James20141 PDF

7 Blastocladiomycota
TIMOTHY Y. JAMES1, TERESITA M. PORTER2, W. WALLACE MARTIN3
CONTENTS I. Introduction
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
II. Occurrence and Distribution . . . . . . . . . . . . . 179 Blastocladiomycota are zoosporic fungi that
A. Saprobic Species . . . . . . . . . . . . . . . . . . . . . . . . 179
B. Invertebrate Parasitic Species . . . . . . . . . . 180 comprise an early-diverging branch on the
memiliki
C. Plant-Pathogenic Species . . . . . . . . . . . . . . . 180 tree of true fungi possessing a number of dis-
D. Mycoparasites . . . . . . . . . . . . . . . . . . . . . . . . . . 180 tinguishing morphological and life history
E. DNA-Based Evidence . . . . . . . . . . . . . . . . . . . 180 characteristics. These aquatic and soil fungi
III. Structure of Thallus and Reproductive include genera typically considered so-called
Characters. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
IV. Phylogeny and Systematics . . . . . . . . . . . . . . . 182 water molds, occurring as saprotrophs on
A. Phylogenetic Placement decaying plants and animals. Other members
of Blastocladiomycota . . . . . . . . . . . . . . . . . . 182 of the clade are obligate parasites of
B. Phylogenetic Classification invertebrates, plants, and algae. Beyond a
of Blastocladiomycota . . . . . . . . . . . . . . . . . . 184 basic understanding of global biodiversity,
V. Life Cycles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
A. Historical Perspective . . . . . . . . . . . . . . . . . . 187 Blastocladiomycota present avenues for excit-
B. Life Cycles of Allomyces . . . . . . . . . . . . . . . . 187 ing research: they have served as models for
C. Life Cycles of Other Blastocladiomycota 189 fungal genetics and physiology (Olson 1984;
VI. Zoospore Ultrastructure . . . . . . . . . . . . . . . . . . 192 Ribichich et al. 2005), they have potential as
A. Historical Perspective . . . . . . . . . . . . . . . . . . 192 biocontrol agents of plant pests and disease
B. Generalized Structure of Motile Cells
of Blastocladiomycota . . . . . . . . . . . . . . . . . . 193 vectors (Chapman 1985; Garcia 1983; Singh
1. Axial Assembly. . . . . . . . . . . . . . . . . . . . . . . 193 et al. 2007), and they interact with aquatic
2. Microbody–Lipid Globule Complex. 194 food webs and nutrient cycling through para-
3. Flagellar Apparatus . . . . . . . . . . . . . . . . . . 196 sitism and consumption (Johnson et al. 2006).
4. Cytoplasmic Inclusions . . . . . . . . . . . . . . 196 Convenient terms for the group include blasto-
VII. Genetics and Physiology . . . . . . . . . . . . . . . . . . 197
A. Hybridization . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 dad and blastoclad, and we adopt the latter in
B. Mitosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198 reference to any fungus belonging to this phy-
C. Taxis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199 lum.
D. Substrate Utilization and Respiration . 199 The blastoclads were historically consid-
E. Genomics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200 ered to be closely related to other zoosporic
VIII. Conclusions and Future Directions . . . . . . 201
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202 true fungi, the Chytridiomycota (chytrids),
because they reproduce with zoospores posses-
sing a single posteriorly directed flagellum
1
Department of Ecology and Evolutionary Biology, University (Sparrow 1960). Blastocladiomycota, as well as
of Michigan, 830 N. University, Ann Arbor, MI 48109, USA;
the two zoosporic fungal phyla Chytridiomy-
e-mail: tyjames@umich.edu
2
Biology Department, Duke University, Durham, NC 27708, cota and Neocallimastigomycota, were shown
USA and Department of Biology, McMaster University, Hamil- to be members of the fungal kingdom in the
ton, ON L8S 4K1, Canada; e-mail: terri@evol.mcmaster.ca earliest ribosomal DNA–based molecular phy-
3
Department of Biology, Randolph-Macon College, Ashland, logenies (Bowman et al. 1992; Bruns et al. 1992;
VA 23005, USA; e-mail: wmartin@rmc.edu
Systematics and Evolution, 2nd Edition

The Mycota VII Part A
D.J. McLaughlin and J.W. Spatafora (Eds.)
© Springer-Verlag Berlin Heidelberg 2014
178 T.Y. James et al.
Fig. 7.1 Characteristic stages of blastoclads include var. iliensis, a parasite of the mosquito Culex antenna-
zoospores and bipolar germination of encysted spores. tus [photo from Couch and Bland (1985), used with
(a) Uniflagellate zoospore of Allomyces javanicus. ffla- permission from Elsevier]. (d) Spiny resting sporangia
gellum, nnucleus, ncnuclear cap, lglipoid granules. (b) of Catenaria spinosa, a parasite of the midge Chirono-
Cyst (c) demonstrating bipolar germination with one mus decorus. (e) Cluster of resting sporangia of Allo-
end enlarging to form a hypha and the other end com- myces moniliformis demonstrating pitted outer wall.
posed of thin rhizoids involved in substrate attachment (f) Germinating resting sporangium of A. javanicus
and resource extraction. (c) Scanning electron micro- releasing meiospores. Scale bar in A–C¼10 mM; D,
graph of resting sporangia of Coelomomyces iliensis F¼30 mM; E¼20 mM
Förster et al. 1990). While it was obvious that istics. The most consistent characteristic of the
posteriorly uniflagellate “phycomycetes” were group is reproduction by a zoospore with a
bersekutu
allied with true fungi, molecular phylogenetic prominent nuclear cap that in hyphal species
studies immediately detected a large phyloge- often demonstrates bipolar germination
netic distance between the blastoclads and the (Fig. 7.1a, b). Another distinguishing feature is
chytrids (Bruns et al. 1992; Nagahama et al. the thick-walled, darkly pigmented resting spo-
1995). Despite an uncertain phylogenetic place- rangium that is often ornamented with pits,
ment, the composition of blastoclads has ridges, or spines (Fig. 7.1c–f) and undergoes
remained largely consistent over time (with germination by the cracking of an outer wall
menonjol
the exception of the genus Physoderma), and through which an endosporangium protrudes.
it has been accepted as monophyletic because The resting sporangium is sometimes referred
of the presence of several distinctive character- to as a resting spore; however, because the
Blastocladiomycota 179
sporelike structure germinates to produce eral trend in the diversity of zoosporic fungi
zoospores by internal cleavage, the term spo- and pseudo-fungi (Sparrow 1960). No marine
rangium is more accurate. Also, in our discus- or halophytic species are known.
