) are formed on a sharply-de-
fined sjiindle during mitosis, and there is no evidence
of "promitosis." according to .Juel's figures. Each of
the eight naked s])ores so(Ui becomes tr;ins formed di-
rectly into a zoospore without developing ;i thick wall
and becoming dormant. The mature zoospores are
small, ijyriform. 4..5X2..') /x, with a tajiering end,
laterally biHagellate and isocont (fig. 7). In addi-
tion they ))ossess ;i brilli;int or.ange-colorcd s))ot or
globule which rtsembles the eye sjiot of algae and
lies at the point of insertion of the tlagella. The zoo-
spores a))]jarently infect the host cells and develop
into the small thalli shown in figures 8 and 9. Cysto-
72
PLASMODIOP MORALES
sori or resting spores have not been observed in P.
marinus.
It is apparent from this description that Juel's
fungns differs primarily from the valid species of
the Plasmodiophoraeeae by its laterally biflagellate,
isocont zoosjjores, naked spore-mother cells and
spores, lack of zoosporangia, resting spores, and by
its saprophytic nature. As .Juel emiihasized, the for-
mation of uninucleate spore-mother cells or sporonts
by fragmentation of the plasmodium and their sub-
sequent division into 4 and 8 cells is strikingly simi-
lar to spore development in Tetramy.ra. Had Octo-
mi/xa been known at that time .Juel would doubtless
have emphasized the relationship of his species with
the Plasmodiophorales even further. It is to be noted,
however, that in these two genera each mitosis in the
sporonts is not immediately followed by cell division
as in Pyrrhosoriis, and that the spores which are
formed encyst and pass through a dormant period
before giving rise to zoospores. It is possible that
under the conditions of .Juel's study the spores of
P. marinus failed to encyst and become dormant. It
is also possible that zoosporangia occur in this spe-
cies but were not present in Juel's material. In tiiat
event P. marinus would be very similar to Octomyxa.
However, its laterally biflagellate isocont zoospores
with an orange-colored eye-spot constitute a serious
obstacle to including it in the Plasmodiophorales at
present, unless, of course, .Juel was mistaken about
the relative lengths and insertion of the flagella.
These possibilities, however, are purely speculative.
On the other hand, the zoospores are similar to those
figured for species of the lower biflagellate Oomy-
cete-like fungi, but until more is known about P. ma-
rinus its relationship will remain obscure. Winge,
nonetheless, considered it closely related to the Plas-
modiophoraeeae and made extensive comparisons be-
tween its life cycle and that of Sorolpidiiim. He re-
garded the sporangiosori of the latter genus as homo-
logous with the aggregates or sori of spore-mother
cells of Pyrrhosorus, and believed that the absence
of wall around the sporonts in the latter is of minor
importance. Cook ('33), on the other hand, regarded
the relationship of Pyrrhosorus with the Plasmodio-
phorales as highly questionable.
BIBLIOGRAPHY : DOUBTFUL GENERA
Barrett, ,T. T. 193 j. Pliytopath. 25: 898.
Cook, W. H. I. 19-'6. Trans. Brit. Mycol. Soc. 11: 310. 1937,
11)1(1.1-2:282.
. 1933. Hoiifr Koiifr Xat. Suppl. 1 : 38.
. 1933. Arcli. Protistk. 80: 333.
Fischer, A. 1893. Kabenhorsts Krypt. 1, aht. +:67.
Fitzpatriok, H. M. 1930. The lower fungi — Phycomycetes.
New York : p. 03.
Guyot, A. L. 1937. Bull. Soc. Path. Yep. I'Ent, Agr. France
14: 181.
Juel, H. O. 1901a. Bill. K. Svensk. Yet.-.\kad. Hand. 26
afd. Ill, No. U: 1.
. 1901b. Rev. Mycol. 34: 111.
Maire, R., and A. Tison. 1911. C. R. .\cad. Sci. Paris, 153:
30G.
Minden, M. 191.5. Krypt. Fl. Mark. Brandenburg 5: 378.
Nemec, B. 1911. Osterr. Ungar. Zeitscbr. f. Zucker u.
Landw. 40.
Palm, B. T., and M. Burk. 1933. Arcb. Protistk. 79: 363.
Rawlins, T. E. 1935. Pliytopath. 15: 737.
Saccardo, P. A. 1936. Sylloge fungorum 34, sect. 1: 17. 1931,
Ibid. 35: 13.
Schroeter, J. 1897. Engler and Prantl, die Nat. Pflanzf. I,
1:5.
Wildeman, E. 1893. Ann. Soc. Micro. Beige. 17: 35.
Winge, O. 1913. Ark. f. Bot. 13, No. 9: 29.
EXCLUDED GENERA
Herewith are presented descriptions and illustra-
tions of three genera which have been included in
the Plasmodiophorales by various workers, prima-
rih' for want of a better group in which to place
them. Uniflagellate zoospores are reported to occur
in Cystospora but are apparently lacking in Sporo-
myxa and Peltomyces. Except for a multinucleate
plasmodial stage, resting spores, and the occurrence
of intranuclear mitosis and schizogony these genera
have little in common with the Plasmodiophorales
as this order is now generally recognized. They are,
nevertheless, described here so that their validity as
members of this order may be judged independently.
PLATE 14
Trematophli/ctis Leptodesmiae
(All figures after Patouillard)
Fig. 1. Leaves of L. congestu with galls.
Fig. 3. Portion of a branch with a large gall and three
open pu.stules.
Fig. 3. Section of a gall showing several sori.
Fig. 4. Naked plasmodium (?) filling greatlv enlarged
cell.
Fig. 5. Group of resting spores formed by segmentation
of Plasmodium.
Fig. 6. Individual resting spores.
Pyrrhosorus niariinis
(All figures after Juel)
Fig. 7. Laterally biflagellate isocont zoospores.
Fig. 8. Uninucleate tballus.
Fig. 9. Two paired young thalli.
Fig. 10. Uninucleate thallus with enlarged primary nu-
cleus.
Fig. 11. Four-nucleate tballus passing through cell wall.
Fig. 13. Jlultinucleate tballus.
Fig. 13. Multinucleate amoeboid thallus.
Fig. 14. Cleavage of tballus.
Fig. 15. A sorus of spore mother cells.
Fig. 16. Isolated spore mother cell.
Fig. 17. A sorus, the spore mother cells of wbieli liave di-
vided into groups of four daughter cells.
Fig. IS. Spindle-shaped spore mother cells (?) in a
branched tballus.
Fig. 19. Spindle-shaped spore mother cells and accessory
sterile cells in an elongate host cell.
Fig. 30. Sorus with spore motber and sterile cells.
Fig. 31. Sorus with spore mother cells undergoing mito-
sis.
Fig. 33-34. Mitosis and cytokinesis of s|)ore mother cells.
TIlKMATOl'llYLCTlS
73
-•«r
20^ '
23 23'
Trematophlyctis, Pyrrhosorus
74
PLASMODIOPHORALES
by research workers. Doubtless, there are numerous
other plasniodiaceous organisms wliicli resemble the
true Plasmodiophoraceae and simple fungi which
must eventually be given serious consideration by
mycologists and protozoologists, and it is hoped that
by presenting the available data here greater inter-
est and research may be stimulated in these border-
line organisms.
SPOROMYXA
Leger, 1908. Arch. Protistk. 12: 111.
(plate 13, fig. 1-25)
Sporomyxa was created by Leger for a virulent
parasite, S. Scauri, which he found in tlie coelome of
the imago of Scaunts tristis in Algeria. The parasite
has a predilection for the adipose tissue and may be
found in enormous numbers there. Unlike most plas-
modioplioraceous fungi, it destroys infected cells
completely without stimulating them to divide or
enlarge. The earliest known stage consists of a small,
naked, spherical, ovoid. 6—8 /j.. or spindle-shaped
body with an unusually large, 5 /a, nucleus and finely
granular cytoplasm (fig. 1). It does not appear to
have a sharply defined membrane and lies embedded
in the host cytoplasm. As it increases in size the nu-
cleus divides mitotically with an intranuclear spin-
dle (fig. 2), and tlie thallus becomes binucleate. In
this stage it may divide by binary fission (fig. 3).
Additional nuclear divisions occur (fig. i). and
larger, naked, multinucleate plasmodium-like thalli
are eventually formed (fig. 6). Leger found no thalli
with more than 8 nuclei, and he believed that from
this stage on the parasite undergoes schizogony into
uninucleate meronts or sporulates, so that thalli with
a large number of nuclei are never formed.
The mature thallus may be splierical, elliptical,
and sometimes amoebiform, according to the jiosition
its occupies in the host tissue, and although it may
have the shape and appearance of an active amoeba,
it does not move or undergo changes in form. Its cy-
toplasm is denser toward the center, but no distinct
endo- and ectoplasmic laj'ers are distinguisliable.
No wall or membrane is present, and the whole thal-
lus may be enveloped by the host protoi)lasm (fig. 6).
In addition to these thalli, Leger found otiier smaller
ones with numerous fat globules and chromatic gran-
ules in the cytoplasm and small nuclei which ap-
peared to be lacking in chromatin (fig. 7). He be-
lieved such thalli occur at the close of the vegetative
phase of iS'. Scauri and mark the beginning of sporo-
genesis.
Unlike the true plasmodiophoraceous genera, no
segmentation of the multinucleate thallus into nu-
merous separate spores or cystosori lias been ob-
served in S. Scauri. Resting spores, however, occur
very abundantly in the adipose tissue, but Leger was
not certain whether they are formed by eneystment
of vegetative uninucleate thalli or are the products
of more or less simultaneous schizogony of a multi-
nucleate body. He admitted the possibility of both
methods, but did not sliow any figures of the latter
process. The spores may sometimes occur in groups,
but it is not evident that these aggregates have been
formed by segmentation of a multinucleate Plasmo-
dium as in Plasmodia phora. The only developmental
stages of resting spores described by I-eger relate
to small, isolated spores. These are apparentlv
formed by the eneystment of uninucleate thalli dur-
ing which process the nucleus shrinks in size as chro-
matic material is extruded from the nucleole into the
cytoplasm (fig. 9-13). As this goes on, the wall
thickens and differentiates into a thick outer and a
thin inner layer. In bi- and multinucleate tlialli,
spore formation may be accompanied by nuclear
fusions (fig. 12. 13) of the type described by Prowa-
zek (0.5) for P. Bras.iicae. Leger interpreted these
fusions as representing rudimentary sexuality. The
majority of spores are ovoid, 8X 10 M> but they may
often be more elongate, iXS/i. spherical, obpyri-
form, constricted in the middle, and unusually large,
SO-iO /x (fig. 15-17). The small spores are usually
PLATE 15
Sporomi/x(t Scanri
(All figures after Leger)
Fig. 1. Uninucleate thalhis.
Fig. J. Mitosis witli intranuclear spindle and minute
chromosomes.
Fig. 3. Binucleate thallus undergoing binary fission.
Fig. 4. Mitosis in a binucleate thallus.
Fig. 5. Tetranucleate thallus.
Fig. 6. Large, amoebiform, eight-nucleate thallus witliin
host cell.
Fig. 7. Thallus with chromatic granules in cytoplasm;
nuclei without (?) chromatin.
Fig. 8-1:3. Successive stages in resting spore formation.
Fig. 13, H. Xuclear fusion (?) in resting spore.
Fig. 15-17. Large, abnormal resting spores.
S. Tertehronis
(All figures after Reitschel)
Fig. 19-30. Developmental stages of thallus.
Fig. 31. Synchronous nuclear division; polar and profile
views.
Fig. 22. Completion of cleavage into spore rudiments.
Fig. 2S. Later stage of same.
Fig. 2i, 25. Uni- and binucleate spores.
f'i/.s'/o.s'/iora hfitntd
(All figures after Elliott)
Fig. 30. Resting state.
Fig. :37. Amoebae.
Fig. 38-33. Nuclear division and multiplication.
Fig. 33. Sixteen-nucleate stage of thallus; nuclei of un-
equal size.
Fig. 3+. Migration of plasmodium through rootlet.
Fig. 33. Cells of host with amoebae and plasniodia.
Fig. 36. Root tip cells with plasmodium and amoebae;
nuclei of unequal size in plasmodium.
Fig. 37-41. Stages in cyst formation from a plasmodium.
Fig. 43. Row of cysts.
Fig. 43, 44. Formation in and Iil)eration of zoospores
from cysts.
Fig. 4J-47. Degeneration of cysts.
EXrU'DKl) OENERA
I'LATK ir,
Sporoniyxa, Cystospora
76
PLASMODIOPHORALES
uninucleate, but the abnormal ones may possess 2
to 30 nuclei scattered about or aggregated in groups.
The wall of the spore is hyaline, streaked, and thick,
and by treatment with iodine and sulphuric acid it
assumes a bluish tint, indicating the presence of
cellulose.
A second species, S. Tenebriones, was found by
Reitschel ('36) in the fat bodies, ovaries, and con-
nective tissues of the larvae and imago of Tenebrio
molitor. The life liistory and development of this
species (fig. 18—25) are similar to tliose of S. Scauri
with the exception that the thalli become larger and
undergo cleavage at maturity. At the time of sporu-
lation they may contain considerably more than a
hundred nuclei and are enveloped by a thin mem-
brane. The protoplasm cleaves into uninucleate seg-
ments (fig. 22, 23) which later round up and become
the resting spores as in Plasmodiophora, The soral
membrane disintegrates shortly thereafter and frees
the spores. These are usually uninucleate (fig. 24'),
rarely binucleate (fig. 2.5), hyaline, smooth, and
measure 9—13 fi by 4.5—7 fj.. In neither of these spe-
cies have spore germination, zoosporangia, and zoo-
spores been observed.
Leger believed that Sporomyxa may be closely re-
lated to Sapphiia because of its method of sporula-
tion. Maire and Tison (09) regarded it as of doubt-
ful affinity with the Plasmodiophorales and stressed
lack of promitosis in nuclear division as a distinctive
character. Fitzpatrick ('30) and Cook ('33) ex-
cluded it on the grounds of its habitat and ellipsoidal
isolated resting spores, but as Palm and Burk ('33)
have pointed out, "the circumstance that it attacks
an animal host could hardly be taken as a serious
objection." However, our knowledge of its life cycle
and cytology seems hardly sufficient to justify its
inclusion in the Plasmodiophorales at the present
time.
PELTOMYCES
Leger, 1909. C. R. Acad. Sci. Paris 149: 239.
Leger founded this genus to include three para-
sites, P. hi/alinus, P. Blatella, and P. Forficulae,
which occur in the malpighian tubes of Olocrates,
Blatella, and Forficula species. His description of the
genus was based primarily on the development and
life cycle of P. hijalinus, apparently the oiil}^ species
which he studied in detail. This species makes its
appearance in the epithelium as a small, 2 //., uninu-
cleate globular body. Its nucleus multiplies mitoti-
cally, and the parasite soon grows into a multinucle-
ate disc-shaped plasmodium which subsequently un-
dergoes schizogony and forms a large number of
small, 2-3 /x, uninucleate sporonts.
At the conclusion of schizogony the sporogonic
phase begins. Each sporont increases in size while
its nucleus divides mitotically several times. Two
types of nuclei are thus formed: small, densely-
stainable somatic nuclei without membranes, and
larger, normal-looking gametic nuclei with well-
defined membranes. The former nuclei disintegrate,
while the latter become enveloped in a small spheri-
cal mass of cytoplasm and are soon transformed into
bowl-shaped, 2 jj., gametes. These fuse in pairs after
their nuclei have undergone a chromatic reduction,
and this is soon followed by karyogamy. The zygotes
or incipient diploid resting spores formed in this
manner develop a wall and assume a cylindrical,
3X9/^, shape. Each mature sporont thus encloses
within its tliin wall 4 to 8 spores arranged side by
side and looks like a sporangium. The gametes in
the sporonts which fail to fuse develop into par-
thenogenetic spores of about half the size of the dip-
loid spores. In some cases prematurely formed spo-
ronts, instead of producing gametes, form small en-
dogenous cells which escape from the sporonts and
behave as schizozoites in the host. Leger did not
illustrate any of tliese species, and his account of
their development is brief and fragmentary. Zoo-
spores, sporangia, and cystosori are unknown in
Peltomyces.
CYSTOSPORA
Elliott, 1916. Delaware Agr. Exp. Sta. Bull.
114: 15.
(plate 15, FIG. 26-47)
This genus was created b}' Elliott for a myxomy-
cete-like organism, C. batata, which is reported to
cause "soil rot," "pit " or "pox" of sweet potatoes in
the United States. Elliott placed it in the Plasmodio-
phorales, but its inclusion here is very doubtful, if at
all warranted. In fact, some workers (Manns and
Adams, '25) have expressed doubt about tlie ex-
istence of an organism of this type and asserted that
some of the stages figured by Elliott may be nothing
more than products of disturbed metabolism of the
sweet potato. Tabenhaus (18), however, reported
tliat he was able to grow tliis organism in pure cul-
ture on sweet potato agar made up according to
Elliott's formula. He further confirmed Elliott's ac-
count of the life cycle of C. batata.
According to these workers, the zoospores are
small, 1—2 ft X 1-5-3 /x, globose with tapering ends
and possess a short flagellum, but it is not evident
from their descriptions whether the flagellum is an-
terior or posterior. The zoospores are nonetheless
produced in great numbers (fig. 43, 44) and may re-
main active from 1 to 7 days in rare instances, ac-
cording to Tabenhaus. The period of activity, how-
ever, is usually short, often less than half an hour.
The zoospores may sometimes fuse in pairs and form
round zygotes which later become amoeboid ( fig.
26, 27). According to Elliott, they bore through the
cell wall and infect the host as amoebae, but Taben-
haus reported that infection may also take place by
means of a plasmodium. The nuclei of the young par-
asite divide mitotically and simultaneously (fig. 28,
29, 32), but unfortunately Elliott's figures are so
small and poorly drawn that it is impossible to deter-
KXCI.rnKD OEXKUA
77
niiiio wlu'tlu-r or not tlic divisions riscinlilo tlu- pro-
mitosis (Itscriluii for otlifr <iinir;i.
Sovcral ;iiiio(l);u- and small plasinodia may co.i-
l«'si-i- and form larjtcr plasmodia. accordinf; to Elliott,
which migratf dcfpcr into the infected tissue (fig.
3i) in much the same manner described l\v Kunkel
for Spoiif/ospora. I.arjie plasmodia may contain from
200 to 300 nuclei, and at maturity form l.irjie multi-
nucleate cysts (fifi. 37-1-2). Klliott reported that
eaeli ))l.ism(idium forms a single cyst, hut liis liirures
sutrjiest that more than one may be j)roduccd. The
plasmodimn fills the host cell at maturity (fig. 36-
38). becomes more dense in the center, condenses,
and eventually forms a tliick. smooth wall (fig.
39-H). .\fter a short rest period the cyst germi-
nates, and in this process the wall becomes very thin
(fig. 13. H). and the protoplasm cleaves into nu-
merous zoospores. In this manner several genera-
tions of zoospores per season are formed in infected
roots and pox lesions, each generation of which mi-
grates deeper into the tissues. Eventually "all plas-
modia seem to collect, cease advancing, turn back-
wards, and leave the pit for the soil," according to
Tabenhaus. These plasmodia are believed to encyst
in the soil and live through the winter in this stage.
Soil rot. Jiit. or ))ox is a widely distributed and
common disease and has been reported from a num-
ber of states (Halsted, '90, '92, '96; Price. '9.5;
Duggar, '97; Townsend, '99; Wilcox, '06; Barre,
'10; Tabenhaus, '14, '16; Harter, '16; Poole, '22,
'24, '2.5; Anonymous. '21', 26; Harter and Weimer,
'29, and others). Pox may also occur on the white
potato, turnips, and possibly beets and tomatoes
(Tabenhaus. '18). The cause of pox. however, has
been the subject of much controversy. Halsted at-
tributed it to a filamentous fungus which he named
Acroci/stis batatas, but from extensive study of the
disease. Tabenhaus ('14) and Elliott concluded that
A. batatas is non-existent and had ])reviously been
mistaken for anotlier organism. The latter worker
claimed that pox is caused by a myxomycetous fun-
gus which he named C. batata. Elliott further as-
serted that Halsted had figured several stages of this
slime mold, and he accordingly listed Acroci/stis
batatas as synonymous with C. batata. Tabenhaus
('18) confirmed Elliott's observations in Texas, and
found that another fungus. .4ctiiwmi/ces poolensis,
may also occur as a suiJcrfieial wound ])arasite in pox
spots produced bv ('. batata.
Since that time the existence of cysts and other
stages of C. batata has been seriously questioned and
denied by Manns and Adam. In mature pox lesions
no evidence of an organism resembling a slime mold
was found by these workers, and they (21) inter-
jireted the so-called cysts of Elliott as "i)roducts of
metabolism in the form of reserve substances." Later
Manns ('24) demounted some of the pox material
which Elliott had stained with Flemming's triple dye
and restained it with Ziehl's earbol fuchsin. and in
each instance he found ."in .Icl'nioin i/crs s|)ccies pres-
ent. He ('2.5. '2(i) and .\d;ims (2!)) l;iter questioned
the existence of ('. batata and m.-uutained that pox
of sweet potato is caused by a s))ceies of Actino-
myces. Harter and Weimer ('29) were also unable
to isolate ('. batata from ))ox lesions or find any evi-
dence of zoospores. ))l.isniodi.a and cysts in fixed and
stained ))repar;itions.
This is the |)resent st;itus of ('. haltifa in relation
to l)ox. Elliott and Tai)enli;nis douiitless iiail some
sal)roi)hytie plasmodial organism .-it hand, but
whether or not it is a species of the Plasmodiopho-
rales is obviously questionable. Fitzjiatriek and Cook
excluded it from this order, but Saccardo ("31 ) listed
it among the valid siiecics. Palm and Hurk. however,
implied that it is valid but stands distinctly ajjart
from the other genera because of its method of cyst
formation. Except for the presence of zoospores,
('. batata is somewhat similar to Leptomi/xa rctice-
lata var. hum'di, a saprophytic proteomyxean organ-
ism which Miss McLennan ('31) found in hops.
There are a large luimber of saprophytic, soil in-
habiting organisms of this tyjie which may become
secondary invaders of roots, and unless they are
earefulh^ studied and cultured they may be readily
mistaken for stages in the life cycle of plasmodio-
I)lioraecous species.
bibliography: E-XCLFded genera
Adams, J. F. 19-'9. Phytopath. 19: 179.
Anony. U)-'4. U. S. Dept. Agr. PI. Dis. Rept. .Siippl. 34.
19Jti, Ibid. 45.
liarre, W. H. 1910. South Carolina Exp. Sta. J3 .\iin. Rejit.,
p. .'3.
Cook, W. R. I. 1933. Arch. Prntistk. 80: 1T9.
Dupfrar, ,1. F. 1897. U. S. Dept. Apr. Farm. Hull. 2G.
Elliott, ,1. A. 1916. Sci. n. s. 44: 709.
Fitzpatrick, H. M. 1930. The lower fungi — Phycomycetes.
New York.
HaLsted, B. D. 1890. New .Tersey Agr. Exp. .Sta. Bull. 76.
. 189:2. Xew Jersey Agr. Exp. Sta. IJth Ann. Rept,
p. 2m. 1896, Ibid. 17tli .\nn. Rept. p. 39.
Harter, L. L. 1916. V. S. Dept. Agr. Farm. Bull. 714.
, and J. L. Weimer. 19J9. U. S. Dept. Agr. Tech,
Bull. 99.
.\Iaire, R., and .\. Tison. 1909. ,\nn. Mycol. 7: -226.
Manns, T. F., and .1. F. Adams. 1921. Delaware .\gr. Exp.
Sta. Bull. 139: 18. 19J-', Ibid. 133: 36. 1934, Ibid. 135:
25. 1935a, Ibid. 139: 34. 1935b, Ibid. 141: 24. 1936, Ibid.
147: 39.
McLennan, E. I. 1931. Australian Journ. Exp. Biol. 8: 9.
Palm, B. T., and M. Burk. 1933. Arch. Protistk. 79: 371.
Poole, R. F. 1933. New .Jersey .\gr. Exp. Sta. Bull. 356.
. 1934. New .lersey .\gr. 6: 16.
. 193.5. Phytopath. 15: 3H7.
Price, R. H. 1895. Texas Agr. Exp. Sta. Bull. 36: 309.
Prowazek, S. 1905. .\rh. Kais. C.esuiidhelt 22: 396.
Rietschel, P. 19.36. Arch. Protistk. 86: .349.
.Saccardo, P. .\. 1931. Sylloge fuMgoriiiii 25: 16.
Tabenhaus, .T. .1. 1918. .Jour. Agr. Res. 13: 437.
'Jownseud. C. O. 1899. .Maryland Agr. Ex|). Sta. Bull. 60.
Wilcox, E. M. 1906. Alabama Agr, K\|i. Sta. Bull. 135.
PLASMODIOPHORALES
Chapter V
Phylogeny and Relationships of the Plasmodiophorales
Historical
The phylooeny and relationships of the Plasmodio-
pliorales have been the subject of great interest and
discussion among mycologists and protozoologists
during the past half century because species of this
order possess certain developmental stages which
are similar to those of the Myxomycetes, Proteo-
myxa. and other Protozoa, and the simple fungi. Be-
cause of inadequate data relative to the order itself
as well as to the groups with which it appears to be
related, these discussions have been largely specu-
lative, and a review of the literature shows that but
few of the workers have agreed on the systematic
position of the Plasmodiophorales.
Woronin ('78) stated that Plasmodiophoia stands
closest to the Myxomycetes but differs by the lack of
a true sporangium and by its parasitic mode of life.
In every other way. in iiis opinion, it resembles most
closely the myxochytridiales. De Bary ('84) de-
scribed P. Brassicae as a doubtful member of the
Myxomycetes, but Zopf ('84) established a sepa-
rate family, Plasmodiophoraceae, for Plasmodio-
phora and Tetramyjca under the zoosporic group of
the Monadineae next to the Gymnococcaceae. He
nonetheless included the Monadineae in the Myxo-
mycetes. and liis exclusion of the latter group from
the fungi in 1890 suggests that he did not regard the
Plasmodiophoraceae as true fungi. A year later Lan-
kester incorporated the Monadineae, Plasmodio-
phora and Tetramyxa in a new class, Proteomyxa, of
the protozoa. As noted elsewhere, Schroeter ('86)
ignored Zopf's family and created a new order,
Phytomyxini. with one family, Pliytomyxaceae, to
include Pla.imodiophorii, Phyiomfixa, and Soro-
sphaera and placed it next to the Myxogastres. In
1897 he placed the Phytomyxinae between the Acra-
siae and ^lyxogastres and pointed out that because
of its free spores P. Brassicae stands close to the
Acrasiae but differs principally from this group by
its true plasmodium. zoospore stage, and intramatri-
cal habit of life. Tubeuf and Smith ('97), however,
excluded Phi/tomi/jra from the Phytomyxinae and
described Plasmodiophora, Tetramiixa, and Soro-
sphaera as pathogenic slime-fungi. Schroeter's dis-
position and viewpoint was supported by Lotsy
('07) and Pavillard ('10) who regarded Plasmo-
diophora as a myxomycete which has retrogressed
because of its parasitic mode of life. Pavillard in
particular stressed tlie presence of an initial flagel-
late stage as the chief indication of relationsliip be-
tween the two groups.
This viewpoint was severely criticized by Maire
and Tison ('09). After a careful cytological study
of Sorosphaera, they refuted Pavillard's claim and
expressed the opinion that the Plasinodioiihoraceae
constitute an entirely distinct group, intermediate
between the Sporozoa and Myxomycetes and derived
more or less directly from the Flagellata. They fur-
ther pointed out that although the type of nutrition
of the Plasmodiophoraceae is plant-like, while the
absence of cellulose and the presence of chitin in tlie
spore membrane are animal characteristics. Later
('11), however, they emphasized the close resem-
blance of Lif/niera to Woronina polycystis and postu-
lated that this genus may have been derived from
Woronina-\i\ie ancestors through the disappearance
of sporangiosori. Maire and Tison thus concluded
that the origin of the Plasmodiophorales should be
sought in the neighborhood of the Cliytridiales.asthis
order was interpreted at that time. Winge ('13) like-
wise maintained that "the relationship of the Plas-
modiophoraceae with the holocarpic Chytridiaceae
is beyond doubt," and pointed out that certain species
of Synchytriiim, Asterocystis, Bhizomyia, Sorolpi-
diiim, Woronina, and Pyrrhosorus occupy intermedi-
ate positions and represent transition forms between
the two groups. Stevens ('13, '25) included the Plas-
modiophorales as the first order under the Myxomy-
cetes. Maire and Tison were supported by Schwartz
('It) who stated that the differences between the
Plasmodiophoraceae and Myxomycetes are too great
to be accounted for by the former's parasitic mode
of life. Although he regarded the two groups as re-
lated, Schwartz, nonetheless, believed that the Plas-
modiophoraceae should form a separate order inter-
mediate between the Myxomycetes and Chytridiales.
Jahn ('14), Cavers ('1.5), and Pascher ('18) con-
curred in general with the views of Winge and
Schwartz. In reviewing Schwartz's paper, Jahn
stated that the Plasmodiophorales have little in com-
mon with the Myxomycetes and are closely related
cytologically with the Cliytridiales. He excluded the
order entirely from the ^lyxomycetes in 1928. Na-
waschin ('24) asserted that P. Brassicae has nothing
in common with the Myxomycetes as far as nuclear
structure is concerned and advocated its inclusion
among the non-amoeboid type of Protista. Cavers
('15) stressed the relationship of the Plasmodiopho-
raceae and chytrids and believed that Sorolpidiiim
may possibly be a connecting link between this fam-
ily and the Synchyiriaceae.
' The view that the Plasmodiophoraceae are closely
related to the Chytridiales has been rather widely
accepted. Gaumann ('26) and Gaumann and Dodge
('28) included the Plasmodiophoraceae with the Wo-
roninaceae. Olpidiaceae. and Synchytriaceae in a
special group, the Archimycetes. apart from the
Phycomycetes. They accordingly linked the Plasmo-
diophorales with Fischer's earlier-named iNIyxochy-
tridiales. Kniep ('28) regarded them as fungi, and
wliile admitting that they may perhaps be included
in the Chytridiales, he said that the last word on
their exclusion from the Myxomycetes had not been
IMlVI.OliKNV AM) ItKI.ATIOXSlIll'S
'!)
spoki-ii. l-'itzpatrick (^'30) was tlit- first to ilctinitily
iiu-ludc this family in tin- C'liytridialcs lu'xt to the
W'tironiiiai-tai- and Syiu-liytriaccai'. and niaintaiiu'd
that tluy havi' inoro in coninion with these two oliy-
tridiaoeoiis families than witli the Myxomycotes. In
so doin^. however, he did not imply a elose relation-
ship. Fitzpatriek exi)ressed the opinion that the Syn-
ehytriaeeae. Woroninaeeae. and Plasmodiophor.a-
ceae "h.ive arisen more or less in p.-irallel from yet
more ))riinitive protozoa and wholly in(Ie])eti(leiit of
the Myxoii.-istres." W'ettstein ('8.">) .ilso ineluded the
I'lasniodiophorales amoiiir the ehytrids next to the
Synehytriaeeae and stated that their eytolo^y as
well as the prcscnee of eliitin in the walls indieates a
close rel.-itionship. Cadnian ('31) and Bessey ('3.5),
however, believed that the Plasniodio])horales show
a closer affinity to the Myxomyeetes. and the former
worker listed them as a sub-group of the Myxomy-
eetes. .Martin ( 3(>) listed the Plasmodio))lioralcs as
the lowest order of the Phyeomyeetes but distinct
from the so-called niyxochytridiales.
On the other hand, Ciwvnne-\augiian .md Barnes
('26, '37) maintained that the Plasniodio])Iiorales
and Myxomyeetes are not fungi and have doubtless
arisen from lower forms along inde))endent lines.
Cook ('26) agreed in general with these mycologists
and expressed the view that "it seems very desirable
to keep the Plasmodiophorales quite separate from
the Chytridiales and other fungi. If there is any rela-
tionship, it is most likely through the Mycetozoa."
In I92S. however, he held that the Plasmodiophora-
ceae and Myxomyeetes originated from a proteomyx-
ean eomiilex through the Lobosa and more s])eeifi-
cally .Ircella vuhfari.s and Amoeba miiscicola and
diverged at slightly different points. On the basis of
the type of nuclear division in the vegetative phase.
Cook lielieved that the Plasmodiophorales diverge
from the Amoeba series at a more distant point than
the Mycetozoa. Later ('33) he asserted that "no
close relationshi}) with either the fungi or ])roto/.oa is
l)robable." and that the Plasmodioiihorales "repre-
sent an independent group having their origin in the
Proteomyxa. " Cook tiuis revived and su))))orted the
earlier views of Zopf , Delage and Herouard. Lankes-
ter, and others on the relationship of the Plasmodio-
phorales to the Proteomyxa.
Zoologists also have asserted their claims to the
Plasmodiophorales and included this order as a sub-
class of the -Myxomyeetes among the Protozoa, ])ar-
ticularly the Khizo))oda. Most protozoologists. how-
ever, have continued to use .Sehroeter's term. Phyto-
myxinae, for the group, although it has been evident
since the beginning of the present century that Phij-
tomi)xa, the genus after which Schroeter named the
order and family, is no longer tenable and relates to
what are now known as bacteria and mycorrhizal
fungi. Protozoologists. furthermore, have ignored
the discovery and presence of zoosjjorangia and bi-
Hagellate, heterocont zoospores in six genera of the
Plasmodiophorales and have adhered to the older,
outworn conceptions regarding these organisms. De-
lage and Herouard ('96) followed Zojjf's disposi-
tion of Plasmoiliophorn and Tetrami/ja by including
them with (1 iiniiiococciix, P.ieiidospora, etc., in the
zoos))orie Proteomyx.i or .Mon.ulini.-ie their first
el.ass uniler the Hliizopod.i. Dotlein ('01) listed the
Mycetozoa as the fifth and last class of the Rhizo-
))oda next to the Poramiuifera and divided it into
two subclasses of equal rank, the Protomyxidea and
Mveetozoidea. Plasmodiophora and Teframi/ja were
pl.ieed in the zoos])oric grouj) of the Protomyxidea.
,1 classification which eorres])onds essentially with
that of ])revious ])rotozoologists. In subsequent edi-
tions of his text-book ('Oi), '11. 'Ki) DoHein placed
the Mycetozoa next to the Radiolaria and limited the
sub-class Protomyxidea to what are now generally
known as the azoosporic and zoosporic Proteomyxa.
For the plasmodiophoraceous genera he adopted
Seiiroeter's Phytomyxinae, made it a sub-class of
the Myxomyeetes, and ))laced it between the Acra-
siae and ]\Iyxogastres. In the sixth edition, however,
which was rewritten by E. Reichenow, the Phyto-
my.xine and Acrasiae were excluded from the My-
cetozoa proper and were discussed merely as an
"anhang " to this class.
I.ankester ('8.5. '09) and Hartog ('06, '09, '22,
'36) also included Plasmodiophora and Tetra?)iy.i'a
in the Proteomyxa along with J ampyrella, Gi/miio-
coccus, Pseudo-spora, etc. Hartog. however, assigned
Plasmodiophora together with Protomi/.ra, Vampy-
rella, and Serumsporidiuvi to the non-flagellate or
azoosporic Myxoidea. In 1909 Calkins referred to
P. Brassicae as a mycetozoan and later ('33) in-
cluded the Phytomyxida (Phytomyxinae) as an or-
der in the Myxomyeetes. He believed that the lack
of peridia and capillitia in the plasmodiophoraceous
s])ecies is due to their parasitic mode of life. Min-
ehen ('12, '21) was uncertain of the relationships
of the Phytomyxinae and merely discussed them as
border-line organisms in relation to the Sarcodina.
Hertwig (19) listed the Mycetozoa as the fifth
class of Protozoa and of equal rank with the Rhizo-
])oda and included Plasmodiophora among the My.x-
omycetes. Galiano (1921) also grouped the Phyto-
myxinae as a suborder of the ^lyxomvcetes, while
Rumbler ('23-'2.5) reverted to DoHein's ('09, '11)
classification. Kudo ('31, '39), on the other hand,
included the Phytomyxinae directly in the Myxomy-
eetes.
It is evident from this review that several ))oints
of origin and lines of develoj)ment and relationship
have been em|)liasized for the Plasmodiophorales.
These suggested relationshi))s involve the Myxo-
myeetes, Chytridiales, Protozoa, Sporozoa, and Pro-
teomyxa. The evidence in support and against these
relationships will now be considered in greater de-
tail.
Plasmodiophorales and My-xomvcetrs
Inasmuch as the belief that the Myxomyeetes and
Plasmodio])horales are closely related is rather
widely held, this view will be presented in consider-
able detail. Proponents of this view have stressed the
presence of a large multinucleate plasmodium and
80
PLASMODIOPHORALES
anteriorly uniflagellate zoospore in both groups as
evidence that they have originated from a common
ancestor. Considerable significance has also been at-
taclied to the reports that the plasmodia of Sponc/o-
spora (Kiinkel, '15) and Plasmodiophora (P. M.
Jones, '28) can live outside of the host and may be
cultivated on synthetic media like those of the Myxo-
mycetes. Careful analysis of Kunkel's paper, how-
ever, shows that the saprophytic plasmodia which
he described apparently do not relate to Spongo-
spora at all, because at maturity they form stalked
Dicti/osfelium-like sorocarps instead of spongy cys-
tosori. I>ike\vise, the peculiar and abnormal life cycle
described by P. M. Jones for P. Brassicae suggests
that he may have been studying some other plasmo-
dial organism instead of Plasmodiophora. It thus
remains to be seen whether or not the plasmodium of
the Plasmodiophorales can be cultivated saprophy-
tically outside of the host.
As to the mode of nutrition, data are accumulat-
ing which suggest that it possibly may be very simi-
lar in both groups. The zoospores, amoebae, the
plasmodia of the Myxomycetes are capable of en-
gulfing food particles, digesting them, and discard-
ing the extraneous waste material. While this type
of nutrition is not particularly evident in the Plas-
modiphorales, claims have nonetheless been made
that the plasmodium at least engulfs starch grains
and masses of host protoplasm. According to Woro-
nin. Nawaschin, Prowazek, and Lutman, starch
grains may often be found in the folds and vacuoles
of the Plasmodium of P. Brassicae. Nawaschin
('99), Favorsky, and Henckel did not believe these
had been engulfed, but Woronin, Eycleshymer, and
Lutman nevertheless inferred that the plasmodium
feeds on these grains. Maire and Tison (11) like-
wise reported that the small plasmodia of Ligniera
Junci may engulf algal cells. The zoospores of some
species also appear to be capable of taking in solid
bodies, but how generally it occurs is not known. In
Polymijxa (jraminis Ledingham reported that the
pseudopods of amoeboid zoospores may flow around
and engulf small objects.