sion we refer to this structure as a resting The geographic distribution of certain spe-
sporangium rather than a resistant sporangium cies within well-studied genera suggests many
or meiosporangium. widespread species of Allomyces, Coelomo-
Blastoclads are the only fungal group myces, and Blastocladia. Allomyces arbusculus
known to demonstrate an alternation of hap- is known to occur on most continents, includ-
loid and diploid generations. On the basis of ing temperate climates, while A. moniliformis
this life cycle, ultrastructural characters, and and the hybrid species Allomyces javanicus are
overall phylogenetic distinctness from chytrids reported in both Old and New World tropical
(James et al. 2000; Nagahama et al. 1995; Seif and subtropical habitats (Emerson 1941; Spar-
et al. 2005), the blastoclads have been consid- row 1960; Wolf 1941). The species Blastocladia
ered a separate phylum, Blastocladiomycota, pringsheimii is thought to be widespread and
di mana-mana
with a single class and order, Blastocladiomy- ubiquitous and is known from all continents
cetes and Blastocladiales, respectively (James except Antarctica (Nascimento and Pires-
et al. 2006b). A distinct life cycle, diverse eco- Zottarelli 2010; Sparrow 1960). Numerous
logical roles, and phylogenetics all suggest that other species of Blastocladia are newly
the group is ancient. This ancient divergence is described and only known from India (Das-
also corroborated by fossil evidence demon- gupta and John 1988). It is important to note,
strating an alternation of generations in the however, that species concepts among blasto-
Devonian blastoclad Paleoblastocladia milleri clads are largely untested, and current phyloge-
(Remy et al. 1994) and Allomyces-like resting netic evidence suggests that species concepts in
sporangia from the Devonian that are remark- Allomyces are in need of revision (Porter et al.
ably similar to those of extant species (Taylor 2011). Other genera, for example, Coelomo-
et al. 1994). myces spp., have species with rather distinct
Here, we provide a basic introduction to the resting sporangium ornamentation, suggesting
blastoclads, covering their distribution and that they should be readily diagnosable taxa;
ecology, phylogenetic relationships, and mor- these species also have been found on multiple
phological characteristics of their spores, and continents (Couch and Bland 1985).
we present an overview of their unique life
cycles and genetics.
A. Saprobic Species
Most saprobic species are known from studies
II. Occurrence and Distribution in which water or soil is baited with appropriate
rami
substrates such as hemp seeds, rosaceous fruits,
Blastoclads are globally distributed in numer- pollen, or insect body parts. These species are
ous aquatic and terrestrial habitats. Within thus likely to perform an active role in the
these habitats, blastoclads can be observed on decomposition of cellulosic, chitinous, or kera-
decaying plant or insect material or as patho- tinic substrates within the ecosystem. Because
gens of aquatic organisms. However, other the majority of saprobic blastoclads are known
unique terrestrial habitats, such as in the pho- to produce a resistant sporangium, they are
tosynthetic tissues of vascular plants, and as readily recovered from soils that are air-dried
parasites of terrestrial invertebrates, such as and then baited using an appropriate substrate
tardigrades and nematodes, are important (Whisler 1987). Soils that are periodically inun-
habitats for blastoclads. Some genera, such as dated represent good collecting locations for
Blastocladiella and Allomyces, seem to be more Allomyces (Sparrow 1960). The blastoclad-
common and speciose in tropical or subtropical resistant sporangium may either provide an
habitats (Emerson 1941; Whisler 1987), a gen- advantage in these habitats that undergo cycles
of flooding and drying or merely explain the resting sporangia. The pathogen is observed
reason they are so readily recovered. Some primarily on the leaves and shoots of aquatic
Blastocladia spp. are facultatively anaerobic or terrestrial plants but may also appear in the
(Gleason and Gordon 1989) and are recovered root system (Sparrow 1965). Hosts are diverse
ranting pakis, sedges
from submerged twigs and fruits in stagnant and include water ferns, sedges, composites,
water or by baiting under anaerobic conditions and the crops Zea mays and Medicago sativa,
(Whisler 1987). but the economic importance of these patho-
gens seems minimal. Experimental inoculation
studies have demonstrated that one unnamed
B. Invertebrate Parasitic Species Physoderma species from Agropyron repens,
common quack grass, could infect all tested
Both aquatic and terrestrial invertebrates are congeneric hosts but not nine other sympatric
hosts for parasitic blastoclads. In cold streams, species from other families (Sparrow and Grif-
the larvae of black flies may be host to Coelomy-
nyamuk fin 1964). Unlike many Chytridiomycota, only
cidium. Midge eggs and mosquito larvae may be one monotypic genus is known as a parasite of
collected along the edges of ponds and streams algae, Paraphysoderma (Hoffman et al. 2008).
and are frequently parasitized by Catenaria spp.
and Coelomomyces, respectively (Martin 1987).
Infected larvae typically die before metamor- D. Mycoparasites
phosing into adults; however, fourth-instar
female larvae infected by Coelomomyces may A single mycoparasitic species is known, Cate-
pupate into adults, become sterilized by the naria allomycis, which grows endobiotically in
infection, and shed Coelomomyces resting spor- Allomyces spp. or Blastocladiella simplex.
angia when they attempt to oviposit (Lucarotti Experimental inoculations (Couch 1945)
1987). Additional hosts of parasitic blastoclads showed the parasite could infect all Allomyces
include nematodes, copepods, cladocerans, and spp. (to varying degrees), only one Blastocla-
trichopterans, where the parasites grow inter- diella sp., but not Blastocladia parva, Catenaria
nally as walled or wall-less thalli, but they may anguillulae, or any saprolegnialean hosts.
be most readily spotted as gametangia or resting
sporangia that may fill the entire body cavity.
Sorochytrium is only known from the tardigrade E. DNA-Based Evidence
Milnesium (Dewel et al. 1985) and has been
collected only from the type locality in North Because most of what is known of the distribu-
Carolina. The genus Myiophagus is recorded tion and diversity of blastoclads is known from
from larvae and pupae from dipterans and cultured studies using baiting rather than direct
scale insects (Karling 1977; Sparrow 1939). The observation of samples, the investigation of
wide distribution of blastoclad pathogens environmental DNA has great potential to
across Crustacea and Arthropoda suggests that enlighten our understanding of the suitable
many more genera and species remain to be habitats and diversity of blastoclads, as it has
detected. A recent review discussed all of the done in other fungal lineages in soil and plant
known genera and species of invertebrate blas- roots (Freeman et al. 2009; Schadt et al. 2003;
toclad parasites (Gleason et al. 2010). Vandenkoornhuyse et al. 2002). These studies
mendapatkan
involve obtaining an environmental sample, for
example, soil or pond water, which is then sub-
C. Plant-Pathogenic Species jected to DNA extraction, polymerase chain
reaction using primers targeting ribosomal
The genera Physoderma and Urophlyctis are RNA genes, and analysis of DNA sequences to
obligate parasites of vascular plants with a determine the organisms present in the sample.
worldwide distribution. Symptoms include At least three published environmental DNA
pustules and leaf streaks of darkly pigmented studies have detected blastoclads. One study
(Slapeta et al. 2005) recovered two sequence structures are holocarpic, whereas thalli bearing
types of unknown blastoclads from the sedi- rhizoids or vegetative portions not contributing
ment of an anoxic pond that clustered with to reproductive structures are eucarpic.
Allomyces and Blastocladiella. Later, when Por- Many blastoclads have been shown to share
ter et al. (2011) produced the first sequences of a life history involving the alternation of two
Blastocladia, these sequences were shown to be developmentally associated phases: a haploid
closely related to the sequences identified by gametophyte generation (which produces
Slapeta et al. (2005). These results are consis- gametes) and a diploid sporophyte generation
tent with the role of Blastocladia as an obli- (which produces asexual spores). Organisms in
gately fermenting saprobic species. Other which the vegetative features of gametophyte
studies have revealed blastoclads from the oxy- and sporophyte are very similar have an iso-
cline (region of lower oxygen concentration) of morphic alternation of generations, whereas
a deep lake in France (Lefèvre et al. 2007) and those in which the vegetative features of one
from the surface water of a tropical lake (Chen generation differ substantially from those of the
et al. 2008). New sequence data from Porter next have a heteromorphic alternation of gen-
et al. (2011) suggest that these two sequences erations. Sexual reproduction occurs when
are related to Blastocladiella. gametes produced from gametophytic thalli
undergo syngamy (fusion) to form diploid pla-
nozygotes that give rise to sporophytic thalli.
Sporophytic thalli carry out asexual reproduc-
III. Structure of Thallus tion through the formation of thin-walled zoos-
and Reproductive Characters porangia (which produce zoospores that renew
the sporophyte generation) and thick-walled
Thalli of blastoclads vary greatly in size, extent, resistant sporangia (which typically undergo
and position in relation to the substratum. Sim- meiosis and produce meiospores that renew
ple thalli may be monocentric (producing a sin- the gametophyte generation). In some publica-
gle reproductive body) or epibiotic (with the tions thin-walled zoosporangia and zoospores
reproductive body produced outside the substra- are referred to as mitosporangia and mitos-
tum). A tube from a young epibiotic thallus pores, respectively, whereas resistant sporangia
penetrates the substratum and branches distally are referred to as resting spores, resting spor-
to form an endobiotic system of smaller branch- angia, or meiosporangia and their products
ing tubes (rhizoids) that functions in the absorp- variously as meiospores, RS zoospores, or RS
tion of nutrients. The complex thalli of some planospores. The resistant sporangium has a
genera are mycelial (filamentous with tubular thick, pigmented outer wall that may be smooth
hyphae) and polycentric (produce multiple or ornamented with pits, punctae, or a complex
reproductive bodies). Blastoclad thalli generally series of ridges (Fig. 7.1c). At germination the
consist of a larger basal axis attached to the outer wall of the resistant sporangium cracks
substratum by rhizoids, which may exhibit open at undetermined points in some species,
determinate (limited growth) or indeterminate while in others it opens along a preformed
(unlimited growth) apical branching and growth. germination slit or a circumcissile lid. An elas-
The hyphae may be septate (with incomplete tic inner wall (also called the endosporangium)
septa having central and lateral perforations) or may swell and protrude through the outer wall
aseptate and coenocytic (without septa). Poly- at the time of germination. Discharge papillae
centric thalli in some parasites take the form of are dome-shaped protrusions of gelatinous
slender rhizoidal elements alternating with material that form temporary plugs in dis-
spindle-shaped swellings (a rhizomycelium), charge pores or slits in the walls of zoosporan-
while in other parasites the thalli may be reduced gia, gametangia, and the inner wall of the
to unwalled coenocytic thalli (hyphal bodies) resistant sporangium. Upon dissolution of the
that lack rhizoids. Thalli lacking rhizoids that plug the spores pass through the pore or slit to
are completely converted into reproductive the outside. Species producing gametangia on a
single thallus whose nuclei are self-compatible affinities to Scherffel’s uniflagellate “Chytridin-
are said to be homothallic, whereas those pro- een” series of fungi (Scherffel 1925). This con-
ducing gametangia on different thalli whose cept was followed by Sparrow in his
nuclei are self-incompatible but cross- monographic treatments in 1943 and 1960.
compatible are heterothallic. Morphologically Sparrow regarded the posteriorly uniflagellate
distinct male and female gametangia or Chytridiales, Blastocladiales, and Monoble-
gametes occur in both homothallic and hetero- pharidales as one of four lines of descent
thallic species and may be distinguished by among the aquatic fungi and erected the class
differences in size, color, and mating behavior. Chytridiomycetes into which they were trans-
The alternative forms of physiologically distin- ferred (Sparrow 1960).
guishable (but morphologically indistinguish- Since the onset of molecular phylogenetic-
able) heterothallic species are designated as based systematics, numerous studies have
plus (+) and minus (–) mating types. Sexual investigated the phylogenetic placement of the
reproduction by fusion of flagellated gametes blastoclads in the fungal tree of life. Currently,
that are equal in size is referred to as isogamy, the placement is disputed and ranges from
while fusion of flagellated gametes that are being sister to the Chytridiomycota to being
unequal in size is anisogamy. With reference related to terrestrial zygomycete fungi
to animal systems, the smaller gamete is desig- (Fig. 7.2). The implications for the placement
nated as male while the larger is female. of the group within the fungal kingdom are
important for understanding the traits of the
most recent common ancestor of all fungi and
IV. Phylogeny and Systematics of evolutionary trends in life cycles. Recently,
Porter et al. (2011) produced the first compre-
A. Phylogenetic Placement hensive molecular phylogenetic study of genera
of Blastocladiomycota and families of blastoclads. The results of these
phylogenetic studies and additional ultrastruc-
The history of Blastocladiomycota began with tural studies led to the establishment of a new
the description of the first so-called chytrid phylum, the Blastocladiomycota (James et al.
genus, Physoderma, by Wallroth in 1833. In 2006b), with the single class Blastocladiomy-
1878, P. F. Reinsch described Blastocladia prin- cetes, into which were placed the genera
gheimii as the single member of a new genus included in Blastocladiales.
whose unusual features were puzzling to sys- The tool of choice for fungal molecular
tematists who included the organism variously phylogenetics has been nuclear-encoded ribo-
among the Saprolegniaceae (Fischer 1892) or somal DNA (rDNA) because this multicopy
the Leptomitaceae (Schroeter 1893). Petersen region contains both conserved and divergent
felt that these fungi differed substantially from regions capable of providing multiple levels of
the Saprolegniales and in 1909 established the phylogenetic resolution and is easy to amplify
order Blastocladiales containing the single fam- using conserved polymerase chain reaction pri-
ily Blastocladiaceae to accommodate the genus mers (Bruns et al. 1991). Early phylogenetic
Blastocladia (Petersen 1909), and a second studies of zoosporic fungi focused on ultra-
genus, Allomyces, was soon added to the family structural characters of the zoospore that have
(Butler 1911). Little additional knowledge of the been used to delimit the orders, families, and
group occurred until Kniep’s researches on genera; these studies suggested a good correla-
Allomyces (Kniep 1930), which resulted in the tion among ultrastructural characters and phy-
discovery of a life cycle with sporic meiosis logenetic relationships based on rDNA (James
and a new type of sexuality (anisogamy) previ- et al. 2000; Letcher et al. 2006, 2008; Simmons
ously unknown in the fungi. These findings et al. 2009). Subsequently, the rDNA operon
stimulated further research and quickly led to (18S+5.8S+28S) also provided a framework
a more refined concept of the Blastocladiales as for suggesting taxonomic revisions in the Blas-
a morphologically distinct group with greatest tocladiomycota (Porter et al. 2011).