The evidence of relationship on the basis of simi-
larity in zoospore structure is not particularly con-
vincing in light of recent discoveries. Until 1931' it
was believed that the zoospores of the Plasmodio-
phorales were like those of the Myxomycetes in hav-
ing one anterior flagellum, but since that time it has
been clearly shown that the zoospores of six genera
of the former group are anteriorly biflagellate and
heterocont. Further study will doubtless show this to
be true in the remaining genera of the Plasmodio-
phorales also. The structure of the zoospores and
the number, position, and relative lengths of the
flagella are very significant phylogenetically, and it
would seem offhand that the presence of biflagellate,
heterocont zoospores in the Plasmodio])horales sepa-
rates this order very sharply from the Myxomycetes.
It must be remembered, however, that although the
majority are uniflagellate, zoospores with two fla-
gella are not uncommon in the Myxomycetes also.
De Bary ('84) and Vouk ('11) early noted zoospores
with two flagella, and since that time numerous re-
ports of similar zoospores have appeared. Gilbert
('27) found that 25 per cent of the zoospores of
Stemoiiitis fiisca are biflagellate, and his figures le
and If show that one of the flagella is considerably
shorter. Similar zoospores have been subsequently
described and figured by Smith ('29) for Dictyae
thalium plumheum, by Howard ('31) for Physarum
polycephalum, and by Sinoto and Yuasa ('St) and
Yuasa ('35) for Physarella ohlonga, Fuligo septica,
and Comatrichia longa var. ftaccida. In the latter
species 13 per cent of the zoospores were biflagel-
late, and in rare cases triflagellate. As is shown in
figures 2 to 5, Plate 17, the flagella are of equal as
well as of unequal length. Stosch ('35) also found
biflagellate zoospores in Didymium eunigripes, D.
xanthopus, D. squamosum, D. difforme, Physarum
cinereum, P. nutans, Trichia favoginea, Comatrichia
nigra, and Lycogola epidendrum.
In most species which normally have uniflagellate
zoospores, bi- and multiflagellate cells are usually
the result of unequal or incomplete cleavage, and
are consequently large and bi- or multinucleate.
Such does not appear to be true of the zoospores
shown in figures 2 to 6, Plate 17, since there is but
one nucleus present regardless of the number of fla-
gella and the size of the zoospore. A more funda-
mental cause may perhaps be operating in these
cases. Of particular interest in these figures are the
basal bodies upon which the flagella are oriented. In
Ceratiomyxa fructiculosa var. flaccida, Physarella
ohlonga, and Fuligo septica, they are double regard-
less of whether one or more flagella are present.
E. A. Bessey, Professor of Botany, IMichigan State
College, believes that this double condition may per-
haps be significant phylogenetically. In correspond-
ence with the author concerning these zoospores, he
asks : "Are these two granules homologous to the
basal granules found in algae and .... sperm cells
of mosses or ferns, where each flagellum arises from
such a granule ? Then do the planocytes with but one
flagellum represent cases where there has been a
loss of one flagellum in progressive evolution from
a normally biflagellate condition, and do tlie biflag-
ellate cells of these slime molds represent the an-
cestral condition which has not been com])letely lost
in this grou]).'' In the Plasmodiophorales, which are
probably closely related to the slime molds, the bi-
flagellate condition has not yet been lost, though one
flagellum is smaller than the other." Bessey thus
suggests that the presence of a second basal granule
in uniflagellate zoospores may possibly be a relic of
the biflagellate condition and that the Plasmodio-
phorales are more primitive than the slime molds.
However, it remains to be seen how general the
double condition is in uniflagellate zoospores. Jahn
('04), Wilson and Cadman ('28), and Cadman ('31)
figured and described only one basal granule, while
Cotner ('30) and Stosch reported the presence of
several bodies at the base of the flagellum. Sinoto
and Yuasa's accounts of the presence of two basal
PIIYI.OCJKNV AND HK.I-ATIOXSIIII'S
81
Inulifs in tin- M\ ictuzo.i Iiuve aocordiiiiily nut lucii
universiilly continnoil. .Ijiliii ( 30) sovcri'ly critiiizid
the belief tliat tlio presence of two H.ifjella aic nl
niueli sijrnilieaiiee, questioned the presence of more
than one liasal jirannle, and rejjarded all liiHauellate
zoospores as alinornial.
In tlie I'lasniodiopliorales little is known about
the l)lei>haro])last and its eoinposition. 'Terhv (lil-a)
and Cook and Sehwartz ('30) tiirnred only oiu' t)lei)h-
aroplast in the uniHairellate zoospores of /'. Hras-
sicar, but later Terby ("'2t-b) reported that the
blepharojilast may divide and form two bodies in
the incipient spore. Neither Ledingiiain ('31, '35)
nor Couch. <-t al. ('39). showed basal fjranules in
their fifrures of the biflai;ellate zoosjiores of Plasmo-
diophora, Spoiifioxpora, and Octomi/.ra. In I'oli/-
mi/ja, on the otiier liand. I.ediniiham ('39. p. t2)
figured the two flagella attached directly to the nu-
clear membrane without the presence of blei)haro-
plasts or basal granules. It is thus obvious that but
little is known about the number of basal granules
in the zoosj)ores of this order and their relations to
the H.igell.i. Nevertheless. Bessey's suggestion con-
cerning the significance of basal granules and the
occasional occurrence of biflagellate zoosjiores in the
slime molds is very stinnilating and merits further
investigation.
Turning now to other differences within the two
groups, it may be noted that sporangia and capil-
litia of the tyi)e found in the slime molds are lack-
ing in the Plasmodio]iliorales. As has been noted
before, mycologists and protozoologists have re-
garded this reduction as due to the jiarasitic mode
of life adojjted by the Plasmodiophorales. Cook
('33) suggested that the membrane around the cys-
tosori in certain ))Iasmodiophoraceous genera, Soro-
discus, Sorosphaera, etc.. may be looked upon as
equivalent to the sporangium wall of the Myxomy-
cetcs. However, there is considerable doubt about
the jiresenee of a soral membrane in these genera.
The Myxomycetes. on the other hand, lack s])o-
rangiosori and thin-walled evanescent zoosporangia,
which have recently been shown to occur in most
genera of the Plasmodiophorales. These zoosporan-
gia may arise directly from zoos])ores which have
entered the host or later from small or large, seg-
mented, vegetative plasmodia. These differences —
lack of thin-walled, intramatrical zoos])orani!:ia in
one grou]) and sjiecialized sporangia and capillitia in
the other — are of fundamental significance, in the
author's opinion, and are difficult to ex))lain wliolly
by differences in mode of life.
Other develojjmental phases and eytological dif-
ferences between the two groups are to be noted
here. Schizogony of the young plasmodiimi has been
described in most genera of the Plasmodiophorales,
but it a])pears to be lacking in tlie Myxomycetes. At
least, no conclusive evidence of its occurrence has
yet been presented. Furthermore, neither the so-
called "promitotic" nuclear divisions nor a marked
"akarvote " stage, which are rejiorted to be charac-
teristic developmental i)hases of the Plasmodiopho-
rales, li.i\ e been found in the Myxomycetes. W'iiether
or not tliese (litl'erenees alone are of much phyloge-
nitie signiHc.incc, however, is questionable.
Comp.-irisons of the two groups on the basis of
sexuality, alternation of generations, time and place
of meiosis, etc., are difficult to m.ake at present, be-
cause so little is kiu)wn about these ])rocesses in the
Plasm()dio|)!iorales. In the Myxomycetes also there
is considerable disagreement among workers about
these devclo|)mental phases. As far as is now known
the resting spores of the slime molds usually form
more than one zoospore in germination, and these in
turn divide once to several times before becoming
gametes. In the Plasmodiophorales, on the other
hand, it is claimed that only one zoospore is formed,
which functions directly as a gamete without di\ id-
ing. Cook ('33) empluisized this distinction and
stated that it is "the chief difference between the
two groups." In light of data in the literature, this
statement is obviously open to criticism. Maire and
Tison.and Home found an additional or third mitosis
after the two meiotic divisions in Sorosphaera and
.S' /;0H r/cs/jora, respectively, where by binucleate spores
were occasionally ))rodueed. I.utman and Terby also
figured binucleate sjjores in P. Brassicac and be-
lieved that these arise as tiie result of division of the
spore nucleus. It is not improbable that such spores
form more than one zoospore or gamete. In addition
to such spores, unusually large multinucleate ones
ha\e been found in several genera, and it is not un-
likely that they also give rise to several motile cells
in germination. Likewise. Cook's assertion "that di-
vision of the swarm cells does not take ])laee in the
Plasmodiophorales i)rior to fusion" is rather dog-
matic and premature in light of our meager present-
day knowledge of the behavior of the zoospores in
this order. The}- have never been cultured with cer-
tainty outside of the host, and very little is known
about their behavior within the host cells. Cook's
assertion is furthermore contradicted by Massee's
(PL 10, fig. 10). Osborn's. Home's and Fedorint-
schik's accounts of tin- multi))lieation of amoebae or
gametes in Spoiu/ospora and Pla.smodiophora by
equal division and budding. In maintaining that the
gametes are the direct ))roducts of the resting spores.
Cook further contradicted his own and Schwartz's
('30) earlier assertion that the gametes of 1'. Kras-
sicae are produced in thin-walled zoos))orangia or
gametangia. The origin .-uid method of formation of
gametes in the Plasmodiophorales are thus some-
what doubtful at jircsent, and it seems jirematurc to
make definite comparison between the two groups on
this basis.
Fusion in pairs of isomorphic amoeboid and flag-
ellate gametes has been reported to be characteristic
of both groui>s, but as noted elsewiiere actual fusion
has so far been seen very seldom in tlie Plasmodio-
phorales. The respective gametes are alike in size
and structure in both groups, but in the Myxomy-
cetes certain other differences between gametes of
the opposite sex have been reported, .\ccording to
Abe ('3f) the male gamete loses its Hagellum as it
82
PLASMODIOPHORALES
flows into tlie female, and its nucleus migrates to-
wards that of the female gamete. Furthermore, the
latter gamete carries a positive charge and has a
low oxidation-reduction potential, while the male
gamete is the opposite in these respects. Kambly
('39), however, was unable to confirm these results
of Abe, and found no marked physiological differ-
ences between swarm cells of various species. Gil-
bert ('35) and Stosch ('37) likewise reported that
the male gamete may be distinguished during fusion
by the migration of its nucleus toward that of the
female. Such differences have not been reported for
the Plasmodiophorales as far as the author is aware.
In the Myxomycetes the gametes fuse by their pos-
terior ends, while in the Plasmodiophorales, accord-
ing to Cook ('33), they fuse at the anterior ends.
However, so little is known about gametic union in
this order that it is premature to regard the latter
type of fusion as characteristic of the Plasmodiopho-
rales.
Comparison of the two groups on the basis of
time and place of sex segregation is also impossible
at present, because little is known about sexuality
in the Plasmodiophorales. No monospore cultures or
infections have yet been made to determine whether
the species are homo- or heterothallic. If, as Cook
('33) maintained, the gametes are the direct prod-
uct of uninucleate spores and no division occurs in
amoebae and zoospores, sex segregation obviously
takes place during one of the meiotie divisions be-
fore or during sporogenesis. Otherwise, it is pheno-
typically determined in the haploid generation, and
the species are accordingly haplosynoecious. In the
Myxomycetes also, there are but few data relating
to sex segregation. Skupienski ('17) believed that
in D. difforme it occurs during one of the divisions
in the zoospores. Miss Clay ley reported its occur-
rence at the second meiotie division in the zoospores
of D. tiif/ripes. Schiinemann confirmed her rejjort of
haplophenotypic sex segregation in tliis s])ecies and
described D. nigripes as haplomonoecious. Miss Cad-
man, however, noted no differences, morphological or
physiological, between the gametes in lieficularia
and D. nigripes and concluded that no sex segrega-
tion is necessary or takes place in these species.
Stosch, on the other hand, implied by his statement
concerning crosses in D. eiinigripes that sex is geno-
typically determined.
As to the time and place of karyogamy, meiosis,
and alternation of liaploid and diploid generations
in the Plasmodiophorales, a detailed account of these
subjects has been given in Chapter III. As is evident
from this description, the majority of workers have
assumed that the isomorphic gametes fuse in pairs,
after which karyogamy soon occurs. Nuclear fusion
in the zygote thus initiates the diploid phase which
includes the plasmodial stage up to the last two nu-
clear divisions preceding or during cleavage where
reduction occurs. Plasmogamy and karyogamy arc
accordingly not followed at once by meiosis. The
haploid })l!ase includes the cystosori, spores, zoo-
spores, and gametes, according to this viewpoint.
However, as noted before, exceptions to this view
have been presented by Prowazek, Osborn, Home,
Webb, and Whiffen.
In the Myxomycetes likewise there is considerable
disagreement and controversy concerning karyog-
amy, meiosis. and alternation of generations. Much
of the controversy about meiosis hinges upon the
question of whether one or two divisions occur prior
to spore formation in the fruiting bodies. Strasburger
('84.). A. Lister ('93), Rosen ('93), Harper ('00),
.7ahn ( '07-36 ), Kranzlin ('07), Gilbert ("3.5), and
Stosch ('3.5, '37) found only one. while Wilson and
Cadman ('28), Cadman ('31), and Schiinemann
('3.5) reported two divisions. In contrast it may be
noted here that most workers on the Plasmodiopho-
rales are in agreement that two divisions precede
spore formation. However, in order to draw com-
parisons between the two groups with respect to
meiosis, it is essential to outline briefly the differences
of opinion concerning this question in the Myxomy-
cetes.
In the Exosporae, Olive ('07a) found stages re-
sembling syna]>sis in the young spores of Ceratin-
7ni)j-a and later ('07b) on observing pairing and fu-
sion of nuclei in the pillars, concluded that the two
mitoses in the spores of this genus are meiotie.
Olive's conclusions on pairing and fusion of gametic
nuclei were confirmed in general by Jahn ('07) who,
however, held that these processes occur earlier as
the Plasmodium creeps out of the wood. On the other
hand, he refuted Olive's contention that meiosis oc-
curs in the spore and claimed instead that the two
divisions which precede cleavage are reductional.
The incipient uninucleate spores are accordingly
haploid. Jahn ('08) reasserted his observations on
nuclear pairing and fusion, but maintained that only
one, instead of two, division occurs prior to cleavage.
This division is heterotypic, according to .Tahn. and
reduction is thus accomplished by one division. The
Plasmodium is formed by the fusion or coalescence of
numerous haploid myxamoebae, the nuclei of which
divide mitotically several times in the plasmodium.
Karyogamy is accordingly delayed until the plas-
modium creeps out to fructify. In 1911, however.
Jahn concluded that his previous observations on nu-
clear pairing and fusion in the mature plasmodium
were incorrect and that the appearances of karyog-
amy were the results of nuclear degeneration. His
observations of endosporus species led him to the be-
lief that nuclear fusion follows plasmogamy of amoe-
bae. Jahn ('1 1, '33, '36) nonetheless persistently ad-
hered to his early view that meiosis occurs during the
last division before cleavage, as is shown in text-
figure 1 2. Gilbert ( '3.5 ) , on the other hand, confirmed
Olive (m meiosis in the spore and in addition showed
that the haploid motile gametes fuse posteriorly in
pairs to initiate the plasmodium (text-figure 13). He
also found that karyogamy follows plasmogamy
within 21' hours, thus refuting Olive's observations
but confirming Jahn's later view.
In the Endosporeae, .lahn (07) reported the same
tvjje of nuclear pairing and fusion in the young fruit-
IMIYI.IKiKNV AM) IlKI.ATIOXSllll'S
88
plasuooma' )cM>o&>ur rctone it^orc rC^^ e a^
PLASuooAf-iy ttcccssopf fusion/ KMrooAMr
vExvsrive mitosis
TDfT-FielB LFEiytLEorCePATiouirxA.MXOKDna to J-wn. i9it-je.
2ND M D 1ST M O
TexT-FidS Life Cvnc OF CeMTioMrxA. ACCOKDiNC to Qlbert. 1935.
FWITING BOO-
ZY<30Tt MITOSIS. OMXTICNUaXI
■O o*\
FIASMODIUM
PLASU03AUY
KAKYOOAMY PLASMODIUM
1ST MB
/^r~~ S 200SP0f€S SPOKES "'
Text-Fic.14 Lfs OrcLE ofD ofFCKne. accofiding to Sklpcnski. i92s.
DIPLOID
sex SEGPECATION ^
ZND M. D BISEXUAL SPORE
Text-Fig 15 Life Cms of D difforme. Accoaoma to CLo-LEy. i929-
rouNG PLASMoauu
"/-''icO"
Division ZOOSPORES
Text-Fig 16 Life Cms of D nigrpes. according to Schunemann. 1930.
Text-fifjurc
Text- Fig 17 Life Cycle OF R LyOiperdon. according toWIlsonano
Cm>MN.I923.
12-17
84
PLASMODIOPHORALES
ing bodies of Amaurochaete, Reticularia, Trichia,
Stemonitis, and Didymium. In these genera karyog-
amy is followed by synapsis, and as the spores are
delimited, one mitosis, the heterotypic division, oc-
curs. Tliis first meiotic division is followed by a long
rest period of the spore, and the second or homeo-
typic division is delayed until the first mitosis in the
germinating spore, according to Jahn. Similar ob-
servations were reported by Kriinzlin (07) and
Vouk (11) for species of Trichia and Arcyria, but
these were later found to be incorrect by Jahn in
1911. For the first time in the Myxomycetes he found
that haploid myxamoebae of Physarum didermoidcs
fuse in ]iairs to form the zygote. Plasmogamy is fol-
lowed shortly by karyogamy. The diploid zygote
may engulf hajjloid amoebae, with the result that
haploid and diploid nuclei may be found in the young
Plasmodia. Likewise, zygotes may fuse with each
other to form larger plasmodia, but fusion of the dip-
loid nuclei does not occur. ]Meiosis takes place during
the last division in the young sporangium and is not
followed by a homeotypic division. Jahn ('33) re-
ported the same type of meiosis in Badhamia iitricu-
laris, and subsequently persisted in this view on the
time and nature of reduction division in the Exospo-
reae and Endosporeae.
Pinoy (08) concluded from his culture experi-
ments that Didymium nigripes is heterothallic and
forms -|- and — myxamoebae which in turn give rise
to -|- and — Plasmodia. Sporangia are formed only
wiien both types of plasmodia are mixed. It is not
certain that Pinoy used monospore cultures, and be-
cause of this his results have been seriously ques-
tioned by Kniep ('28) and Schiinemann ('30). Sku-
pienski ('17— '28) also reported heterothallism in D.
ni(/ripes and D. difforme. In 1928 he asserted that
the sjjores of D. difforme are unisexual and that no
sporangia will develop in monospore cultures. Ac-
cording to him the plasmodium arises by the fusion of
two myxamoebae of opposite sex (text-figure It).
Other myxamoebae may unite with the zygote, but
the gametic nuclei remain separate and divide mitot-
ically in the young plasmodium. The daughter nu-
clei later unite in pairs and fuse in the older plas-
modium. wliile those whicli fail to find partners de-
generate. Meiosis occurs during the last two divisions
in the sporangium, according to Skupienski.
In the same year Wilson and Cadman showed in
Reticularia Lycoperdon that haploid motile gametes
fuse in pairs by their posterior ends to form a zygote
(text-figure 17). Other gametes may coalesce with
the zygote, but their nuclei divide amitotically, de-
generate, and are digested by the zygote. Karyogamy
of the gametic nuclei follows shortly after the coal-
escence witli the non-functional gametes, and meiosis
occurs during the last two divisions in the sporogenic
protoplasm. Miss Clayley ('29) refuted Skupienski's
contention of heterothallism in D. difforme, showed
that the s))ores are bisexual, and secured sporangia in
monosjjore cultures (text-figure l.'j). She also found
that plasmogamy takes place between motile gametes
instead of myxamoebae, as claimed by Skupienski.
Schiinemann likewise secured plasmodia in mono-
spore cultures of Skupienski's own D. difforme and
thus refuted the latter's contention of heterothallism.
In D. .ranihopus, however, neither plasmodia nor
sporangia were formed in monospore cultures. In 7^.
niciripes, Schiinemann found that several haploid
myxamoebae coalesce to form plasmodia but their
nuclei remain separate until the plasmodia become
older (text-figure 16). Karyogamy eventually oc-
curs, and reduction is accomplished during the two
divisions preceding spore formation. ScIiUnemann
tlius concluded that a true antithetic alternation of
generations occurs in I), nic/ripes. Cadman ('31),
however, found that karyogamy occurs shortly after
plasmogamy, and that the diploid zygote can ingest
zoospores and haploid myxamoebae and coalesce
with other zygotes. She nevertheless confirmed Schii-
nemann on meiosis. In the same year Howard re-
ported fusion in pairs of motile gametes in Physarum
polycephalum and expressed tlie belief that plasmo-
gamy is followed at once by karyogamy. Abe ('33,
'SI) likewise found fusion of motile gametes in
Fulif/o septica, Erionema aureum, D. nic/ripes, P.
crateriforme, and Stemonitis fusca. The gametes
were found to be isomorphic but differ physiologi-
cally, as has been noted previously.
In D. nigripes, Stosch ('35, '37) reported the dis-
covery of two forms, Z). eunigripes and D. aantho-
pus, which are hetero- and homotliallic, respectively.
In D. eunigripes, sexuality is well defined, while D.
jranthopus is apogamous. Didymium squamulosum
and Physarum cinereum were also reported to be
apogamous, the first report of which Jahn ('36)
characterized as fantastic. Jahn furtlier refuted
Stosch's report of heterothallism in D. eunigripes
and claimed that tlie failure of the gametes to fuse
and form plasmodia and sporangia in Stosch's mono-
spore cultures was due to the fact that tliey had not
gone through tlie encystment and rest period which
are necessary before fusion occurs. For sexual spe-
cies of the Didymaceae, Stosch reported that motile
gametes fuse in pairs to form zygotes, which in turn
fuse with other zygotes in the formation of large
])lasmodia. Plasmogamy of gametes is apparently
followed shortly by karyogamy. Onlj' one vegetative
mitosis occurs before cleavage in the sporangium,
and meiosis takes place in the spore, according to
Stosch. Separation of homologous chromosomes may
occur in the first and second divisions. Stosch thus
supported Olive's and Gilbert's contention that meio-
sis occurs in the spore instead of before cleavage in
the sporangium. In ajjogamous species, he reported
that fusion may occur between amoeboid as well as
motile gametes, and tliat instead of meiotic divisions
in the spore, one or ))erliai)s two vegetative divisions
occur which arc followed by amitosis.
It is apparent from this survey that there are
marked differences in observations and interpreta-
tions concerning karyogamy, meiosis, alternation of
generations, and sex segregation in the Myxomycetes
as well as in the Plasmodioi)horales. Nonetheless,
certain fundamental similarities do exist, and if the
•IIYI.OUKNY AM) HKI.ATIDN.SIl ll'S
85
diajiranis rfjircsoiitiiiji the life oyi'lcs of tin- I'l.is-
niodi(i|)lioraU's in Chapter III an- compartd with
those of the Myxoinycctts tliese siniilaritii's bci'onif
iiioro strikinir. .Most rciciit workers in hotli iiroii])s
aftree that tlie dijjhiiil phase is initiated liy the fusion
of anioehoid or motile ijainetes and karyo-ianiy and
extends to the time of the last two nuelear divisions
preecding sporojjenesis during whieh reduetion oe-
curs. while the haploid phase ineludes the sjiores,
zoospores, amoebae, and g.-imetes. However, the
presenee of :i zoosporanjri.-il st.-ige in the Plasmodio-
Jihorales and the possibility th;it tlie zoosporangia
may be gametangia eoni|)lie.ites the situation, and
until more is known about this developmental ))hase
it is impossible to say how elose the Plasmodiopho-
rales and Mycetozoa are to each other.
PlASMODIOPHORALES AN-D CllVTRIDIALES
As has been noted in the historieal review, the sug-
gested relationship of the Plasniodiophorales with
the Chytridiales involves principally the families
Woroninaceae. Synehytriaceae. and certain members
of the Olpidiaceae. Reports of relationship with the
Synehytriaceae are based ])riiuarily on tlie fact that
the thallus in this family functions as a prosorus and
segments into a number of zoosporangia as in some
genera of the Plasniodiophorales. It must be noted,
however, that this thallus is haploid in the Synehy-
triaceae. according to Curtis, Kusano, Kohler and
others, while in the Plasniodiophorales it is believed
by numerous workers to be di]jloid. Outside of the
formation of sporangiosori in both families, there is
little or no further similarity. The presence of pos-
teriorly uniflagellate zoospores and gametes in the
Synehytriaceae jirecludes, in my opinion, any close
affinity. Furthermore, the presence of a membrane
around the mature tliallus, lack of amoebae and
naked plasmodia. and the absence of schizogony, as
well as the fact that the zygotic thallus does not seg-
ment and form numerous resting spores or cystosori
are other outstanding differences which are difficult
to reconcile.
In certain members of the Olpidiaceae, particu-
larly species of Rozella, the thallus has been de-
scribed as naked, plasmodium-like, and indistin-
guishable from the host protoplasm. In the septi-
genous species of this genus, the thallus is further-
more reported to segment into numerous portions
which develoj) into zoosporangia or resting s))ores.
However, as the author ('1-2) has pointed out else-
where, the ))resencc of a plasmodium with this type
of development has not yet been conclusively dem-
onstrated for Rozella. In Prinffsheimella, on the
other hand, the evidence of segmentation of the thal-
lus and the formation of sjiorangiosori is more con-
clusive, according to Coucli's ('39) observations.
Certain genera of the Olpidiaceae like Rnzt'Ua and
Prinrishi-imi'Ua have thus been described as resem-
bling species of the Plasmodiophorales in the devel-
opment of s))orangiosori. On the other hand, they
differ fundamentally by their posteriorly uniflagel-
late aoos])ores. The contention of Winge that Sorol-
pidiiim lU'tac, Rhlzomij.va hypoijaea, and Aiimomiixa
l*lanta<iinis are transition species between the Plas-
inodiojihorales and Chytridi;des is no longer ten.able,
bee.'iuse these species li.ave siiu'c been shown to be-
long to the former order. Therefore, the evidence of
rel.itionsiiip between these two grou))s is very mciger
;ind inconelusi\e at ])resent.
The family Woroninaceae is .'it present a conven-
ient dumping ground for all holocari)ic, Oomycete-
like species with biflagellate zoospores, and as such is
not a coherent group of closely related genera. In
light of |)resent-day knowledge it should be seiiarated
from tlie Chytridiales ])roper, which have uniHagel-
late zoos))ores. Therefore, a discussion of the rela-
tionship between the A\'oroniiiaeeae and Plasmodio-
phorales under the present heading is in a sense con-
tradictory. Nevertheless, it may be conveniently in-
serted here without offense to logic. The life cycle of
some species of IVoronina, particularly W . poli/-
ci/stis, as far as is now known, is strikingly similar
to that of several members of the Plasmodiophorales,
as Zopf, Maire and Tison (11), A\'inge, and others
have already eniiihasized. In light of the recent dis-
covery of Polyrntjjra and Octomyia by Ledingham,
Couch, ct al., these similarities have become more sig-
nificant and need to be emphasized again. With the
l)ur])ose of so doing I have reproduced in Plate 16
the life cycle of JV. poli/c//stis. In this species the
contents of the zoospore enters the host hypha as a
naked jjrotoplasmic mass (fig. 6-10). undergoes
amoeboid changes in shape, develops into a plasmo-
dium-like thallus as it feeds on the host protoplasm,
and causes local liy])ertrophy (fig. 11, 12).
At maturity the thallus cleaves into segments (fig.
13. 1 1) which develop into zoosporangia (fig. 1.5, 16)
and form a typical sporangiosorus. As in Octomifxa,
the jieripheral zoosjjorangia are usually independent
with a single exit pa])illae, while the deeper lying
ones may be confluent with a common papilla for
zoospore emission. Each sporangium produces a
number of biflagellate zoospores (fig. 18—21) which
reinfect the host hyphae. As the culture becomes
older, the thalli cleave into small segments which be-
come the resting spores. These remain closely at-
tached and form compact cystosori of various sizes
and shajies (fig. 23-2.5). As in Lif/niera and Poh/-
mi/JTii, the cystosori may be elongate, irregular, flat-
tened, oval and almost spherical, and include a few
to numerous polygonal spores, whieh j)roduce zoo-
spores in germination.
As to the structure of the zoospores of li'. poli/-
ci/xlis, there is. however, considerable disagreement
among students of tliis s))ecies. Fischer described and
figured them as ellipsoidal (fig. 1) with a slight in-
dentation at one side and two unequal flagella. The
shorter flagellum arises from the anterior end and ex-
tends forward in swimming, while the longer one is
inserted laterally and ))rojects backward. It must be
noted, however, that I''iseher's descrijition was not
.•ip|)lied directly to If ■ pi>li/ci/sti.i but relates to the
zoospores of Rozi'lla, Olpidiopsis, and IVoronina as a
group. Cook and Nicholson ('33), on the other hand,
86
PLASM ODIOPH OR ALES
described the zoospores as spherical (fig. 3, I) with
two anterior flagella which lasli back and forth in
breast-stroke fasliion in swimming. These workers
were non-committal as to the relative lengths of the
flagella, but most of the figures show them to be equal
in length. One of their figures (fig. 3), however,
shows flagella of unequal length. If the zoospores are
anteriorly biflagellate, as Cook and Nicholson con-
tended, and heterocont as Fischer reported, they do
not difter fundamentally from those of the Plasmo-
diophorales. In view of the wide differences in ob-
servations it is not altogether improbable that what
is now called W. polycystis may relate to more than
one organism or species. Further critical studies on
this species are therefore highly essential.
So far schizogony has not been reported in Jf.
polyci/stis, and nothing is known about the type of
nuclear divisions in the vegetative thallus. This para-
site has never been studied critically from fixed and
stained material, and it is not improbable that fu-
ture investigations may reveal the occurrence of schi-
zogony and "promitotic" divisions. It should be
noted in this connection, however, that the sporangia
and resting spores of W. poli/ci/slis give a definite
cellulose reaction, while those of the Plasmodiopho-
rales do not. Furthermore, in germination the content
of the zoospore enters the host through a penetration
tube, leaving the empty case on the outside of the
host cell as in Olpidiopsis, Rosella, etc. In the Plas-
modiophorales the zoospores are reported to enter
directly. The latter difference may not be important,
but the presence of cellulose is fundamentally sig-
nificant, according to present-day students of phy-
logeny.
The other species of Woronina, W. glomerata,
JV. af/c/regata, W. elegans, and W. asterina, are not
well known, and it is difficult to compare them with
the Plasmodiophorales. Woronina glomerata para-
sitizes J'aucheria and causes septation of the fila-
ments without hypertrophy. It forms both sporan-
gio- and cystosori, but the resting spores and spo-
rangia are not closely aggregated and compact like
in 11'. polyci/stis. Motile zoospores have not been
illustrated, so that nothing is known about the num-
ber, position, and relative lengths of the flagella. The
zoospores apparently enter the host directly, divide,
according to Zopf ('9-i, p. 54), and form amoebae,
which may in turn divide. The amoebae feed on the
host i^rotoplasm and engulf starch grains, chloro-
phyll granules, etc., whereby they may become quite
green in color. This food is held in well-defined vac-
uoles, according to Scherffel ('25), and shortly be-
fore the parasite fructifies, the extraneous waste ma-
terial is extruded as in typical proteomyxean species.
The amoebae later unite by fine strands or pseudo-
pods and form a reticulate plasmodium, which may
completely fill the host cell. The amoebae may sepa-
rate again, but at maturity tlie plasmodium cleaves
into segments or "Theilplasmodien," each of which
becomes a sorus of zoosporangia or resting spores.
This division of amoebae and plasniodia is sugges-
tive of schizogony in the Plasmodiophorales. The
resting spores of Jf. glomerata, unlike those of W.
polycystis and the Plasmodiophorales, function as
zoosporangia in germination and produce numerous
zoospores. Because of its type of nutrition, Zopf and
Scherffel regarded W . glomerata as an organism
with animal and fungal characteristics and included
it with tlie zoosporic Myxozoidia or Proteomyxa. It
may be noted, however, that W. polycystis also feeds
directly upon the host protoplasm by bodily taking
in globules of oil, according to Cook and Nicholson.
Except for the possession of biflagellate zoospores
and an intramatrical holocarpic thallus, the other
known genera of the Woroninaceae, with the pos-
sible exception of Rosellopsis Karling ('4'2b), do
not appear to have much in common with the Plas-
modiophorales. In the polysporangiate, septigenous
species of Rosellopsis, the thallus has been described
as naked and plasmodium-like, and undergoes seg-
mentation to form numerous zoosporangia which be-
come separated by cross septa in the host. Further-
more, in R. simulans the zoospores are anteriorly bi-
flagellate and heterocont, according to Tokunga
('33). However, so little is known about the devel-
opment and cytology of these species that it is im-
possible to draw further comparisons. Tliere are
nevertheless striking similarities in the development
of the Plasmodiophorales and certain species of the
Woroninaceae, particularly W. polycystis, which
suggest a close relationship and common origin. Cook
('33), on the other hand, contended that these simi-
PLATE 16
Fig. 1, 3. Biflagellate zoospores. Fischer, '83.
Fig. 3, 4. Anteriorly biflagellate zoospores. Cook and
Nicholson, "33.
Fig. 5, G. Early infection stages. Fischer, I.e.
Fig. 7. Same. Cook and Nicholson, I.e.
Fig. 8-10. Amoeboid changes in shape and position of
young parasite in host cell. Fischer, I.e.
Fig. II, 13, 13, 15. Successive stages in develojmient of
the parasite and its cleavage into a sporangiosorus. Note
local hypertrophy and septation of host hypha. Fischer, I.e.
Fig. 14. Vacuolate thallus undergoing centrifugal cleav-
age. Fischer, I.e.
Fig. 16. Sporangiosorus. Cornu, '73. According to Couch
('39) this figure relates to P. dioicii.
Fig. 17-30. Maturation, cleavage, and emission of zoo-
spores from a sporangium. Fischer, I.e.
Fig. 31. Small empty sporangiosorus. Cornu, I.e.
Fig. ^2-2. Cleavage of thallus into a eystosorus. Fischer, I.e.
Fig. 33. Mature eystosorus. Cornu, I.e.
Fig. 34. Septate, locally hypertrophied hypha of Sapro-
leffiiid with five cystosori of various sizes and shapes and
two emiity sporangiosori. Fischer, I.e.
Fig. 35. Elongate irregular eystosorus. Cook and Nichol-
son, I.e.
Fig. 36. Variously-shaped resting s))ores from a eysto-
sorus. Fischer, I.e.
Fig. 37, 38. Thick-walled resting spores. Cook and
Nicholson, I.e.
Fig. 39. Germination of eystosorus. Resting spores swell-
ing and vesiculating to become zoosporangia. Fischer, I.e.
Fig. 30. Germination of resting spores. Cook and Nichol-
son, I.e.
lMlYI.()(iKNV AN"1) IlK.I.ATIONSllll'S
IM.ATK 1(5
87
Woronina polycystis
88
PLASMODIOPHORALES
larities are incommensurable and that the two groups
have but little in common. Most of the objections
raised by Cook, however, are no longer tenable in
the light of more recent discoveries in the Plasmodio-
phorales.
Plasmodiophorales, Proteomyxa, and Other
Protozoa
Inasmuch as the names Monadineae, Myxozoidia,
and Proteomyxa are more or less synonymous and
have been ratlier loosely used in the literature, a brief
discussion of tiieir terminology is essential before
proceeding to the questions of relationship with and
origin of the Plasmodiophorales from this group of
simple organisms. The term Monadineae was first
employed by Cienkowski ('65) for a number of
primitive organisms whose vegetative reproductive
cell develops into amoeboid or plasmodial thalli
which are capable of engulfing solid food particles.
Following the feeding and growing stage the thalli
develop distinct membranes, discharge the extrane-
ous food material into a large vacuole, undergo cleav-
age, and form zoospores or small amoebae. At the
conclusion of this phase, resting spores are formed.
Cienkowski divided these organisms into two groups,
Monadineae zoosporeae and Monadineae tetraplas-
tae, depending on whetlier zoospores or Actinophrys-
like amoebae are produced. Many of these aquatic
monadinaceous species were later included by Klein
('82) in a new family, Hydromyxaceae, but this
name was not widely accepted at that time. More re-
cently, however this family was emended by Jahn
('28), raised to ordinal rank, and included as the
first order of the Myxomycetes. In 1884 Zopf gave
an extended account of the Monadineae in his book
on the "Pilzthiere or Schleimpilze" in which he con-
tinued Cienkowski's terminology for the whole group
but changed the division Monadineae tetraplastae to
Monadineae azoosporeae. The following ye ir, how-
ever, Lankester created a new class, ProtL.imyxa, of
protozoa to include the Monadineae of Cienkowski
and Zopf as well as Plasmodiophora and Tetramyxa.
In 1 893 Klebs pointed out that continued use of the
term Monadineae in the sense of Cienkowski would
lead to confusion inasmuch as this name had pre-
viously been applied to a group of flagellates of
which Monas is the type genus. Zopf ('91) accord-
ingly proposed an alternate name, Myxozoidia, for
Cienkowski's Monadineae. Doubtless because Zopf's
paper was not published in a prominent journal, his
term did not become generally known. Lankester's
term was accepted by most protozoologists and has
accordinglv displaced the terms Monadineae and
Myxozoidia in the literature on protozoa. Proto-
phytologists, however, have continued to use Cien-
kowski's term. According to present-day interpreta-
tions the Proteomyxa embraces several families of
incompletely known rhizopod-like species, which
protozoologists include in the sub-class Rhizopoda
of the Sarcodina. For the sake of emphasis and clar-
ity, relationships with the Proteomyxa will be dis-
cussed here apart from the Protozoa in general, but
such treatment does not imply that this order is to
be excluded from the Rhizopoda.
As Zopf early pointed out, the life cycles of cer-
tain monadinaceous species, particularly of the fam-
ily Gymnococcaceae, are similar in many respects to
those of the Plasmodiophoraceae, and for this rea-
son he included both families in the same division of
the Monadineae. Subsequent studies by de Bruyne
('90), Scherffel ('2.5), and others have supported
Zopf's observations and emphasized these similari-
ties even more fully. As a result of such studies, some
of these proteomyxean species are now known to
have anteriorly biflagellate, heterocont zoospores,
PLATE 17
Physarella, Fulii/o, and Diclymiiim
Fig. 1. Anteriorly uniflagellate zoospore of Physarella
oblonc/a with two "basal bodies." Sinoto and Yuasa, '34.
Fig. 3. Biflagellate heterocont zoospores of P. ohlonga
with two "basal bodies." Note tail piece at end of flagella.
Sinoto and Yuasa, I.e.
Fig. 3. Biflagellate isocont zoospore of P. ohlonga with
two "basal bodies." Sinoto and Yuasa, I.e.
Fig. -1. Triflagellate heterocont zoospore of Fuligo sep-
tica with two short flagella attached to one "basal body."
Yuasa, '35.
Fig. 5. Biflagellate heterocont zoospore of F. scptica
with "two basal bodies." Yuasa, I.e.
Fig. 6. Biflagellate heterocont zoospore of D. Xanthopus
with several "basal bodies." Stosch, '35.
PgeiidoKporopsis, Amijlophagus. Gymnococnts, and
Aphelkliopsts
Fig. 7, 8. Anteriorly biflagellate heterocont zoospores of
Pseudosporopsis sp. (Bodo ylobosus) with numerous en-
gulfed food particles. Short flagellum extending forward.