a Basidiomycota
b
Basidiomycota
Ascomycota
Ascomycota
Glomeromycota
Kickxellomycotina
Nuclear genes
BLASTOCLADIOMYCOTA
Entomophthoromycotina
Mucoromycotina
Kickxellales + Zoopagales
+ Harpellales
Glomeromycota
Mucoromycotina
Monoblepharidales BLASTOCLADIOMYCOTA
Neocallimastigomycotina + Chytridiomycota
remaining Chytridiomycota
Choanoflagellida Microsporidia
c d
Mitochondrial genes
Basidiomycota Basidiomycota
Ascomycota Ascomycota
Mucoromycotina Mucoromycotina
BLASTOCLADIOMYCOTA Chytridiomycota
Chytridiomycota BLASTOCLADIOMYCOTA
Holozoa Holozoa
e
Basidiomycota
Ascomycota
Pan genomic sampling
Mucormycotina
Glomeromycota
Mucoromycotina
BLASTOCLADIOMYCOTA
Neocallimastigomycota
Chytridiomycota
Nucleariida
Fig. 7.2 Hypothesized phylogenetic placements of Blas- maximum likelihood (c) or a distance method (d). (e)
tocladiomycota among fungi. (a) James et al. (2000) Liu et al. (2009) with 150 concatenated proteins (40,925
with SSU rDNA analyzed using maximum parsimony. amino acids) analyzed using Bayesian inference and
(b) Liu et al. (2006) with RPB1+RPB2 concatenated maximum likelihood. Dashed lines: branches whose
protein sequences analyzed using Bayesian inference placement in phylogeny was not strongly supported
and maximum parsimony. (c, d) Lang et al. (2002) by bootstrap analyses (<70 %)
with 11 concatenated mtDNA proteins analyzed using
In many of the following cited studies, spe- been used with varying levels of success to clas-
cies in the Blastocladiales are still classified with sify the basal fungi. James et al. (2000) used small
the Chytridiomycota; however, in Fig. 7.2 they subunit (SSU) rDNA (18S rDNA) sequences to
are classified according to their present place- produce the first well-sampled phylogeny of zoo-
ment in Blastocladiomycota. Nuclear genes, sporic true fungi and addressed the phylogenetic
such as rDNA and protein-coding genes, have consistency of zoospore discharge type, thallus
development, and ultrastructural features of the the most recent classification of the Fungi (Hib-
zoospore (Fig. 7.2a). Three members of Blasto- bett et al. 2007). Currently, the International
cladiomycota were included in this study, and Committee on Botanical Nomenclature is con-
they clustered separate from the other Chytridio- sidering whether description of a phylum of the
mycota as sister to Entomophthoromycotina same name by Doweld (2001) meets standards
(zygomycetes); however, this placement was not for valid publication and has priority.
statistically supported. Another study used The Fungal Mitochondrial Genome
Bayesian inference of aligned amino acids from Sequencing Project has targeted several key
the RPB1+RPB2 (the two largest subunits of representatives of the basal fungal lineages
RNA polymerase II) nuclear protein coding (Paquin et al. 1997). In the most inclusive analy-
sequences from representatives of the major fun- sis, Lang et al. (2002) used maximum likelihood
gal lineages (Liu et al. 2006). They recovered high and neighbor-joining phylogenetic analyses with
Bayesian posterior probability but low maxi- 11 mitochondrial genes from representatives
mum parsimony bootstrap support for the clus- from the major fungal lineages. Depending on
tering of Blastocladiomycota as a sister group to the method and taxon set used for phylogenetic
the nonzoosporic fungi, i.e., Dikarya+zygomy- reconstruction, Blastocladiomycota branches
cetes (Fig. 7.2b). sister to either Dikarya+Mucoromycotina or
Altogether, a large number of studies have Chytridiomycota (Fig. 7.2c, d). In each case, the
included taxa from the Blastocladiomycota in statistical support for placement of Blastocladio-
phylogenies of the basal fungal lineages using a mycota is low, while support for the placement
variety of markers, such as SSU rDNA (Tanabe of other groups is quite high.
et al. 2000, 2005), RPB1 (Tanabe et al. 2004), With the increasing publication of fungal
complete mitochondrial sequences (Bullerwell genomes, it is now possible to include larger
et al. 2003; Lang et al. 2002), and elongation combinations of markers in phylogenetic ana-
factor subunit 1-alpha (EF1-a) indels (Tanabe lyses. Liu et al. (2009) used Bayesian inference
et al. 2002). Taking these results into account, and maximum likelihood phylogenetic analyses
Tanabe et al. (2005) proposed a new supraor- to target 150 nuclear protein-coding genes com-
dinal phylogeny with unresolved basal nodes prising 40,925 amino acids from representatives
and placement of Blastocladiomycota with of the major fungal lineages. The placement of
Entomophthoromycotina. A combined gene the Blastocladiomycota was sister to the non-
approach used maximum likelihood and Bayes- zoosporic fungi but with low statistical support
ian inference with the rDNA operon (SSU+5.8S (Fig. 7.2e). In conclusion, the ancient Blastocla-
+LSU rDNA)+EF1-a+RPBI+RPB2 for a rep- diomycota seem to be monophyletic in each of
resentative collection of fungal sequences the numerous phylogenetic studies. However,
(James et al. 2006a). The resulting phylogeny the precise placement of the lineage relative to
placed the blastoclads sister to nonzoosporic other phyla and subphyla of both zoosporic and
fungi. Altogether, studies using multiple com- nonzoosporic fungi is uncertain. In the future,
binations of phylogenetic markers have repeat- additional genome and large-scale expressed
edly found that the Blastocladiomycota are sequence tag (EST) sequencing of many more
monophyletic and usually group separately representatives of the basal fungal lineages will
from other lineages of zoosporic fungi. be needed to resolve the question of when the
Until 2006, the blastoclads were treated as an blastoclads diverged among the fungi.
order (Blastocladiales) in Chytridiomycota. The
distinctiveness of Blastocladiales from Chytri-
diomycota was formally addressed by James B. Phylogenetic Classification
et al. (2006b), who described Blastocladiales as of Blastocladiomycota
a separate phylum, Blastocladiomycota. This
was based on rDNA phylogenetic analysis and Blastoclads comprise 5 families (Blastocladia-
ultrastructural characters. Blastocladiomycota ceae, Catenariaceae, Coelomomycetaceae, Phy-
was also recognized as a separate phylum in sodermataceae and Sorochytriaceae), 14
rDNA operon clades and Blastocladiomycota

lineages (Porter et al., 2011) Families (Karling,1977)
Allomyces (13) +
Blastocladia (2) + Blastocladiaceae
Microallomyces (1)
Catenaria spinosa (3)
Catenariaceae
Catenaria s.s. (7) +
Catenophlyctis (1)
Blastocladiella (3) +
Blastocladiella emersonii (1) Blastocladiaceae
Coelomomyces (4) + Coelomomycetaceae

Coelomycidium (2)
Physoderma (4) +
Urophlyctis (3) Physodermataceae
Paraphysoderma sedebokerense (1)

50 changes
Fig. 7.3 Schematic phylogeny of Blastocladiomycota Numbers following generic names: number of
based on rRNA operon sequences (Porter et al. 2011) sequences included
with taxonomic classifications from Karling (1977).
genera, and approximately 180 species. It is of thallus organization. Allomyces is the only
likely that many additional species, genera, genus that displays truly indeterminate growth
and higher taxa remain to be discovered and as a mycelium with septa, and Microallomyces
described. Figure 7.3 summarizes the results is similar to Allomyces but smaller in stature
from a Bayesian rDNA (SSU+5.8S+LSU) phy- and lacking pseudosepta. Members of Blasto-
logeny, including 45 gene sequences from the cladia typically have a single trunklike basal
Blastocladiomycota representing 4 of the 5 cell, with septations only at reproductive
families (Porter et al. 2011). Here we review organs. The poorly known Blastocladiopsis is
the phylogenetic placement of the various distinguished from Blastocladia on the basis of
families, the evidence of monophyly of genera, an unpitted, loose resting sporangium. In
and the morphological characters that separate Fig. 7.3, strains from Allomyces, Blastocladia,
the various genera. and Microallomyces form a clade, three strains
The Blastocladiaceae Petersen 1909 cur- of Blastocladiella and Blastocladiella emersonii
rently comprises five genera: Allomyces Butler Cantino and Hyatt 1953 cluster separately, and
1911, Blastocladia, Microallomyces Emerson the genus Blastocladiopsis has yet to be placed
and Robertson 1974, Blastocladiella Matthews in a molecular phylogeny. Though Allomyces
1937, and Blastocladiopsis Sparrow 1950 (Kar- forms a clade, Porter et al. (2011) showed that
ling 1977). Genera can be separated on the basis these taxa do not necessarily group according
to current subgenera defined by life cycle char- Kirk et al. 2008). Physoderma includes some
acteristics (Emerson 1938, 1941). Instead, Por- 80 or more species that are obligate parasites
ter et al. recovered two major Allomyces clades of plants whose effects on stems, leaves, and
with multiple strains of the type species A. inflorescences may vary from simple discolor-
arbusculus found in each. The only subgenus ation to significant hypertrophy. Those species
that formed a clade was Cystogenes, whereas the that were known to induce gall formation in the
subgenera Euallomyces and Brachyallomyces host were segregated into Urophlyctis (Sparrow
were recovered as paraphyletic. 1962). The synonymy of Physoderma and
Catenariaceae can be distinguished from Urophlyctis has been debated (Karling 1977;
Blastocladiaceae by the presence of a catenulate Sparrow 1962), but Urophlyctis differs from
(chainlike) rhizomycelium with swellings or Physoderma in several microscopic characters
sporangia separated by narrow isthmuses. The as well as in inducing gall formation in its host.
Catenariaceae Couch 1945 currently comprises Lange and Olson (1980) studied the ultrastruc-
three genera: Catenaria Sorokin 1889, Cate- ture of motile cells of Physoderma and trans-
nophlyctis Karling 1965, and Catenomyces ferred the family Physodermataceae to
A.M. c 1944 (Karling 1965). Catenophlyctis is Blastocladiales from Chytridiales. Physoderma
distinguished from Catenaria by having a more and Urophlyctis are closely related (Fig. 7.3),
chytridlike monocentric growth form, though and Porter et al. (2011) showed that Urophlyctis
some isolates of the former are highly polycen- is nested within Physoderma, which together
tric. In Fig. 7.3 Catenaria and Catenophlyctis form a monophyletic clade. Additional sam-
form a clade that includes the type species of pling of taxa and markers/loci will be required
Catenaria, Catenaria anguillulae Sorokin 1876. to determine whether Urophlyctis and all gall-
The sole isolate of Catenophlyctis groups inducing species are monophyletic. A newly
among Catenaria, suggesting the distinction of described genus, Paraphysoderma, is only
the genera is likely artificial. Catenomyces, cur- known as a parasite of the Chlorophycean alga
rently classified in the Catenariaceae, however, Haematococcus. It clusters sister to Physo-
clusters with Chytridiomycota (James et al. derma+Urophlyctis (Hoffman et al. 2008;
2006b). Two additional strains of Catenaria James et al. 2011). Paraphysoderma is further
isolated from midge larvae, Catenaria spinosa distinguished by producing nonflagellated
and Catenaria uncinata, form a separate clade, aplanospores rather than zoospores.
suggesting that Catenaria is polyphyletic (Mar- Sorochytriaceae (Dewel et al. 1985) currently
tin 1975, 1978; Porter et al. 2011). contains a single species, Sorochytrium milne-
Coelomomycetaceae Couch ex Couch 1962 siophthora, which grows endobiotically within
currently comprises two invertebrate patho- the tardigrade host and typically forms a poly-
genic genera, Coelomomyces Keilin 1921 and centric rhizomycelium. The species has yet to be
Coelomycidium Debais 1919. Both genera placed in a molecular phylogeny; however, a
grow inside their hosts in the form of naked study of the ultrastructure of the zoospores of S.
protoplasts. Coelomomyces is distinguished milnesiophthora clearly places the family with
from Coelomycidium on the basis of hosts, Blastocladiales (Dewel and Dewel 1990).
mosquitoes, and ostracods or copepods in the
former and blackflies in the latter. In Fig. 7.3
Coelomomyces and Coelomycidium are The time-consuming nature and specialist knowledge
reciprocally monophyletic sister clades. required to collect and identify new isolates means that
many described members of Blastocladiomycota, par-
Physodermataceae Sparrow 1952 comprises ticularly pathogenic species, have yet to be sequenced
two plant pathogenic genera, Physoderma and placed in a molecular phylogeny, echoing a com-
Wallr. 1833 and Urophlyctis J. Schrot. 1886. mon pattern in science (Hibbett et al. 2007). Several
Both genera form an epibiotic, monocentric, additional organisms have been described in recent
sporangial stage and an endobiotic, polycentric years whose affinities are clearly with the blastoclads
but whose life cycles or development are incompletely
phase. These two genera were synonymized known or understood. These include Polycaryum laeve,
(Karling 1950) and are generally still consid- an endoparasite of Daphnia previously considered a
ered synonymous to this day (Karling 1977; haplosporidian. Phylogenetic evidence was used to
affiliate Polycaryum with blastoclads, but only a partial include isolates in which the gametophyte thallus
sequence is available, precluding more precise place- is reduced to a single-celled cyst). Since that time,
ment (Johnson et al. 2006). An effort to collect and
place type species in a molecular phylogeny would
new members of the Blastocladiomycota have
help to catalog the phylogenetic diversity in Blastocla- been interpreted and described in relation to
diomycota and provide a framework for further ecolog- the life cycles of Allomyces, and this practice is
ical studies. Mention should also be made of reflected in much of the present classification. To
Callimastix cyclopis, a parasite of the copepod Cyclops understand the diversity of life histories now
whose zoospore structure most resembles that of Coe-
lomomyces (Vavra and Joyon 1966).
known for the blastoclads, it is necessary to
review in some detail earlier research on the
sexuality and life cycles of Allomyces.