Scherffel, '-'5.
Fig. 9, 10. Zoospores of same with contractile vacuoles
and nucleus. Scherffel, I.e.
Fig. 11. Anteriorly biflagellate heterocont zoospores of
Amylophayus algarum with two contractile vacuoles. Long
flagellum extending forward. Scherffel, I.e.
Fig. li. Amoeboid stage of same. Scherffel, I.e.
Fig. 13. Anteriorly biflagellate heterocont zoospore of
P. rotatoriorum witb two contractile vacuoles; long flagel-
lum extending forward. Scherffel, I.e.
Fig. U. Anteriorly biflagellate zoospores of .1 phelidiop-
six epithemiae. Scberftel, I.e.
Fig. 15. Large plasmodium ( ?), J. epithemiae, with ex-
traneous food material in a large central vacuole. Scherf-
fel, I.e.
Fig. 16. Zoocysts of J. epithemiae. Scherffel, I.e.
Fig. 17. Deliquesced zoocysts and emerging zoospores of
./. epithemiae. Scberffel, I.e.
Fig. 18. Eleven zoosporangia, five of which are filled
with zoospores, from a single tballus of G. Cladophorae :
extruded waste material between sporangia. De Bruyne,
'90.
Fig. 19. Zoocyst of -/. algannn. Scherffel, I.e.
Fig. -20. Emergence of zoospore through zoocyst wall in
./. algarum. Scherffel, I.e.
Fig. 21. Sporocyst of P. rotatoriorum with six resting
spores. Scberffel, I.e.
Fig. 22. Resting spores of J phelidiop.iis epithemiae.
Scherffel, I.e.
I'llVUMiKNV AMI HKl-ATlO.NSIlll'S
ri.ATE 17
89
Myxomycetes, Proteomyxa
90
PLASMODIOPHORALES
naked plasmodium-like thalli, zoocysts, and sporo-
cysts. When aggregated the latter two structures are
comparable with the loose sporangio- and cystosori
found in plasniodiophoraceous and woroninaceous
species. Aphelidiopsis, Gymnococcus, Pseudosporop-
sis and Amylophagits may be taken as examples, and
for the sake of more concrete comparisons drawings
by de Bruyne and Scherffel of the zoospores and
some developmental stages of these genera have been
brought together in Plate 17. The zoospores of Pseu-
dosporopsis sp. {Bodo filobosus Stein, fig. 7-10),
Amylophagiis algarum (fig. \\-\2).P.rotatoriorhim
(fig. i3). and Aphelidiopsis epithe7nine (fig. li),like
those of the Plasmodiophora, Octomyxa, etc., have
two unequal flagella at the anterior end. In B. c/lo-
hosus and A. cpithemiae the short flagellum extends
forward and the longer one backward in swimming,
while in the other species the relative positions are
reversed. The zoospores may become amoeboid, and
engulf solid food particles (fig. 7, 8), and include a
well-defined contractile vacuole. In tiie latter two
characteristics they appear to differ sharply from
the zoospores of the Plasmodioijhoraceae, but as has
been noted before the zoospores of Polymyxa gra-
minis and the young plasmodia of /,. J unci are said to
engulf algae and particles of food.
In all these species, except A. epithemiae and
Gymnococcus Cladophorae, the developing thallus
becomes invested with a membrane and forms one
zoocyst or zoosporangium (fig. 19). There is no
cleavage into segments and development of a spo-
rangiosorus, according to Scherffel. In A. epiihe-
miae, on the other hand, the type of development is
more like that of the Plasmodioplioraceae. The con-
tent of the zoospore enters the host, leaving the
empty spore case on the outside, feeds upon the host
protoplasm, and develops into an oval vacuolate thal-
lus (fig. 15) which appears to be naked or devoid of
a well-defined membrane. At maturity this plasmo-
dium-like thallus cleaves into from 2 to 8 segments
(fig. 16) which round up, form tliin membranes, and
become zoocysts. These vary greatly in size and in
the number of zoospores they produce. Small zoo-
cysts may form only 3 to 4. zoospores. No exit papillae
for the emission of zoospores are developed, and at
maturity the wall deliquesces and disappears (fig.
17) freeing the zoospores simultaneously. In G. Cla-
dophorae, however, the wall is thicker, more perma-
nent, and remains after the zoospores have emerged
(fig. 18). No exit papillae are present here also, and
the zoospores doubtless bore through the sporan-
gium wall as in A. algarum (fig. 20). Scherffel did
not observe resting spore formation, but his illus-
trations (fig. 22) suggest that they may be formed
in the same manner as the zoocysts. They lie free in
the host cell without an enveloping membrane. In P.
rotatoriorum as many as 8 resting s])ores are formed
in a sporocyst (fig. 21), but in this species they are
held together by a membrane. Germination of the
resting spores has not been observed.
It is to be particularly noted that the type of nutri-
tion in these species is animal-like. The zoospores.
amoebae, and developing thalli engulf chlorophyll
granules, starch grains, oil globules, etc., apparently
digest them in the food vacuoles, and extrude the
waste material shortly before sporogenesis. No con-
clusive evidence of this type of nutrition has been
found in the Plasmodiophoraceae, and this appears
to be one of the chief differences between these two
groups of organisms at present.
Comparison on the basis of sexuality, time and
place of meiosis, alternation of generations, etc.,
cannot be made, because very little is known about
these processes in the Proteomyxa. No good evidence
of fusion of amoeboid or motile gametes has been ob-
served in the biflagellate species. Likewise no evi-
dence of schizogony, "promitosis," "akaryosis" or
anj^ other reported cytological characteristics of the
Plasmodiophoraceae have been observed, but so far
Pseudosporopsis, Aphelidiopsis, and other similar
genera have not been intensively studied from fixed
and stained material. It is accordingly premature to
draw conclusions on these grounds.
The belief that the Plasmodiophoraceae are re-
lated to Protozoa, exclusive of the Proteomyxa which
have already been discussed, stems primarily from
the views of the protozoologists who have included
this family among the primitive animals. Proto-
phythologists in general have opposed this view on
the grounds that the Plasmodiophoraceae are fungi.
There are, nonetheless, certain specific structural,
developmental and cytological similarities among
the Rhizopoda and Sporozoa on which this belief is
based. The suggested relationship with the Sporozoa
relate to similarities in life cycles and asexual repro-
duction by schizogony, while in the Rhizopoda, ex-
clusive of the Proteomyxa, it concerns the occurrence
of "promitosis" and the extrusion of chromidia. The
Sporozoa are spore-forming parasites of animals,
some species of which may cause marked hyper-
trophy of the host cell and form galls or cysts. In
certain species of the Myxosporidiae the spores give
rise to amoebula which penetrate the host tissue,
grow in size, and undergo schizogony, cutting off
uninucleate schizonts. Each schizont develops into
a multinucleate amoeboid plasmodium or trojiho-
zoite and divides into sporonts at maturity. The lat-
ter grow in size as their nuclei divide several times,
become sporoblasts, and form a variable number of
spores, which are usually liberated as the host tissue
degenerates, and cause secondary infection. In these
respects certain sporozoan species resemble the Plas-
modiophoraceae, but further than this the similarity
is not very striking. However, the occurrence of schi-
zogony is particularly noteworthy. This is a common
and widespread method of asexual propagation in
the Sporozoa, and has also been reported to occur in
most genera of the Plasmodiophoraceae. That its oc-
currence in both groups together with the production
of numerous spores indicates jihylogenetic relation-
ship is, however, highly questionable and doubtful,
as Maire and Tison ('09) have already pointed out.
The contention that the Plasmodioiihoraceae show
affinities to the strictly amoeboid Rhizopoda or
I'li'i 1 i)(;knv and Hi:i..\rioNfimi"s
91
AnuH'biiia is IkisoI primarily on tlu' nportiil simi-
larity hftwccn till' vi-_s{i'tiitivc mu-K'ar divisions in the
plasniodiuni and the (iroinitotic divisions in the liina.r
srronp of .tmoilui. Cook (^'28), as noted elsewhere,
held this similarity to he of ureat ])hyloiienetie sijr-
nitieanee and aeeordinijly helie\ed that the I'lasnio-
diophorales have oriicinated from the lohosoid amoe-
bae. Home (^'30) severely eritiei/ed Cook's view.
and after reviewing the variations of nuelear division
exhibited by the fungi, algae, and i>rotista. eon-
eluded that "the use of criteria relating to the type
of nuelear di\ ision is of very doubtful \alue at the
present time in diseussing the aetual relationshi)) be-
tween grou)) and group."
The reported similarity of promitosis in certain
amoebae and the Plasmodiophorales has been fully
presented in Chapter 1 1 and need not be discussed
further at this point. Suffice it to repeat that Home,
Terby and Webb have refuted the rci)orts of pro-
mitosis in the Plasmodiophorales and described the
formation of well-defined chromosomes during the
vegetati\ e divisions. Furthermore, Miss Terby found
that the mieleole does not persist and divide into two
parts which are later ineorjiorated in the daughter
nuclei as the new nucleoli. Instead, the nucleole may
fragment and portions of it become stranded in the
cytoplasm between the nuclei, while the daughter
luicleoli are formed anew in the telo|)hases as in
higher i)Iants. There is accordingly no universal
agreement that jiromitosis, in the strict sense of
Xagler. occurs in the Plasmodiophorales. Xor is pro-
mitosis, in the modified sense of later workers re-
stricted to the lobosoid amoebae. Intranuclear divi-
sion with ill- or jjartly-defined chromosomes and
large persistent elongating, constricting, and divid-
ing nucleoli have been figured and described in spe-
cies of the Rhizomastigina. Thecamoebina, Coccidia.
Mvxosporidia, Englenoidina and .Siphonales. A simi-
lar persistence and behavior of the nucleole during
division has been recorded by N'emec (00). Mano
('Oi), Wager {'01). I.undegardh ('12), and Tahara
('1.5) for Alniis, Phaseolus, Solatium, Cucurbiia, and
Helianthiis, resi)ectively, where the process has been
referred to as ))seudoprotomitosis. On this basis, ac-
cording to Cook's line of argument, the Plasmodio-
phorales ;ire related in varying degrees to a large
number of .inim.il and plant families. Persistence
and division of the nucleole in the manner described
above, therefore, does not appear to be of much sig-
nificance, and as Doflein, Ti.schler ('22), Terby
('24). Belar, and others have |)ointed out. it may be
found in various grou])s of organisms under certain
conditions. In light of these data it seems highly
doubtful that certain similarities in type of nuclear
division are an index of ])hylogenetic descent and
relationship.
It is obvious from this discussion of ijhylogcny
and relationshij) that the Plasmodiophorales have
some develo))mental phases and cytological char-
acteristics in conmion with the Myeetozoa. Protozoa.
and jjolysporangiate s])ecies of the \\'oroninaceae.
Whet!ier this order has originated directly from such
groups or de\el(>peil along |).'ir.illel lines with them
from a distant eonnuou ancestor, however, is still
UMt'crtain. Our kiunvledge of the critical stages in
the life cycle of the Plasmodio])horales as well as in
the groujis with which this order shows .-iftinity is too
incomplete to w.-irrant detinite conclusions at |)res-
ent. I'urther intensive study of these st.iges as wi'll
as the discovery of new sjiecics will (buibtless in-
validate many of the iiresent-day beliefs concerning
the Plasmodiophoraceae. Likewise the similarities
this family has in common with other groujis, which
now ])oint to definite lines of origin and relationshi|),
may in the future ))ro\e to be ])hylogenetically insig-
nificant.
Xe\ ertheless. the Plasmodiophorales at jiresent
appear to be similar to JVoronlna pol i/ci/slis and the
biflagellate heteroeont species of the Proteoniyxa in
zoospore structure, and general type of development.
This similarity, of course, does not necessarily mean
a eonnuou origin and close relationship. It may
equally well be nothing more than ))arallelism in
development from se)iarate ancestors. This rela-
tionshi)) has. nonetheless, been emphasized rather
strongly in the discussions above, primarily with the
hope of encouraging intensive research along these
lines.
\'ery little can be said at present about relation-
ships within the order itself, because the life cycles
of many species are not fully known. Furthermore
the genera are not sharply defined. As is indicated
in Cha))ter III, the relation and arrangement of the
resting spores is rather generally regarded as an
index of relationships and relative complexity. On
this basis Plasmodiophora has been regarded as the
most primitive genus, because its resting spores are
not united in cystosori. Tetrami/.ra, and Octomi/.ra,
with spores in tetrads .and oetads res])ectively, are
accordingly next in line. Sorosphaera and Sorodi.sciis
at present seem similar to these two genera in that
uninucleate spore mother cells or sporonts are de-
limited in wliich the meiotic divisions later occur.
Whether or not this is an index of relationship is,
however, questionable. Poli/mi/xa has the most ex-
tensive and complex zoosjiorangial stage of all
known genera, but its cystosori resemble those of
Lif/niera, a genus which Cook ('33) regarded as
primitive.
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CLl"!! HOOT OF inr< IKKRS
98
riiMpt.r VI
Diseases Caused by Species of Plasmodiophoraceae
ALTHoriiii ALL known species of tliis family arc
parasitic only two members are economically ini))or-
tant as pathosrens of food crojis. As noted elscNvhcrc.
Plaxmodiophora linisxicac and Sponc/ospora siihtcr-
ranra cause diseases of crucifcrs and potatoes re-
s])ectivcly. which are eonimoidy known as eluh root
and powdery seal). The other species jjarasiti/.e
fungi, aljiae. cryijtojiams. ;ind wild or seldom culti-
vated higher plants.
CLIH HOOT OF CRrCIFERS
Club root is a destructive root disease of wild and
cultivated erueifers which is world-wide in distribu-
tion in temperate climates and known throughout the
world by a large number of common names. In Eng-
land. Scotland, and ^^'ales it is known as finger and
toe disease, anbury, hanbury. ambury. club root and
clubbing; in Russia as hernia or Kapoustnaja kila ;
Kro|)fkrankheit des Koliles. Kohlhernie. Klumpen-
fuss. Knotensucht. Fingerkrankheit. Kelch, Galle.
Knolle. Huas, Kuss, etc.. in Germany. Switzerland
and Austria ; Gros pied, maladic du Chou, and hernie
du Chou in France; Tubereulosi dei cavoli and Mai
de gozzo dei cavoli in Italy; Knoelvoet in Holland;
Kwab. Kwabbe. Kwabbeziekte. Knol. Knolziekte,
Kiinker. Knoo]). Knuist, Knobbcl and Kwabbel in
Belgium; Kaalbrok in Denmark: Klum))rots juka in
Sweden ; Dik Voet in South Africa ; club foot and
club root in U. S. A. ; and by various other names in
other countries. According to ^'anderyst ('04, p. 518)
the name Vingerziekte used by Woronin and numer-
ous subsequent writers for the disease in Belgium is
unknown in that country.
From the economic standpoint club root is the most
important disease of cultivated erueifers. In badly
infested fields entire cro])s may be destroyed unless
stringent control measures are employed. In Ger-
many. England. Russia, the U. S. A., and other coun-
tries in Europe, Asia, and Africa .50 to 100 per cent
destruction of turnips, swedes, cabbages, etc., has
been rel)orted ( Brunchorst. '87; Rostrup, '93. '91;
Halsted. '93-'99; Eyeleshymer. '94; I.aubert, '0.5;
Reniy and Liistner. '11 ; (ieorgeson, '16; Gleisberg.
'20; Korff and Boning. '27. and others). \\'oronin
('78) rejjorted that in 18()9 the loss in the vicinity
of St. Petersburg alone amounted to more than
$20,000,000. while Heri)ers ('25) estimated that the
annual loss in Ciermany runs into millions of marks.
In New York .State alone a loss of sever;d thousand
tons of cabbage were reported by Haskcl and Mar-
tin in 1918. Edson. Miller and Wood ("3.5, '3(>. 37)
have subsequently rei)orti(l losses of 5 to 100 per
cent in cruciferous ero])s throughout the U. S. A.
The most significant fact about club root is that it
spreads ra))idly, and once it lias become established
in the soil, it uiakts the fields almost useless for
crueifer cultivation for a number of years.
Tlie origin of club root is unknown, but its symp-
toms had been well described more than a century
before \\'oronin showed it to be due to a ))lasniodio-
])lioraeeous organism. According to Biiliner ('22),
the disease is as ancient as its hosts. The occurrence
of spongy, fungus-like roots (radices fungosae) of
erueifers noted by Albert the (Jreat as early as tlie
i;ith century is supposed to relate to club root, and
his control practice of avoiding fresh stable manure
and the disposal of chaff appears to have been ac-
quired from the Roman Pallatius, according to
Bohiur. The disease was well known in Spain in the
l.)th century where cabbages were described as being
sy))hilitic (see \\'oroiiin. '78, p. .552), and the swell-
ings were thought to be due to the organism causing
syjihilis (Ruiz Diaz de Isla). The first report of its
occurrence in England was made by Ellis in 1736,
who believed the disease was contagious and due
probably to an excess of barnyard manure. Adam
discussed its wides])read occurrence in England in
1789. and it was subsequently reported in Scotland
from 1829 to 1831 by Farquharson. Abbay. and
Birne who thought it to be due to unsatisfactorv soil
conditions or unbalanced fertilizer practices. Abbay
saw the disease as early as 1801, and Anderson
stated tliat it first became troublesome in Scotland
about 1813. Renard rejiorted that it was first ob-
served on cauliflower in 1820 in France. By 1853 it
was fairly abundant around Hamburg. Wurzburg,
in the Rhine valley and other |)arts of Germany
(N. N. '53), and from 1855 on it appeared in vari-
ous parts of Norway (Jorstad, '30). Other workers,
including Curtis ('IS), Kiihn ('58), Henderson
('67). Sorauer ('7^), Slingerhand ('94'), and others
(see Woronin '78, pp. 552-55 1) believed it to be
due wholly or in jiart to various insects and other ani-
mals. Buckman ('5i), however, claimed that club
root was due to reversion to the original wild forms.
By 1872 the disease had become so widespread and
destructive around St. Petersburg that the Royal
Russian Gardening Soeietv in St. Petersburg offered
a iirize for the solution of the cause and control of
hernia. \A'oronin began to study the disease inde-
))endeiitly of this ofl'er in 1873. and two years later
he announced th;it it is caused by a |)lasniodiopIio-
raceous organism to which he subsequently ('78)
gave the name I'Jasmudiopliora Brassicae.
Symptoms
Club root disease is iisu.'illy characterized by
marked enlargement of the infected roots (PI. 2. fig.
1 ). and in exceptional eases tlie galls on cabbage may
reach the size of a man's fist and appear greasy-gray
and pale-yellow in color. In most cases the clubs are
91
PLASJIODIOPHORALES
regularly spindle-shaped, but when several infec-
tions occur togethtr the swellings may fuse and pro-
duce irregular growths or compound spindles (fig.
3). According to Kiister ('11) and M. T. Cook ('23)
these galls are kataplasniic, since the affected tissues
usually remain parenchymatous and do not undergo
differentiation. Other root symptoms have also been
reported. According to Appel and ^^'erth ('10), no
hypertrophy occurs in radishes, and the disease is
here characterized only by darkened and decayed
areas. Honig ('31) found similar symptoms on Lu-
naria biennis. Ravn ('22) and Pape ('25) likewise
reported tlie occurrence of deep wounds or lesions on
turnip roots which were filled with spores. Accord-
ing to Pape, such symptoms appear when the galls or
nodular excrescences on the roots decay.
In a study of 101 species from 28 genera, Cun-
ningham ('li) found definite types of hypertrophy
and symptoms more or less characteristic for certain
crucifers and classified them accordingly :
1. Complete clubbing of main and lateral roots.
Brassica oleraceae.
2. Clubs on main root, laterals free. Sisi/mbriiim
altissitnum.
3. Clubs on lateral roots, main root free. Sisi/m-
brium officinale and Erysimum cheiranthoides.
4. Clubs on main and lateral roots with club-free
rootlets above the diseased portion. Lepidium
sativum.
5. Clubs as tumors of the roots. Raphanus sati-
I'US.
6. Dark, decomposing spots on the roots. Rapha-
nus satii'us.
In the last category true hypertrophy does not
occur. The disease is here characterized by cracks,
fissures, and darkened areas in the host tissue whicli
turn black, decay, and serve as sites of secondary
infections by other fungi. As has been noted above,
Appel and Werth claimed that these are the charac-
teristic symptoms of the disease on radishes, but
Cunningliam found them only on the Everlasting
radish, in addition to spindle-shaped swellings of the
rootlets.
Club root disease may also stimulate branching of
the roots and shoot and lead to the production of buds
where they do not normally occur, as has been de-
scribed by Caspary, Woronin, Favorski, and Kunkel.
The secondary roots may attain a length of several
inches or become stunted as short knobs. On tlie other
hand, the production of secondary rootlets may be
greatly inhibited, according to Laubert ('0.5) and
Schlumberger ('11). The diseased buds on infected
roots and shoots are often unable to respond normally
to fi;ravitv, and they may grow downward and hori-
zontally as well as upward. In the latter instances the
infected buds may push uji above the surface of the
ground and give rise to tiiick, distorted, fleshy, and
abnormally succulent leaves and petioles, so that
the disease may occasionally manifest itself above
ground in the shoot, petioles, and leaves. In addition
to tliese above-ground symptoms, club root causes
yellowing of the leaves, wilting on hot days, and in
tlie case of cabbage, atrophy, or complete lack of
head development. Seedlings which are infected
earlv usually die within a few weeks. The wilting
of large diseased plants is partly due to hypoplasia
of the xylem region and to splitting up of the woody
cylinder by infection and expansion of the medullary
rays.
All galls or swellings on roots of crucifers, how-
ever, are not due to P. Brassicae. Nematodes, insects,
and other factors may cause malformations which
are superficially very similar to club root, and unless
microscopic examination of the tissues is made, these
galls may be easily mistaken for those of the finger-
and-toe disease.
Anatomically, the causal organism of club root
affects the cortical parenchyma most conspicuously,
but it also produces marked changes in the cambium,
xylem, and medullary rays. When roots of consider-
able size are infected the amoebae and small Plas-
modia migrate through the cortical parenchyma into
the cambium. Here they follow the path of least re-
sistance, according to Kunkel and Larsen, and
spread up, down, and around the central cylinder
through the delicate thin-walled cambium cells and
form tlnis a cylinder of infected tissue. From the
cambium they may travel laterally into the cortex,
medullary rays, and xylem. Their migration up and
down in the cambium ceases after a while, and the
distance of the infection in these directions deter-
mines the ultimate length of the spindle-shaped club.
Each club, in Kunkel's opinion, is a morphological
unit which has resulted primarily from the abnormal
growth of the cambium. In comparatively old in-
fected roots the medullary ray cells divide a number
of times and enlarge and thus form large bands of
pathological tissue which split and force the xylem
tissues apart, until the latter becomes distorted and
shifted out of their natural position. Separated from
each other in this manner, the vascular bundles grow
out fan-wise instead of remaining wedge-shaped and
are no longer able to function normally. Plasmodia
and amoebae have frequently been found in the tra-
cheids, but they do not seem to have any appreciable
effect on the normal functions of such differentiated
cells. In young roots medullary ray infection is less
common, and most of the abnormal growth occurs in
the region of the cambium and the cortex. The xylem,
nonetheless, may fail to differentiate properly and
is often supplanted by a mass of partially differen-
tiated cells.
As is shown by figure 4, one of the most strik-
ing appearances in sections of diseased roots and
shoots is the presence of more or less isolated groups
of hypertrophied infected cells which Nawaschin
named "Krankheitsherde." He believed that these
groups arise by repeated anti- and periclinal division
of one or more originally infected cells, whereby the
])lasmodia are passively distributed in a radial di-
rection around the region of infection. Cliupp also
reported that a single amoeba might give rise to as
many as six such groups by multi]ilication and migra-
I I.rH ll<)t)T OF ( lUl IKKltS
95
tioii from cell to itll. His ;u'COUllt was sllbscqucntlv
c'oiiririiicd liy K\inktl who holicvfil tliat a siiiitK' in-
foi'tioii may l»'a(l to tlif formation of tlioiisands of
sejtaratf and ilistiiu't " Kraiikluit>lurdc." Kiinkil as-
sumed that as a plasmodium migrates Irom cell to
cell it may divide, whereby portions are left inhind
and lieconK- established here and there in the tissue
and irive rise to siroiijjs of infected cells.
Cclluliir Intenelfitions Hetweeii Host and
I'litliogeri
Plasmotiuiphora lirassicaf has a iironouneed etfect
on infected and healthy cells. Infection may be tem-
Jjorary or permanent, and if the iilasniodium mi-
grates out of a cell before stimulatinn- mueli change,
the latter m.-iv recover and continue to function nor-
mally. Permanently infected cells, however, may ex-
|)and to more than 10 to 20 times their normal size.
In the early stages of infection the presence of the
jiarasite does not inhibit nuclear (PI. 2, fig. 5) and
cell division (fig. 6), so that some cells may function
normally in this respect for a short time. Other cells
m;iy begin to enlarge directly after infection with-
out dividing. Occasionally, cell division may be
affected to the extent that the cell wall is only partly
develo))ed across the mother cell (fig. 6). Even-
tually the jjower to divide is lost completely, and the
infected cell gradually expands to its large size.
Prowazek found that karyokinesis may continue
after cell division has ceased, resulting in binucle-
atc cells. I.utnian also found abnormal types of mito-
sis which al)l)eared to be a modified form of amitosis.
The first visible effect of the parasite on the host
nucleus is an enlargement of the nucleus as a whole
followed by an increase in the number of nucleoli,
according to Lutman (fig. 8-11). By the time the
parasite is mature, the host nucleus has lost its regu-
lar outline, and the nucleoli lie (fig. 1 1 ) in clear
spaces surrounded by a distinct membrane, an ap-
pearance which led Prowazek to assume that smaller
nuclei may be formed in a mother nucleus. In the
final stages of degeneration the chromatic material
collects into irregular strands (fig. 12) and assumes
a peripheral jjosition in the distorted and hypertro-
phied nuclei.
The relation between the protoplasts of host and
|)athogin appears to be very intimate, and little or
no visible antagonism is exhibited. The amoebae and
voung Plasmodia of the parasite lie embedded in the
host proto])lasm (fig. .■), (i. 2(5. 28). and in the living
condition the two are indistinguishable, according to
Woronin, Xawaschin, Lutman, and others. This
close association together with the fact that the in-
fected host cells may continue to divide and function
normally for some time led Xawaschin. f J.iylord. .and
Vanderyst to believe that there is a symbiotic rcl/i-
tionshi)) between the host and ])atliogcii during the
hitter's early developmental stages. The host cyto-
plasm has been described as becoming more vacuo-
late as the jilasmodium enlargj's, but part of the
early change is probably due to the great increase in
xolumc of the host cell whcriby the cytopl;isui is
tliinni-d out. Later, iiowcx cr. .-is the plasmodia mature
.111(1 .ipproacli sporogeiicsis the proto))lasm is .ilmost
completely gone. Infected cells develo]) .m unusually
large amount of tr.insitory starch. ;iccording to Wal-
ker. H;ilsted, and Naw.ischin. whi<-li m.iy be grouped
.1 round the nucleus as l.utni.in h.is shown. These
grains may later be found in the plasmodium (fig.
7-i) and are apparently wholly or jiartly digested be-
fore sporogenesis. Reed ('11) noted an appreciable
iiu'rease in calcium, m.-ignesium, ])otassium, phos-
phoric acid, sulphuric acid, etc., in diseased cabbage
roots. The increase w.is greatest in the case of ))otas-
sium. which he attributed to an accumulation of jiro-
toi)lasm and starch in diseased tissues. Nicolotf and
Stefanova ('22), however, found that roots of dis-
eased cabbage plants were high in protein and lower
in phosphorus and potassium than those of healthy
plants.
Noninfected cells are also stimulated to di\ ide by
the presence of the parasite and may often enlarge
considerably. This is jiarticularly true of medullary
rav cells, which may ex])and until they have lost all
characteristics as such. The nuclei of these cells en-
large also and keep pace to some extent with the in-
crease of cell size. According to Kunkel, the stimulus
travels in advance of the infection, so that increased
cell division may be noted before the parasite reaches
a particular, undifferentiated tissue, which suggests
that a growth-stimulating substance is released by
the causal organism and travels ahead of the plasmo-
dium. Nawaschin, on the other hand, believed that
the division of noninfected cells around the "Krank-
heitsherde" is due to the stimulus of mechanical out-
ward pressure exerted by the enlarging parasitized
cells.
Kunkel suggested that the limitation of the para-
site in groups of cells might be due to a ijrotective
substance or antitoxin ))rodueed by the infected cell
which diffuses out into the adjoining healthy cells
and renders them imnmne to attack. Levine and I.e-
vine ('22) believed that the surrounding cells are
not only immune but present a reactive protective
barrier against the spread of the parasite. The ques-
tion of whether or not infected jjlants can recover
from club root and become immune has often been
debated. Woronin ('78), Eycleshymer ('91), Lau-
bert ('0.5a) and Miiller-Thurgau and Osterwalder
('23) maintained that recovery is impossible, but
Massee ('96), Mathieu-Sanson ('97). Apjiel and
Schlumberger ('13). .Schlumberger ('1 !■), and Wahl-
ing ('22b) rejiorted varying degrees of recovery
when infected ))lauts were treated with a 2 jier cent
(jotash solution, milk of lime, planted in ore mud. and
sterile soil, and watered with sulfur and solibar
solutions. Miiller and Osterwalder transplanted in-
fected plants to heavily limed soil, but found no in-
hibitory effects or recovery. Honig ('31) believed
that if infected i)l:mts are transjjlanted to sterile and
d'sinfcctcd soil the progress of the disease may be
halted, but such ))lants can recover only if they are
sufficiently healthy to begin to grow anew.
9ti
PLASMODIOPHORALES
Entrance and Spread of P. Brassicae
in the Host
Actual penetration of P. Brassicae into the host
was not observed by the early workers, but most of
them assumed that it occurs only when the plants are
young and susceptible. Honig and Rochlin, however,
subsequently demonstrated its entrance through the
walls of root hairs and epidermal cells, although
Woronin, Chupp, Cook, Schwartz, and others had
previously held that the amoebae gain entrance
through the root hairs (fig. 28, 29) and migrate into
the deeper lying tissues. W. G. Smith ('SI), on the
other hand, maintained that the parasite enters as a
Plasmodium. Favorski reported that infection may
take place through ordinary epidermal cells and
stated that Woronin's figures of amoebae in root
hairs relate to Olpidiiim Brassicae. Kunkel found
that old plants are as susceptible as young ones and
that infection of old roots is very common. He fur-
ther refuted the claim that root hairs are of any im-
portance as avenues of infection and concurred witli
Favorski's belief that Woronin had figured thalli of
0. Brassicae and O. borzii in the root hairs instead
of P. Brassicae. Cook and Schwartz, Honig. Roch-
lin, and otiiers, however, have subsequently dem-
onstrated quite definitely that P. Brassicae occurs
in root hairs and thus confirmed the observations of
M'oronin and Chupp. Kunkel, nonetheless, showed
that old plants are susceptible and may become in-
fected as long as they live. Infection through me-
chanical wounds and ruptures caused by adventitious
roots and by the removal of lower leaf petioles at the
time of transplanting is fairly common, according to
Larson ('S-l). The enlargements, however, which are
formed at the region of injury on the stem are defi-
nite spheroid galls in contrast to the spindle-shaped
clubs on the roots.
As to the spread of the parasite in the host tissues
and the channels involved, it is now generally agreed
that it occurs in two ways : by migration of amoebae
and young plasmodia from cell to cell, and by passive
distribution of the parasite through repeated divi-
sions of infected cells. Woronin contended that amoe-
bae and Plasmodia migrate only througli pits and
sieve plates, while Atkinson believed that amoebae
are able to spin out into sucli fine tlireads that they
can enter the roots along with nutrients in solution.
Eycleshymer found plasmodia in xylem vessels and
thought therefore that tliey may travel in the fibro-
vascular bundles. Nawaschin believed that migra-
tion of amoebae from cell to cell is impossible after
secondary thickening begins in the roots, and hence
distribution by division of infected cells is the princi-
pal method of dissemination in old roots. Subse-
quently, Lutman figured and described tlie passage
of small plasmodia from cell to cell, and since that
time Cluipp, Kunkel, Honig, Rochlin, and others
(fig. 31-33) have demonstrated its occurrence. Cook
and Schwartz, more than a decade later, however,
still expressed doubt as to its occurrence. Fedorint-
schik ('3.5) believed that in the early stages of the
disease, migration of amoebae is the principal method
of distribution in tlie host tissues, but after the plas-
modia have formed and begun to mature, further
spread is by division of infected cells. While it is now
generally believed that division of the host cell
greatly increases the number of infected cells, it
nevertheless appears to play a minor role in distrib-
uting the parasite throughout the roots and shoots.'
Dissemination of P. Brassicae in Nature
The club root organism is readily disseminated in
nature in various ways and by numerous agents. It
was formerlj' believed (Atkinson, '89; Carruthers,
'93; Miiller and Osterwalder, '19) that the motility
of the zoospores in moist soil spread the disease, but
Chupp ('17) lias presented evidence to show that
zoospores and amoebae rarely travel more than five
inches. It has also been claimed (Carruthers. Ravn,
'08, and otiiers) that wind is an important agent of
dissemination, but this factor apparently operates
only in the case of light, dry, loose soils and where
strong winds prevail. It has been demonstrated in
heavier and more compact soils that unless the patho-
gen is transferred by some other agent, wind does not
usually spread it from one field to another. Rains and
water are doubtless more important, particularly on
rolling land where the water following a heavy rain
runs off quickly and carries the spores to lower-lying
fields. According to Naumov ('2.5), however, disper-
sal in a radial direction by such means is not very
extensive. Miiller-Thurgau and Osterwalder ('23)
reported tliat in the course of a year club root does
not spread laterally more than 1 Vo to 2 meters in the
ground. Earthworms have also been found to be ac-
tive in the dissemination of club root in small gardens
(Gleisberg, '22; Bremer, '2-t; Fedorintschik, '3.5).
The spores may be carried in the mucilage on the
skin or in the intestinal tract, and virulent forms of
P. Brassicae have been found in the excreta of worms.
Ground moles, root nematodes and insects feeding on
diseased roots doubtless spread the disease to some
extent (Favorsky, '10; Esmarch, '2-1; Beyer. '25;
Chupp, '25; Erickson, '26), but how important they
are as active disseminators is not known.
1 In a paper presented before the meeting of the Ameri-
can Phytopatholofjical Society at Dallas, Texas, December
19+1, Walker reported system infection of cabbage and dis-
tortion of buds, stem, and leaves as follows: "Under green-
house conditions when cabbage seedlings are grown in soil
infested with P. /Jivi.v.fiVfic the pathogen, after infecting the
root, may migrate through the cambium into the stem.
There is relatively little camhial proliferation in the inter-
nodal regions abo\'e the third or fourth leaf. Dormant buds
at the leaf sears, however, are stimulated to grow and be-
come invaded by the pathogen. They become malformed
due to hyperplasia. The organism may reach the growing
point in young |)lants and cause extreme distortion of stem
and leaves. Wlien ]ilants are incK'ulated at above ground
leaf nodes, the pathogen may migrate down the stem, leav-
ing no evidence of proliferation in its path until the hypo-
cotyl is reached, where a typical club is formed. There is
evidence that the reaction of the host is influenced by the
nutrient sujiplied to it." (Phytopath. 'iJ: 18)
I
( l.llt HOOT OK CRl't'IFERS
97
I)is|HTsal l>y tlif (hmp; of livostoi'k fid with dis-
«';isfd roots is wry i-oimiion. 'VUv s])orts rciiiaiii alive
diiriiiii passaiTf tliroiia:li tlu- dijivstive tract, and if
animals wliicli liavc lucn fed on distascd i-rucifers
are let out to i)asturf, the spores are disseminated in
the dropi)ings. Gihbs (,'31) found that the s])ores
may remain viable in fresh cattle droppinjjs for at
least fifteen weeks. They also remain alive for long
periods of time in dung piles around stables, and it
has long been known that the a])plieation of sueh
maiuire to virgin soil introduces the parasite. 'I rans-
port of infected soil on farm implements, laborer's,
lior.se's and livestock feet. etc.. is also ettcctive in
spreading the disease.
Numerous wild cruciferous plants are suscejitiblc
to club root, as has been shown by Halsted ('96-'99),
Ravn ('08), Cunningham ('12), Ssaeharoff ('16),
Nauuiova ('26). Gibbs ('32). Rochlin ('33). Jaraa-
lianen ('3() ) and others, and these hosts often harbor
and peri)etuate the disease in the absence of culti-
vated crueifers. Sueh wild infected hosts have been
found in grass pastures, wayside ditches, river beds,
gardens, and cultivated fields, and their presence on
infected soil reduces the effectiveness of crop rota-
tion in club root control.
Environmental Factors
The degree of infection, development and severity
of club root depends to a large extent on environ-
mental factors, but the manner and extent to which
each factor operates are not clearly understood. The
disease is connnonly believed to be favored by wet,
poorly-drained, acid soils and temperatures slightly
higher tlian those optimum for host root development,
but reports to the contrary have often been made.
Motte ('33). for instance, reported that club root is
most prevalent in light soils and during the dry sea-
son in Denmark.
As to spore germination, many workers have found
it occurs mostly abundantly in acid media. Bremer
('23. '2i. '26). however, reported that H-ion con-
centration is not the sole determining factor. He
found that strong alkalinity inhibits germination of
the sjjores without killing them and that germina-
tion occurs over a j)H range of .5.1- to 7.-5 but not at
pH 8.0. Honig ('31), on the other hand, reported
that sijores germinate as well in alkaline as in acid
solutions: all of which indicates that other little-
known soil factors operating in combination are
equallv as ini]>ortant as H-ion concentration.
Most workers liave. nonetheless, found a fairly
close correlation between incidence of infection and
pH range (^Nlassee, '96; Christensen, Harder and
Ravn, 11 : Ravn, '12-13; Hiltner and Korff. '16;
Neger. 17; Atkins, '22; Bremer, '2J-'28; Lindfors,
'2i. '2.5 : Naumov, '2.5 ; Ludwigs, '2.5 ; Riehni, '25 ;
Tessenow, '26; Cileisberg, '26; Chupp, '28; Briinnle,
'28; Martin. '28 : Blunck. '29; SchafTnit and Meyer.
*30; Beaumont and Staniland, '33; Wilson. '3Ketc.).
I.indfors ('24) observed a marked decline in per-
centage of infection with an increase in soil alkalin-
ity. In .1 pH range of 7.1 to 7. .5, 8.5 ))er cent of the
plants were diseased while .'it ])H 7.8 to 8.0, all
plants remained healthy. Naumov ('2.5) found that
infection occurs most rc;i<lily ;it pH fi.O to 6. .5 with
the optimum near neutrality, .litliougii infection of
seedlings took j)lace within a range of 5.7 to 8. K In
a more intensive study of the problem in 1927 he fur-
ther found that percentage of infection is not con-
sistently correl.-ited with tlic \)\l r.inge. as is shown
bi'low :
300pnis. BaOs per 100 cc. soil pi I. (i.S Infection (1.00%
100 •' pi 1.7.3 " 0.00%
(10 ■• ' ]ni.i.2 " 0.0070
SO •• ' " pH.(i.9 " 11.30%
1,; •• " " " " " pH.7.* " 20.90%
Blunck ('29) likewise found infection occurring at
1)H. 8.8. Further inconsistencies in the literature on
the effects of raising the pH value is shown by the
reports of Martin ('28). Schaffnit and Meyer (30),
\\'ilson ('3rt). and others that club root can be effec-
tively controlled or serious loss prevented by adjust-
ing the pH of the soil to 7.1' and above. Chupp ('28)
;ilso reported that infection does not ordinarily occur
in soils with pH ranges above 7.2 to 7.4.
In 1930 Wellman made a survey of 116 club root
infested fields in Wisconsin and found a pH range of
3.0 to 7.8. In Lithuania. Vilkaitis ('33) found the
range to extend from kO to 7.6. By the addition of
certain chemicals to the soil Wellman modified the
pH value experimentally and found that raising the
H-ion concentration did not consistently inhibit the
disease as is shown below :
).H value Ca(OH)2 CaCO.'s K^COs
7.1 Diseased Diseased Diseased
7.2 "
7.3 Healthy "
7.4 Diseased ■
7.5 Healthy "
7.6 " " Diseased
7.T "
7.8 Diseased
7.9 Healthy
8.0 Healthy
8.1 " Diseased
ft is to be partic\ilarly noted that addition of suffi-
cient amounts of K^jCO:. to bring the (iH up to 8.1 did
not inhibit the disease. In thoroughly infested fields
treated with lime Wellman further found that 3 per
cent of cabbages were destroyed at pH 8.1, and 54
per cent and 49 per cent destroyed at pH 6.7 and 7. .5
respectively. Wellman accordingly concluded from
his tx])eriments that club root occurs in such a wide
pH range that to consider H-ion concentration alone
as an important factor in the occurrence of the dis-
ease is highly questionable.
Since that time other workers have also shown that
club root may occur in a high ])H environment. Beau-
mont and Staniland ('33) reported that while infec-
tion is most common in acid soils, swedes and broc-
98
PLASMODIOPHORALES
coli may become badly clubbed in soils adequately
provided witli lime. In 193 1, however, they reported
that turnips and swedes are unaffected by club root
in soil the pH value of which was raised to 6.76 and
7.02 by liming and concluded tliat pH 6.6 is the prob-
able limit for the disease. Larsen and Walker (31)
also observed that the addition of calcium hydroxide
and calcium or magnesium carbonate in doses suffi-
cient to raise the pH to 7.1 and above did not gener-
ally inhibit development of club root in silty clay
loam soils. In the greenhouse, however, infection was
reduced by the addition of these substances suffi-
ciently to bring the pH up to 7.0. At the pH 7.2 or
above infection was completely inhibited. Whitehead
('36) likewise noted that the disease is generally less
prevalent in alkaline soils but he also found a high
percentage of infection in cabbage, cauliflower and
Brussel sprouts in soils with pH ranges of 7.4.5 to
7.81.
It is obvious from the data presented above that
H-ion concentration in the soil is not the sole deter-
mining factor in infection, development, and severity
of club root. As Naumov and others have pointed out
the intensity of infection is intimately associated
with many external and internal factors, such as de-
gree of soil infestation, moisture content, anatomical
structure of the hosts, specific and varietal suscepti-
bility, etc.
Temperature does not appear to be as important
as other factors in spore germination, infection, and
development of club root, because these processes
may occur under a fairly wide range of temperature.
It was commonly believed that outbreaks of disease
were most severe in cold countries and during the
cool seasons in warm regions, but this belief was not
based on exact experimental data. As to spore germi-
nation Chupp (17) found that it does not occur at
room temperature (16° to 21° C) and that the opti-
mum lies between 27° C and 30° C. He, nevertheless,
obtained host infection at room temperatures, which
indicates that temperature was not the only impor-
tant factor in his experiments. Wellman, on the other
hand, found that spores will germinate within a
range of 6° C to 27° C, with an optimum range of
18° to 25° C. Honig ('31) likewise found that spores
may germinate readily below 21°. As to the direct
effect of soil temperature alone on infection and club
root development very little experimental evidence is
available, but temperature doubtless operates indi-
rectly in conjunction with other soil factors. In care-
fully controlled tests Montieth ('2i) showed that
club root develops at 9° to 30° C. One case of club-
bing was found at 35°, but it occurred on the main
stem near the surface of the soil where contact with
air probably lowered the temperature. Clubbing was
most severe at 25°. ISIontieth concluded that the tem-
perature range over which the disease occurs is more
or less the same as that required by the host and that
temperature itself is not a limiting factor in club
root development. In similar controlled tests Well-
man found that no clubbing occurs below 12° and
above 27°. The optimum temperature for greatest in-
fection and disease production ranged from 18° to
2i°, with the peak for severity slightly above 2i°.
In soil temperatures of 12°, 15° and 27° a fair per-
centage of plants became infected, but clubbing was
distinctly inhibited. The optimum temperatures for
spore germination, infection and development of the
disease determined by Wellman are 5° higher than
those which Tisdale (Jour. Agric. Res. 25 : 55) found
to be optimum (20°) for cabbage root development.
Soil moisture is more significant than temperature
in relation to infection and severity of club root. The
early student of this disease as well as later investi-
gators, including Halsted, Ravn, Cunningham,
Chupp. Whitehead, Reed and others, noted that the
disease is most prevalent in low lying, poorlv drained
soils and severest after periods of wet weather, and
concluded that soil moisture is perhaps the most im-
portant determining factor. These conclusions, how-
ever, were based more on general observations than
on direct experimental evidence. Montieth demon-
strated experimentally the dependence of club root
on high soil moisture and sliowed that cabbage could
be grown free of the disease in heavily infested soil
by keeping the moisture down to t5 per cent of the
total water holding capacity. At 60 per cent club
root was uniformly present. He believed that the
failure of club root to develop in infested soils with
low moisture content is probably due to insufficient
water for spore germination. Montieth's results have
been by and large confirmed by Wellman and Nau-
mov. Wellman, however, demonstrated that con-
tinued high soil moisture is not necessary for infec-
tion and development of the disease. Plants which
had been exposed only 18 hours to infested soil with
80 per cent moisture content became badly diseased
when transplanted to relatively dry infested soil. He
believed that even in a dry season a heavy rain or a
few moderate rains at short intervals might raise the
moisture content sufficiently to insure infection.
Wellman's results may be the explanation of Motte's
report that club root is prevalent during the drv sea-
sons in Denmark. Naumov ('33) likewise found that
cabbage seedlings became infected within a range of
soil moisture from 45 to 100 per cent of the total
water-holding capacity, with the optimum at 80 per
cent. At 30 per cent no development of the disease
occurred.
The physical character of the soil has also been re-
garded as a significant factor in club root infection,
development, and severity. Sandy, humus-rich,
clayey soils favor the disease, according to McAlpine
('03), Bos ('04), Janson ('20), and Naumov ('28).
In Belgium, Vanderyst ('04) reported that club root
occurs abundantly on sandy soils, is generallv ])res-
ent in soils rich in shale, sparse on limey and clavev
soils, and unknown on soils rich in lime. Huniphrev
('92) and Read (11) found the disease to be most
severe on heavy soils and those rich in humus. Ravn
('08) reported that turnips were more susceptible
than cabbage on sandy soil, while on clayey soil the
degree of susceptibility was reversed. Hayunga
('19), Jan.son ('20) and Bremer ('23) found club
« I.III HOOT OK < Hl'( IFEHS
99
root to W loss sovt-rc on niarsli .-iiul Iicatli soils. Soils
poor in liiiu- jifiit-rally favor dtvi-lopniciit of the dis-
ease, accordin'T to Kv(Ksli\ nu'r ('91). Masscc ("5I(>).
Laubcrt ('35a) Hiirkhardt ("15). Tricschniann
("17). Hos ('18). Hronu-r ('23-28) Kindshoven
(•2n. Hall (10). and .\tkins ('22). Nauniov ('27)
found that soils with a lime (in terms of oxide) con-
tent of 0. 1 per eent or more are sienerally free of the
disease. Init Honig ('31 ) reported tiiat in the vicinity
of Munich soils with a 58 per eent linu- content were
heavily infested with clul) root. Herjiers ('2!») and
Honiir ohstrved tli.it the di.sease is very aliundant in
soils which heat up readily.
The jihysical character of the soil also influences
the infective ability of the fungus spores according
to Fedotova ("28). In ordinary grey garden soil with
40.000 s|)ores |>er ec. of soil. 66 l)er cent of the ])lants
became infected, wliile in lilack. greenhouse dirt witli
100.000.000 s])ores per ce. only 12.5 per cent of the
plants were clubbed. N.uimov ('28) also found that
in clayey soils 20.000.000 spores per ce. of soil were
necessary for optimum infection, while in humus-rich
soils 100.000.000 were essential. He. furthermore,
reported that in the vicinity of Leningrad the spores
do not remain viable in the soil in the absence of hosts
for more than three years unless fairly high tempera-
tures and humidity are maintained.
The observations of most of the workers men-
tioned above were not correlated with exact data on
the water-holding capacity and acidity of the respec-
tive tvpes of soil, and it is quite probable tliat the in-
creased infection and severity of club root reported
on clayey, heavy soils and those rich in humus are
due not so much to the pliysical nature of the soils
as to their high acidity and water-holding capacitv-.
Hosts and Dcfjrcc of Infection
Club root was first observed on cultivated cru-
cifers. but later it became evident that wild species
of the mustard family also are susceptible to this dis-
ease. Woronin reported hyi)ertrophied roots of
Ibi'ri.s- in 1878. and some years later Magmis ('93)
and Henning ('96) found other genera and species
attacked by /'. Brass'icao. Halsted ('92-'99) ap]jears
to be the first to have undertaken a more extensive
study of the host range, and since that time this
phase of the disease has been intensively investigated
in various ])arts of the world. Club root is confined to
species of the mustard family, and although reports
of its occurrence on plants outside of this family are
to be found in the literature, they have subsequently
been proven false. The number of hosts is large, and
in the following table are listed the cruciferous spe-
cies which have been examined for the presence of
club root. Included also is the degree of infection
found bv investigators who have studied the host
range of /'. liraxsictie. Previous authors have usu-
ally arranged the genera and species according to
sub-families, but for the sake of convenience they are
listed in alphabetical order below.
Index to .\i-thohs Citko .vxd Deouee of
IxKEiTio.v or Hosts
.\pi)cl = A)i|><-I iiiul Werth ('1(1)
fun. = C'uniiiii;;li!ini {'II)
Clint. = Clinton ClUi)
Da. = Davis {'-■'>)
Erick. = Erirksson ('9(i. ",'())
Gi. = Giblis (•;}-')
Gl. = GleisluTf; (V3)
F. S.= F. .S. (•-'())
Hal. = Halsted (•<).' 'OO)
Ham. = Haininarlund ("l."))
Henn. ^ llinninp ('9())
Hon.= H()nif:C3I)
Host. = Hiisterniann ('-1)
,Tam. = Jamalainen {"Mi)
Katt. = Katterfeld ('23)
Mag. =: .Mapiuis ("93)
Mass. ^Massee ("96)
Mil. =^ Miiller-Tliurgau and (Jsterwalder ('23)
N. N.^ Anonymous ('53)
Naum. ^ Naumann ("13)
N. = N'aumov (■14-' -'8)
Rain.^ Rainio ("303)
Ravn. = Ravn ('08)
Roc. = Roclilin ('33)
Ros.= Rostnip ("93)
Schl. = Schleycr ("07)
Sit. = Sitensky ("98)
Ssach. = SsaciiarofF ('16)
Svec. = Svec. ('-'3)
Weiss. = Weiss ('18)
Wor. ^Woronin ('78)
0 = no infection
-f = weak infection
-|--|- = medium infection
-|--|--|- = severe infection
Aethionema arahicum
A. hujcbaum'ii
A. cappad'icum
A. rotuudifolitim
AUiaria nffic'inaVis
Al i/xsinii al pest re var.
odor at u m
.1. alpestre
A . ahjusoides
A. argenteum
A. hornmiilleri
A. beiithami compactum
A. eali/chium
A. cam pest re
A. condensatum
./. corymbosum
A. desertorum
A. edeiif Ilium
.1. lischerianiim
A. r/emonense
A. idaeinn
A. marilimum := Lobii-
laria maritime
X. ('21) 0
Katt. 0
N. ('25) 0
N. ('15) 15%
Mil. 0; Ravn; Jam. 0
N. ('13) 107f ; Roc. 17%
Hal.; Ravn.
Gl. 20%;N. ('12)+;N.
('13)4-. Cun. 51.1%;
Jam. 0
GI. 0; Jam. 0
Jam. 10.5%-11.6%
GI. 71.13% ;N. ('12)+;
N. (-13) +
Jam. 3.8%
Cun. 33.1%
Jam. 3l7ri
N. ('25)0; Roe. 57%
N. ('15) 507o
Jam. 0
N. ('15) 5%
.lam. 1 l-.5%
HaI.4-;Ravn. Cun. 11.2-
50%;X. ('15) 5%;
Jam. 0
100
PLASMODIOPHORALES
A. minimum
A. moellendorfianum
A. monianiim
A. podoUcum
A. rostratum
A. sa.ratile
A. serpyllifolitim
A. sinuatum
A. Strihrnyl
A. umbeUatum
A. Wierzhichii
Arahis alhida
A. alhida var. grandiflora
A. alhida var. nana
A. alhida var. umbrosa
A. Allionii
A. alpestris
A. alpina
A. areiiosa
A. hellidifolia
A. brachycarpa
A. Canadensis
A. coeridea
A. glabra
A. halleri
A. hirsuta
A. holboelli
A. laevigata
A. muralis var. collina
rosea
A. pendula
A. petraea
A. procurrens
A. ptimila
A.Stelleri
A. suecica
A. Turriia
Aubretia Bougainvillei
A. deltoidea
A. eyrei
A. graeca
A. hendersoni
A. LeichtUni
A. olympica
A. pinardi
A. purpurea
Barbarea arcuata
B. hracteosa
B. intermedia
B. I y rata
B. plantaginea
B. praecox
B. rupicola
B. stricta
B. verna
Gl. i.76%;N. ('15)0
Cun. 100%
G1.0;N. ('12)+;Cun.
22.2%; Jam. 18.8%
Jam. 3.9%
Cun. 86.7%
Hal.;N. (■l4)3%;Cun.
32%,
Cun. 8.3%
N. ('15)0; Gl. 100%
N. ('15) 0
Gl.O
Cun. 0
N. ('1-t) 0; Jam. 0
N. ('U) 0; Jam. 0
X. ('14) 0
N. ('13) 60%
Jam. 0
N. ('13) 50%
Cun. 52.4% ; N. ('12)+;
Roc. 27% -18%
N. ('12) +
Jam. 1.9%
Hal. +
Hal.
Jam. 0
Hal.
Cun. 0
N. ('12) + ;N. ('13)
80%; Jam. 1.5%
Cun. 50%
Hal. + ; Ravn.
Jam. 0
N. ('14)0
N.('12)^-
N. ('15) 0; Jam.O
N. ('14) 0;N. ('25) 80%
N. ('25) 44%)
N. ('15)+;72.2%
Jam. 7.4%
Cun. 0
Roc. 0
Cun. 0
Cun. 0
Cun. 0
Cun. 37.5%
Roc. 0
N. ('15)0;F. S. ('20)-j-
Cun. 67.7%
Gl.O
Roc. 0
Gl.O
Roc. 0
Roc. 65 7o
G1.0;N. ('12)+; X.
('15)0
Roe. 99%
Cun. 4.3-7% ;G1.0:Gi.O
Gi. 0
B. vulgaris
B. vulgaris fol. variegatis
Berteroa incana
B. mutabilis
B. obliqua
Biscutella auriculata
B. cichorifolia
B. did y ma
B. laevigata
B. leiocarpa
Brassica arvensis
B. balearica
B. cernua
B. chinensis
B. cretica
B. elongata
B. incana
B. insularis
B. junci
B. macrocarpa
B. napus
B. napus var. oleifera
B. napus var. esculenta
B. nigra
B. oleracea
B. oleracea var. acephala
B. oleracea hotrytis
B. oleracea var. capitata
B. oleracea gemmifera
B. rapa L. (== B. cam-
pestris?)
B. pekinensis
B. pe-isai
B. rapifera
B. robertiana
B. sabularia
B. Tinei
B. tournefortii
B. sp. 1
JS. sp. 2
Braya alpina
Cun. 0-70.1% ; Ham., Gl.
0;N. ('14) 0; X. ('25)
1.6%; Gi. 0; Rain.
66.7%; Jam. 3.5%,
Roc. 0 ; Jam. 0
X. ('14)0;N. ('24)0;N.
("25) 7.97c; Jam. 0
N. ('15)0
N. ('15)0
X. ('24)0;X. ('25) 0;
Katt. 257c; Roc. 40 7o
X. ('15)0;X. ('24) 0
N. ("25) 0;Katt. 137c
X. ('14) 0; Jam. 11%
X. ('15) 0
Cun. 99.8 7o;Gi. 100 7c;
Roc. 1007c
X. ('15) 307c
Gl. 1007cN. ('25)337o;
Katt. 100%
X. ('25) 10070 Katt.
10070
X. ('15) 407o
Jam. 207c
X. ('15) 8O70
X. ('15) 40%
Cun. 9970 ; Gl. 1007o ; X.
(25) 967o
X. ('15) 807o
Wor. ; Ravn. ; Cun. 83.7 7o
—49.270; Gl.O
Cun. 83.77o;Roc. 11 7c;
Jam. 84.87:
Ssach. 0 ; Roc. 0
Hal. +; Ravn. +; Cun.
28.27o; Gl. 207c; X.
('15) 0; Hon. 4.5-
62.l7o; Roc. 0; Jam.
3.470
Ravn. ; Cun. 94.2 —
81.67c ;G1.16.67o;Gi.
0-100%; Roc. 10070
Cun. 92.87o
Cun. 88.8%
Cun. 93.170
Cun. 88.2%
Wor. -f ; Ravn. ; Cun. 100
— 1.3%; Gl. 0; Ham.;
X. ('25) 16.67c; Gi.
75-10070; Roc. 35-
507o; Jam. 62.5%
Da.; Ikeno ('29)
Cun. 10070
Hal.
X. ('15) 50%
X. ('15) 1007o
X. ('15) 607o
X. ('15)0
X. ('14) 307o
N. ("14) 2070
Jam. 53.370
CLril HOOT OF C nrclFEHS
101
Riiiiias Dritiilalis
Camcliiia deniata
C.foetida
C. linifolia
C. macrocarpa
C. sativa
C. sp.
Capsella bursa pastoris
C. heegrri
Cardamine heterophylla
C. pratensis
Carpoceras sibirictts
Carrichtera veUa
Cbfiranthii.i AUioni
('. alpiniis
C. annus
C. Cheiri
C. incanus
C. marifimus
C. scoparlus
C. semper florens
C. Senaneri
Clypeola jonthlaspi
Cochlear! A morac'ta
C . ant/lica
C. dan tea
C. groenlandica
C. officinalis
Conrinffia orientalis
Coronopus didyma
C. prncumhens
Crambe abyssin'ica
C. cordifolio
C. hispanica
C. maritima
C. lartarica
N. ('12)+; N. (-13) 2
outof 2;N. ('11) 0; X.
("25) 0; Jam. 28.6%
Cun. 1007c ;G1. 100 fc
Katt. 1007o
N. {ir,)90'/o
Cun. 9 Ko 7c
Hal. -\- ; Ravn. ; Cun.
80%; Gl. 1007c; Mii.,
637o; N. ('II) 0; Jam.
91.9%
X. ('11) ioo7c
Wor.; Hal. ++; ^lass.;
Ravn. +; Cun. 10.87c;
Host. 62 7o; Katt. 0;
Mu. 95.77c; N. ('12)
+ ; N. ('13) +; N.
(•24) +;N. ('25) +;
Gi. 78-1007o; Rain.
32.57c; Jam. 467c
X. ('21) 507 ; Katt. 907c
Gi. 50-100%
Ravn.; Cun. 1007o;Erik.
(•26)
X. ('25) 0
N. ('24) 80-1007c;Katt.
1007c; Roc. 1007
Cun. 76.27c ;G1.207c;
Mii. 99%
Gl.O; Jam. 0
Hal.
Hal.; Sit.; Ravn. +;
Xaum. -| — I — \- ; Sor.
('21); Host. 85 7o; Mu.
997o; Gl. 1.3%; Gi.
78%; Jam. 0
Cun. 0
Cun. 43.67c
N. ('15) 5076
Mu. 1007o
X. ('25) 287c
X. 2 out of 2
X.X.;Schl. ('07); Roc. 0
Gl. 1007c
Gl. 95.59% ; Roc. 757c;
Jam. 8.67o
Gl. 97.56%
Gl. 86.5470; Mii. 50%;
X. ('14) 0; Roc. 0;
Jam. 107-59.370
Cun. 40.8%, 87c; X. ('15)
207c; X. ('24) 0; Katt.
10070
Gi.O
Gi.O
X. ('25) 17% ;Katt.
100 7c
Cun. 1007c;X. ('12)+;
X. (^15)0
Cun. 6.37c ;X. ('lo) + ;
Jam. 207-98.1%
Cun. 68.27 ;X. ('15)0
Cun. 100%
Desviirniiiia sopliia
Diptota.ri.s itik aides
1). iiiiiralis
D. tenuifolia
Draba aizoides var.
oblonijata
I), aizoon
D. altaica
1). ampicjicaulis
1). androsajcea
I), aniiata
D. borealis
D. caroliniana
D. Corsica
D. dorneri
D. fladnizeiisis
D. friffida
I), oj i/carpa
D. cjlacialis
D. rupestris
1). f/ra7idiflora
1). hai/naldii
I), hirstita = repens ( ?)
D.hirta
I), hispanica
I), incana
D. johannis
D. nemorosa
D. montana
D. 7iivalis
I), nori'er/ica D. scan-
dinavica
D. pi/renaica
D. subamplejicaulis
D. tomentosa
D. verna
I), xcahleiibergi
Eriica cappadocica
K. nrthu.sepala
E. saliva (vesicaria)
Kriica.striim obiitsangu-
1 II m
Eri/siminn alfaicuiii
E. as per urn
E. aiirantiacum
E. Barbarea
E. cheiranthoides
Ham.; Gl. 41.677c; X.
(•12)+; N. ('13) +;
X. ("24) 20 7o; Katt.
100%; Gi. 75%; Jam.
8.3%
X. ('25) 3.570
X. (^24) 10%;Gi. 4-
10070
(ii. 19-10070
X. ('u) 0
X. ('14) 0
X. ('25)0; Jam. 370
Jam. 0
Cun. 0
Cun. 0
X. ('14) 0
Cun.O
X. ('14) 0
Roc. 337c
Cun. 507c
X. ('14)0
Jam. 28.67o-37.57o
X. ('14) 0
Jam. 14.770
X. ('15) 0; Jam. 7270
Jam. 0
X. ('12) +
X. ('12) +
X.('14) 0
X. ('25) 0; Jam. 0
Jam. 9.87c
X. ('12)0
Jam. 0
X. ('14) 0
Roc. 26% ; Jam. 1.97o-
60 7f
Roc. 637o
Roc. 44% ; Jam. 0-107o
Jam. 0-22.270
X. ('24) 80%
X. ('14) 0;X. ('15) 0
X. ('25)0; Katt. 100%
X. ('15) 50%
Cun. 96.37c. 637c; Jam.
18%-27.37c; X. ('15)
90%; N. ('15) 507o;
X. ('23) 507c; Roc.
307o ; Ravn. ; Sit.
Gl. 6.857c ;N. ('25)0;
Katt. 1007f
X. (•15)0;X. ('25) 2.570
Hal. : Ravn. + : Cun.
50%
Jam. 48.9%
Cun. 76.3%
Hal. -| — |-; Mass.; Ravn.;
Cun. 72.1% ; Ham.; Gl.
1007c; X. ('12)+; X.
('13)+; Rain. 13.97c;
Jam. 11.1%
102
PLASMODIOPHORALES
E. comaium
E. crepidifolium
E. helveticum
E. hieractifolium
E. leptophijllum
E. ockroleucum
E. orientale
E. parviflorum
E. perowskianum
E. piilchellum (E. rupe-
stre)
E. sfrictum
E. virgaium
Heliophila amplexicaule
Hesperis alpina
H. fragrans
H. lute a
H. matronalis
H. matronalis var. nivea
H. matronalis var. nana
H. runcinata
H. tristis
H. violacea
Iberis amara
I. coronaria
I. qihraltarica
I. hybrida
I. intermedia
I. lagascana
I. odorata
I. pinnata
I. sempervirens
I. taiirica
J. Tenoreana
I. umbeUata
I. zenoreana
I. sp.
Isatis glauca
I. tinctora
I. undulata
Jonopsidium acanle
Koniga libi/ca
Lepidiiim apetalum
L. campcstre
Cun. 0
Sit. ; Ravn.
Cun. 2.l7c; Jam. i.8%
Gl. 457c;N. ('1-i) 30%;
Katt. 0
N. ('15) 20%
Cun. 57.270
Gl. 25%
Cun. 85.7%
Hal. ; Ravn. + ; Naum. 0 ;
N. ('15) 0-1.3%; Roc.
62%
N. ('15) 0; Jam. 4..370
Appel.;Gl. 14.29%
N. ('15) \%
N. ('24)+;N. ('25)0;
Roc. 46 7o
Roc. 0
Roc.O
Roc. 100%; Jam. 11.3%;
Hal. +; Cun. 32.1 7c;
Ham.; Gl. 5.367o ; Mii.
1007c ; N. ('14) 507c;
N. ('24) 7570; Jam.
2.8 7o
N. ('15)0
N. ('14)0; Roc.O
N. (15) 0
Jam. 107c
Jam. 23.67c
Cun. 877o;Gl. 1007c; N.
('25) 0; Roc. 18-5l7o;
Jam. 41.470
Cun. 73.770
Mii. 24.2%
Cun. 52.(i 7o
Gl. 10070
Cun. 47.370
Cun. 41.67c ;N. ('25)0;
Jam. 85.1 7o
Gl. 4.4270 ;N. ('25)0;
Roc. 827c
Cun. 43.5%; N. ("25)0;
Jam. 10.570
N. ('15)307o;N. ('25)0
Jam. 34.370
Wor. ; Hal. ++; Ravn. ;
Cun. 927c; N. ('15)0;
Gl. 99.1470; Roc. 7370;
Jam. 60.7 7o
Cun. 2.37c
Cun. 10070
Cun. 68.47c ;F.S. ('20)
33% ; Roc.O
Hal. ; Cun. 42.570; Roc.
1770; Jam. 0-9.570
N. ('25) 0;Roc. 0
N. ('24) 0
N. ('25) 0
Cun. 527c
Hal.; Ravn.; Cun. 42.87o;
GI.O;Gi. 0-100%
L. draba
L. hirtum
L. intermedium
L. latifolium
L. menziesii
L. micrantum
L. montanum
L. perfoliatum
L. reticulatum
L. ruderale
L. sativum
L. tenuicaule
L. virginicum
Lunaria biennis
Malcomia africana
M. flexuosa
M. graeca
M. maritima
Matthiola bicornia
M. fenestralis
M. incana ( ^ annua)
M. oyensis
M. tricuspidata
Melanosinapis communis
Meniocus ehrenbergii
Myagrum perfoliatum
Nasturtium amphibium
N. officinale
N. palustre
N. silvestre
Neslia paniculata
Notoceras canariense
Peltaria alliacea
P. turmena
Kaphanus maritimus
R.sp.
R. niger
R. odessanus
R. oleiferus
R. radicula
R. raphani.strum
R. rosiratus
Jam. 0
N. ('15) 0
Hal.
Jam. 0
Hal. ; Ravn.
N. ('13) 507o
Hal.
N. ('15)0
N. ('25) 0
N. ('25)907c;Gi. 50-
7570
Cun. 1.8%.; N. ('13) 0
Katt. 0; Gl. 0; Mu. 0
N. ('25) 0; Roc. 0
Jam. 0
Gi.O
Hal. ++; Ravn.; Cun.
23%.; N. ('25) 177o;
Gi. 10 7c
Hal. ; Cun. 97.2% ; Naum.
+ ; Mii. 10070; Hon.
-|-;Gi. 27-1 007c
N. ('25)0
N. ('15)0
N. ('15)0
Ravn. ; Roc. 9% ; Jam.
4.3%-ll.l%
Hal. +; Cun. 7.9-4.37o ;
Gl. 0; N. ('15) 0; Jam.
0
GI.O
Wor. +; Hal. 0; Ravn.;
N. ('15) 0;Host. 0;G1.
0;Mii. 0;Gi. 0
N. ('25) 0
Cun. 0; GI.O
N. ('24) 0 out of 1 ;N.
('25) 0
N. ('24)+;Katt. 0
N. (15) 1 out of 1
Ham. (after Naumann,
'13)
Gi.O
Hal. ; Ham. ; Ham. ; Gi. 0
Hal. ; Mag. ; Ham.
Cun. 100% ;N. ('12) +
N. ('24) 75%; Katt. 7570
Jam. 0
Jam. 0
N. ('I5)0;N. ('25) 0
Gi.O
N. ('15) 0
N. ('15) 0;Katt. 157c
Honig8.5-877o
Cun. 53.4%; Ssach. I07c
Hen. -\- ; Ravn. ; Ham. ;
Mii. 36.47o; Svec. +
+ +; N. ('12) +;
Weiss +; N. ('25,
'28); Rain. 14.87o;
Jam. 39.1 7c
N. ('14) l7o
(Ml) HOOT OF < Hl( IFKHS
103
II. satix'us
li. sativiis v;ir. li. niger
Jiapistriitii hispaiiiciim
Ik. prrrnne
li. riifiosum
Hicolia liinaria
lioripa amoracia
li. palu,ttri.s
]{. .1 i I fi\<! Iris
Seiii'hifra lordiiopus
S. pinnatitiila
Sinapis abi/xsiiiica
S.alha {B'.alba)
S. apula
S. arx-ensis {Brassica
sinapistrum)
S. chitien.<!i.i
S.geniculata
S. turgida
Sist/mbrium AUiaria
S. altissimiim
S. asperum
S. austriacum
S. bursifolium
S. crepidifoUum
S. cumingianum
S. hirsiiliim
S. in CIS urn
S. irio
S. loeselii
S. officinale
S. orientate
S. Pallasii
S. persicum
S. poli/ceratiiim
S. sinapistrum
S. strictissimum
S. taraxacifolium
S. Thalianum
S. vulgare
Sophia pinnata
Succovia balearica
Hal. + ; Sit. + ; Clint. + ;
Ravn. + ; Cun. S7.i</c ;
N. (■l3)+:Gi.O
X. ("2;). '28) 0;S.s:u-li. 0
N. ('24) 0 out of I ; N.
('2.')) 1 out of 1 ; Katt.
60</c
Jam. 88.9^/c
N. ('21) 2 out of 2
N. ('21) 1 out of 1
Hal.
Ravn.
Ravn. Jam. 18.97c
X. ("21) 0:X. ('25) 0
X. ('21) 0;X. ('2.5) 0
X. ('15) 307c
Hal. + + +; Ravn.; Cun.
1007; Gl. 1007o; Mil.
100% ;X. ('15) 1007,;
Rain. 61.l7r; Roc.
817c.; Jam. 95.6 7o
N. ('25) 9070; Katt.'
10070
Hal.; Ros.; Clint.; Roc.
10070; Jam. 58.l7o;
Mass. -|- ; Ravn. ; Cun.
1007; Ham. +; N.
('12) +
N. ('25) 50%;Roc. 507o
X. ('15)0
X. ('15) 95%
Mass. + ; Gl. 0
Hal. ; Cun. 38.37 ;X.
('15)0
X. ("15)0
Appel; Gl. 1. 25 7o; N.
("14) 57c; Jam. 12.5-
44.70
N. ('15)0
Hal.
Jam. 21.4%
G1.257c
Cun. 8I.370
Roc. 64 7o
Gl. 1.31%
Hal.; Ravn.; Cun. 40 7c ;
Erick.; X. ('12) +; X.
('13) 3%; X. ('24)
100%; Gi. 55-10070
Gi. 11-10070
X. ('15)0
Gl. 0
X. ('15) l7o
X. ("15) 70%
AppchX. ('15)0; Jam.
]07o
X. ('15)307o
X. ('24) 10%
Ravn.
Hal.; Cun. 53.970
X. ('15) 100% ;X. ('24)
10070; Katt. 100%
S. bali-arica Mi'dis
Roc. 10070
Tlilaspi alpestre
X. ('15) 207c ; Roc. 87o ;
Jam. 27.370
T. arvcnse
Hal. + + +; Ravn. +;
Cun. 97.67o ; Gl.
25.8I70; X. ('13)
9970; X. ('24) 667o;
N. ('25, '28) 9970;
Rain. 99.5%; Jam.
97.67o
T. bellidifolium
X. ('14)0; Jam. 2.270
T. Lovacsii
X. ('14)0; X. ('25)0;
Jam. 0-13.7%
T. oVn'eri
Roc. 0
T. perfoliatiim
X. ('15)4070
Thiaspi s)).
X. ('14)0
T. violascens
Jam. 9.570
Tiirritis glabra
X. ('14)0; Roc. 7970
Tysanocarpus curvipes
X. r'24) 10070
J'isicaria gracilis
X. ('15) l7o
So far 318 species in 59 genera of crueifers have
been examined for club root, and among these all but
89 species and 8 genera were found to be infected.
It is to be noted that the percentage of infection re-
ported by the various workers for the same species
varies considerably. Such differences are largely due
to the small number of plants examined. In some
species, particularly wild crueifers, the percentages
are based on the examination of only two or tliree
plants. This is also true of some of the genera and
species which have been reported to be uninfected.
Doubtless when a larger number of plants have been
examined these species also will be found to be sus-
ceptible to club root.
As has been noted elsewhere, club root is limited
to the mustard family, and all rejiorts of its occur-
rence in species outside of the Cruciferae have been
disproven. In 1910 Marchand reported a disease of
melon, celery and sorrel in France wliicli he thought
was caused by P. Brassicae, but subsequent examina-
tion of these plants by Grignon ('10) showed that
the swellings on the roots were caused by the nema-
tode, Hcterodea radicicola. Griffon and Maublanc
('12) later confirmed (jrignon's observations.
.Several attempts liave been made to infect Jilants
closelv allied to the mustard family with P. Bras.u-
cae, but these have been unsuccessful. In 1897 Hal-
sted tested the following species in Xew Jersey:
Abutilon abutilon
Agrostevtma Githago
Argrmonc mcjricana
Chelidonium majus
Krodium cicutarium
Hibiscus triunum
Malva roiundifolia
Melilotus alba
Papaver sp.
Reseda odorata
Saponoria officinalis
Silene nocti/tnra
Xo indication of club root was found in any of these
species. Potts ('35) likewise found that non-crucif-
erous plants, including Reseda odorata, Carydalis
f/lauca, Fumaria officinalis, Allium schonprusum,
i'rtica pillulifera and Spinacia oleracea, are unsus-
ce|)tible.
104
PLASMODIOPHORALES
Control of Club Root
Because of the great economic importance of club
root extensive attempts to control the disease have
been made for almost a century and a half, but so
far no completely effective measures have been de-
veloped. The resting spores of the causal organism
are produced in prodigious quantities, have a fairly
high degree of resistance, and may remain viable in
the soil without the presence of host plants for seven
to eight years ; all of which makes effective control
very difficult. Control is furthermore hampered by
the wide range of wild and cultivated hosts which
harbor P. Brassicae and the fact that crucifers are
susceptible as long as they are alive.
Control measures against club root have involved
sanitary practices, sterilization of the seed, disin-
fection of soil in seed beds, applications of fungi-
cides to the soil in fields, adjustment of the soil re-
action, addition of lime, judicious use of basic fer-
tilizers, soil drainage, crop rotation, eradication of
wild cruciferous hosts, and the development of resist-
ance varieties or races of cultivated crucifers.
One of the main factors which makes club root dif-
ficult to eradicate in the soil is the longevity of the
resting spores. Longevity is not influenced by graz-
ing, crop rotation, plowing, or the application of car-
bonate of lime and sulphur to the soil, according to
Gibbs ("39). Fedorintschik ('35) found that soil
from fields wliich had not been sown to crucifers for
seven years contained enough viable spores to infect
26.6 per cent of aseptically grown cabbage seedlings
after transplantation. In cabbage fields rested one
year the viability of the resting spores was reduced
from 81.2 per cent to 13.7 per cent, but in one field
rested five years the reduction was only 40 per cent.
Plowing the fields two or three times a year has no
effect on resting spore viability, according to Fedo-
rintschik. In badly infested fields up to 100 million
spores per cc. of soil have been found (Naumov,
'28). which may extend to and infect plants at depths
of 10 to 30 cms. in soils of various types (Gibbs,
'32; Motte, '34; Potts, '35; Fedorintschik). The in-
tensity of attack is directly correlated with the lumi-
ber of spores in tlie soil, according to Gibbs ('31b)
and Fedorintschik, but Naumov ('28) found but
little evidence of correlation in Russia. Gibbs found
that one plant out of 42 became infected when there
were approximately 25,500 spores per seed box, and
43 out of 44 when 530,000,000 spores per box were
present. According to Fedorintschik's calculations,
less than 10,000 spores per cc. of soil cause isolated
attacks on lateral roots but does not reduce the crop
weight of cabbage. More than 10,00 spores may cause
50 per cent infection of lateral roots but no reduction
in crop weight, while 300,000 spores per cc. of soil
usually leads to over 50 per cent infection of the
whole root system and reduces the crop weight to 50
per cent.
In the soil the spores are also fairly resistant to
fungicides in concentrations low enough to avoid in-
jury to the host. Bremer ('35) found that a 0.5 per
cent solution of uspiilun poured over spores in the
soil killed only 24 per cent to 38 per cent, and that
5 days were required to kill the spores *hen im-
mersed directly in a 0.25 per cent solution of the
same fungicide. Likewise, relatively strong solu-
tions of formalin were ineft'ectual. Fedovota ('29)
found tliat treatment with 0.1 per cent mercuric
chloride has little or no toxic effect on the spores. On
the other hand, Honig ('31) reported that 0.001
per cent mercuric chloride when applied directly to
the spores caused general plasmolysis, while higher
concentrations were more or less ineffective. He also
found that solutions of MgS04, NaCl, KNOo, and
NH4CI in molar concentrations of 1:100, 1:10,000,
1:100.000 plasmolysed tlie spores within 4 weeks.
Immersion of spores for 30 minutes in 70° C. water
and heating the soil 5 to 30 minutes at 60° to 80° C,
renders them inactive (Naumov, '28 ; Vladimirskaya,
'30; Anony., Ger., '39). Polyakoff ('39) reported
that immersion of spores for 5 minutes in condensate
(containing 5 per cent formalin) kills the spores,
and that this solution added to the fields at the rate
of 1.8 by volume of soil reduces infection 70 to 100
per cent. Desiccation has a marked effect on spore
viability, according to Naumov ('25). Spores kept
in a relative dry cellar over winter caused infection
of seedlings the following spring, but a year later
they were no longer viable. If desiccated completely
the spores lose tlieir infective power within a year.