V. Life Cycles B. Life Cycles of Allomyces
A. Historical Perspective
Euallomyces The subgenus Euallomyces includes
By the early twentieth century the concept of an long-cycled Allomyces species such as A. javanicus
alternation of haploid and diploid generations and A. arbuscula in which the vegetative thalli of
in the life histories of lower plants and major both gametophyte and sporophyte generations are
algal groups was firmly established. However, the same in appearance (an isomorphic alternation
the discovery by Kniep of an alternation of of generations). The life history of A. arbuscula
sporophyte and gametophyte generations in a (Emerson 1941; Hatch 1935) is shown in Fig. 7.4.
new zoosporic fungus (A. javanicus) was unex- A simplified diagram of the Euallomyces life cycle is
pected and aroused great interest in the myco- presented in Fig. 7.6c. In these species the homo-
logical community (Kniep 1930). Kniep thallic gametophyte generation bears gametangia
established ploidy in the new fungus by that are typically paired and sexually dimorphic
reported nuclear volume ratios of 1:2 between with smaller orange male and larger colorless
gametophyte and sporophyte, and Emerson female gametangia. Smaller, more active orange
and Wilson (1949) and Wilson (1952) provided gametes released from male gametangia undergo
the cytological proof of “sporic” meiosis in the anisogamous fusion with larger colorless gametes
resistant sporangium. These studies, along with from female gametangia to produce biflagellate
the later electron microscopic observations, planozygotes that give rise to the diploid sporo-
confirmed that meiosis in A. macrogynus
phyte generation. Sporophytes produce a mixture
begins during early resistant sporangium for-
of thin-walled zoosporangia and thick-walled,
mation with the appearance of a synaptonemal
brown, pitted, resistant sporangia. Zoospores
complex, is halted as the resistant sporangium
from zoosporangia give rise asexually to additional
enters the resting phase in the late prophase
(diplotene) of meiosis I, and is completed dur- sporophytic thalli, and resistant sporangia undergo
ing germination (Olson 1974). meiosis and release haploid meiospores that pro-
Emerson’s 1941 monograph was a seminal duce the gametophyte generation. Deviations from
work detailing the results of a 6-year study these so-called normal patterns have been observed
involving the comparative development of 51 frequently, including the parthenogenetic develop-
Allomyces isolates from around the world (Emer- ment of both gametophyte and sporophyte thalli
son 1941). In this work Emerson recognized from single (nonfusing) female gametes and the
three life cycle types that formed the basis of his development of sporophytic thalli from meiospores
classification of the genus into three subgenera: (Emerson 1941).
Euallomyces (to include so-called long-cycled
species in which there is an isomorphic alterna- Cystogenes Emerson (1938, 1941) and Wilson
tion of generations), Brachyallomyces (to include (1952) described a very different type of life cycle
so-called short-cycled isolates in which there is in A. moniliformis and A. neo-moniliformis (¼A.
no indication of sexuality), and Cystogenes (to cystogenus) (Emerson 1941), a heteromorphic
Fig. 7.4 (a–m) Life cycle of Allomyces arbuscula. (a) encysted planozygote. (j, k) Young thallus (j) develops
Germinating resistant sporangium with ruptured outer into mature sporophytic thallus (k) bearing resistant
wall and swollen inner wall with discharge papilla. (b) sporangia (R) and thin-walled zoosporangia (Z). (l)
Release of uniflagellate meiospores. (c–e) Stages in Release of zoospores from thin-walled zoosporangia.
growth of young thallus (c, d) into mature gameto- (m) Germination of encysted zoospore to form young
phytic thallus bearing papillate male () and female () thallus (j). Drawing from Emerson (1941), used with
gametangia (e). (f) Release of male and female gametes permission from Lloyd Library and Museum; American
from paired gametangia. (g) Syngamy of anisogametes. Society of Pharmacognosy
(h) Biflagellate planozygote. (i) Germination of
alternation of generations in which the gameto- mitotic division to produce four haploid cells (iso-
phyte thallus is reduced to a single-celled cyst gametes) that exit upon deliquescence of the single
(Figs. 7.5 and 7.6d). The sporophytic thalli of papilla. The fate of the quartet of cells emerging
Cystogenes species are like those of Euallomyces from the cyst was unknown to Emerson; however,
in structure and size, and meiosis takes place in the the cells were shown to function as uniflagellate or
resistant sporangium (Emerson and Wilson 1949; aflagellate amoeboid isogametes that fuse to form
Olson 1980; Wilson 1952). However, in Cystogenes zygotes (McCrainie 1942; Teter 1944).
isolates meiosis is followed by a pairing of haploid
nuclei prior to cleavage into spores. Meiospores Brachyallomyces Isolates in which the motile
exit the resistant sporangium as binucleate cells spores from the resistant sporangia regularly gave
that move sluggishly as biflagellate motile cells or rise to asexual (sporophytic) rather than sexual
as nonflagellated amoeboid cells before rapid (gametophytic) thalli were placed in a new species,
encystment. The two cyst nuclei undergo a single A. anomalus, and included in the subgenus
Fig. 7.5 (a–m) Life cycle of Allomyces neo-monilifor- tion of encysted zygotes. (j, k) Young thallus (j) devel-
mis. (a) Germinating resistant sporangium with rup- ops into mature sporophytic thallus (k) bearing
tured outer wall and swollen inner wall with two resistant sporangia (R) and thin-walled zoosporangia
discharge papillae. (b) Beginning of meiospore release. (Z). (l) Release of zoospores from thin-walled zoospor-
(c) Biflagellate meiospores exiting resistant sporan- angia. (m) Germination of encysted zoospore to form
gium; some have encysted. (d) Cysts, each with single young thallus (j). Drawing from Emerson (1941), used
papilla, clustered at mouth of empty resistant sporan- with permission from Lloyd Library and Museum;
gium. (e–h) Stages in emergence of uniflagellate American Society of Pharmacognosy
gametes from cysts; syngamy not shown. (i) Germina-
Brachyallomyces (Emerson 1941). Emerson found diploid condition (Fig. 7.6f) (Wilson and Flanagan
that by varying the substrate he could induce some 1968). The sporophytic thalli of A. anomalus iso-
putative Brachyallomyces isolates to form gameto- lates are entirely like those of Euallomyces species
phytes, and he was careful to ascribe only those but lack a sexual stage.