SANITARY PRACTICES
Since the spores of P. Brassicae will survive pas-
sage through the digestive tract of animals and may
be carried to the fields in contaminated manure, it is
obvious that diseased roots should be thoroughly
boiled before being fed to livestock. Stable and liquid
manure should be avoided as much as possible, since
it is conducive to club root development if applied
directly to a crop of crucifers. If it is to be used at
all it should be applied during the season preceding
a susceptible crop. If contaminated it should be steri-
lized or disinfected before application to the soil.
^'incent. Herviaux, and Coic ('38) advocated the ad-
dition of 90 kg. nitrogen in the form of cyanamide
to stable manure before using. It is interesting to
note in this connection that Naumov ('28) reported
that, contrary to all expectations, the addition of
stable manure to the soil exerted a slight detrimental
action on the parasite.
Other sanitary practices involve collecting and
burning diseased plants. These should not be allowed
to rot in tlie soil or in piles, since this liberates the
spores in the soil again. Plowing under of diseased
plants to various depths has been advocated. Frank
('96), Potter ('97), L. R. Jones ('01), Laubert
('05a), Kock ('11) and Lindner ('11) recommended
a depth of 1 meter; Naumann ('13), Neger ('17),
Trieschmann ('17) and Ludwigs ('25) 80 cms.; and
Miillers (Honig, '31) 20 to 30 cms. The latter depth
is obviously inadequate, since it has been sliown that
infection may occur at 30 cms. Esmarch ('24) con-
tended that burial is worthless and that burning is
the only safe method of disposal.
< I.VH HOOT OK ( HIH'IFERS
105
Youiiir sfcininjis may often tii- infccti-d and not
show rocoiinizalili- symptoms of tlu- disfjiso at the
timo of tr.inspl.iiitinir. C anful tx.-miination of tin-
plants at tin- tiino of removal from tlic seed lii-ds is
therefore essential if there is any suspicion that the
disease may be present. Should a single seedling
from a seed frame show symptoms of club root it is
advisable, in the opinion of Sehlumberffer ("1 !■),
Chupp ('2->) and (Heisberg ('2(>). to avoid or de-
stroy all plants from tliat particular bed. since it is
only rarely that infected seedlings recover.
Seed, Seed Bed and Seedlitifi Disinfection. — Seeds
of infected crucifers occasionally bear the fungus
spores externally, and in such cases seed steriliza-
tion is necessary. Soaking seeds in tillantin B and
0.25 per cent to 0.5 per cent usi)ulun for one-half
to one hour before planting has been reported by
Mothes ('25). Bronnle ('2(i) and Leines ('26) to
reduce the incidence of infection if followed by fun-
gicidal treatment of the soil. Such seed treatment,
however, is wortliless unless it is followed by seed
bed disinfection.
^'arious fungicides and chemicals as well as heat
have been used in seed bed disinfection. Heating
the soil 1^2 hour at 60° C. or above kills the spores,
according to Vladimirskaya, Jorgensen, and Shew-
ell-Cooper. Commercial formalin (1 part to 10),
0.05 per cent to 0.2 mercuric chloride (1 to 2 gals.
per sq. yd.). 0.1 per cent to 0.5 per cent liquid
ceresan. corrosive sublimate (1 oz. in 2-10 gals.
water). 0.5 per cent uspulun solution, uspulun and
solibar mixed (1 to 5). 10 per cent solution of wash-
ing soda, folosan and brassiean ( 1 8 oz. per cubic yard
of soil) mixed with lime, carbolic acid, mustard oil,
etc.. applied 1 to 5 times to seed beds have been re-
ported to reduce or completely control seedling in-
fection bv the following workers: Anony. (Australia,
■-to), Somnier ('22). Jorstad ('23). Bremer ('23-
'2 1). Darnell-Smith ('24). Kind.shoven ('24).
Chupp ('25), Hofferichter ('26). Clayton ('26),
Blunck ("28), O.sterwalder ('29). Preston ('30),
Hoffman ('32). .Jorgensen ('33). Gibbs ('34),
Woodman. Benchley and Hanley ('34), Kiipke
('35). and Smieton ('39).
Effective control has been reported from the use
of uspulun on seed beds, but some workers have
claimed that it is less satisfactory than mercuric
chloride. According to Clayton ('26) the spores of
/'. Brassicae in the soil are fairly sensitive to mer-
curic compounds, but such substances have been
found to be more or less toxic to the host, especially
in dry hot weather, and may reduce the cro]) to some
extent. Wellman ('30). however, found that mercury
compounds used according to Clayton's methods
were ineffective in Wisconsin unless applied in con-
centrations high enough to be injurious to the host.
Copper carbonate and sul))hate. and carbonates and
sulphates of calcium were likewise ineffective. Hy-
drated lime worked into the soil at the rate of 1 .500
pounds to 5 tons per acre gives good control in seed
beds, according to Wellman. Motte ('34) found that
the fungus spores r;irely exceed a dc|)th of 20 cms.
in tlie soil, ;ind .-is a control measure for seed beds he
.Khoe.itfil rcmov.d of the upper 25 cms. of soil.
.Seedling disinfection alone before or at planting
has not i)roven gener.illy i)r,ictic;il in controlling
club root. l)ii)|)ing seedlings uj) to the coll.ir in weak
solutions of uspulun, mixtures of uspulun ;ind solibar
solutions (1:5), mercuric eldoride. 0.1-1.5 i)er cent
liquid ceresan, etc., before planting has been recom-
mended by Kind.shoven ('24), Preston ('29), Rabbas
('30). Kiipke ('35). and others, but Jamalainen
('.•}6) asserted that seedling treiitment at and after
planting is ineffective. While such disinfectants may
inactivate the spores in the soil .idhering to the roots
and root hairs, they obviously cannot destroy the
amoebae and plasmodia within the tissues, if such
stages are already jiresent, without killing the host.
It is doubtful that enough fungicide will remain on
the roots during transplantation to kill or inactivate
the siJores which may be present in the plant holes.
Seedling treatment, as recommended above, must ob-
viously be followed by soil disinfection in the field
to be effective.
The addition of 1 , 2. and 25 gms. uspulun dust per
plant hole (Esmarch, '25; Blunck, '28), 1 liter of
.25 per cent uspulun solution, 10 liters of .20 per cent
uspulun, tillantin B, and germisan per plant (Lind-
fors, '25; Hertel, '26; Rabbas. '30). 10-15 gms.
humus carbolineum per plant (Popp, '25), V2 pt.
.01 per cent (or 1 oz. in 6 gals, water) corrosive
sublimate per plant (Preston. '27; Holmes-Smith,
'30). chloropicrin in plant holes (Anony.. Rhode
Island. '39), 1/, pint .062-. 1 per cent mercuric chlo-
ride per plant (Pre-ston, '29; Olgilvie and Mulligan,
'34 ; Smieton. '39), and other chemicals have been re-
ported to reduce or completely control infection.
Preston ('28) found that Vj pt. per plant of .2 per
cent methyl green, malachite green, methyl violet,
and Brilliant green applied at planting was ineffec-
tive. Likewise clubicide and Clieshunt Brown com-
pounds as well as .2-.5 per cent formalin and .2 jjer
cent lysol were unsatisfactory for seedling treatment
at and after transl)lanting.
Soil Disinfection in the Field. — In attempts to
combat club root in the field by soil disinfection a
wide assortment of chemicals, fungicides and spe-
cial remedies have been employed as is shown in
table 2 and the accompanying i)ages. In pots, seed
beds, small gardens, and ex|)crimental plots these
substances are fairly effective, but with the excep-
tion perliajjs of usjjulun they have not jiroven com-
mercially satisfactory and exi)edient in the field. As
Larsen and Walker ('34) have pointed out. green-
house pot tests are not always a true index of what
may be expected in the field. The cost of materials
and expense of apjilication often outweigh the bene-
ficial results obtained, and in many instances the
fungicides directly injure or reduce the ero]). Accord-
ing to Motte ('33) very little is now being done to
combat the disease in Denmark beside avoiding ma-
nure, using basic fertilizers, and growing resistant
varieties.
106
PLASMODIOPHORALES
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I Mil HOOT OK < nil IFEHS
109
Till- nsults sliiiwii in t.ilili- 2 ari' t-oiitr;uliitor_v in
seviT.'il cases. 'I'liis is iloulitlcss due in many in-
stances to outside factors sucli as those wliicli iiiHu-
ence tlie cfTectivencss of lime and other basic fer-
tilizers. DitTerenees in time .-iiid methods of ai)l)lic;i-
tion. de};ree of soil infestation, soil moisture, etc.. ob-
viously operate here also. As is shown in table 2
uspulun has been extensively used, especially in Eu-
rope, and wiieii applied at rates of 0.5 to 1 gm. per
ksr. of soil or 120 to 300 gms. per sq. ni. in the field
two weeks or more before }>lanting it is the most
etl'ectivc and practical of all fiiiijiicides for the con-
trol of club root, according to the data in the litera-
ture. On the otiicr iiand. numerous workers have re-
ported it to be unsatisfactory. It may be used as a
solution and jjoured over the soil or as dust mixed
with fertilizers, but Honig ('31 ) stated that its eft'eet
is less certain and complete when used in solution.
\\licther or not uspulun will jirove practical in large-
scale operations is uncertain, according to Blunck
("29). but Honig claimed that its practicability in
this respect has already been demonstrated. In com-
bination with solibar. lime and other basic fertilizers
its use may be greatly extended, but even when mixed
with soil alone it is too expensive for practical pur-
poses, according to Riehm ('2.5).
The effect of uspulun on the parasite and host is
not definitely known. Whether it kills the spores or
prevents germination is uncertain. Bremer ('23)
found that 1 gm. per kg. of soil destroys about one
half of the spores, and held that it acts primarily in
killing the amoebae. Honig ('31 ) believed that uspu-
lun may possibly stimulate spore germination and
kills the amoebae as they emerge, or that it increases
the resistance of the host, along with a weakening of
the amoebae.
Mercuric chloride is generally reported to be
eflTective. but whether or not it is economically prac-
tical in large-scale operations is still uncertain. For-
malin has been extensively employed, but the results
obtained are very conflicting, as is shown in table 2.
Its efficacy in the field is doubtful, and Hammarlund
("I.t). Burkhardt ('15), and Lindfors ('21) .stated
that it is too expensive for commercial use.
Sulphur has proven ineffective, and in only a few-
instances has corrosive sublimate reduced infection,
Bordeauj mixture is also of little or no value in com-
bating club root. C arbolineum alone and mixed with
various types of humus, however, has been reported
to be fairly satisfactory.
In addition to fungicides listed in table 2 various
other chemicals, substances, and remedies have been
used in combating club root. These have been used
singly or in combination, and with or without alka-
line fertilizers, but here again the results obtained
are contradictory and generally unsatisfactory.
Segetan, a mercury compound, is ineffective ac-
cording to Osterwalder ('29).
Cresol (2 kg. per 1. of water) applied at the rate
of 2.5 1. per c. m. of soil is effective, according to
I.ocw (12), but .JO gms. per eu. m. of soil lias no
<llVcl.
Liquid ammonia. 1 i)er cent solution, has no in-
hibitory properties (Osterwalder, 29).
Sultjine is worthless, according to Lindfors ('2 I).
Soot or lampblack has been used in England to
control club root, .Kcording to \\'oronin ('78), but
Eggemeyer ('20) found it to be useless.
Petroleum was re])ortcd to be effective by Pfeiffer
and Stacs ('02). Miillers (Honig. '31) got 80.41 per
cent healthy plants by its use in Cjcrmany.
Chloropicrin in the jjlant holes or added to the soil
reduces infection in cabbage to \ i)er cent or less
(Aiiony., R. I., '39).
Pure carbolic acid added to the soil completely
eliminates club root from experimental plots, ac-
cording to Jorgensen ('33).
Mustard oil (3 cc. per 1. of soil) gives complete
control (Anony., Ger., '39).
Parachlorbenzine gives only partial control and
injures the host plants ( Vladimirskaya, '30).
Germisan, 20 gms. in 10 liters of water per plant
is not effective, or only partially so (Hertel, '26;
Vilkaitis, '33).
Sulcan is less satisfactory than Beka-Wurzel-
schutz (Esmarch, '25) but sufficiently effective for
practical purposes.
Potassium and calcium permanganate applied di-
rectly to the soil are ineffective. (Miiller and Oster-
walder, '23, '24; Osterwalder, '29).
Mercurous chloride is less satisfactory than mer-
curic chloride, according to Bailie and Muskett
('33). but Preston's ('31) earlier report contradicts
their results. Palmer ('H), however, secured strik-
ing control in cabbages with mercurous chloride sus-
pended in water with the aid of gum arable at the
rates of 5 and 7.5 lbs. per acre.
Folosan (pentachlornitrobenzine) and brassisan
(trichlornitrobenzine). 18 oz. per c. yd. of soil, are
superior to an equal concentration of mercuric chlo-
ride in seed boxes, but in tlie field they are less effec-
tive (Smieton, '39). All three compounds check
growth to some extent, but nonetheless give good con-
trol. Eolosan and brassisan are more effective when
used with lime. Brown ('35) likewise found brassi-
san to be effective against club root.
Semesan is equally as effective as mercuric chlo-
ride (Clayton, '26).
Liquid ceresan, 0.1-0.15 per cent, applied to seed
bed at time of jjlanting, to seedlings a day or two
before transplanting, and 6 to 8 days after setting
out gives excellent control, according to Kiipke
(•35).
110
PLASMODIOPHORALES
Tillantin B in solution sprinkled over seed beds
gives complete control, according to Mothes ('25).
Hertel ('26), however, reported that 20 gms. per
10 1. water poured over each plant or used as dust
in conjunction with uspulun are ineffective. Like-
wise, tillantin B dust alone (100 to 150 gms. per
sq. m. of soil) has no effect on club root, according to
Blunck ('28).
Cheshunt compound, clubicide, and 0.2 per cent
h/sol are ineffective, according to Preston ('28).
Carbon bisidphide when applied to the soil is also
ineffective (Miiller and Osterwalder, '24).
Copper sulphate powder applied at the rate of
600 and 1.200 lbs. per acre (Halsted, '96), or as a
solution (1:1,664, 1 gal. per .30 ft. row) directly to
growing plants (Glo3'er and Glasgow, '24) has no
effect on club root. Miiller and Osterwalder ('24) got
similar negative results.
Bewley's solution (2 oz. copper sulphate and am
monium carbonate) applied in a concentration of 1
oz. to 2 gal. water increases infection (Gloyer and
Glasgow, '24).
"Hochst mittel," according to Hertel ('26) re-
duces infection considerably, but Blunck ('28)
found that 150 gms. per sq. m. of soil is ineffective.
He also found Elhardt's Wurzelschuts and ftorium
(150 g. per sq. m.) to be of little value against club
root.
Copper carbonate is reported to be fairly effective
by Naumov ('27) and an anonymous worker in the
U. S. ('22), but Vladimirskaya ('30) got only par-
tial control with it.
Red copper oxide is fairly effective, according to
Naumov ('27) and McLeod and Howatt ('34).
Lime copper dust increases infection, according to
Gloyer and Glasgow ('34).
Sodium carbonate, 3,000 lbs. per acre is ineffec-
tive, according to Halsted ('96). Lindfors ('24)
confirmed Halsted's results, but Naumov ("27) and
Vilkaites ('33) found it to be slightly effective.
Bordeaux mixture alone in amounts up to 5,280
gals, per acre or mixed with corrosive sublimate has
little or no effect on club root, according to Halsted
('96, '99), but later an anonymous worker (U. S. A.,
'22) reported it to be effective.
Sodium chloride, 300 to 600 lbs. per acre, has no
appreciable effect on club root, according to Hal-
sted ('96). Naumov ('97), however, found that cal-
cium and barium salts (KmCO;,, NaOH, KOH, and
Ba(OH)o) are to some degrees effective, while
CaCU and BaCU are of little value. Wellman ('30),
on the other hand, reported that K'^COs does not in-
hibit club root.
Radium, x-rai/, and ultraviolet light treatments
are reported by Petri ('24) to be effective in reduc-
ing club root infection.
LIMING
Liming the soil before planting appears to be the
most widely used and practical control measure in
the field, although numerous workers have failed to
secure satisfactory results by such treatment. Who
first discovered the efficacy of lime is not known, but
Ellis reported that before 1742 farmers in England
had been using clay or marl for dressing diseased
fields before planting turnips. In 1831 Farquahar-
son advocated the addition of powdered lime shells
to manure before using, while Abbay (1831) recom-
mended the addition of 256 bushels of "knottingsley"
lime per statute acre as a control measure. Subse-
quent workers, including Anderson ('55), Hunter
('57), A. Voelcker ('59), and Henderson ('67), of
this early period also noted the great prevalence of
club root in lime-free soils and reported varying de-
grees of control with the addition of lime, ground
oyster shells, and flour of bone to the soil, but they
found tliat the effectiveness of these substances varied
markedly and that all kinds of lime were not equally
effective. At the close of the 19th century numerous
other pathologists, including J. A. Voelcker ('94),
Evcleshvmer ('91), Sommerville ('94-97), Massee
('95), Halsted ('96-99), Seltensperger ('96), Pot-
ter (■96-'97), Sitensky ('98), Gilchrist ('98-'00),
L. R. Jones ('01 ), and others reported varying bene-
ficial results from the use of lime. Halsted. in par-
ticular, carried out an extensive series of tests in
America, and after seven years of field experimenta-
tion concluded that air-slaked lime at the rate of 75
bushels per acre was commercially satisfactory as a
control measure. Later, however, Cunningham ('14)
reported that 150 bu. per acre were necessary for
effective control. Extensive experiments along the
same line were carried out in Denmark by Ravn and
his associates ('02-'ll) with calcium carbonate and
calcium oxide in quantities varying from 2.5 to
nearly 10 tons per acre. They found that the largest
treatments were the most effective, and although in-
fection still occurred the crops produced were com-
mercially satisfactory. Following these long-time ex-
periments of Halsted and Ravn, beneficial results
from the use of lime in the field have been reported
by numerous workers, including the following: Dia-
kanoff ('11), Brick ('13), Cunningham ('14),
Georgeson ('16), Bos ('18), Weiss ('18), Popp
('19), Miiller-Thurgau and Osterwalder ('19, '23).
Janson ('20), Whitehead ("22, '36), Jorstad ('23).
Katterfeld ('23), Harter and Jones ('23), Bremer
('23-24), Hollrung ('23), Anony. (Nova Scotia,
'23), Montietli ('24), Darnell-Smith ('24), Lind-
fors ('24), Kindshoven ('24), Naumov ('25, '27),
Tennent ('25, '30), Siemaszko ('25), Riehm ('25).
Gleisberg ("26), Tessenow ('26), Vaughan and
Wellman ('26), Appel ('27), Chupp ('28), :Martin
('28, '34), Blunck ('28), Wellman ('30), Rabbas
('30), Gibhs ('31, '32), Anony. (Germany, '31),
Kreuzpointer ('31), Beaumont and Staniland ('33,
■34), Nielsen ('33), Wilson ('34), Potts ('35).
( I.I H HOOT OK < nil IFERS
111
ArktT ^'.'J.">). IJroMii (,'."i7). Murpliy (^'■"(7) .-ind l$rn-
m-tt ('3!»).
On tlu- otluT liaiul, unsatisfactory and incoiu'lu-
sivo results from tlu- uso of linio as a control meas-
ure have been reported l)y the followiiifi: workers:
Potter ('in). Hiltner ('08). Naiiniaiin ('12. '13).
Appel and Schlumberfier ('13). Sehliiniberger (It).
I'ettera ^' 1 7 ). .lanson ('20), Kjrirenieyer ( '20), \'iel-
hauer ('20). Vogel ("22). Whiteliead ('22). I.indfors
('21-), Ksmarch ("2.5). Korff and Boninp; ('27),
Flachsaiid Kronberger ("30), Vilkaitis ("33), Motte
('33), Bailie and Miiskett ('33). and .Tanialainen
('3(5).
The .■iniount of lime used and reeominended by
many of these workers varies greatly, and this may
partly explain some of the inconsistencies in the re-
sults obtained. The investigators listed below have
used and advocated the following quantities of lime
in the control of club root:
.\bluiy (1831), :?.5(i bu. per ;nre.
Hunter ("-i'). 14— 1(> tons per acre.
Sommerville ('!U), "DO lbs. per acre in drill.s witli seed.
.1. A. Voelcker (94), 2 tons ))er acre.
Stewart ('9.5), 90 bu. per acre.
Mathleii-Sanson ("9"). 400 liters per acre.
Hawk ('98), ()-8 tons per acre.
Mc.Mpine ('03), 0.3-'-0.(>7 liters per sij. in.
I.aubert ("0.5), 1..5 kp. per sq. m.
Seliluinherjrer (14), --3 kjr. per sq. ni.
Hurkart ('lo), 0.5-0.0' fnn. per sq. m.
Neper ("l"), 0.5-1.0 kp. ))er sq. ni.
Triesehmann ("17), ;?-3 kp. per sq. m.
Popp ('19), 0.5-0.6 kp. per sq. m.
Biibner ("--), 1.4 kp. per sq. m.
Hosterinann and Noak ("J3), 0.5-0.6 kp. per sq. ni.
Darnell-Smith ("-4), 1.50 bu. per acre.
Herpers {'-H), O.ij kp. i)er sq. m.
Beyer ('-5), 0..5 to 0.6 kp. i)er sq. m.
Tessenow (':J6), 400 pms. (ler sq. m.
Gleisberp {'26), 0.5-0.6 kp. per sq. ni.
Kirsebner ('27), l-J kp. per sq. m.
Blunek ('i?9), 1-2 kp. per sq. m.
.\lbert ('31), 1—4 tons ])er acre.
Anony. (Australia, "40), 2 tons bydrated lime per acre.
Stubbs ("41), 1-2 tons per acre.
The majority of workers listed above did not
specify the kind of lime used, and it is im])ossible to
determine whether they used pure calcium hydrate,
air-slaked lime, carbonate of lime, etc., or calcium
cyanamide. Since all kinds of lime are not equally
effective in controlling club root many of the differ-
ences in results reported in the literature arc doubt-
less due to tliis factor. .Soil difl'erences. degree of
spore infestation, environmental conditions, soil
moisture, variations in technique and time of lime ap-
plication before ))lantiiig, use of manure and acid
fertilizers with lime, etc., are factors which may in-
fluence the effectiveness of lime, and unless they are
kejit as constant as possible in cx|)erimental work,
ditfereiices in results are certain to occur. That such
factors are im))ortant is well shown by the jirecaii-
tions reconnnended for the use of lime. Schlumberger
('14), for instance, claimed that lime is effective only
it the soil is thoroughly ;ur,iti(l at the time of .ippli-
c.-ition, while I.arscn and Walker ('SI) rcjiorted that
acr.-ition in relation to liming increases infection.
They also found that fluctuations of soil moisture at
a relatively low moisture content influenced the de-
gree of infection in limed soils. A|)pel .-iiul .Schlum-
berger (11) noted th.it liming becomes less effective
on a given i)lot the second year, and I.indfors ('21-)
.asserted that lime is ineffective if the disease is
already present. If not, lime is a good club root in-
hibitor. Murphy ('27) m;iintained that lime does not
take effect until the tliird or fourth year after a])-
l>lication, and Kreuzpointer ('29) stated that lim-
ing .ind other control measures are worthless if stable
and liquid manure are used in conjunction. All of
these re])orts as well as others to be found in the lit-
erature, show that several factors operate and iiiHii-
ence the inhibitory properties of lime.
Some of the workers who have specified the kind
and quantity of lime used are listed in table 3, which
is obviously very incomplete because much of the
Euro))ean and Asiatic literature has not been avail-
able since the jiresent war began. Table 3 shows
quite clearly that the amount of lime used and rec-
ommended as well as the effects produced vary
greatly. Calcium hj'drate is generally believed to be
the most effective, but Walker and I.arsen ('3.5)
found that calcium cyanamide is about twice as effec-
tive as Ca(OH)^. in reducing infection in cabbages.
Martin ('31') and Haenselcr and Moyer ('37) have
likewise found calcium cyanamide to be effective
when used alone, and when used in combination with
calcium hydrate the decrease in clubbing was even
greater. Wellman ('30) got complete inhibition with
calcium hydrate, and found that limes consisting of
CaCO-., and CaSO^ ■ 'ZH.^O are not good club root
inhibitors. On the other hand, limes which are of CaO
or C'a(OH)2 composition are good inhibitors. The
effectiveness of air-slaked lime varies greatly. The
relative amounts of hydrate and carbonate in air-
slaked lime varies considerably depending on the
conditions under which the oxide is slaked, and this
factor doubtless influences its effectiveness. Burnt
quick lime (CaO) is usually beneficial, but calcium
carbonate is generally regarded as ineffective. Al-
though Massee and Carricklee reported gas lime to
be inhibitory it has been found to be of little or no
value ( Halsted, '96-'99). Calcium chloride not only
fails to arrest club root infection but also reduces the
croj) materially. Raw ground limestone is rc|)orted to
be effective (I,. R. .lones, '01), but Wellman ('30)
found no inhibitory effects by its use. Later, however,
I.arscn and Walker ('S^) rejiorted that finely ground
dolomitic limestone distinctly inhibited infection
when a))|)lied in sufficient quantity to bring the jiH up
to ().9. .ind completely i)reveiited infection at |)H 7.2
and 7.6.
In Germany and other countries of Euroi)c a jiat-
ented preparation called Steiner's remedy, consist-
ing of relative ))ro])ortions (Popp, '19b) of lime,
ashes, and refuse or waste, has been used with con-
siderable success in controlling club root. In addi-
112
PLASMODIOPHORALES
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CI.l'H HOOT OF CRUCIFKRS
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iLlll HOOT OF (Hit IFKIIS
115
tioii. it is sjiid to lead to a more richly liraiu-lu'd and
(ilaiiuntous root systciii on tin- host (Apptl and
Si-lilunilicrgcr, '13. ' 1 I- : MiilK-r and Osfirwaldcr,
'■_';!). It is jifiicrally applii-d 10 cms. deep on infested
soil (Nauniann. '13 ; ."^chllnnl>erger. 1 I- ; 1 liltner .ind
KortV. 'Ki: l'oj)p. '1!»; and Hosterni.-nin and Noak.
'23). or at the rate of 1.000 cu. in. per hectare. Nau-
mann (12. '13), Schlumbcrger (1 0- Hiltner and
Kortf ('16), Ncger ('17), Popp, Schmid ('19),
.^eliatfnit .-md I.ustner ('20). Hiisterniann and Xoak
^'23). and others have rel)ortid iuiieficial ert'eets
from the use of this prej)ar;ition. .\))l)el and .Schlum-
bcrger ('13. '\i). however, found it to he unsatisfac-
tory, and claimed that its ett'ectivcness is dependent
to a large degree on the weatlier. While .Steiner's
remedy has proven to be fairly cflfective in control-
ling club root, the detailed and bothersome method of
preparing and ai)])lying it as well as the high cost of
materials and transportation have not made it po))u-
lar and connncreially profit.-ible.
.\s to the most suitable time and method of ap])ly-
ing lime for club root control various i)ractiees and
recommendations are to be found in the literature.
Eydeshymer ('91), Halsted ('96. '97), Laubert
('0.5). Schlumberger ('!!■), Chupp ('25) and Ko-
blischek ('29) advocated application 3 to 6 months
before planting, wliile Erickson ('26) recommended
6 to IS months. Ciibbs ('32) found that if ])lanting
took ])lace too soon (less than 3 months) after lim-
ing, club root occurred 2^ .j-i inches below tlie sur-
face, while in fields planted 12 months after liming
infections were present only at 9—1 1 Yo inches. Gibbs
accordingly advised at least 3 and up to 12 months
between ])lanting and liming. As to the method of
application. .Sommerville ('94). Seltens])erger ('96),
Roger ('12). Koblischek ('29), and others recom-
mended drilling lime in with the seed or apjilying it
directly to the plant holes at the time of trans])lant-
ing. According to Ravn ('12, '13) it is immaterial
whether the lime is hoed in or plowed under. Since
infection appeared to be [jrevented to the depth to
which lime penetrates. Cunningham (1 l) advocated
mixing the lime down to 6 to 9 inches in the soil.
Miiller and Osterwalder ('23) also advised a thor-
ougli mixing of lime and soil.
The manner in which lime o])erates against club
root is not very well understood. .Most workers have
believed that it prevents spore germination by rais-
ing the H-ion concentration of the soil, since the
spores germinate more readily in acid media, accord-
ing to inimerous investigators. Likewise, it has been
reported that infection rarely occurs above pH 7.2 to
7.1- ( Chup|). '28). That an increase in ))H is not the
sole determinating factor is indicated by the re])ort
of Honig ('31) that spores will germinate equally
well in alkaline media, and by the fact that club root
may occur in a high ))H environment. Whether or not
lime has a direct toxic and lethal effect on the resting
spores is uncertain. Bremer ('2:}) refuted this idea,
but later Whitehead ('36) claimed that lime is toxic.
Naumov ('27) found that calcium hydrate has no im-
munizing effect on cabbage, and concluded that its
ecuitroUing efieet is due to direct .action on the ])ara-
site itself. .Seedlings which had been grown for two
months in sterile soil with ;i very higli lime content
were as susceptible .as the controls when tr.insferred
to infested soil. Naumov .also found tli.-it s.ilts of
other metals, p.articularly b.irium and magnesium,
have a controlling etVcct. and from these exi)eriments
he concluded that the deciding factor in the inhibi-
tory action of the salts on the parasite is not so much
on the nature of the metallic ion as the presence of
free hvdroxyl ions in the soil. In the case of calcium
cvan.'imide. Walker and I.arsen ('St) stated th.it its
toxicity is not due only to the basic substances
formed from it but also to the CHo anions in the soil
before hydrolysis is comi)letc.
Basic Fertilizers
While the nature of the inhibitory effect of lime is
not clearly known, it is nonetheless obvious from
experimental work that lime makes the soil environ-
ment unfavorable for club root infection and develop-
ment. Any fertilizer, therefore, which neutralizes
this effect is to be avoided. The selection of a fertil-
izer to be added to the soil previously or sown with
the seed determines to a great extent whether or not
liming will be effective. Acid fertilizers in general
and J)articularly superphosphates, basic su])erphos-
jjhates. superphosphates and carbonate of lime,
turnip manures, etc.. have been found to nullify the
effects of lime and stimulate club root. The substitu-
tion of basic fertilizers and their use with lime is ac-
cordingly essential and has been widely advocated
and l)racticed. A review of the literature shows, how-
ever, that the results have not always been strikingly
beneficial or commercially satisfactory. In t.ible i
are listed the most commonly used of these fertilizers
and their effect on club root.
In addition to the fertilizers listed in table 1 oth-
ers have been used with varying success. Calcimn and
potassium nitrate give favorable results, according
to Brezhnev ('31'). Kindshoven ('21', '28) likewise
secured good results from calcium nitrate when used
at the rate of 50 gms. per sq. m. of soil. Sodium ni-
trate is effective when used in combination with lime,
according to Murphy ('27).
Animnnium sulfate is ineffective as a fertilizer in
combating club root, according to \\'hitchead ('25)
and Osterwalder ('29).
Mar/nesium carbonate reduces infection in well-
w.itered soil when used in sufficient amounts to raise
the ])H to 7.0 and usually inhibits the disease at pH
7.2 or above ( Larsen and Walker. '31).
(ii/psum stimulates the development of club root,
according to I.indfors ('2 J), and in the o|)inion of
\\'ellman ('30) is comi)letcly ineffective as a control.
"Schlick" or ore slime is a good fertilizer to be
used against the disease, according to Hayung.a ( '12,
'I.')). .\i)|)el and Schlumberger (13), and Schaffnit
and I.ustner ('20).
116
PLASMODIOP MORALES
Table 4. Showing the effects of basic fertilizers on the control of club root.
Arker ("35)
Blunck CJ9)
Deutelmoser (,'-20)
Eriksson, '13
Farsky, '^^6
Flachs and Kron-
berger ("30)
Gibbs {'32)
Halsted, '95-99
Hayuna, '1-\'19
Hiltner, "08
Hiltner, KorfT, '16
Kindshoven, '2i, '2S
Kreuzpointer, ':?3
Magin, '02
Miller, '23
Motte, '33
Murphy, '27
Naumann, '13
Osterwalder, '29
Schmidt, '-22
Vogel, '22
Wagner, '09
Whitehead, '35
Kainit (potash)
Favorable results
2,000 kg. per hectare —
favorable
Favorable results
Favorable
500, 1,000, 2,000 lbs. per
acre — poor results
Favorable results
Unfavorable results
Inconclusive results
Unsatisfactory results
Basic slag
Favorable results
Favorable results
Basic slag -\- lime —
favorable results
Calcium hydroxide
and calcium
cyanamide
(Beka-Wurzelschutz)
Unfavorable results
Calcium hydroxide
and waste
(Herniol)
Effective
Good results
Basic slag + lime —
effective control
8-12 kg. per acre -|- lime
— good results
Favorable results
Favorable results
Favorable results
More or less unfavor-
able
Unfavorable results
Favorable results
More or less unfavor-
able
8-18 kg. per acre -f- lime
— good results
Favorable results
Haage's remedy has been found to be of little
value by Appel and Schlumberger (13) and Nau-
mann (13).
Superphosphate fertilizer stimulates club root de-
velopment, according to Ravn ('10, '12), Osterwal-
der ('29) and Gibbs ('32). but McAlpine ('03) and
Flachs and Kronberger ('30) reported favorable re-
sults from its use.
Jassen's remedy (calcium carbide dust and cal-
cium cyanamide) is ineffective, according to Miiller-
Thurgau and Osterwalder ('23).
Saltpeter, superphosphate and potash as a combi-
nation fertilizer increases turnip yields, according to
Ravn (10). but also stimulates club root develop-
ment.
Various kinds of ashes have also been tried as fer-
tilizers in relation to club root, with varvinij success.
Lime, peat, and briquett ashes are effective accord-
ing to Ponkler ('96), Mathieu-Sanson ('97), Seel-
hoff ('12), K. M. ('19) and Straube ('22). Wood
ashes were reported by N. N. ('93), Massee ('96)
and Katterfeld ('23) to be effective against club root,
but Halsted ('96, '99) and Schlumberger ('14)
found them to be useless.
The beneficial effects of alkaline fertilizers as con-
trasted with acid ones on club root has been shown in
experiments involving so-called complete fertiliza-
tion. Kindshoven ('21) succeeded in reducing infec-
tion from 30 per cent to 2 per cent by application of
an alkaline fertilizer consisting of calcium cyana-
mide, basic slag and 40 per cent jjotash at the rate of
50 gms. per sq. meter. Honig ('31 ) likewise got strik-
ing results in comparing the effects of alkaline and
acid fertilizers on infection of kohlrabi in pots of
heavily infested soil, as is shown below.
fl.ni HOt)T OF (lll'l Il'KHS
117
I'ori'ciitdpe
Alknliiie of infet-tion
5.55 gms. sodium nitrate 0-20
10.50 " basic slaj;
13.11 " calcium carlionatc
i.li.) " jiotasli
.\cid
i.-2 gm.s. ammonium sulfate
8.9+ " supcrphosiihate 90-100
17.S4 " jTj-psum
5.J5 " Kainit
Controls 26- 31
Plants treated witli tlie alkaline fertilizers showed
0 to 20 i)er cent infection, while those watered with
acid fertilizers were !»0 to 100 |)er cent infected.
(iihhs ('32) also found a marked ditierence in cluh
root development when basic slag was compared with
superphosphate in conjunction with lime, as is shown
below: Percentage of Infection
Seeds drilled Seeds drilled
with basic with super-
Treatment slag phosphate
Control — no lime 59 95
3 tons commercial ground
limestone per acre 23 53
3 tons superfine ground lime-
stone per acre 10 87
2 tons air-slaked lime ])er acre 0 78
2 tons burnt lime per acre ... 0 36
2 tons water-slaked lime per
acre 3 82
Kirschner ('27) has likewise advocated the use of
comjilete hasic fertilizer composed of basic slag and
potassium nitrate in conjunction with calcium cyana-
mide to control club root in the field. In this connec-
tion may be noted Pryor's ('10) study on the effect
of sulphur, nitrogen, and potassium nutrition on club
root develoj)ment in suscejitible, resistant and im-
mune strains of crucifers under controlled green-
house conditions in Wisconsin. Varying nutrition has
a pronounced effect on disease development in sus-
ceptible plants but does not influence resistance in
immune varieties, according to Pryor. An abundance
of potassium or nitrogen and a deficiency of sulphur
or nitrogen increased the disease in susceptible
plants. The percentage of infection was decreased
markedlv by a jiotassium deficiency. In the case of
resistant plants club root was increased somewhat by
a high supply of nitrogen ; increased further by a de-
ficiency of sulphur or nitrogen, and definitely de-
crea.sed by lack of potassium.
Soil Drainage
Since club root is frequently most severe on low.
wet and water-logged soils, proper soil drainage has
often been advocated as an effective cure. .Anderson
('.5.5) and Ravn ('08) cited several instances where
club root had been markedly checked by drainage,
and Montieth ('21) and Naumov ('33) have demon-
strated by controlled experiments that crucifers can
be grown free of tlie disease in tlioroughly infested
soil by keeping the soil moisture down to 30 to 10
per cent of the water-holding capacity ; all of which
indicates the effect of excessive water in the develop-
ment of club root. However, there is considerable
evidence to show the niainten.ince of proper soil
moisture bv drainage is not in itself effective. Severe
clubbing li.-is often been found on liigii. well-drained
soil and in fields which were carefully under-drained
with tile. Furthermore, Wellman ('30) has shown
that club root may occur generally in roots which are
exposed to only 18 hours of excessive soil moisture.
During the last two decades it has become increas-
ingly obvious that other soil fa<'tors, relative acidity,
humus content, etc., are involved and influence the
efficacy of drainage as a curative measure. \\'liile soil
drainage aerates and improves the physical condition
of the soil, it cannot be relied upon alone as an in-
Iiibitor, but must be used in conjunction with other
control measures to be effective.
Crop Rotation
Crop rotation is now generally recognized as es-
sential in combination with other control measures
against club root. Since the type of soil most favor-
able for intensive cultivation of crucifers is relatively
limited, farmers and gardeners have a tendency to
grow these crojis on the same land for several suc-
cessive years. If club root is present, such practice
obviously leads to heavy infestation with fungus
spores, and unless stringent control is exercised the
land may become worthless for crucifers within a few
years. "The earlier students of club root, including
Heinzelmann ('82), Eycleshymer ('91), Laubert
('0.5a), Kock (']]), Burkhart ('1.5). and I.udwigs
('25) advocated only 2 to 3 years between successive
crucifer crops, but since it has been shown that the
resting spores of P. Brassicae may remain alive in
the soil without hosts up to 7 and 8 years, it is ob-
vious that a long rotation period is necessary for
heavily contaminated fields. Jorstad ('23) recom-
mended 5 to 6 years, Lindfors ("21) 1, Siemaszko
("25) -i to 5, De Andres ('29) 3, Nielsen ('33) 6 to 8,
Motte ('33) 7, Fedorintschik('35) 1, Gibbs ('39) 6,
and .Stubbs (H ) 1 years or more between successive
crops of crucifers. .Short intervals are aiijiarcntly in-
effective if Fedorintschik's observations that soil not
))lanted to crucifers for seven years contain enough
viable spores to infect 26.6 per cent asceptically
grown cabbage seedlings are correct. The practice of
liming during rotation is of questionable v;ilue in
light of (iibb's ('39) observation th.-it the addition of
lime and sulpluir does not affect sjiore longevity.
Crop rot.ition is further com|>licated bv the fact that
wild cruciferous hosts or weeds are also susccjitible
to club root and may keep the fungus alive during the
rotation interval.
\'arious cro|)S have been advocated as beneficial in
rotation. Halsted ('99) reported a fivefold increase
in turni))S on land whicli had been ])lante(l to buck-
wheat the previous season, but these beneficial re-
sults were not evident the second year. Pettera ('17)
118
PLASMODIOPHORALES
maintained tliat Thysostetjia virginica, Achillea
pharmica, Astilbe sp., and Pi/rethrtim have an in-
hibitory effect on club root and inactivates the spores
within three years. Miiller-Thurgau and Osterwalder
('23) also found that the spores remain viable only
three years if beans are rotated with cabbage. Ac-
cording to Murphy ('27) turnips should be alter-
nated with carrots. Blunck ('29) found that beans
were particularly favorable as an alternate crop.
Arker ('35) advocated rotation with beets, and
Fedorintschik recommended rotation with grass and
clover during the last two years of the interval to
avoid plowing.
Eradication of Wild Hosts
Numerous cruciferous weeds are susceptible to
club root, as Halsted ('92-'99), Ravn ('08), Cun-
ningham ('I2,'ll.),Ssacharoff ('16),Naumov ('26),
Gibbs ('32), Rochlin ('33), Jamalainen ('36), and
others have shown, and these hosts may harbor and
perpetuate the disease in the absence of cultivated
crucifers. Infected weeds have been found in grass
pastures, wayside ditches, river beds, gardens, and
cultivated fields (Halsted, '98 ; Gibbs, '32), and their
presence on infected soil reduces the effectiveness of
crop rotation in club root control. Even when only a
few weeds are present in infected fields enough
spores will be produced and perpetuated to infect
subsequent cruciferous crops. Eradication of wild
crucifers is therefore highly essential as a control
measure and has been advocated and practiced to
some extent as such, but in certain places it is not al-
ways practical. As Gibbs has pointed out, eradica-
tion is impractical in cereal grain crops, grass lands
and pastures. In crop rotation on cultivated fields,
eradication is obviously important, but unless it is
combined with other control measures such as liming
and growing resistant varieties of crucifers to keep
down spore multiplication, its effect is limited.
Other special control measures involving winter
ridging of the land and hilling up the soil around
cabbage stalks have been practiced without consist-
ent success. In the autumn of 1898 Halsted plowed
infected plots deeply and piled the soil up in long
2 ft. higli ridges to expose the spores to the maximum
weathering during the following winter months. Less
clubbing was present on the ridged land (31 per
cent) the following season than on the level plots
(38 per cent), but the small difference does not
justify ridging as a satisfactory remedy for club
root, according to Halsted. He also tested the eft'ect
of shading on the disease in turni])s and found that
it does not have an inhibitory effect. Hilling up the
soil around cabbage stalks leads to increase of ad-
ventitious roots on the stalk above the infected por-
tion, according to Cunningham ('ll). Such adventi-
tious roots are comparatively free of clubbing, and
since they occur above the diseased and useless main
root the nutriments which tliey absorb are readily
available to the developing heads. Cunningham
found that liilling increased the yield ten-fold in
some plots during 1912, but in the following year no
beneficial results were attained.
Resistant Varieties
Cultivated and wild crucifers vary in degree of
susceptibility to P. Brassicae, and several cultivated
strains and varieties have been developed which are
fairly resistant to club root. A certain measure of
control may accordingly be achieved by the cultiva-
tion of these varieties. Particularly promising are
the results obtained by Olsson ('39, '40) in breeding
resistant varieties of swedes and turnips in Sweden.
The data on relative degree of resistance, however,
are often conflicting, and in certain varieties where
some investigators have reported complete immunity,
others have found 100 per cent susceptibility. These
differences in results are doubtless due in part to
variations in experimental conditions and methods
employed. As has been shown elsewhere, soil types
and moisture, H-ion concentration, number of spores
in the soil, etc., are important factors in infection,
and unless they are kept constant in experimental
work, it is diflicult to determine the inherent degree
of susceptibility or resistance of a particular variety
or strain. Doubtless many of the reported cases of
immunity relate to plants which have escaped infec-
tion in tlie field. The literature relating to varietal
susceptibility is nonetheless very extensive, and in
a brief treatise of this nature no attempt will be made
to enumerate and discuss all tlie data relative to this
subject.
The range of susceptibility in turnips is very great
and some varieties are reported to vary from 100 per
cent susceptibility to almost complete resistance. No
varieties, however, have been developed or found
which are consistently immune. Southern Curley
Top, Rutabaga, and Large Flat Green were re-
ported by Cunningham ('14) to be particularly sus-
ceptible. In the first named variety clubbing was so
extensive that the turnip root was converted into a
system of branched hypertrophied rootlets. On the
other hand, the following commercial strains have
been reported to be relatively resistant :
Bruce Purple Yellow Top
Bruce Purple Top Yel- Purple Yellow Top Aber-
low deen
Bruce Wallace Rutabaga
Dale's Hybrid Scarlet Kashmyr
Early Snowball Seefeld
Earlv White INIilan Snowball
Golden Ball Svaliiv's Yellow Tankard
Green Top Victor
Hinkenborstel Weibull's Immune
Irvine's Green Top Yel- Weibull's Sekel
low White
May White Fleshed May
New Bronze Top ^^'hite Milan
Ostersundom Yellow Aberdeen
Pomeranian Tankard Yellow Bruce
Purple Top Milan
cLfn ROOT or imc ikers
119
l>y Hiilsti-d ('J»!>). R.-ivn (,'11). Cunningliam {'it),
Anony.. (Nova Si-otia. :>3). I-indfors ('at, '25),
■r.iiiunt ('•-'■). '30. '.•tn.Ciil.ks ("31). rindlay ('31).
Mad. rod ('31). Ihiidru'k ('32). Ik'.iuiiKiiit and
.•^taiiiland ('33. '31-). Walker and I.arsiii ('31.).
WalkiT (^'3(>).()lsson ^'3!>. 'K)). Hriv.liniv ('3<t) and
Pryor ("10). Early \\'ihte Milan and Early
Snowball showi-d only 1.1 per cvnt to O.G per cent
susoi'ptibility, accordiiifi to t'unniniiliani.
Swedes in general .-ire reported to l)e more resi.st-
ant tlian turnijis. but tliey likewi.se exliiliit a wide
ran<;e of .susceptibility and resistance, 'llie following
v;irieties:
Balmoral Ostergiita
IJ.ingholm Otofte
Bangliolm Hcrning Sweet German
Bangliolin .Studsgaard .Sweet Russian
Danish N'arieties !■ and White Necklace
'2ii White Russi.m
Green Top Swedish White Swede
Ma j rova \\'ilheuisburger
May
have been reported by Ravn ('H). Cunningham
('1 t). .\nony., (Nova Scotia, '23), Lint'ors ('21., '25),
Whitehead ('22, '25). Hockey (•26).Gussow ('26),
Tenncnt ('25. '30. '3I-), Davis, Griffith, and Evans
('28). Osterwaldcr ('29). Gibbs ('31), Findlay
('31). MacLeod ('31). Beaumont and Staniland
('33. '31). Walker and I.arscn ('31-). Olsson ('89.
'40). Bennett ('39). and Pope ('39) to be relatively
resistant. Ravn ('11). I.indfors, Ciiissow, and Pope,
however, found that the so-called resistant Bang-
iioLM PfRPLE Top. Studsraard Bangholm, Wil-
HELMsniRGER. and Yellow Tankard varieties may
be 100 ))er cent infected and completely destroyed.
Cabbages, likewise, show a wide range of suscepti-
bility to club root, and none of the commercial varie-
ties are highly or eomiiletely resistant, according to
Cunningham, I.indfors, \\'alker and I.arsen. .lania-
lainen, and others.
.\11 Seasons Dark Red Erfurt
.\mager Hvidkaal
.\meriean Savov Mammoth Red Rock
Blomkaal Perfection Savoy
Braunsweig Gribkova Rodkaal
Braunsweig Hos Hos \'olga
Brunswick White Russian
Copenhagen
have been reported by Ravn ('08), Cunningham
('12. 'U). Naumov ('25, '28), Rochlin ('33). and
Fedorintschik ('35) to be particularly susceptible.
-Ml of these varieties may show 98 per cent to 100
])er cent clubbing in badly infested soil. On the other
hand.
Blue Large Late Flat Dutch
Bodenkohlrabi Late Moscow
Bronka Red
Griinkaal .Short Stiinmed Amager
Henderson's Early Sum- Slovianka
mer .Stone Maxon
Hollander Valvatievka
are said to be less susceptible (C'unuinghani, ' 1 !■ ;
Hdstermann. '22; IL-irter and .Jones, '2t; Oster-
waldcr. '29; Tedin. '3:i ; Motte. '33; Fedorintschik,
'3(1 ; 15re/,hnev '39).
U.idishes are also very susceptible to club root,
and it is doul)tful whether any eomi)letely immune
eonunereial varieties exist. Halsted ('99) reported
tJIANT StI'TTCiART, LoN(i BlaI'K Sl'ANISII, NeW-
coMu White, and Yellow Summer Ti'rnip to be
wholly free from clubbing. Cunningham found that
susceptibility varied from 92.2 per cent in Long
Scarlet Radish to 5.6 jier cent in Giant Stutt-
gart. In addition to the latter variety. Early Scar-
let Turnip, Delikatess, DHKiKNiiHrNNEN, Im-
mune, Long Black Paris A\'inter, Ruuin. and
Sa.xa have been reported by Cuiuiingham (ll),
Gleisberg ('23) and .Jamalainen ('36) to be fairly
resistant.
Other commercial cultivated crucifers have not
been so extensively studied for varietal resistance as
those noted above. Cunningham and .Jamalainen
found all varieties of kohlrabi to be very susceptible,
but Schatt'nit reported that the varieties which he
studied were relatively immune. Honig ('32) tested
five varieties of kohlrabi and found the following
incidence of infection: (jelbe Schmalz 7.3 per cent,
AVeisse Schmalz 27.7 per cent, Weisse Wester
0 per cent, Gelbe Wester 32.6 per cent. Apfel gelb
6.2 per cent. Among Brussel sjjrouts. Hercules is
fairly resistant (.Jamalainen, '36). All varieties of
cauliflower are equally susceptible, according to
Cunningham, Lindfors, and Jamalainen. Marrow
Stem and Dreinenbrunnen Curley Kale are said
to be highly resistant by Osterwalder, and Beaumont
and .Stanland, while April Queen and Victory
broccoli were found to be resistant by Bailie and
Muskett. Rape shows almost 50 per cent susce]5tibil-
ity. according to Cunningham, but (ileisberg re-
ported it to be immune to club root. Ssacharotf and
Rochlin also reported B. Napiis var. S. esculenta to
be immune. One variety of B. Rapa sliowed 100 per
cent susceptibility, while another exhibited only
10.9 iJcr cent clubbing, according to Cunningham.
Gleisberg. however. re])orted B. rapa to be unsus-
cejitible. Mustard is rejjorted to be highly susce])tible
by Hcistermann. while Cunningham. Naumov. Motte
and Rochlin found black mustard to be highly resist-
ant or completely immune. Chinese cabbage sliows
100 per cent suscejitibility. according to Naumov and
Katterfeld.
Nature of Siisceptihility and Resistance. — The
differences in degree of infection exhibited by the
wild .ind cidtivated crucifer varieties listed above
were believed by some w-orkcrs to be l)artly due to
the ))rescnce of more or less virulent biological
strains of P. Brasxicae which are sjjceitic for certain
hosts. Considerable doubt has been ex))ressed about
the presence of such strains and it is rather generally
believed that relative susceptibility and resistance
are largely inherent host characters. The nature of
resistance is not yet well understood, but .Ssacharoff
believed it to be due to substances in the cell sap.
120
PLASMODIOPHORALES
He found that resistance was correlated with a low
sugar content in the cell sap and a pungent, bitter
taste of the expressed juice, while the cell sap of
susceptible plants was comparativel.v rich in sugar
content. Whitehead ('25), however, asserted that the
factor determining resistance is not related to total
dry matter or sugar in the roots. Further observa-
tions and experiments on the nature of resistance
were made bj- Rochlin in 1933, who tested i7 wild
and cultivated species belonging in 11 genera of the
Cruciferae for their susceptibility to P. Brassicae.
He found that the reaction varied from complete
immunity in some species to susceptibility in others,
independently of their taxonomic position, as Cun-
ningham had previously shown. All gradations of
susceptibility occurred in one and the same genus.
Rochlin also made a comparative anatomical study
of the roots of numerous species and found that in
the early stages of growth immunity or susceptibility
is not correlated with any marked differences in root
structure. In adult plants, however, the penetration
and spread of P. Brassicae is hindered to some de-
gree by the development of cork layers, collenchyma,
and by the compact structure of the wood layers.
The degree of resistance exhibited by a species or
variety is directly correlated with tlie amount it con-
tains of those glucosides which on fermentation with
my rosin produce highly pungent mustard oils, ac-
cording to Rochlin. Chief among such glucosides in
crucifers are sinigrin (particularly abundant in B.
nigra and horseradish and in smaller amounts in
Sinapsis juncea, B. rapa, B. Napus, etc.), gluconas-
turtiin (in Barharea praecox and Nasturtium offi-
nale), glucotrapaeolin (in Lepidium sativum), etc.),
and glucocochlearin (in Cochleari officinalis). Sina-
blin, a glucoside present in B. alba, which does not
yield a pungent mustard oil, was found to be of no
protection against infection with P. Brassicae.
An indication of the possible use of active gluco-
sides or their derivatives as fungicides is shown by
the results obtained by Rochlin in a small experi-
mental plot in which seeds of tlie very susceptible
Brunswick cabbage were sown in highly infected
soil in pots, some of which were abundantly watered
with a water extract from B. nigra seeds. Only 20
per cent of the seedlings became infected and showed
a very slight swelling of the roots, while all the con-
trol seedlings were infected. Considerable doubt has
been thrown on Rochlin's theory of the nature of re-
sistance by the subsequent studies of Walker ('36),
Walker, Link, and Marcell ('36). These workers
found that some collections of B. nigra are very sus-
ceptible and that there is no correlation between mus-
tard content and resistance.
From the practical standpoint, Rochlin suggested
the possibility of controlling club root b}' crossing
cruciferous species deficient or meager in active glu-
cosides with those which contain greater amounts of
these substances. Pryor investigated this possibility
by direct experiments involving variation of the mus-
tard oil content of crucifers and noting their sus-
ceptibility to the disease. All mustard oils in cruci-
fers contain sulphur and nitrogen, while their gluco-
sides also contain potassium. Thus, by lowering or
increasing these nutrient elements, it is possible to
change the mustard or sulphur oil content of experi-
mental plants. From the results obtained by this
procedure, Pryor concluded that sulphur oils do not
inhibit or prevent infection and development of club
root in crucifers — thus refuting the observations of
Rochlin.'
Geographical Distribution of Club Root and
Bibliography of Literature
Club root is now world wide in distribution, and
the countries from which it has been reported up to
the present time are listed below. The number of
publications on the occurrence, distribution, hosts,
life-history, cytology, relationships, eradication and
control of P. Brassicae and club root is quite large
and many of them are to be found in local journals
which are not readily available. In the bibliography
which follows many such publications have doubt-
less been overlooked and omitted.
Alberts, H. W'. 1930. Rept. Alaska Agric. Exp. Sta.
1930: 6.
Georgeson. 1914. Ibid. 191 i: 27. 1915, Ibid. 1915:
39. 1917, Ibid. 1917: 8. 1919, Ibid. 1919: 21.
1927, Ibid. 1927: 10.
ARGENTINA
Marcliionatto, J. B. 1929. Phys. Rev. Soc. Argentina
deCien. Nat. 9:455.
AUSTRALIA
Anony. 1940. Agr. Gaz. New South Wales 51: 559.
Darnell-Smith, G. P. 1924. Agric. Gaz. New S.
Wales 35: 180, 488.
McAlpine, M. D. 1898. Proc. Linn. Soc. N. S. Wales
1898: 82.
. 1901. Dept. Agric. Victoria 1901.
. 1903. Dept. Agric. Victoria 1903.
Noble, R. J. Intern. Bull. PI. Protect. 5 : 202.
Stubbs, L. L. 1941. Jour. Dept. Agric. Victoria 39:
208.
AUSTRIA
Anonymous. 1933. Bundesant. f. Pflanzensch. Mit-
teil. 167.
Kock, G. 1911. Landesamtbl. Erzherogtums Osterr.
a. d. Enns 1911, no. 1.
Kornauth, K. 1913. Zeitschr. Landw. Versuchsw.
Osterr. 17:395. \915, Ibid. 19: 180.
1 In a paper presented before the December 29, 1941,
meeting of the American Phytopatholofjical Society,
Dallas, Texas, W. J. Hooker (see Phytopathology 32: 9)
reported that two mustard oils (alhi isothiocyanate and
beta phenyl ethyl isothiocyanate) were consistently effec-
tive in preventing spore germination at 80 ppm. and some-
times at as low concentrations as 10 ppm. of allyl isothio-
cyanate and 5 pi)m. of beta phenyl ethyl isothiocyanate.
Concentrations of both oils below the toxic level were found
to be capable of stimulating spore germination.
CLrn ROOT OF CRUCIFER8
121
I'ii-lilor. r. 1!)1!». Willi. I.jindw. Zt-it. liUi): ;i83.
Stift, A. 1!)0."). iistiTr. L'ngarisclu- Zt-itsrlir. Ziickcr
II. I.;milw. l!tO.->: !).
Tcrby. J. l!>-':t. M<ni. Roy. .Vcad. Btlj;. 7: 1-28.
• . l!)-'ta. Hull. Hov. Hot. .Soi-. Htljiiiim .">(5: 18.
. li)2U). Hull. Hov. -Vend. H.li;. .Tser. 10: .-)li).
. 15)32. M(m. Roy. Acad. Hclg. 11 : 120.
Vanderyst, H. U)OK Bull. Agric. 20: 533.
Ur LOAD I A
Nicoloff. I., and M. Stefanova. 1922. Zeiitralbl. f.
Agrikultiluiuic .-)1 : 101-102.
Anonymous. 15)23. Rcpt. Suiiorint. Keiintville. X. S.
Exp. Sta. 15)22. Canad. Dept. .\j;ric. Domiii.
Exp. Farm.
Clark. J. 15)21. Rept. Superint. Cliarlottetown,
P. E. I. Exp. Sta. 1923. Canad. Uept. Agric.
Domin. Exp. Farm.
Giissow. H. T. 1925. Rept. Domin. Botanist for
1921. Div. Hot. Canad. Dtpt. Agric. pp. 27-28.
Hockev. J. F. 1920. Rept. Domin. Botanist for 1925.
Div. Bot.. Canad. Dept. Agric. pp. 29. 1927,
Ibid. 1927: 28. 1928. Ibid. 1928: 139.
I.cdingham, G. A. 1931. Nature 133: 531.
McRostic. G. P. 1936. Rept. Canad. Seed Grow.
Assn. 193.5-36: 31.
Mcl.arty. H. R. 1929. Rept. Domin. Botanist for
1928. Div. Bot., Canad. Dept. Agric. p. 142.
MacLeod. D. J. 1931a. Rept. Domin. Botanist for
1930. Div. Bot. Canad. Dept. Agric. p. 25.
1931b. Ibid. p. 181.
CEYLON
Fetch, T. 1906. Trop. Agric. 25: 839.
CZECHOSLOVAKIA
Baudys, E. 1911. Zeitschr. Pflanzenkr. 21: 342.
Bubait. F. 1902. Zeitschr. Landw. Versuchsw.
Osterr. 5: 675. 1901, Ibid. 7: 731.
Farsky. O. 1926. Ochr. Rost. 6: 114.
Kohnc. 1928. Landw. F'achpresse Tschechoslow. 6:
201.
Milovidov. P. F. 1931. Arch. Protistk. 73: 1. 1933,
Ibid. 81: 138.
Nemec, B. 1913. Sekarske Rozliledy. Abt. i. Ira-
munitat u. Seriol. 1913: 481.
Schmidt. 1922. Land. u. Forstw. Mitt. Bfilimen 1922:
24.
Sitensky. F. 1896. \'estnik. kriil. Ceske .Spolecnosti
naiik Trida Matem. Proiodov. 1896: 8-20.
Svec. F. 1923. Oehr. Rost. 3: 18-19.
Uzel. H. 15)1 i. Wiener Landw. Zeit. 1904: 917.
— . 1907. Zeitschr. Pflanzkr. 17: 85.
. 1908. Zeitschr. f. Zuckerind in Biihrncn 32:
622. 1910. Ibid. 34: 349.
DKNMAllK
Aiioiiyiuoiis. li)22. Stat. I'orsoksvirk. Pl.-mtek.
Mcdd. 95: 1.
Christensen, O. 15)03. \'ort Laiidbrug. 22: 157.
Christcnsen. H. R.. H. Harder, and F. K. Ravn.
1909. Tidsskr. Laiidbr. I'lanteavl. 16: 430.
. 1911. Zeitschr. i'llaiizciikr. 21: 424.
Fcrdiiiandsen. C. li)_'3. Tidsskr. f. Landkon. 1923:
256.
, and S. Rostrup. 1921. Tidsskr. I.andbr.
Planteavl. 27: 697.
Gram, E., and S. Rostrup. 1922. Tidsskr. Landbr.
Planteavl. 24: 236.
, C. A. Jorgensen, and S. Rostruj). 1928,
Ibid. 34: 778.
Hennings, P. 1895. Verb. Bot. \'ercin Prov. Bran-
denburg 37: LVIII. 1896. /6/V/. 38: 58..
. 1922. Kgl. Landtbr. Akad. Handl. Tidsskr.
1 922 : 26.
Jorgen.sen, C. A. 1922. Tidsskr. Landbr. Plant. 39:
316.
Mortensen. M. L.. S. Rostrup. and F. K. Ravn. 1908.
Tidsskr. Landbr. Plant. 15: 153. 1910. //«V/. 17:
306. 1911. Ibid. 18: 317.
Motte, M. H. 1933. Jour. d'Agric. Prat. 97: 177.
1935, Ibid. 99: 93.
Nielsen, N. .1. 1933. Tidsskr. Landbr. Plant. 39:
361.
, and C. J. Christensen. 1914. Tidsskr.
Landlingetspl. 21 : 87.
Ravn, F. K. 1905a. Dansk. Landbrug. 1 : 39.
. 1905b. Gartner-Tidende 1905: 109.
. 1905c. Beret. Foren. Jyd. Landbofor. 31:
89. 1906. Ibid. 32: 86. 1907, Ibid. 33: 166.
. 1907a. Smaaskr. udg. of Dansk Landbr.
1907.
. 1907b. Beret, om lokale Markforsoy i Jyl-
land 1906: 85.
. 1908. Tidsskr. Landbr. Plant. 15: 527.
. 1909. Zeitschr. Pflanzenkr. 19: 473. 1910a,
Ibid. 20: 45.
. 1910b. Tidsskr. Landbr. Plant 17: 163,
1911a. Ibid. 18:357.
. 1911b. Biol. Arb. 1. Eng. Warmung 1911:
167.
. 1913. Zeitsclir. Pflanzenkr. 23: 140. 1917,
Ibid. 27: 141.
, and A. Madsen-Mygdal. 1906. Udg. of de
Samvirk Landbofor. i Fyns Stift, p. 14.
and A. Madsden-Mygdal. 15)09. Zeitschr.
Pflanzenkr. 19: 473.
Rostrup, E. 1871. I.anilin.iiis-Blad 1871: 57. 71.
. 1884. Meddcl. Bot. Foren. Kobenhavn 1:
1 19.
. 1891. Tids.skr. Landokon. 5 ser. 10: 498.
1892, Ibid. 11 : 326. 1893a. Ibid. 12: 625.
. 1893b. Zeitschr. Pflanzenkr. 3: 146.
. 1891a. Tidsskr. I.andbr. Plant. 1: 131.
. 1891b. Zeitsclir. Pflanzenkr. 4: 285.
. 1891c. Bot. Tidsskr. 19: 201.
. 1896. Tidsskr. Landbr. Plant. 3: 123.
122
PLASMODIOPHORALES
. 1897. Zeitschr. Pflanzeiikr. 7: 158. 1898,
Ibid. 8 : 278.
. 1899. Tidsskr. Landbr. Plant. 6. 1900, Ihid.
7: 13-32. 1901, Ibid. 8: 109. 1902, Ibid. 9: 115.
1903, Ibid. 10: 3(31. 1901, Ibid. 11: 395. 1905,
Ibid. 12: 352. 1906, Ibid. 13: 79.
ENGLAND
Adam, E. 1789. Practical essays on agriculture,
vol. 2.
Anonymous. 1868. Country Gentleman's INIag. I : 40.
'—. 1911. Gard. Chron. 3 ser. 19: 150.
. 1912. Worcester County Exp. Gard., Droit-
wich. Ann. Rept. 1912.
. 1933. Bull. Min. Asric. Fish. 68. 1931, Ibid.
Bull. 79.
Beaumont, A., and L. N. Staniland. 1933. Ninth
Ann. Rept. Seale-Hayne Agric. Coll., Newton
Abbot, Devon. 1932. "1931, Ibid. 1933.
Bennett, F. T. 1939. Ann. Appl. Biol. 26: 837.
Berkeley, M. J. 1856. Gard. Chron. 1856: 500.
Bilfen, R. 1927. Jour. Roy. Agric. Soc. England 187 :
346.
Brown, W. 1935. Jour. Pom. 13: 247. 1937, Ibid.
15: 69.
Buckman. 1851. Jour. Roy. Agric. Soc. England 15:
125.
Caricklee, H. T. W. 1903. Gard. Chron. 3 ser. 31:
163.
Carruthers, N. 1893. Jour. Roy. Agric. Soc. Eng-
land 3 ser. 4:334.
Collinge, W. E. 1911a. Jour. Land Agent's Soc. 10:
1-1.
. 1911b. Gard. Chron. 50: 150.
Cooke, M. C. 1903. Jour. Roy. Hort. Soc. 27: 801.
. 1906. Fungoid pests of cultivated plants.
London.
Cook, W. R. L 1933. Arch. Protistk. 80: 179.
, and E. J. Schwartz. 1930. Phil. Trans. Roy.
Soc. London B 218: 283.
Curtis. J. 1843. Jour. Roy. Agric. Soc. London 4:
100.
Ellis, W. 1742-'44. The modern husbandman, or
the practice of farming. 4 vols. London.
Gilchrist, D. A. 1898. Ann. Rept. Distr. of Grants
Agric. Education. 1897/98: 89; 1898/99: 110;
1899/1900: 96.
. 1905. County of Northumberland Bull. No.
3, New Castle.
1913. County Northumberland Educ.
Comm. Bull. 19: 86.
Hall, A. D. 1904. The soil. London. 2nd ed. 1910.
3rd ed. 1920.
Holmes-Smith, E. 1930. Gard. Chron. 89: 371. 1931,
Ibid. 90: 35.
Marshall. 1795. Rural economy of Norfolk. 2nd ed.
London.
Massee, G. 1895. Proc. Roy. Soc. 57 : 330.
■ . 1896. Rev. Mycol. 1896: 22.
Milburn, T. 1853-55. Jour. Agric. 1853-55: 73.
Ogilvie, L., and B. O. Mulligan. 1934. Fifth Ann.
Rept. Agric. and Hort. Res. Sta. Long Ashton,
Bristol for 1933: 98.
Potter, M. C. 1896a. Gard. Chron. 19: 332.
. 1896b. Jour. Newcastle Farm Club. 1896.
. 1896/97. Nature 55: 33.
Potts, G. 1935. Trans. Brit. Mycol. Soc. 19: 114.
Preston, N. C. 1926. Rept. Advis. Dept. Harper
Adams Agric. Coll. Newport, Salop 1 : 9. 1927,
Ibid. 2: 2. 1929. Ibid. 4: 4. 1930, Ibid. 5: 5.
. 1934. Jour. Min. Agric. 41 : 329.
Preston, W. P. R. 1903. Gard. Chron. 3 ser. 4: 293.
Russel. 1857/59. Jour. Agric. n. s. 1857/59: 529.
Shewell-Cooper, W. E. 1932a. Gard. Chron. 91 : 387.
1932b. Ibid. 92: 83.
Smieton, M. J. 1939. Jour. Pomol. 17: 195. 1931,
Ibid. 90: 35.
Smith, W. G. S. 1883. Ibid. 20: 625.
Smith, E. H. 1930. Ibid. 87: 371.
Sommerville. 1894. Jour. Roy. Agric. Soc. England
3 ser. 5 : 808. 1 895, Ibid'. 6 : 749.
. 1897. Ann. Rept. Distr. Grants Agric. Edu-
cation. 1896/97: 39.
Stephens. 1828/29. Quart. Jour. Agric. 1: 429.
Voelcker, A. 1854. .Tour. Roy. Agric. Soc. England
1 ser. 20: 101.
Voelcker, J. A. 1894. Ibid. 3 ser. 5:318. 1898. Ibid.
3 ser. 8 : 650.
Wakefield, E. M., and W. C. Moore. 1896. Trans.
Brit. Mycol. Soc. 20: 97.
Woodman, R. M.. G. H. Brenchley, and F. Hanley.
1934. Jour. Soc. Chem. Ind. 53, 4: 35.
FINLAND
Anonymous. 1925. Nachrichtenbl. Deut. Pflanzen-
schutzel. 5: 106.
Jamalainen. E. A. 1936. Valt. Naatal. Julk. 85:
1-36.
Karsten, P. A. 1884. Soc. Fauna et Flora Fennica
10.
Rainio, A. J. 1930a. Valt. Naatal. Julk. 23: 275.
IdBOh, Ibid. 23: 306.
FRANCE AND COLONIAL AFRICA
Dufrenoy, J. 1923. Rev. Bot. Appl. 33: 241.
Foex, E.", and E. Marchal. 1931. Ann. Epiph. 17:
1-61.
Gav, A. 1913. Jour. d'Agric. Prat. 77: 816.
G. M. 1920. La Terre Vaud. 1920: 192.
Griffon and Maublanc. 1912. Bull. Soc. Mycol.
France 26: 469.
Mathieu-Sanson. 1897. Rev. Hort. 69: 394.
Maire, R. 1917. Bull. Soc. Hist. Nat. I'Afrique du
. Nord. 8: 134.
, and A. Tison. 1909a. C. R. Acad. Sci. Paris
150: 1768.
, and A. Tison. 1909b. Ann. Mycol. 7: 226.
Mangin, L. 1902. Rev. Hort. 74: 432.
Marchand, E. F. L. 1910. C. R. Acad. Sci. Paris
150: 1348.
Noel, P. 1902. Natur. 1902. no. 374: 226.
CU'll 1U)(>1' 1)1' < Ul( IKEllS
128
Ojitr. A. I8i»7. Uiv. Hort. (ii): L'l.'t.
PJissv. 1". I!)I i. .lour, a Ajjrii-. Pr.it. 78: 87.
Pinoy, K. 1!»0.-). C. H. .'^l>(■. Hiol. .58: 1010.
^ . 1!)07. Ann. Inst. P;istiiir '-'1: ()8(i.
Prillioux. v.. 18!).>. .Maladies des Plantes Agricolis 1.
Paris.
Rcnard. P. 1!)3.'). Vio .\j;rif. rur. 2 1- : 1()7.
Siltciisporaer. 189(i. Rev. Mycol. Frame 18!)(i: 2.*}.
Vandcrvst; H. 1901. Bull. I'.Vgric. U)0i: 535.
Vincont. V. H.. J. Herviaux. and Coic. 1936. C. H.
Acad. Agrie. Franco '22 : 85 1 . 1938. Ibid. 2 i : 83.
Vcrcicr. .1. 1930. Rev. Horti. Paris 102: 86.
Wcsdiiodcr. 1898. Ibid. 70: .>6().
OK H MANY
Anonymous. 191 1. Gartcmvclt 18: 96.
. 1922a. Prov. Sachs. Monatsclir. Obst.-,
Wcin. -u. Gartcnb. 33: 3 k 19221.. Ibid. 33: 50.
. 1922c. Prakt. Ratg. Olist. -u. Gartcnb. 37:
87.
. 1922d. Handdsbl. Deut. Gartenb. 37: 180.
. 1923a. I.andw. Woclienschr. Westfalcn u.
I.ippe 80: 130.
. 1923b. Dcut. Obst. -u. Gcnuiscbau Zcit. 69:
99.
. 192:Jc. Dcut. Erwcrbsg. 1 : 92.
. 1923d. Prakt. Ratg. 1923.
. 1923e. Wcgweis. Obst. -u. Gartenb. 31: 67.
. 1923f. Prakt. Obst. -u. Gartenb. 15, no. 3.
. 1926. Landw. Jahrb. 61, suppl. II: 67.
1931. Ibid. 71. suppl. 1: I-llO.
. 1932. Mitt. Biol. Reichanst. f. Land. -u.
Forstw. 43.
-. 1939. Landw. .I.ihrb. 87: 567.
Appcl. O. 191 1. Mitt. d. ^Lalirens Landw. Landes-
vers. Briim 1911: 39.
. 1928. Handbuch der Pflanzenkr. 2. Berlin.
• . and E. Werth. 1910. Mitt. Kgl. Biol. Anst.
Land. -u. Forstw. 10: 176.
. and O. Schlumberger. 1913. Ibid. 11: 18.
191 1. Ibid. 15: 13.
Arker. H. 1935. Naclir. .Scliiid. Bekanipf. Lever-
kusen 10: 162.
Aue. W. 1913. Erfurt Fuhrer Obst. -u. Gartenb. 13:
315.
Bayer, F. 1922. Ibid. 22: 415.
Becker. J. 1912. Schleswig-Holstein Zeitsclir. Obst.
-u. Gartenb. 1912: 3.
. 1921. Handbuch der (iemiisebau. Berlin.
. 1935. D.iit. Landw. Presse 64: 588.
Behla, R. 1898. Centr.ilbl. Hakt. Parasitk. 21: 829.
. 1899. Zeitsclir. Hyg. 32: 133.
. 1903. Die Pflan/.enparasitare Ursachc des
Krebses und die Krebs])roi)hylaxe. Berlin.
Beyer. T. 1925. Erf. im Obst. -u. Gartenb. 1925: 96.
Blumberg. 1922. Kleintierz. u. Gartenb. 47: 100.
Blunck. H. 1929. (iartenbauw. 1 : 15 1.
Biilincr. K. 1922. Friinkisclicr Kuritr. Niirnbrrg S.
no. 111.
Bottner. 1916. Prakt. Ratg. Obst. -u. Gartcnb. 32:
50.
Bremer, H. 1923. Landw. .lahrb. 59: 227.
. 1921a. Naciiriclitenbl. Deut. Ptlanzcn-
schutzd. I: 16. 1924b. Ibid. 4: 73.
. 1921c. Landw. .lahrb. 59: 673.
. 1928. Erfurt Fiilircr Obst. -u. {;,irt(iii>. 28:
3 11.
Brick, f. 1912
. 1913.
.I.ihili. Hamburg. Wiss. Anst. 30.
.St.it. f. PH.inzcnscli. z. IL-iiiiburg
15: 1.
Bronnle, H. 1926. Obst. -u. (iartenb. 72: 358.
. 1928. Raiffeisenbote, Braunschweig 1928:
103.
Bruck. C. 1912. .lahrb. Hamburg. Wiss. Anst. 30.
. 1913. Stat. PHanzensch. z. Hamburg 15: 1.
Bruck. W. F. 1907. Sanimlung (Jiischen. Leijizig.
Huvkhardt. F. 1915. Flugbl. no. 19. Abt. Pflanzenkr.
Kais. A\ilh. Inst. Landw. Bromberg.
Caspary, R. 1873. Schr. Physik.-Oekon. GeselL
Konigsberg 1873: 109.
. 1877. Gard. Chron. 3: 148.
Dankler. 1919. Der Gartenfreund 1919: 100.
Deutelmoser, E. 1926. Obst. u. Gemiisebau 72: 291.
Eggemeyer. 1920. Prakt. Ratg. Obst. -u. Gartenb.
35 :' 264.
Esmarch, F. 1921. Die Kranke Pflanze 1 : 169. 1925,
Ibid. 2: 207.
Feinberg, L. 1901. Ber. Dcut. Bot. Ges. 19: 533.
. 1902a. Deut. Med. Woclienschr. 28: 43.
. 1902b. Berlin Klin. Wocbenschr. 39: 572.
. 1902c. Das Gewebe und die Ursache der
Krebsgeschwulste. Berlin.
Felsberg, L. 1916. Prakt. Ratg. Ob.st. -u. (iartenb.
31: 172.
Flaclis, F. 1930. Prakt. Bl. Pflanzenbau u. Pflan-
zensch. 8 : 250.
, and M. Kronberger. 1930. Ibid. 8 : 74-80.
Fleishman, C. 1927. Gartenwelt 31 : 781.
F'rank, A. B. 1896. Die Pilzparasitaren Kraiikheiten
der Pflanze 2: 14.
Fruwirth. 1918. Handb. I.andwirtscb. Pflanzensuch.
2.
. 1920. Algemeine Zuchtungslehrc der Land-
wirtssehaflicheii Kultur])flanzen. 5 ed. Berlin.
F. S. 1920. Deut. (iartenbauzcitg. 22: 66.
Gleisberg, W. 1920. Deut. Landw. Presse 1920: 705.
. 1922a. Xaehrbl. Deut. Pflanzenschd. 2: 89.
1922b, Ibid. 3: 10. 1923b. Ibid. 4: 10.
. 1926. Obst. -u. Gemiisebau 72: 28.
(Jretschel, F. 1 9 Hi. Prakt. Ratg. Obst. -u. Gartenb.
31: 172.
Gross-Schlachters. \916. Ibid. 31: 198.
Habernall. 1919. Der Gartenbau 12:6.
Hayunga, J. 1909. Mitt. Deut. Landw. Gesell. 1909:
" 677.
. 191 I. Pr.ikt. Ratg. Obst. -u. Gartenbau 11 :
100.
. 1912. Der Handelsgart. 14: 173.
. 1919. Mitt. Deut. Landw. GeselL 1919: 52.
Hcllmann. A. 1926. Erfurt Fiihrer Obst. -u. Gartenb.
27: 91.
Herpers, H. 1913. (iartcnwclt 17: 674.
. 1923. Prakt. Ratg. Obst. -u. Gartenb., Beil.
Prakt. Landw. no. 2.
124
PLASMODIOPHORALES
. 1924. Erfurt Fiihrer Obst. -u. Gartenb. 25:
49. 1925a, Ibid. 50: 39.
-. 1925b. Gartenwelt 29: 706.
Hertel. F. 1926. Obst. -u. Gemiisebau. 72: 67.