isolates that remained consistently asexual to the
subgenus. It was later revealed that asexuality was
maintained by mitosis in the resistant sporangia of C. Life Cycles of Other Blastocladiomycota
some A. anomalus isolates (Fig. 7.6e), while in
other isolates meiosis was presumably followed In the 70 years since the publication of Emer-
by endomitosis (nuclear replication without divi- son’s monograph on Allomyces, many new blas-
sion) in germinating meiospores to reestablish the toclads have been discovered, and the diversity
d
190
a Meiosis
b Meiosis
c Meiosis Meiosis
Meiospores Meiospores
♂/+ ♀/- ♂/+ ♀/- (binucleate)
Meiospores Meiospores Meiospores Meiospores Eucarpic, Mycelial
Gametophyte
Eucarpic, Monocentric Eucarpic, Monocentric Holocarpic, Monocentric Holocarpic, Monocentric Holocarpic, Monocentric
Gametophyte Gametophyte Gametophyte Gametophyte (Cyst) Gametophyte
Gametangium Gametangium Gametangium Gametangium ♂ ♀

Gametangium Gametangium
Gametes Gametes Gametes Gametes (+) (-)
Gametes Gametes Gametes Gametes
Syngamy Syngamy
Syngamy Syngamy
Planozygotes Planozygotes Planozygotes

Planozygotes Planozygotes
Eucarpic, Monocentric Eucarpic, Monocentric
Holocarpic, Mycelial Eucarpic, Mycelial Eucarpic, Mycelial
Sporophyte Sporophyte
Sporophyte Sporophyte Zoospores Sporophyte Zoospores
Zoospores
Resistant Resistant Resistant Resistant
Zoosporangium Zoosporangium Zoosporangium
Sporangium Sporangium Sporangium Sporangium
e f g
Mitosis Meiosis Meiosis
T.Y. James et al.
Zoospores Meiospores Meiospores
Endomitosis
Eucarpic, Mycelial
Eucarpic, Mycelial Gametophyte Zoospores
Sporophyte Zoospores Eucarpic, Mycelial
Sporophyte Zoospores
Resistant Resistant Resistant

Zoosporangium Zoosporangium Endomitosis Zoosporangium
Sporangium Sporangium Sporangium
Fig. 7.6 Diagrams illustrating life cycles and patterns of sexuality in selected sporophyte produces RS and TWZ; Allomyces neo-moniliformis. (e) Asexual
members of Blastocladiomycota. RS, resistant sporangia, TWZ, thin-walled zoospores give rise directly by mitosis to sporophytes bearing RS and TWZ;
zoosporangia. (a) Isomorphic alternation of generations, gametophytes het- some Allomyces anomalus. (f) Meiospores resulting from meiosis in RS
erothallic with isogamy, separate sporophytes bear RS or TWZ; Blastocladiella undergo endomitosis at germination to form sporophytes; sporophyte pro-
variabilis. (b) Isomorphic alternation of generations, gametophytes heterothal- duces RS and TWZ; some A. anomalus. (g) Meiospores resulting from meiosis
lic with isogamy, sporophyte bearing RS only; Coelomomyces punctatus. (c) in RS give rise to gametophytes bearing TWZ and young RS; endomitosis or
Isomorphic alternation of generations, gametophyte homothallic with anisog- selfing in early RS development restores diploid condition; Catenaria anguil-
amy, sporophyte with RS and TWZ; Allomyces arbusculus. (d) Heteromorphic lulae
alternation of generations, gametophyte a monocentric cyst with isogamy,
of life cycle types has increased. The Euallo- (Cantino 1956) and in B. brittanica in response
myces life cycle of Allomyces (Fig. 7.6c) has an to darkness (Horenstein and Cantino 1962).
isomorphic alternation of generations with The life cycle of the Coelomomyces species
homothallic mating of morphologically distinct that have been thoroughly studied is that of an
male and female gametes. Anisogamy has been isomorphic alternation of generations involving
reported only in Euallomyces species. Homo- heterothallic mating of isogametes (Fig. 7.6b).
thallism of the type displayed by Allomyces has While this heteroecious life cycle is classified as
not been reported in other isomorphic genera, isomorphic, the gametophytic thalli in crusta-
but such a pattern may have existed in Paleo- cean hosts are smaller and with fewer branches
blastocladia milleri (Remy et al. 1994), a fossil than sporophytic thalli in dipteran hosts. Some
blastoclad from the 400 million-year-old Rhynie species of Coelomomyces have strikingly dimor-
chert. In addition to sporophytic thalli bearing phic gametangia, with the male mating type
zoosporangia and resistant sporangia there are bright orange and the female amber or colorless.
similar (gametophytic?) thalli bearing paired In other species the+and – gametangia have
cells that resemble rather remarkably the game- similar pigmentation or are colorless. The
tangia of A. arbuscula. thin-walled zoosporangia produced in some
The Cystogenes life cycle of Allomyces Coelomomyces species do not seem to be homol-
(Fig. 7.6d) is a heteromorphic alternation of ogous to the thin-walled zoosporangia of other
generations with homothallic mating of isoga- blastoclads as they are structurally similar to
metes. This pattern has been reported in spe- resistant sporangia and, like them, produce
cies of Blastocladiella (subgenus Cystocladiella) meiospores rather than zoospores.
and in the mycoparasite Catenaria allomycis.
However, the life cycle of these fungi differs Physoderma species reported to be heterothallic have a
slightly from that of Cystogenes in producing life cycle similar to that of Coelomomyces, with notable
exceptions. In Physoderma there is a heteromorphic
uninucleate and uniflagellate meiospores that alternation of generations owing to significant differ-
undergo two mitotic divisions prior to gamete ences in the size and structure of the monocentric and
formation. epibiotic gametophyte thalli and the polycentric and
An asexual or Brachyallomyces life cycle endobiotic sporophyte thalli. In some species of Physo-
seems to be widespread in many blastoclad derma the epibiotic thalli are reported to mature into
gametangia that produce isogametes or zoosporangia
genera, particularly those of the Blastocladia- whose zoospores form additional epibiotic thalli. As in
ceae. The types represented by mitosis in the Coelomomyces, gametangia may be distinguished as
resistant sporangium (Fig. 7.6e) and by meiosis orange or crimson males and colorless females in
followed by diploidization by endomitosis in reportedly heterothallic species (Karling 1977).
germinating meiospores (Fig. 7.6f) have been
reported only for A. anomalus isolates. A third Blastocladiella is similar to Allomyces but is
asexual pattern (Fig. 7.6g) has been reported in monocentric and thus may produce only spor-
C. anguillulae (Olson and Reichle 1978a), and a angia or gametangia at any given phase of the
modification of this pattern is likely present in life cycle. Karling (1977) noted the similarity
B. emersonii (Olson and Reichle 1978b). In both between the life cycles of Blastocladiella and
organisms synaptonemal complexes and meiotic Allomyces and erected subgenera of Blastocla-
divisions are present during resistant sporan- diella corresponding to those of Allomyces:
gium formation and germination; however, Eucladiella (corresponding to Emerson’s Eual-
both meiospores and zoospores are reported to lomyces), in which there is an isomorphic alter-
be haploid. Induction of diploidization and nation of generations, Cystocladiella
resistant sporangium formation in C. anguillu- (corresponding to Cystogenes), in which the
lae occurred when the haploid zoosporangial gametophyte generation is a single-celled cyst,
thalli were transferred from a nutrient medium and Blastocladiella (corresponding to Brachyal-
lacking starch to one containing it. A similar lomyces), for short-cycled or asexual forms. The
transformation of zoosporangia into resistant sporophyte generation of Blastocladiella gener-
sporangia occurred in B. emersonii when bicar- ally consists of separate thalli bearing zoospor-
bonate and other salts were added to media angia or resistant sporangia, although in some
species zoosporangial thalli are lacking. In spe- (one bearing zoosporangia and the other
cies of Eucladiella the gametophyte generation bearing resistant sporangia) (Harder and Sörgel
consists of separate but equal-sized male and 1938).