Heyder. 1911. Oldenburgisch. Landw.-Blatt 1911:
65.
Hiltner, L. 1908. Ber. Tatigkeit Kgl. Agric. -Bot.
Anst. Miindien in Jahre 1907. 1908: 98-99.
, and G. Korff. 1916. Prakt. Bl. Pflanzenb. ii.
Pflanzensch. 1916. h. 3:25.
Hofferichter, K. 1926. Gartenflora 75: 262.
Hoffman, W. 1932. Ratschl. f. Hans, Garten, Feld.
7: 162.
Hollenbach, O. 1911. Gartenwelt 15: 8.
Hollrung. 1923. Die Mittel zur Bekampfung der
Pflanzenkrankheiten. Berlin.
Honig, F. 1931. Gartenbauwiss 5: 116.
. 1932. Nachr. iiber Schadlingsbekampf. 7:
22.
Honigmann. 1926. Pflanzenbau. Halbmschr. f. Saat-
wesen Anbau u Pflege d. Kiilturpflanz. 2: 290.
Hostermann, G. 1909. Ber. Kgl. Gartenlehranst.
Dahlem b. Steglitz 1908/9: 124. 1921, Ibid.
1920/21 : 100.
■ , and M. Noack. 1923. I.elirbuch der Pilz-
parasitaren Pflanzenkrankheiten. Berlin.
Hsf. 1914. Mitt. Deut. Landw. Gesell. 29: 12.
Hurrle, A. 1916. Prakt. Ratg. Obst. -u. Gartenbau
31: 69.
Kalchschmid, W. 1941. Deut. Landw. Presse 68:
185.
Kappen. 1922. Mitt. Deut. Landw. Gesell. 37: 660.
Kellerman. 1903. Prakt. Bl. Pflanzenb, u. Pflan-
zensch. 9: 103.
Kimppel, K. H. 1922a. Prov. Sachs. Monatachr.
Obst. -Wein-Gartenb. 23: 78. 1922b, Ibid. 23:
172.
Kindshoven, J. 1924. Mitt. Deut. Landw. Gesell.
39: 259. 1928, Ibid. 43: 522.
Kirschner, L. 1906. Die Krankheiten und Bes-
chadigungen unserer landwirtschafiichlen Kul-
turpfianzen p. 371. Stuttgart.
. 1927. Atlas d. Krankh. u. Beschad. Landw.
Kulturpf. 2nd ed. Stuttgart.
Klebahn. H. 1912. Grunziige der algemeinen Phyto-
pathologie. Berlin.
Klemm, M. 1938. Deut. Landw. Presse 65: 239.
Knorr, L. 1920. Prakt. Ratg. Obst. -u. Gartenb. 35:
344.
K. M. 1919. Erfurt Fiihrer Obst. -u. Gartenbau. 21.
Koblischek. 1929. Mitt. Deut. Landw. Gesell. 1929:
250.
Kock, G. 1911. Centralbl. Landw. 1911: 45.
Kohne. 1928. Nachr. iiber. Schadlungsbekampf. 3:
61.
Korff, G.. and K. Boning. 1927. Prakt. Bl. Pflan-
zenb u. Pflanzensch 5: 192.
Kreuzpointer, J. 1922a. Wegweiss. Obst. -u. Gar-
tenb. 30: 131.
. 1922b. Deut. Gemusebau-Zeit. 10: 263.
. 1923. Lehrm. Gart. Kleintierk. 21 : 68.
. 1929. Prakt. Bl. Pflanzenb. u. Pflanzensch
7:96.
1931. Ernahrungder Pflanze 27: 172.
Kriiger, R. 1920. Erfurter F'iihrer Obst. -u. Garten-
bau 21: 112. 1927. Ibid. 28: 31.
Kiihn, J. 1858. Die Krankheit der Kulturgewasche,
pp. 252, 253.
Kupke, W. 1933. Gartenwelt 37: 182.
. 1935. Nachr. Schiidl. Bekamp. 10: 46.
Kiister, E. 1911. Die Gallen der Pflanzen. Leipzig,
Langenbeck. 1904. Deut. Landw. Presse 1904, no.
68.
Laubert, R. 1905. Prakt. Bl. Pflanzenb. u. Pflan-
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HOLLAND
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Montieth, J. 1924. Jour. Agr. Res. 28: 549.
Murphy, P. A. 1927. Jour. Dept. Lands and Agr.
27: 12.
Nance, N. W. 1941. PI. Dis. Rept. Suppl. 128.
Owen, C. E. 1928. Principles Plant Pathology. New
York.
Palmer, R. G. 1941. Phytopath. 31: 18.
Pryor, D. E. 1940. Jour. Agr. Res. 61 : 149.
Reed, H. S. 1911a. Phytopath. 1: 159.
. 1911b. Virginia Agr. Exp. Sta. Bull. 191.
Russel, H. L., and F. B. Morrison. 1922. Wisconsin
Agr. Exp. Sta. Bull. 339.
Schwarze, C. A. 1917. New Jersey Exp. Sta. Bull.
313.
Slingerhand, M. V. 1894. New York Agr. Exp. Sta.
Entom. Div. Bull. 74: 481.
Smith, W. G. 1894. Diseases of field and garden
crops. Pp. 94-104.
Smith, R. E., and E. H. Smith. 1911. California Agr.
Exp. Sta. Bull. 218.
Stevens, F. L. 1925. Plant disease fungi. New York.
Stewart, F. C. 1895. New York Agr. Exp. Sta. Ann.
Rept. 14: 519.
Tabenhaus, J. J. 1920. Diseases of greenhouse crops
and their control. New York.
Tillinghast, L F. 1879. Cult, and Country Gentle-
man 44 : 807.
Tompkins, C. M., and P. A. Ark. 1939. PI. Dis. Rept.
23 : 4.
Vaughan, R. E. 1924. Ibid. 34: 192.
, and F. L. Wellman. 1926. Wisconsin Agr.
Exp. Sta. Circ. 200.
Walker, J. C. 1934. U. S. Dept. Agr. Farm Bull.
1439.
. 1935. Jour. Agr. Res. 51 : 183.
. 1936. Phytopath. 26: 112.
. 1937. Rept. Wise. Agr. Exp. Sta. Bull. 438.
. 1939. Jour. Agr. Res. 59: 815.
. 1941. Botanical Rev. 7: 458.
<i.rii HOOT or ( mciFKHS
I'ii)
Walker. J. C. aiul H. H. I.arscn. 1!);U. Wisconsin
Aftr. Kxp. Sta. Hull. I-28.
. K. 1*. Link, and .^. Morrll. l!i:»7. Wise. .Xgr.
Exp. .>^ta. Hull. t.-C).
Willman. 1'. I,. liL'tO. f. .S. Dipt. .Vijr. T.cli. Hull.
7S1.
Wilson. J. D. 193t. Ohio .Xsir. Exp. .Sta. Hiniontlily
Hull. 19: 58.
Davies. 1). W., M. (irittitli. and G. Evans. 192S.
Welsh .lour. .\gr. !•: 293.
Preston. N. C. 1928. //>»/. i: 280.
. 1931. Jour. Min. Agr. 38: 272.
Whitehead, T. 1922. Ihid. 29: 362.
. 192.5. Welsh .lour. .Vgr. 1: 17(i. 193."). IbitL
11:228. 1936. //'»/. 12: 183. 19 K), //)/(/. 16:99.
POWDERY SCAB OF POTATOES
Powdery scab of potatoes is now almost world
wide in distribution. Lagerlieim's discovery of its
presence in Ecuador suggests that it may be endemic
to South .\merica. since that continent is generally
regarded as the native home of the potato. In that
event powdery scab may be of greater antiquity
than is generally supposed. It has doubtless attained
its extensive distribution by the shipment and im-
portation of infected tubers. From South America
it may have been imjiorted to Europe and then back
to North .\merica and other parts of the world. Pow-
dery scab was first re))orted from Germany by Wall-
roth and Martius in 18 12. but it had doubtless been
known by potato growers for many years before that
time. Shortly afterwards, it was described from Eng-
land by Berkeley {' i6) and later from Wales, Scot-
land. Norway and Ireland. The first record of its
occurrence in North America was made in 1913 on
potatoes in Quebec, and in the same year it was also
found in Maine and other states. This disease is
known by a variety of names throughout the world.
In (iermany it is described as Knollenbrand, Kartof-
felgrind. Kartoffelgnatz. .Schorfkrankheit. and Kar-
toffclschorf. In England, .Scotland, Wales, Ireland
and the U. S. A., it goes by the names of potato
canker, corky end, corky scab, spongy scab. Spoiif/o-
gpora scab, and jiotato tumor, although powdery
scab is the term most commonly used. The names,
potato canker and tumor are employed when the
lesions and tumors are unusually deep and conspicu-
ous.
As a destructive disease of potatoes, powdery
scab is of secondary importance compared with late
blight, virus, Fuxarium wilt and rot, and common
scab. In relatively dry and warm regions the dam-
age caused may be so slight as to go unnoticed, while
in other places with high )irecipitation and low tem-
peratures the losses may lie quite serious. ))articu-
larlv if the disease is of the cankerous type and is
followed by powdery scab dry rot in storage. In
England, VVales (Pethybridge, '24), New Zealand
(Anony., '27), Peru (Abbott, '31), and Russia
(I)orojkin, '36), destruction of 30 to 50 per cent
.•nul more of the cro)) h.is been rejiorted in years of
he.ivy rainfall .-iikI low teui|)eraturc. Likewise, Mel-
luis. (•/ al., found that 30 to 73 ))er cent of infected
tubers may be destroyed by dry rot in storage or
rendered useless for table or ))lanting. Such losses,
however, appear to be exceptional, but the disease is
nevertheless of sufficient importance to warrant the
establishment of strict (pi.-irantine .md tuber inspec-
tion and certification laws by most tountries througll-
out the world.
Predisposing Factors
The occurrence of powdery scab and incidence
of infection are dei)endent on climatic conditions.
Heavy rainfall, fairly low tenii)eratures, damp,
poorly-drained and water-logged soils favor infec-
tion and development of the disease. Melhus, et al.,
observed that periods of rainfall, followed by cool,
damp, cloudy weather during the growing season are
highly essential to the development of the disease,
and these observations were subsequently confirmed
by Ramsey ('18) from greenhouse experiments. He
found 83 per cent infection in pots of potatoes grown
at 57°-60° F. under moist conditions, while no in-
fection occurred in pots at 76°-80° E. and in rela-
tively dry soil. \\\\A ('29), on the other hand, found
no clear correlation between incidence of scab and
the prevalence of any particular climatic conditions
in Switzerland. Koltermann's ('31), Phillips' ('32),
and Naumov's ('36) observations on the disease in
Germany and Russia confirm those of Melhus. Ram-
sey, and others in America. Naumov found powdery
scab to be more prevalent in soils with 60-90 per
cent moisture content and with pH values from (■.7
to 5.9 than in soils with 40 jier cent moisture and
high pH values.
That unfavorable climate is an etieetive barrier
to the spread of the disease is evident from experi-
ments conducted by Melhus, et al., which involved
])l.uiting of heavily infected tubers in fifteen differ-
ent regions along the Atlantic Coast from Massa-
chusetts to Florida. All of these plantings yielded
clean crops. These results are sup])orted by the ob-
servations of She])herd ('35), Nattras ('38), and
Littlejohn ('39) that heavily infected imported
tubers planted in Mauritius and Cyprus give
healthy crojis and that iS'. suhicrranea does not re-
main viable under prevailing climatic conditions on
those islands.
Hydrogen ion concentration ap])arently does not
influence the incidence of infection, since .S'. nuhtcr-
ranea appears to tolerate both .alkaline and acid re-
actions. Wild. Phillii)s, and Naumov found that in-
fection mav readily occur in soils with pH values
ranging from 1.7 to 7.6. Furthermore, the incidence
of infection is not affected by the carbonate or
hexosan content of the soil, according to \\'ild.
The ])hysieal character of the soil, however, is an
imi)ortant factor. A close correlation between cer-
130
PI/ASMODIOPHORALES
tain soil types and the degree of infection was ob-
served bj' Melhus, et al., in Maine, and they were
accordingly able to predict the extent of develop-
ment of the disease from the type of soil and its
drainage. Wherever the Washburn silt-loam type of
soil occurred infection was unusually Iieavy. Wild,
likewise found that powdery scab flourishes in
Switzerland in soils with a large pore space, high
humus and methylpentosan content, coarse texture,
and high water-holding capacity.
Symptoms
Powdery scab may manifest itself as shallow,
scabby lesions or deep eroded cankers on the tubers,
and galls or warts on the roots and stems. These
phases of the disease may be followed by powdery
scab dry rot after the tubers have been harvested
and stored. The first evidence of infection on the
tubers is the appearance of faint brownish-purple
spots of pinhead size, which doubtless indicate the
point of entry of the parasite. Each spot is usually
surrounded by a circular translucent, 1 to 2 mm.,
area which apparently marks the distance to which
the Plasmodium has spread beneatli the epidermis,
according to Kunkel ('15). In the course of 6 to 8
days the areas may increase to l/o cm. in diameter,
lose their brownish color, and protrude as a meta-
plastic, jelly-like mass of i)roliferating host cells and
fungus spores. According to Home ('12) these pro-
trusions may be so prominent that they look like
cushions or wart-like excrescences. The diseased
areas gradually die, leaving shallow, crateriform
depressions filled with a fine powdery mass of spore
balls (PI. 10, fig. 1), These are the so-called pow-
dery scab symptoms of the disease which may be
readily mistaken for those of the common scab.
Further development of the disease on the tubers
depends to a great extent on the relative amount of
moisture in the soil or in the storage bins after the
potatoes have been harvested. If the infected tubers
are growing in fairly dry soil, wound cork is rapidly
formed under and around the lesions, so that the
diseased areas are delimited. With abundant mois-
ture and in poorly drained soil, however, the para-
site may continue its depredations. As a result the
lesions become deeper, larger and sometimes coalesce
to form extensive eroded cavities or cankers as much
as 1/2 inch in depth. This is one of the most severe
types of the disease and is referred to as the canker-
ous stage (fig. 2). This type appears to be common
in Ireland, England, and Europe, but is not very
prevalent in Maine and Canada. Melhus, et al., at-
tributed the latter to the shorter growing period of
tlie potato in the northern regions of North America.
In addition to causing shallow lesions and deep
cankers S. subterranea may also lead to the forma-
tion of tuberous outgrowths and extensive warts on
the tubers with the result that the latter are often
misshapen and deformed, according to Home (12).
These outgrowths are apparently formed in tlie
same manner as the galls on the roots and stems,
although Home did not describe their development.
They ma3' be more or less uniformly infected and
covered with scabs and bear a superficial resem-
blance to the tumors caused by Si/nchi/trium endo-
bioficum.
The galls on the roots and stolons of potatoes and
other related species vary in size from minute tu-
bercles to balls as large as garden peas (fig. 3).
They usually precede tuber infection and may be
present in abundance before there is any indication
of lesions on the tubers, but their presence does not
appear to have any great injurious effect on the
growth of the host. These galls are simple in struc-
ture and consist primarily of enlarged and fre-
quently divided undifferentiated cells, so that they
are typically kataplasmic in structure. The causal
organism is confined largely to the phloem and meri-
stematic tissues, as in the case of club root of cruci-
fers. Amoebae may be found occasionally in the
xylem, but they do not occur in great numbers or
cause distortion of the vessels. The presence of the
parasite in the phloem stimulates the cells to en-
large and divide, and this hyperplastic growth often
puslies the xylem out of its normal position.
Powdery scab dry rot usually sets in after in-
fected tubers have been in storage for some time,
and in some cases is abetted by numerous other
fungi. This rot was first described by Melhus ('l-i)
in North America, but it has been found subse-
quently on ])otatoes collected in Ireland, Holland,
Chile, and other countries. It is accelerated by poor
storage conditions, but even in good storage as much
as 30 to 73 per cent of the tubers may be partly or
wholly decayed and rendered useless for seed or
table use, according to INIelhus, et al. Although
tubers may be often totally decayed, powdery scab
dry rot is usually less severe and occurs in localized
spots, 1 to 10 cms. in diameter. These areas may be
only slight depressions in the superficial layers or
extend to the center of tlie tubers. The extent of in-
jury, however, depends to some extent on the time
of harvesting, degree of infection, storage condi-
tions, and the stage of development of the parasite
when the tubers are stored. Dry rot may accordingly
exiiibit various types of symptoms. Desiccation or
loss of water from the open lesions is a common
occurrence when tubers are placed in warm dry stor-
age and results in discoloration of the affected areas,
wrinkling, shrinkage, and marked loss in weight.
However, this type of dry rot is retarded as storage
temperatures drop with the advent of the winter sea-
son. Another type of dry rot is caused by secondary
infection and invasion of tissue around the old pus-
tules by the jjlasmodium of S. subterranea. If mois-
ture and temperature are favorable, the resting
spores in old lesions may germinate and give rise to
Plasmodia which invade and kill the surrounding
healthy cells. The plasmodium usually feeds on the
tissue immediately beneath the epidermis, but occa-
sionally it may be found at depths of 6 to 8 mm. in
the tuber. In such extreme cases of penetration the
I>()\V1)KHY SCAH <)l' I'OTATOKS
i:n
svniptonis ])ro(liu'i'd may resemble tliosi- of tlio can-
ktTous stai;c in the (iild.
Till- open K'sions may also bo invaded liy womul
parasites of tlu' •ti-nera Phonta, Fusarium, lihizoc-
tonia, Papulospora, etc.. and tliis initiates the most
destnietive type of powdery seal) dry rot. Phomn
tiihrrosa, aeeordinir to Melluis, <-t al., is commonly
associated witii the early stages of rot and prodnees
brownish to gray lesions in the bottom of the old
pustules. .\s these lesions progress they become more
sunken, darker and often hard and bony. .\t later
stages the lesions may vary from 2 to 5 cms. in diam-
eter and extend to a depth of 2 to 1- cms.
.\t this ))oint it may be noted thatShajJOvalov ('23)
contended that the skin-spot disease of tubers, which
had been attributed to several causal organisms, in-
cluding Ooxpora piistiilans, is an early stage of ))0W-
derv scab, but this was innnediately refuted by Mil-
lard and Burr ('23). They reported that the former
disease is caused solely by O. ptistulaii.s and is in no
way related to jjowdery scab. Powdery scab is co-
extensive with late blight, caused by Phi/tophlhora
infrsians, and both diseases are favored by the same
climatic conditions. The latter disease may often be
greatly increased by tuber and root infection by S.
suhtrrranea, according to Beregovoy ('39).
Cellular Relations Between Host and
Pathogen
Sponc/ospora suhtt-rranea has a marked efifect on
the host cells. Young infected cells as well as adja-
cent healthy ones are stimulated to divide by the
presence of the parasite. The repeated division of
healthy cells results in the formation of a new peri-
derm around the regions of infection. When this
periderm is invaded further cell divisions follow,
which lead to the development of a second wound
periderm, according to Wild ('29). Kunkel found a
marked difference in reaction between the yoimg
growing cells of tubers and mature cells in the tis-
sues around the old lesions. The former are not
killed by invasion of the parasite but are stimulated
to expand and divide. The latter, on the other hand,
are quickly killed, and their contents are partly or
wholly consumed. The increase in cell multijilication
noted above is usually accomjjanied by <ell enlarge-
ment. .\ceording to Kunkel, the latter )>rocess may
begin while the plasmodium is still in the intercellu-
lar spaces and before it has entered the cells (fig.
17). This reaction suggests that the plasmodium may
secrete a stimulating substance which precedes its
invasion of the cells.
Infected cells may become .5 to 10 times their nor-
mal size, but enlargement is not equal in all direc-
tions. The expanding cells generally elongate out-
ward towards the surface of the tuber, which finally
results in the lifting and ru))turing of the e])idtrniis
and the formation of cushion-like excrescences. In
galls on the roots of Solatium 7carce7cicsii and L.
esculentum the infected cells occur in groujjs (fig.
1() ). according to Melhus. ct al., like the "Kranheits-
herde " described by Nawascliin for club root of
erueifers. These grou|)s origin.ite by continual divi-
sion of one or more infected cells whereby the .-imoe-
bae and young ))lasnu)dia are jiassively distributed.
The nuclei of infected cells may divide mitotieally
.•md i)ossibly amitotically also, as in the case of Tri-
(flochini.i cells ))ar;isiti/ed by Tt'tranti/jca Triylo-
chhiis. When normal mitosis occurs, a cell ))late is
formed between the d;iughter inu-lei (fig. It), but
in c.ises of amitosis the giant cells become multinucle-
ate and l;iter dividi- into numerous smaller cells, ac-
cording to Kunkel. However, it is not obvious from
his description whether these latter divisions occur
by cell plate formation or cleavage after which walls
are laid down. The host nucleus may be enveloped by
or embedded in the ))l;ismodiuni and become greatly
enlarged, lobed, and distorted (fig. 18, 19. 26). Sev-
er.al nucleoli may frequently develoj). while the chro-
matin strands become abnormal in appearance or
disappear entirely. The nuclei are usually destroyed
before the parasite is mature, but in exceptional
cases it may remain intact until after the spore balls
have been formed and lie between them.
The presence of S. subterranea ajjparently also
stimulates an undue production of starch in and
around infected cells. At least the starch ap{)ears to
be more abundant in the regions of infection in the
potato and tomato. In S. u-arscexclczil, however,
Melhus, et al., found that numerous infected cells
may be found which are totally lacking in starch.
The starch grains usually do not disap)jear entirely
until after the spore balls are mature, but it is not
certain that they are consumed directly by the jiara-
site. Osborn claimed that the i)lasmodium feeds on
starch, but Melhus, ei al., pointed out that if this
were true an abundant supply would not always be
present. Kunkel also reported that the starch grains
are only slightly changed by the parasite and may
remain after the cytojjlasm and nuclei have been
destroyed. Other workers, however, have claimed
that the su])])ly of starch diminishes as the parasite
matures, ^^'ild found that starch disappears below
the diseased areas, being utilized in the process of
cell division, or for nutrition of the parasite. It may
also be noted here that infection with S. suhterranea
reduces the ])H value of tubers from .5.70 to l'.3.5,
according to Robertson and Smith ('31).
The physical relations between the protoplasts of
host and pathogen a))))ears to be close and intimate
in light of Kimkel's .and Melhus' observations. No
antagonism is exhibited, and the two blend into each
other in such a way that it is often imi)ossible to de-
termine clearly where one ends and the other begins.
In fixed and stained preiiarations. on the other hand,
the parasite st.iins more intensely with Congo red
and Orange (i th.an the host |)rotopl;isni (Massee .■md
Kunkel). In the initial develo))mental stages there
seems to be a marked attraction between the host
nucleus and the amoebae, according to Melhus, et al.
As is shown in figures 1.5 and 1(5 the latter may be
crowded around the nucleus, which suggests that the
132
PLASMODIOPHORALES
nutritional conditions are more favorable in that re-
region of the cell.
The walls of the infected host cells are also mark-
edly changed by the parasite. As the pseudopods of
the Plasmodium push down between the cells, the
walls become swollen, gelatinous and wavy. These
walls have a greater affinity for Orange G than those
of healthy cells, according to Kunkel's and Wild's
observations, which indicates that they have under-
gone a change in composition. The middle lamella is
also usually dissolved by the action of the Plasmo-
dium.
Control
The shipment and importation of infected tubers
appear to be the primary means of dispersal of pow-
dery scab from one region or country to another.
Most countries have accordingly enacted legislation
against the importation of diseased potatoes and es-
tablislied inspection and certification bureaus within
their boundaries to insure planting of healthy tubers.
Locally, the disease may be transferred from one
field to another by fertilizing with contaminated ma-
nure, by farm implements, contaminated sacks, and
soil on the shoes of laborers. Sanitary practices must
accordingly guard against dispersal by such means.
Since fungus spores will survive passage through
the digestive tract, infected tubers and parings
should be boiled or sterilized before feeding to hogs
and other animals to avoid contaminated manure.
Other sanitary measures involve selection of disease-
free tubers for planting and the avoidance of con-
taminated land.
Inasmuch as the spores of S. suhterranea may re-
main viable in the soil for 3 to 5 years or longer
(Melhus, et al.). crop rotation, fallowing, or pastur-
ing the land are essential in regions where the dis-
ease is abundant and destructive. In such regions the
potato crop may be largely destroyed if rotation is
neglected (Petlivbridge, '26). Dorojkin ('36) thus
advocated compulsory crop rotation of no less than
3 years in Russia, but it is apparent that a longer
period may be necessary to starve out the parasite.
The rotation period obviously depends to some ex-
tent on climatic conditions, and the character of the
soil. In Scotland, for instance, a rotation of 6 to 10
years or longer lias been recommended for loamy soil
in regions where high rainfall and low tempartures
normally occur during the potato growing season.
Eradication of wild hosts is of doubtful value at
present because S. suhierranea has a comparatively
limited host range and very little is known about its
occurrence outside of the potato. Since the fungus
develops on tubers only after they are partially ma-
ture early harvesting may sometimes be effectual in
avoiding the disease, provided infection does not
occur early in the season. However, it is not prac-
ticable because no marked above-ground symptoms
of infection occur, which would indicate whether or
not the tubers are infected.
Liming the soil as practiced in the control of club
root of crucifers stimulates instead of inhibiting
the development of powdery scab. Massee ('10, '15)
recommended dressing the land with quicklime in
the spring when the spores germinate in the soil, but
Pethybridge, Home ('12), and others found that
lime increases the amount of diseased tubers. Mel-
hus, et al., likewise noted that lime at the rate of
3,000 lbs. per acre increased infection 13.2 per cent
in one case but reduced it in another. These varia-
tions, however, were probably due to differences in
soil types in the two test blocks. Phillips ('32) ad-
vised the application of lime to loosen the soil and
make it more porous and thereby increase drainage.
Since damp, water-logged soil favors the develop-
ment of the parasite proper drainage is essential.
Other control measures involve seed tuber disin-
fection before planting, soil disinfection with chemi-
cals and fungicides, and the use of resistant potato
varieties. As to tuber sterilization various disinfec-
tants have been advocated and used. Johnson ('08)
found that soaking infected tubers for 18 to 2i hours
in 2 per cent Bordeaux mixture, 1 Vo hours in corro-
sive sublimate, or 2 hours in a weak formalin solu-
tion is effective in killing the spores of S. suhierra-
nea. Subsequent workers have confirmed these re-
sults to some degree. Pethybridge ('13) in particu-
lar observed that seed tubers treated with weak solu-
tions of formalin, copper sulphate. Burgundy mix-
ture, or rolled in flowers of sulphur checked the dis-
ease to a marked degree. Tubers soaked in 1 per cent
copper sulphate for 3 hours yielded no diseased off-
spring, while those rolled in sulphur gave only 1.03
per cent infection. Melhus, et al., however, found
that tuber treatment with 2 pts. of formalin per 30
gals, water at -16 to 50° C. for 5 minutes, or mer-
curic chloride, 1 ozs. to 15 gals, water at -i-l to -IS C.
for 5 minutes, gave better results than the usual
long cold treatments with either of these substances.
Rolling wet tubers in sulphur or soaking them in 5
per cent atomic sulphur for fl/o hours was less effec-
tive than treatment with formaldehyde and mercuric
chloride. While these disinfectants reduce infection
considerably, the results obtained are not to be re-
garded as absolute, according to Melhus, et al., since
other factors such as variations in soil moisture and
texture, drainage, and temperature have a marked
effect on the results. Later workers, including Ab-
bott ('28), Dorojkin ('31, '36) and Rovdo ('36),
iiave reported similar beneficial results from the use
of corrosive sublimate, formalin, and mercuric chlo-
ride on infected seed tubers. Dorojkin found that
soaking tubers 20 to 30 minutes in a .2 per cent solu-
tion of meranin, a liquid organic mercury prepara-
tion containing less mercury than mercuric chloride,
gave excellent control in Russia.
Disinfection of contaminated fields by the appli-
cation of sulphur at the rate of 300 to 900 lbs. per
acre has been reported by Melhus, et al.. Cotton
('22), Abbott, and Boning and Wallner ('38) to re-
duce the incidence of infection considerably. Melhus
and his collaborators reported that better results
IMnVDKUY SCAH OF I'OTATOKS
188
may bo si-rurcd with liroadi'ast sul|ilmr than when it
is applied in drills. Cotton (''2'2) loiind tiiat tin- ad-
dition of (iOO lbs. per acre redueed the iiieideiiee of
infeetion from St to 7.5 per eent, while Hoiiiiif; and
Wallner ('3S) reported that the incorporation of
sulphur .it the rate of K)0 klg. per heet.ire with t)rdi-
n.-irv fertilizers diniiuished infeetion of the Parnas-
sia \;iriety from '2 ^ to 17 per eent.
The .tiiditioii of eertain fertilizer ingredients to
the soil has also been reported to reduee infeetion.
Petliybridjie noted very early that the applieatiou
of superpiiosphate and sulphate of potash reduced
the number of diseased tubers, and later tliis asjiect
of control was investigated more thoroughly by Mel-
hus and his collaborators in M;iine. Each of fifteen
plots of soil of v.irying composition and texture were
fertilized seiiaratcly with sodium nitrate, old horse
manure, new horse manure, ijliosjihorie .icid. ammo-
nium suliihate and phosphoric aeid, ammonium sul-
phate and jiotassium chloride respeeti\ ely and tested
against 7 controls treated with commercial fertilizers
at the rate of 1..500 lbs. per acre and 7 untreated con-
trols. These plots were then seeded with Green
Mountain variety tubers which had been disinfected
with the usual strength of mercuric chloride. All of
the fertilizer ingredients tested alone reduced infec-
tion 5 to 12 per cent below that of the controls. Am-
monium sulphate and acid phosphate gave nearly the
same yields as the fertilized checks and diminished
infection 7.6 per cent, while potassium chloride
yielded the least infection, which may have been
partly due to the jirolonged growing season in this
case.
So far no completely resistant and immune potato
varieties have been found or developed. Although re-
ports of partial to complete varietal resistance have
often been made, it is not certain whether the re-
ported resistance is due to inherent immunity or to
the fact that the jilants escaped infection. Soil com-
position and texture as well as the number of spores
present doubtless vary considerably, and it is not
improbable that these factors are often the cause of
variations in infeetion. This is probably true in the
ease of Melhus' experiments conducted in 1915 in
Maine. Melhus and his co-workers found four named
varieties (Ei.dohado, Farys. Wohltmann, and
Senator) and seven seedlings the tubers of which
were free of the disease, while otliers showed very
slight to severe infection. However, inasmuch as the
control variety, Grkkx Mountain, also showed wide
fluctuations in degree of infection, Melhus, et al.,
concluded that the variations in varietal response
were partly due to the fact that some of the varieties
cscajjed infection. They further believed that the na-
ture of varietal resistance jirobably rcl.ites to the
abilitv to form cork cambium. Gomolyako ('30) re-
ported that SviTKZ, Dkodora, I'ihoi.a, Kihia. Pau-
NASSiA, Gavroneck and Ji'bel were least affected
bv powdery .scab in Russia, but he was not eertain
that tliev are consistently resistant. Naumov like-
wise rel)orted these varieties to be parti/illy resist-
ant, while onlv one, Rose of Milet, remained free
of infection in l!).'t.'). Dorojkin ('Jfi) found no com-
pletely rcsist.ant conunerci.d varieties but regarded
.IiHF.i,, CoHHLKH. .•uiil Pahnassia jis wcaklv Suscep-
tible. However, eight varieties of Solaniiin from
South America jirovcd to be innnune, as well as nine
hybrids develo])ed by the Pan Soviet Institute of
Pl.int Breeding. Herogovoy ('39) reported that none
of tlie varieties tested at the Kief (luar.-iutine labo-
ratory were comjiletely resistant, although the de-
gree of infection w;is (luite low. The variety \\'ohlt-
ma.vn showed the highest degree of resistance and
was recommended for sub-sandy soil.
It is obvious from these reports that varieties such
as Parnassia, Wohltmann, Svitez, Juhel, Pirola,
and Cobbler possess some degree of resistance to
])owdery scab. Tlie use of these varieties in connec-
tion with other control measures such as ))roper soil
drainage, tuber sterilization, soil disinfection, etc.,
will doubtless do much to alleviate infection with
powdery scab where it is particularly abundant and
destructive.
Geographical Distribution of Powdery Scab
and Bibliography of I^iteraturc
.Vnony. 1923. Bull. Agric. Algerie-Maroc. 2nd ser.
29 : 69.
Cujoutantis, A. 1921. Rev. Path. Veget. Entom.
Agric. 1 I : 60.
ARMENIA
Rovdo, A. S. 1936. White Russ. Acad. Sci. Inst.
Biol. Sci. Minsk 1936: 39.
AUSTRALIA
Anony. 1927. -Jour. Dept. Agric. Victoria 25: 613.
1936, Ibid. 3t: 161. 1938, Ibid. 36: 301.
Bald, J. G. 1911. Painphl. Coun. Sci. Ind. Res. Aus-
tralia 106.
Darnell-Smith, Cj. P. Ann. Rept. Dept. Agric. New
South Wales. 1920-21: 27.
Norwood. R. B. 1933. Queensland Agric. .lour. 40:
382.
Noble, R. J. 1921. Agric. Gaz. New South Wales
35 : 883.
Hccke. L. 1923. Wiener Landw. Zeit. 73: 273. 281.
Janchen, E. 1921. Oesterr. Zeitschr. f. Kartotfelbau
1: 3.
Kock, G. 1922. Wiener I.andw. Zeit. 72: 82.
. 1927. Oesterr. Zeitschr. f. Kartoffclbau
1927, no. 3.
Wahl, B. 192K Zeitschr. Landw. Versuehsw. Deut-
Oesterr. 1921: 1-8.
CANADA AND .MARITIME PROVINCES
Dickson. B. T. 1922. 1 Ith Ann. Rept. Quebec. Soc.
Protect. Plants, p. 67.
134
PLASMODIOPHORALES
Eastham, J. W. 1914. Canada Agric. Exp. Farms
Circ. no. 5: 7.
. 1922. 16th Ann. Kept. Dept. Agric. British
Cohimbia 1921: 64: 69.
Gorham, R. P. 1914. Dept. Agric. New Brunswick
Hort.Div. Leaf. III.
Gussow, H. T. 1913. Phytopath. 3: 18.
Henry. A. W. 1934. Circ. Coll. Agric. Alberta, no. 15.
Hurst, R. R. 1926. Rept. Dominion Botanist, Div.
Bot. Canada Dept. Agric. 1925: 20. 1929, 76;W.
1928: 165.
Ledingham, G. A. 1934. Nature 133: 534. 1935,
Ibid. 135: 394.
Partridge, G. 1923. Agric. Gaz. Canada 10: 121.
Sanford, G. B. 1924. Alberta Agric. Coll. Bull. no. 5.
Tice, C. 1922. Scient. Agric. Canada 2: 249.
Tucker, J. 1921. Canada Dept. Agr. Pamph. no.
129. 1927, Ibid. Pamph. no. 84.
COLOMBIA
Franco, R. M. 1938. Agric. Bogota 10: 344.
CZECHOSLOVAKIA
Anony. 1930. Ochr. Rost. 10:1.
Blattnv, C. 1935. Rec. Inst. Rech. Agron. Rep.
tchecosl. 137:21.
DENMARK AND FAROE ISLANDS
Ferdinandsen, C. 1923. Tidsskr. f. Land0konomi.
Gram, E., and S. Rostrup. 1925. Tidsskr. f. Plan-
teavl. 31: 353.
, and M. Thomsen. 1927. Ibid. 33: 84.
Rostrup, E. 1905. Ibid. 12: 352.
Weber, A. 1922. Tomatsvgdomme. Copenhagen.
Winge, O. 1913. Ark. f.'fiot. 12, no. 9: 26.
ENGLAND AND WALES
Anony. 1909. Jour. Bd. Agric. London 15: 749.
Berkeley, M. J. 1846. Jour. Hort. Soc. London 1 : 33.
" 1 850. Ann. Mag. Nat. Hist. 2nd Ser. 5 : 464.
Cotton, A. D. 1922. Min. Agric. Miscl. Pub. 38.
Cooke, M. C. 1903. Jour. Roy. Hort. Soc. 27: 801.
Cook, W. R. I. 1933a. Arch. Protistenk. 80: 179.
— . 1933b. Glamorgan County Hist. Nat. Hist.
1: 213.
Home, A. S. 1912. Jour. Roy. Hort. Soc. 37: 362.
. 1930. Ann. Bot. 44: 199.
Massee, G. 1908. Jour. Bd. Agric. England 15: 594.
. 1909. Proc. Linn. Soc. London 1909 : 6.
. 1910. Diseases of cultivated plants and
trees. 1st ed. New York; 2nd ed. 1915.
Millard, W. A., and S. Burr. 1923. Gard. Chron. 72:
255.
Ministrv Agric. and Fish. 1934. Bull. 79.
Osborn,"T. G. B. 1911. Ann. Bot. 25: 271, 327.
Pethybridge, G. H. 1913. Jour. Roy. Hort. Soc. Lon-
don 3S: 524.
. 1926. Min. Agric. Miscl. Pub. no. 52.
. 1927. Nat. Farmer's Union Year Book 1927:
162.
Potter, M. C. 1908. Jour. New Castle Farmer's Club
1908.
Preston, N. C. 1928. Rept. Advis. Dept. Harper
Adams Agric. Coll. Newport Salop. 3: 4.
Robertson, I. M., and A. M. Smith. 1931. Biochem.
Jour. 25: 763.
Schwartz, E. J. 1914. Ann. Bot. 28: 227.
FRANCE
Chauzit, J. 1923. Prog. Agric. et Vitic. 40: 63.
GERMANY
Appel, O. 1918. Landw. Hefte 35: 1.
Behrens, J. 1915. Jahrb. Deut. Landw. Ges. 80: 48.
Bartling, E. Versammelung Deut. Nat. und Aerzte
zu Braunschweig im September 1841. Vieweg
und Sohn, 1842."
Boning, K., and F. Wallner. 1938. Prakt. Bl.
Plflanzenb. 15: 268.
Focke, E. 1846. Die Krankheit der Kartoffeln in
Jahre 1845. Bremen.
Frank, E., and C. Krieger. 1896. Zeitschr. f. Spiritu-
sind. 1896.
Fulmek. L., and A. Stiff. 1917. Centralbl. Bakt.
Parasitenk. II. 47: 545. 1920a, Ibid. 51: 97.
1920h, Ibid. 51:315. \920c. Ibid. 52: 81.
Koltermann, A. 1931. Fortschr. d. Landw. 6: 292.
Korff, E., and K. Boning. 1927. Prakt. Bl. Pflanzenb.
u. Pflanzensch. 5: 192.
Martius, C. F. P. 1842a. Die Kartoffelepidemie.
Miinchen.
. 1842b. C. R. Acad. Sci. Paris 15: 314.
Phillips, W. 1932. Die Kranke Pflanze 9: HI.
Schlumberger. O. 1915. Deut. Landw. Presse 41:
369.
. 1927. Mitt. Deut. Landw. -Gesell. 42: 637.
1933, 76;</. 48:317.
Schneider. G., O. Schlumberger, and K. Snell. 1930.
Mitt. a. d. Biol. Reichsanst. 38: 84.
Stiff, A. 1912. Centralbl. Bakt. Parasitenk. II. 33:
447. 19\6. Ibid. 45: 305.
Stranak, F. 1918. Ibid. 48: 520.
Wallroth, F. W. 1842a. Linnaea 16: 332.
. 1842b. Beitr. zur Bot. 1: 118.
Wehmer, C. 1896. Centralbl. Bakt. Parasitenk II. 2:
261.
Wollenweber. H. W. 1926. Mitt. Gesell. Vorrats. 2:
32.
HAWAII
Carpenter, C. W. 1920. Hawaii Agric. Exp. Sta.
Bull. 45: 1-42.
Lyon, H. L. 1936. Rept. Hawaii Sugar Exp. Sta.
1935:26.
HOLLAND
Quanjer, H. M. 1916. Med. R. H. L.-. T.-en B.
School. Wageningen 9 : 94.
Van Poeteren, N. 1926. Versl. en Meded. Plantenz.
Dienst Wageningen 44.
Ziekten van Cardappelknollen. 1909. Meded. Phyto-
path. Dienst te ^^'ageningen no. 9.
l'(l\\Di:HY SI AH OF I'OTATOKS
135
(i.illoway. I.. I). !!).•}(!. Sci. Hcpt. Res. Inst. Pusa
l>t3l-l})3r): 120.
Maun. n. M.. ,-t nl. U»21. Dipt. Agiii'. H.uiiliay
Hull. 102.
IRELAND
Johnson. T. ISIOC). .I.-ilircsli. W-rcin. Vererts. Angew.
Hot. 1.
. 1!K)7. F.ion. I'rof. Hoy. Duliliii Soc. 1: :H5.
1908. Ihid. 1 : l.-)3.
. 1909. Si'iint. I'roc. Hov. Dublin Soc. n. s.
12: 16.5.
Pcthybridge. G. H. 1909. Irish Nat. 18: 118.
. 1910. Jour. Dept. Agrio. Tech. Instr. Ire-
land 10: 2H. 1911. //>;</. 11: U7. 1912. 7/j/V/.
12: 33i. 1913. Ihid. 13: !«(). 1918. Ihiil. 18:
410.
ITALY
Catoni. G. 1931. Trento. Fitographia Edit. Mutilati
Invol.
Pcrotti. R. 191-0. Biologia vegetale applicata all'
agricoltura. Ill, Mieologia-uialatti parassitarie.
Turin.
KENYA, AFRICA
Gillett. S.. J. McDonald, and T. J. Anderson. 1931.
Kenya Dept. Agric. Bull. No. 10 of 1931.
McDonald. J. 1928. Ann. Re])t. Dept. Agric. Kenya
1928:22.3.
MADAGASCAR
Bouriquet. 1938. Int. Bull. PI. Protect. 12: 191.
Borg. P. 1927. Append. F. Repts. Depts. Malta
1925-1926.
MAURITirS
Shepherd. E. F. S. 193.5. Re))!. Dept. Agric. Mauri-
tius 1931: 19.
MOROCCO
Bouhelier, R. 1936. I'ruits Primeurs 6:213.
NEW ZEALAND
Anony. 1927. N. Z. Jour. -Sci. Tech. 9: H.
Blair! I. D. 1937. Bull. Canterbury Agric. Coll. Lin-
coln 9 K
Cockayne, A. H. 1921. N. Z. ,Iour. Agric. 21 : 169.
NORWAY
Brunchorst, J. 1887. Bergens Mu.s. Aarsberet. 1886:
22.5.
Jorstad. I. 1932. I.andbruksd. Bcretning Tellegg C.
Lundcn. A. P. 1938. Meld. Norge Landbr. Hoisk.
18: 183.
PERU
Abbott, E. V. 1928. E.stac. Exp. Agric. Soc. Nac.
Agrar, Lima Circ. 7.
. 1929. Phytojiath. 19: 0 15. 19:M. Ihid. 21:
1061.
L.igerluini. (i. lS91..Iour. Mycol. 7: 103.
Patouillard. N.. and G. I.agcrheini. 1891. Bull. Soc.
M\ (111. I'raiue 7: 1.58.
Siemaszko. W. 1929. Centralbl. Bakt. Parasitenk 11.
78: 113.
PORTIGAL
(ronzales, de Andres, C. 1930. Junta Admin. Scr-
vicios. Agric. l)i\ul. no. 3: l-i6.
RHODESIA
Hopkins, J. C. F. 1940. Rhod. Agr. Jour. 37: HI.
SCOTLAND
Anony. 1927. Bd. .\gric. Scotland Miscl. Pub. no. 3.
Cuthbertson, D. C. 1925. Jour. Roy. Hort. Soc. 1:
21.
SOUTH AFRICA
Doidge, E. M. 192L Bot. Survey S. Africa Mem. no.
6:1-56.
Pole-Evans, J. B. 1910. Transvaal Agric. Jour. 8:
462.
. 1910. Transvaal Dept. Agric. Farm Bull.
110.
SWEDEN
Henning, E. 1915. Tradgarder. 1915. no. 3.
.1922. Kungl. Landb.-Akad. Handl. Tidskr.
1922: 26.
, and T. Lindfors. 1921. De viktigare potatis-
sjukdomarna, 1921.
SWITZERLAND
Anony. 1920. Schwciz. Landw. Zeitselir. 1920: 7.
Wild." N. 1929. Phytopath. Zeitschr. 1: 367.
TASMANIA
Darnell-Smith. G. P. 1922. Ann. Rcpt. Dept. Agric.
New South Wales 1920-21. 1922.
Anony. 1921.. PI. Disease Rept. Suppl. 34: 168, 178,
183.
Bailey, F. D. 1915. Sci. n. s. 42: 424.
Barrus, M. P., and C. Chupp. 1926. Cornell Exp.
Sta. Bull. 135.
Brigham, E, S. 1914. Vermont Dept. Agric. Bull.
18:2.
Clinton, G. P. 1915. Re))t. Conn. Agric. Kx]). Sta.
Bull. 1915: 163.
Cook, M. T.. and G. W . Martin. 1911. New Jersey
Agric. Exj), Sta. Circ. 33 : 3.
Haskell. R. J., and J. 1. Wood. 1927. PI. Dis. Re-
porter Suppl. 54: 209.
136
PLASMODIOPHORALES
Kunkel. L. O. 1915. Jour. Agric. Res. 4: 265.
Link, G. K. K., and G. B. Ramsey. U. S. Dept. Agric.
Misc. Pub. 98.
Lutman, B. F., and G. C. Cunningham. 19U. Ver-
mont Agric. Exp. Sta. Bull. 184.
Lyman. G. R.. and J. T. Rogers. 1915. Sci. n. s. 42:
940.
McCubbin. W. A.. R. E. Hartman. and K. M. Lauer.
1926. Penn. Dept. Agric. Bull. 420.
Melhus, L E. 1913. Sci. n. s. 38: 132.
. 1914. U. S. Dept. Agric. Bull. 82.
, J. Rosenbaum, and E. S. Scliultz. 1916.
Jour. Agric. Res. 7:213.
Morse, W. J. 1913. Sci. n. s. 38: 61.
. 1914. Maine Agric. Exp. Station Bull. 227.
Orion. W. A. 1913. U. S. Dept. Agric. Farmer's
Bull. 544.
Ramsev. G. B. 1918. Phytopath. 8: 29.
Sands," H. C, and G. G. Atwood. 1914. New York
State Dept. Agric. Circ. 111.
Shapovalov. M. 1923. Jour. Agric. Res. 23: 285.
, and G. K. K. Link. 1924. U. S. Dept. Agric.
Farmer's Bull. 1367.
Shear, C. L. 1914. Phytopath. 4: 36.
Beregovoy, P. 1939. PI. Protect. Leningrad 1939:
163."
Djelaloff, R. 1933. Azerbaijan Agric. Inst. Pamph.
1933.
Dorojkin, N. D. 1934. Crop. Protect. Moscow 1934:
n.
. 1936. White Russ. Acad. Sci. Inst. Biol.
Sci. Minsk 1936: 5.
Gomolyako, N. J. 1930. Morbi Plant. 19: 79.
Khrobrvkh, N. D. 1938. Summ. Sci. Res. Inst. PI.
Protect for the year 1936. 1938: 27.
Kiyanovski. P. M. 1936. White Russ. Acad. Sci. Inst.
Biol. Sci. Minsk 1936: 39.
Mercklin, E. 1856. Bull. Soc. Nat. Moscow 29 pt. 2:
301.
Naumov, N. A. 1936. Summ. Sci. Res. WK. Inst. PI.
Protect. Leningrad 1935: 520.
Rovdo, A. S. 1936. White Russia Acad. Sci. Inst.
Biol. Sci. Minsk 1936: 87.
Rybakova, S., and H. Nedoshivina. 1936. Ibid. 1936:
67.
Speschnew, N. N. 1897. Arb. Tiflis Bot. Gart. IJef.
11-199.
SlllJKl T INDEX
137
Anisoinvxii,(58
I'laiitayiiiis, 70
Clathrosonis, 5-4
Campanulae, 56
Cvstosporn.TG
liatata, 76
Ligniera, 58
Isorlfs, 62
J unci, 60
piloriim, ()2
radicalis, 60
-cascularum, 63
I'vrriicosa, 62
Mcmbranosonis, 52
HftiTaiitht-rai', 52
MoUiardia. .'57
Triglochinis, 37
Octomvxa. 40
AcMar, 10
Ostenfeldiella, -22, 32
Diplantherae, 32
Peltoniyces, 76
hi/alinus, 76
Blati-llae, 76
Forficulae, 76
SPKdKS INDEX
>li
PlasinodiopiiDiJi, :
lira.isicac, 22
hicatidata, 33
californiae, 31
Diplinitlurae, 32
Klafayni, 31
Fici-reprtitis, 32
llalopltitac, 32
IIiimnli,35
Orchidis, S5
Solani, 36
tahaci, 35
tomati, 35
vasciilariini, 35
/■;■<;*■, 31
Polymyxa, 63
f/raminis, 6i
Pyrrhosorus, 71
marinus, 71
RlH/omyxa,64
hi/pof/eae, 61
Sorodiscus, 46
Callitrichis, i7
Heieraniherae, 52
karlitui'ii, 50
radicicohis, 18
Sorolpidimii, ()()
yyc/nc, 66
Sorospliacra, 41
radical IX, 13
ICronicac, 12
Spoiiffosporn, .54
Campanulae, 58
Cotulae, 58
scabies, 57
,So/«n;, 57
xiihtcrraiica, 57
siihterraiiea var. radiricola, 57
subterranea var. tiibcricola, 57
Sporoinyxa,74
Scaur/', 71
Tenebronis, 75
Tetramyxa, 37
Elaeaf/ni, 38
parasitica, 37
Triglochinis, 37
Trematoplilyctis, 70
Leplodesmiae, 70
SUBJECT INDEX
Achilla, 10
Acrasiae. 57
Acrocystis, 77
Actinomi/ces, 77
Af/ropi/ron, 64
Agrostis, 66
Aira, 66
Akaryote stage, 2, 10. U . 12, 20,
Si'
Alisma, 60
Allomi/ces, 10
.i/n«.^31-.91
Alternation of generations, 15, 82.
84
--1 maurochaete, 84
.\mnioniuni siil|)hatf. I 15. 133
./mo</)fl, 8.9.79
./ mochas piiriis, .35
J m.v/o/^'ifl.^"*, 88,89,90
Anagallis, 66
Aphanomijces, 10
Aphelidiopsis, 88. 90
.Ipodachli/a, 10
Arcliimycetes. 78
A reel la, 11.79
Asterocysiis, 67, 78
Bacteria. 26
Badhamia, 84
Barisia, 66
Baitati.1, 76
Basic fertilizers, 115
Be//M, 60
Bc^a, 62. 66
Binuclearity hypothesis, 2, 1 1
Biological races, 26
Bisciitclla, 6()
BlatcUac, 76
Bli'iiliaroplast, 2, 80, 81
/Jorfo, 90
Borrago, 66
Bordeaux mixture, 109, 110
Brassican. 109
Zir/sa, 66
Bromii.i, 62
Calendula, 66
fn//;(r;r/iP, 17, 48.60
Campanula, 58, 66
Cancer. 28
Cai)illitia.2.81
Capsclla, 66
C'arholiniiini. 105
Carbolic acid, 109
Catabro.sa, 13
Carijoiropa, 8
Centrosomes. 9, 1 1
Cerastium, 60
Ceratiomi/xa, 18, 80
Ceratiuvi, 34
Ceresan, 109
Chara, 50
Chennpodium, 62
Chesliunt brown, 105. 1 10
Cblorojiicrin. 105
Cbroinidia.2. 10. II
Clironiidia liy))otlusis. 2. 1 1
Clironiosomc ninnbcrs. I 1
Chri/santhemum, 60
Cliytridiales. 78
Cleavage, 11
Cliihicide. 105. 110
Club root. i)3
Comatrichia, 80
Cop|)cr oxide. 1 1 0
Colipcr carbonate. 1 10
Cojjper sulpiiatc, 110, 132
Corrosive sublimate, 105, 132
Cotula, 58
Cresol, 109
138
PLASMODIOP MORALES
Crop rotation, 117, 132
Cruciform divisions, 2, 8
Cuciirbita, 91
Cysfoclonium, 71
Cystosorus, 2
Degree of infection, 99-103
Delphinium 66
Dicii/aethaliiim, 80
Did i/osteliiim, 57, 80
Didi/miitm, 80, 88
Dinaria, 66
Diplanthera, 32
Disease control, lO-t, 132
Double anchor stage, 2, 8
Economic losses, 93, 129
Elaeaf/nus, 34, 38
Equatorial ring stage, 7, 8, 9, 10
Erif/eron, 66
Erionema, 84
Erysibe, 57
Eucjlena, 8
Eucarpy, 2
Fedia, 66
Festiica, 62
FicHi, 32
Flagellata, 78
Folosan, 109
Forficula, 76
Formalin, 105, 132
Frankia, 34
Frankiella, 34
Fuelgen's nuclear reaction, 9
Fulif/o, 80, 88
Fitsarium, 129
Garland stage, 12
Germisan, 109
Glucococlilearin, 120
Gluconasturtin, 120
Glucotrapaeolin, 120
Gi/mnococcus, 78, 79, 88. 90
Gymnococcaceae, 78, 88
Gynandropsis, 48
Gyjisum, 115
Halophila, S2
Haplomonoecious, 3, 82
Haplophenotypic, 82
Haplosynoecious, 3, 82
HeHa7ithus,9\
Heterocont, 3
Heteranthera, 52, 53
Heterothallic, 3, 84
H-ion concentration, 97, 98, 129
Hippophae, 34
Holocarpy, 3
Homothailic, 3, 84
Hordeum, 64
Hosts, 99-103
Humulus, 35
Hydromyxaceae, 88
Hyjjerplasy, 3
Hyi>ertrophy, 3
Hypoplasy, 3
Idiochromatin, 3, 6
Immunity, 118, 133
Iris, 60
Isocont, 3,71
Isoetes, 63
Isogamy, 3, 81
Isomorphic, 3, 81, 84
Jiinciis, 59, 60, 66
Karyogamy, 3, 15, 16, 18, 82
Karyosome, 5, 8
Kataplasmic, 94, 130
"Krankheitsherde," 55, 94, 131
Lacjeiiidium, 63
Latnium, 66
Leptode.smia, 70, 71
Leptomyxa, 35, 77
Leptothrix, 34
Liming, 110-115
Lotus, 66
Lycogola, 80
Lycopersicon, 57
Magnesium carbonate, 115
Medicago, 66
Meiosis, 12,16,83,84
Mentha, 60
Mercuric chloride, 105, 106. 109,
132
Meront, 3, 14
Methyl green, 105
Monadineae, 78, 88
Monas, 88
M on ilia, 43
Mustard oil, 109. 120
Mycetozoidia, 88
Mvxoidea, 79
INIyxomycetes, 78, 79, 82, 83
^lyxosporidia, 90
Myxocliytridiales, 78
Myzocytium, 63, 66
Naegleria, 36
Nematodes, 96
Newton's gentian violet method, 9
Nuclear dimorphism, 4
Olpidiaceae, 85
Olpidium, 23, 66, 96
Olpidiopsis, 85
Oospora, 131
Papulospora, 131
Parachlorobenzine. 109
Petroleum, 109
Phaseolus, 91
Phoma, 131
/'/!;/.Vflr('//a, 80, 88
Physarium, 80
Phytotnyxa, 78, 79
Phytomyxaceae, 2, 78, 79
Phytomyxini, 2, 78, 79
Phytophthora, 131
Planocyte, 3, 80
7^/aH(ar/o, 60, 70
Plasmodiocarp, 3, 80
Plasmodium, 3, 80, 81
Plasmogamy, 3, 15, 16, 18, 82
Poa, 43, 60,"62, 66
Polygonum, 60
Polysphondylium, 57
Potassium permanganate, 109
Potomogeion, 37, 60
Powdery scab, 129
Powdery scab dry rot, 129, 130
Preplasmodium, 25
Pringsheimella, 85
Promitosis, 3, 4, 10, 11
Protomitosis, 3, 5
Proteomyxa, 35, 79, 88
Protista," 78
Protomyces, 57
Protomyxidea, 79
Protozoa, 79, 88
Pseudocommis, 34
Pseudospora, 79
Pseudosporopsis, 88
Quarantine, 129, 133
Radium, 110
Ranunculus, 60, 66
Resistance, 1 18, 1 19, 120, 133
Reticularia, 84
Rhizoctonia, 131
Rhizopoda, 90
Rhizosporium, 57
Rozella, 85
Rozellopsis, 86
Rumex, 64
Ruppia, 37
Saccharum, 35
Sappinia, 76
Saprolegnia, 40
Sarcodina, 88
Saltpeter, 116
Saturn stage, 3
Scaurus, 74
Schinzia,3l
Schizont, 3.14
Schizogony, 3, 14, 15,90
Schizozooites, 90
Sclerotia, 25,29
Scolochloa, 64
Secale, 64
Segetan, 109
Semesan, 109
Septol pidium, 63
Serumsporidium, 79
Setaria, 66
Sexuality, 15,81,82
Silene, 66
Sinablin, 120
Sinigrin, 120
Sodium carbonate, 110
Sodium chloride, 1 10
Soil drainage, 98, 117, 132
Soil rot, 77
Soil moisture, 98
Soil pox, 77
Al'THOH INDKX
139
^So/(inH»i.3(>.."i7.!ii. i;n
SoliKir. 105
Soroi-.-irp. 3
SdrospDriiiin, I'J. .57
Sorus. 1. 3
Soot. 10!)
Sporanjiiosorus, 1 . 3
Spore ficrinin.-itioii. i)7. 1 2i)
Spore ionju-vity, lOt, 132
Sporoi-yst. 3, S)0
Sporoiianu'tfs. 23
Sporoiii'iR'sis, 10
Sporoiit. 3. 14. 13
Sporozoa. 75). !)0
St ell aria, (5(5
Stemonitis. 80, 8 1
Sulcaii. 109
SulsriiK'. 109
Sulplmr. 105. 132. 133
Syiiil'iosis, 2iS, 38
Si/iich i/triiini, 71. 7S. 130
S\ ncliytriaii ac, 70. 7.S. 85
Synkaryoii, 3
Temporature etlVits. 98. 129
Tfiirhrio, 76
Tillaiitinl}. 110
Trichia, 18, 80
Trifdiiiiiii, (i(i
Triglochiii, 37. (56
Tr'iiicum, (i !■
Trophoclironiatiiij 6
Trijpanosoma, 8
'ruhiTc'inia, 12. 37
'I'i/lii(l(iiiiix, 2
I 'lliifux, 57
L'spulim. 105. 109
I' ampjirilla, 79
}' auchrria, 8(5
/■(•rwHita, 12, (iO, 62
Vitis, 31
Woronina, M, 78, 85, 86, 91
Woroniiiaceae, 85, 86, 91
X-ray, 110
'/lannichella, 37
Zoocyst. 3. 90
Zusteria, 33
AUTHOR INDEX
Al>l)ay.93, no. I II. 127
Abbey. 35
Abbott. 129. 132. 135
Abe. 81,82
Adam, 93, 121
Adams. 77
Albert. 111. 120
Alexieff. 1.9
Almeida. 126
Anderson. 93, 1 10, 1 17, 127
Andreueei, 32
Appel.26,9K95, 106. 110. 115
Archer, 131
Arker. 106. 111. 116. 118, 123
Atkins. 97. 99. 125
Atkinson. 96. 127
Atwood. 136
Aue. 123
Bailey. 127. 135
Bailie. 109. 125
Bald, 133
Earner, 36
Barnes, 2, 79
Barre. 77
Barrett. 18. i3. 58. 39, 66
Barms. 133
Bartlinsr. 58, 131
Bandy s, 121
Bayer, 123
Beaumont, 97. 110, 119, 121
Becker, 111, 123
Behla.30. 123
Belirens.31-
Belar.91
Benehley, 105
Bennett', 111,121
Berefjovy. 131. 133, 136
Berkeley. 57, 121, 129, 134
Bernatsky, 125
Bessey,7"9.80, 81
Bever". 96. 1 11. 123
Biffin, 121
Bird, 127
Birne. 93, 127
B jorkenheim, 34
Blair, 135
Blattny,57, 134
Blomfield. 4. 10
Blumberg, 123
Blunek, 97, 105,110,111.116,118, 123
Boluier,93, 111. 123
Boning. 93. 132. 133, 131
Bondarzew, 126
Borg, 135
Borzi, 1, 64, 66
Bos, 34, 98, 110, 135
Bottner, 123
Bouhlier, 133
Bouriquet, 133
Braun, 106
Breiimer, 36
Bremer, 96.97,98. 105,109, 110, 123
Brezhnew. 115, 119, 126
Briek, 106, 110, 123
Brigham, 135
Briosi, 34, 125
Bronnle, 106, 123
Brown, 109. Ill, 121
Bniek. 123
Bnineliorst. 2, 34, 54, 57, 93, 135
Bubac. 121
Buehinan.93. 121
Burk. 20, 22.42,47
Burkliardt. 99, 106. 109, 111,117,123
Burr. 131, 134
Busse. 34
Cadman, 1,79,80.82,81
Calkins, 8, 79
('ari)enter, 13 1
Carrieklee, 11 1, 112, 121
Carruthers. 96, 121
Casali, 34
Caspary,94, 123
Catoni, 133
liO
PLASM ODIOPH OR ALES
Cavara. 34
Cavers, 78
Chardon, 35
Chatton, 4
Chauzit, 134
Chodat, 34
Christensen.97, 121
Chupp. 16. 23. 24, 28, 96, 98, 105, 1 10, 1 12
Cienkowski. 1,88
Clark. 121
Clavlev. 82
Clavton, 105,109, 127
Clinton, 128, 135
Cockayne, 135
Coic. 104
Collinge, 121
Cook. M. T.. 35. 63, 94, 128, 135
Cook, W. R. I., 1, 10, 16, 18.22,37,42,48,50,54,
59,67.81,85,86,91,134
Cooke, 34. 121. 134
Coons. 128
Cotner, 80
Couch, 1,4,18,40,81,85
Crosby, 128
Cotton, 132. 134
Cuboni. 34
Cujoutantis, 133
Cunningham, 94, 97, 99, 110, 115, 128
Curtis, 93, 121
Cutlibertson, 135
Dankler, 106, 123
Darnell-Smith, 105, 110, 133, 135
Davies.129
Davis. 119.128
De Andres, 117,127
DeBary,78, 80
Debrav, 34
De Briiyne, 88, 90
Delage, 2, 79
Deutelmoser, 116. 123
Diakonoff. 110. 126
Dickson. 133
Diedicke, 42
Djelaloti. 136
Doflein. 14, 79, 91
Dodge. 78
Doidge.48.127, 135
Donald. 42
Doppler,127
Dorojkin, 129, 132, 133, 136
Ducomet. 34
Dufrenoy, 121
Duggar,77, 128
Eastham, 134
Edison. 128
Edson.93
Eggemeyer. 106, 109, 123
Elenkin, 126
Elliott, 76, 77
Ellis, 93. 121
Ericksson, 96, 115
Esmarch, 3,24, 104, 109, 123
Evans, 119, 129
Eycleshymer, 1, 24, 93, 95, 117, 128
Farquharson, 93, 127
Farsky, 116. 121
Favorsky.23.80.96. 126
Fedetova,28.126
Fedorintschik. 1 . 10. 16. 23, 24, 81, 96, 104, 117
Feinberg, 30, 123
Feldman, 32, 33
Felsberg, 123
Ferdinandsen, 5. 32, 54, 57, 58
Findlav.119, 127
Fischer, 78. 85. 127
Fitzpatrick, 2, 3, 66, 70, 77, 79
Flachs, 106, 116,123
Fleishman, 123
Focke, 134
Fowlie, 127
Franco, 134
Frank, 34, 123, 134
Fron, 62
Fruwirth.123
Fulmek, 134
Gaillat, 62
Galloway, 134
Gaumann, 78
Gav, 121
GaylDrd,23.24,30, 128
Georgeson, 93, 1 10
Gibbs, 26,97, 104, 106, 1 12, 1 15, 1 16, 117. 1 18
Gilbert,80, 82, 128
Gilchrist, 110,121
Gillett. 135
Gilman, 128
Glasgow, 106, 110, 128
Gleis\ierg, 26, 93, 96, 105, 11 1, 123
Glover, 106, 110.128
Goebel, 2, 37
Gomolyako, 133, 136
Gonzales, 135
Gorini, 32
Gorham, 134
Gram, 121, 134
Gravis, 35
Gretschel, 123
Grevillius. 42
Griffith, 119, 129
Griffon, 103
Grigon. 103
CJross-Schlacters. 123
Giissow, 119, 121,134
Guyot, 62,66,67
Gwvnne-Vaughan, 2, 79
Habernall, 123
Haddon,37
Haensler, 111, 112,128
Hall. 99, 121
Halstead, 1,77.93,99, 110, 128
Hammarlund, 106, 109, 127
Hanley,105
Harder, 97
Harper, 82, 92
ArriioH ixDKX
141
Harslilurjit-r. 128
Martrr.TT. 1 10. lli). 128
I l.irtniaii. l.'Ui
H.irtojl. ~i>
H;i>kdl.!)3. 135
Hawk. 111. 128
Ha\imfra.!»8. I 1(>. 12.3
Hiald. 128
Heokf. 133
Htdluiul. 127
H.jryi. 12.-)
} Iiin/.clniaim. 117. 127
H.lliiian. 123
Hernki-l.SO, 12r>
Henderson. 93. 110. 128
Hendriik. 119. 127
Hennin£:s.42.!)9. 121. 13.5
Henry. 13 t
Heroii.ird. 79
Her))er.s.93. 107. 111. 123
Hertel. 10."). 109. 110. 124
Hertwig. 79
Hertznian. 127
Hcrviaux. lOt
Hevder. 121.
Hil'delirand.fi2.63
Hiltner.97. 107. 1 l.->, 116, 12 1
Hissinger. 37
Hockey. 119.121
Hofferiehter, 10.5, 124
Hoffman. 10.5, 121
HoUenbach, 124
Hollriing. 107. no
Holmes-Smith. 10.5. 106. 121
Hopkins. 13.5
Honig, 23,26, 94, 95, 96, 97, 98, 99, 1 04, 1 06, 1 1 6,
124
Honigmann. 124
Hooker. 120
Home. 2. 9. 13. 16. 18.56.81.91. 129,134
Hostermann. 26, 107,111, 119, 124
Howard. 80, 84
Hiilst.128
Humphrey, 98. 128
Hunter. 110. 111. 127
Hurrle, 121
Hurst, 134
Ikeno, 125
Iwanoff, 126
.lahlonowski, 125
.lahn. 1.78.80,81,82,83,84
Jaap.31. 126
Jaczewski, 126
Jamlainen,97,99, 105. 118, 119
.Tanchen. 133
.Ianson.98, I 10
,Iohnson.56. 132. 135
.Jones. L. R., 101, 1 10, 1 12, 1 19, 128
Jones, P. M., 1 , 4, 10, 15, 24, 26, 35, 80, 128
Jorgenson. 105, 109
Jorstad,23,93, 105, 110,117, 135
,hiel 71
K.idow. rjs
K.iiiihly..S2.92
KaUhselmiid, 124
K.ip])en, 12 1
Kareltsehikott. 17
Karling, 50, 60, 63, 85, 86
Karsten, 121
Katterfcld,9!). I 10. 1 l(i. 1 19. 126
Keissler. 34
Kellermaiin. 124
Khroliyrkli. 57. 136
Kiiiippel. 124
Kiiidslioven,99, 105, 106, 116, 121
Kirk, 35
Kirschner, 107, 1 11 . 1 17. 124
Kiyanovski, 1 36
Klebahn, 124
Klehs.88.92
Kleimenov, 126
Klein, 88, 92
Klemm, 124
Kiiiep. 78. 84
Koblischek, 107, 115, 124
Koek, 104,117, 124,133
Kohne, 107,121
Koltermann, 129, 134
Korff. 115, 124,134
Kornauth, 120
Knorr. 124
Kranzlin, 84
Kreuzpointer. 110. 111. 124
Krieger, 134
Kronberger. 106. I 16
Kruger. 124
Kudo. 79, 92
KUhn,93, 124
Kupke, 105, 109, 124
Kunkel, 1, 18,23,54,57,80,95,96,128, 129
Kuster,94, 124
Lagerheim, 42, 43, 46, 57, 135
Langenbeck, 124
Lankester. 79, 88
Larsen, 23,96,98. 11], 115, 128
Laubert, 93, 9 1. 95. 104, 111,117
Lauer, 136
Ledingham, 1 . 1 0, 18,23, 56, 63, 8 1
Leger, 74, 76
Leines, 107, 124
I^eitncr, 40
I.evine,30,95.128
I.inder, 104
I.indfors,97. 107. 109. 110. 115,127
Link. 35, 120, 136
Lister, 82
Littlejohn, 129
Joew, 108, 109, 112
Lohwag, 34
Lotsy. 78, 92
Lowcnthal,30. 121
Ludwig. 126
Ludwigs, 97, 101, 108, 117
142
I'LASMODIOPHORALES
Lunden, 135
Lundegardh, 91
Lustnfr,93, 108
Lutman, 8, 15,21,95, 128, 136
Lyman, 136
Lyon, 134
MacDonald, 135
MacLeod, 26, 108, 110. 119. 121, 128
Maire. 2, 8, 18. 34. 37, 58, 62, 78
Magnus, 99, 124
Mangin, 116
Mano. 91
Marchand, 103
Marcell, 120
Marcliionatto. 120
Maneval, 128
Manns, 77
MarshaU, 121
Martin,93, 97, 110, 112, 128, 135
Martins, 129. 134
Massee, 1, 18, 34, 35, 54. 57, 132, 134
Matz, 35
Mathieu-Sanson, 95, 1 1 1 . 11 6
Maublanc, 103
Maun, 135
McAlpine, 111.116
McCubbin, 136
McLarty, 121
McLennan, 35
McRostie, 121
McRue, 125
Merkenschlager, 108
Melluis,57, 129, 130, 131, 133, 136
Mercklin, 136
Meyer, 97, 124
Middleton, 128
Milburn.121,128.131
Millard, 134
Miller. 93. 116, 124
Milovidov,5,n,12, 15, 121
Minden, 66
l\Iinclien,79,92
Moeller, 34
Moesz,36,125
Moldenke, 128
Molliard,37,38
Montieth,98, 110, 117, 128
Moritz.34, 126
Morozov, 126
Morse, 136
Mortensen, 121
Motte,26,97. 105. 112. 116, 117
Mothes, 110, 124
Mover, 111,112
Muiler,96, 109
Miiller-Thurgau. 95. 96. 108
Murphy, 111,115, 116, 128
Muskett, 109
Nagler,4,9,91
Nance. 128
Nattras, 129
Naumann, 104,115,116,124
Naumov. 28,96,97, 110,129, 133,136
Nawaschin, 1,4, 10, 14, 24
Nedoshivinia, 57
Neger. 104, 111, 115, 124
Neill, 126
Nemec, 1,66.67.68,70
Newodowsky. 126
Nichols. 35, "l27
Nicholson, 85,86
Nicoloff,95, 121
Nielsen, 114, 117, 121
Noak, 111,115
Noble, 120,133
Noel, 121
Notzel, 124
Norwood, 133
O'Brien, 127
Oger, 123
Ogilvie, 105, 108,121
Olive, 82
Olsson, 118, 119, 127
Orton, 136
Osborn. 1, 5, 10, 12, 18, 56, 81, 134
Ostenfeld, 47, 52
Osterwalder, 95, 96, 108, 109, 1 16
Owen, 128
Palm, 18,22.42,47,62
Palmer, 108, 109, 128
Panck, 124
Pape,94, 124
Pardy, 127
Partridge, 134
Pascher. 78,92
Passv, 123
Patouillard, 70, 71,135
Pavillard, 14, 16,78,92
Perotti, 125, 135
Petch, 121
Petersen, 52
Pethybridge, 129, 132, 133, 134, 135
Petri, 110, 125
Pettera. 117. 124
Pfeiffer, 125
Phillips, 129, 132, 134
Pichler, 121
Pinoy.26,28,84
Podwyssozki, 30, 126
Poetern, 125, 134
Pollacci,32, 125
Pole-Evans, 127, 135
Polyakoff, 10 K 126
Ponkler, 116. 124
Poole. 77
Pope, 119
Popp. 105, 108.110. 111. 115,124
Potebnia. 126
Poter, 124
Potter, 104, 134
Potts, 103, 104, 110
Preston, 105, 108,110, 114, 129, 134
Prillieux, 34, 123
Price, 77
Al THOU l.NUKX
lia
Prowaztk. .5. 12. 1 5. •_> t. 30. SO. I2t
I'nor. 1 17. I IJt. 120. 12S
(^UJlIljlT. 13i
U.ilil)as. 10.-.. 108. 1 10. 121.
Haht'iiliorst. .57
K.iiiiio. 121
Rainstv. 129. 13(5
Raiiffoi. 127
Rath. 121
Rattkf. 12t
Rail. 12 t
Ravaz.St
Ravn.S)K97. 98. 1 10, 1 1 1, 1 Hi, 118, 121
Rawlins. 67
Rayes. 126
Read. 98
Reed. 9.1. 128
Regcl.l2l
Reic-lu-now. 79
Rcitsilid.76
Rcmy.93. 121
Renard.93. 111. 123
Rluinibler. 79.92
Rielini. 108. 109. 110. 121
Robertson, 131
Roehlin.23. 21-.96.97. 1 IS. 119. 120. 126
Roger. 1 15. 125. 136
Rosanoff. +7
Rosen. 82. 92
Rosenbaum. 57, 136
Rosenfeld. 48
Roth. 125
Rostrup. 12. 93. 131
Rovdo. 132. 133, 136
Roze. 31
Rump. 12.5
Russell. 121. 128
Rybakova.57, 136
Saccardo. 67. 77. 1 25
Sanderson. 127
Sands. 136
San ford. 131
Sattler. 121
Sauvageau, 31
SchatTnit. 97. 108. 115
Schaudin. 1 1
Scherffel, 88,90,92
Schibata, 31
Schilberszky, 125
Schinz. 127"
Schlodder. 125
Schlumberger. 91.95. 105. 125, 131
Schmid. 1 15
Schmidt. 116. 121, 127
Schneider. 131
Schoyen, 126
Schroeter, 1,20,31,11,78
Schultz.57, 136
Schiinemann, 83. 81. 92
Schwartz, 1, 10, 13, 37, 42, 59, 60, 78, 137
Schwarze, 128
Seeloff, 116, 125
Seifert, 125
Setehell.37
.Selt.nsiHrger. 1 10. 115
.Sh,ir;mga))ani, 125
-Shapovalov. I ;) I . I :«)
Sharpies, 57
Shear, 136
Shephard, 129. 135
Shewell-Cooper, 111
Siemazko. I 10. 117. 126. 135
Sinoto. 80. 92
Sit.nsky. 1 10. 121. 126
Skujiienski. 1. 18. 82.81
Slingerhand. 93. 128
Sniieton, 105, 109
Smith. 26. 78,80. 96, 128
Snell. 131
Sonimer, 105, 125
Sonimerville, 1 10
Sorauer,93. 125
Spesehnew, 126. 136
Ssaeharotf, 97, 99. 1 18, 1 19, 126
Staes, 125
Staniland, 97, 110
Stefanow, 95, 121
Stephens, 121
Stevens, 78. 128
Stewart, 111. 128
Stift. 121. 131
Stoseh.80.81
Strasburger, 82, 92
Stranak, 131
Straube. 116, 125
Strohmeyer. 125
Stubbs,ill, 117
Svec, 121, 126
Sydow. 31
Tabenhaus, 76, 77, 128
Tahara,91,92
Takase, 12, 13,38
Taliaferro, 36
Tedin. 119, 127
Tennent, 110. 1 1 K 1 19. 126
Terby. 1,8,9. 12.81
Tessenow, 1 10, 1 1 1, 125
Tiee. 131
Tillinghast, 128
Tison, 2, 8, 18. 31, 37, 58, 62. 78, 85
Tischler, 91
Tokunaga. 86.92
Toni])kiiis. 128
Townsend, 77
Trieseliniaii.99. 10 K 108. 125
Troitzky, 126
Trotter, 12, 16
Truseott, 57
Tul)euf,2,78
Tueker. 1 3 I
Uzel. 121
Vanderyst. 93, 95. 98, 121
Vaughan, 110, 128
Vercier, 123
144
PLASM ODIOPHORALES
Viala, 34
Vielhauer, 108, 125
Vilkaitis,97, 108, 109, 114, 126
Vincent, 104,123
Voelcker, 110, 111,121
Vladimirskaya, 108, 109, 110, 114, 126
Vogel, 114, 116
Voglino, 125
Vogt, 108
Vohman, 125
Vonwiller, 125
Vouk,28, 80, 84, 125
Wager, 91
Wagner, 116
Wagner-Ettelbruck, 125
Wahl, 133
Wahling, 95, 108,125
Walker;26, 96, 98, 11 1. 1 14, 1 15, 1 19, 120, 128
Waldheim, 57
Wallner, 132,133
Wallroth,57, 58, 134
Webb, 8,9,13
Weber,57, 127, 134
Weimer, 77
Weiss, 110, 125
Wellman, 97, 98, 105, 110, 111,114,117,128
Wenyon, 14
Werham, 4, 13, 18,52,54
Werner, 37
Werth, 26, 94
Weseheider, 128
Wettstein, 79, 92
Whiffen, 10, 18,24,40, 82
Whitehead, 98, 110,115.116,119, 120,129
Wilcox, 77
Wild, 56, 129, 135
Wildemann, 66
Wilson, 1, 80, 84, 108, 1 10, 1 14, 128
Winge, 5, 10, 13, 22, 32, 46, 54, 58, 67, 71, 78, 85,
134
Winter, 42
Wisselingh, 125
Wood, 93^ 116, 135
Woodman, 105, 121
Wollenweber, 134
Woronin, 1, 22, 78, 93, 95, 96, 99, 109, 1 26
Wright, 127
Yendo, 12,38
Yuasa, 80,92
Zopf, 2, 78, 79, 85, 86, 88, 92, 125
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