female thalli. While the life cycles of Cystocla-
diella species such as B. cystogena are similar to
those of Cystogenes, they differ in that they lack VI. Zoospore Ultrastructure
thin-walled zoosporangia (they produce thalli
bearing resistant sporangia only) and produce A. Historical Perspective
cells from resistant sporangia that are uniflagel-
late and uninucleate rather than biflagellate and In 1896 Thaxter examined the zoospores of B.
binucleate. The subgenus Blastocladiella pringsheimii and noted the posterior cilium and
includes short-cycled species such as B. simplex the broad and distinct mass of granular proto-
(Matthews 1937), B. britannica (Willoughby plasm in front of the large and subtriangular
1959), and B. emersonii (Cantino and Hyatt nucleus (Fig. 7.1a). Couch and Whiffen (1942)
1953), in which no sexual reproduction has provided excellent illustrations of the zoos-
been reported. Although much has been pores and meiospores of Blastocladiella cysto-
learned about the physiology of B. emersonii, gena and rather prophetically stated, “This cap
questions remain about its sexuality and life is undoubtedly of phylogenetic importance,”
cycle. Even though flagellated swarmers from and noted that such a structure had been
orange and colorless (OC) cells were never reported previously in Coelomycidium simulii
observed to undergo karyogamy, they were (Debaisieux 1920). Subsequently, the discovery
reported to undergo plasmogamy and cytoplas- of a new zoosporic fungus with posteriorly uni-
mic exchange (Cantino and Horenstein 1954). flagellate cells with a nuclear cap of the Blasto-
Investigators have generally agreed that B. cladia type became regarded as clear evidence
emersonii has a Brachyallomyces (or subgenus of a relationship to the Blastocladiales.
Blastocladiella) type of life cycle. Olson and Zoospores of the Chytridiales and Blasto-
Reichle (1978) found synaptonemal complexes cladiales were among the earliest biological spe-
and meiotic nuclear divisions in germinating B. cimens to be examined with the electron
emersonii-resistant sporangia, and Horgen microscope (Manton et al. 1952; Koch 1956).
et al. (1985) studied the fluorescence of As new zoosporic fungi were discovered and
mithramycin-stained nuclei and determined the extent of variation in their vegetative and
that meiospores contained half the DNA of reproductive structures became known, the
zoospores of ordinary colorless cells (thin- validity of morphology as revealed by light
walled zoosporangia). The life cycle of B. emer- microscopy for taxonomic distinctions was
sonii is most similar to the Brachyallomyces questioned (Powell and Koch 1977a, b). Begin-
pattern in which meiosis is present (Fig. 7.6f). ning in the 1960s detailed ultrastructural stud-
The life cycle of Blastocladiella variabilis ies of the motile cells of various chytrid and
(Fig. 7.6a) is worthy of note because it perhaps blastoclad genera were conducted in search of
has the greatest potential for development as a additional characters of taxonomic and phylo-
model genetic system among the flagellated genetic value. These studies revealed the iden-
fungi. Like Coelomomyces and Physoderma, its tities of organelles previously observed with the
life cycle is an isomorphic alternation of genera- light microscope and demonstrated new cyto-
tions with heterothallic mating. However, in plasmic similarities and differences among
Blastocladiella the thalli of both gametophyte blastoclad genera. The nuclear cap was
and sporophyte generations are monocentric, observed to be a membrane-bound cluster of
epibiotic, and, thus, separate. Four distinct ribosomes at the tip of a linear axial assembly
reproductive structures are produced on sepa- found in all members of Blastocladiales. The
rate thalli in B. variabilis: two distinct heterothal- side body (or Seitenkörper) of earlier studies
lic gametangia (one with reddish male was seen to be a mitochondrion and a compo-
gametangia and the other with colorless female nent of a side body complex also found in all
gametangia) and two distinct sporophytic thalli members of Blastocladiales.
a b
G
N
B
N
M
Nkc
K
M
P R Mb
K
Fig. 7.7 (a, b) Blastocladiella emersonii. Interpretive lus; Nc nuclear cap; F flagellum; K functional kineto-
drawings of zoospore showing ultrastructural details some, Nkc nonkinetosomal centriole, P prop, R
based primarily on several studies (Cantino and Trues- rhizoplast, M mitochondrion, Mb microbody, L lipid
dell 1970; Lessie and Lovett 1968; Reichle and Fuller globule, B backing membrane, G gamma body, T cyto-
1967; Shaw and Cantino 1969). (a) Median longitudinal plasmic microtubule, V vacuole, open arrow, amor-
section through zoospore. (b) Detail of kinetosomal phous perikinetosomal material
region and side body complex. N nucleus; Nu nucleo-
B. Generalized Structure of Motile Cells in distinguishing major clades, subclades, and

of Blastocladiomycota component genera.
Surveys of ultrastructural characters in motile

cells of the Chytridiomycetes have found four 1. Axial Assembly
basic patterns of side body complexes or micro-
The remarkable homogeneity of the nucleus,
body–lipid globule complexes (MLCs)
nuclear cap, and associated structures is
corresponding to the various orders of posteri-
revealed in drawings and photographs of motile
orly uniflagellate fungi (Lange and Olson 1979;
cells of representatives of major clades of Blas-
Powell 1978). The MLC of the Blastocladiales
tocladiomycota, including a zoospore of B.
(type 4) was distinguished as an ordered
emersonii (Fig. 7.7a, b), a zoospore of Allomyces
arrangement of one or more mitochondria,
macrogynus (Fig. 7.8a, b), a meiospore of Coe-
microbodies, and lipid globules located along
lomomyces punctatus (Fig. 7.9), and a meios-
one side of an axially arranged nucleus and
pore of Physoderma maydis (Fig. 7.10). The
nuclear cap and enclosed by a backing mem-
flagellated cells of all known members of Blas-
brane. Molecular phylogenetic studies provided
tocladiomycota are characterized by a linear
most of the evidence by which Blastocladiales
arrangement of organelles (axial assembly)
was raised to phylum status (James et al.
consisting of a posterior flagellum with
2006b); however, the formal description of phy-
contained axoneme, functional kinetosome,
lum Blastocladiomycota was based largely on
nucleus with contained nucleolus, and anterior
ultrastructural details. In the following account
nuclear cap. The flagellum has the nine-plus-
ultrastructural characters defining the phylum
two arrangement typical of microtubules and
are discussed along with characters believed to
narrows distally to a short whiplash portion. At
be of systematic and phylogenetic importance
the point where the flagellum joins the spore
Fig. 7.8 (a, b) Allomyces macrogynus. Interpretive cap, Ns nuclear spur, K functional kinetosome, Nkc
drawings of the zoospore showing ultrastructural nonkinetosomal centriole, P prop, R rhizoplast, M
details based primarily on two studies (Fuller and mitochondrion, Mb microbodies, L lipid globule, B
Olson 1971; Hill 1969). (a) Median longitudinal section backing membrane, T cytoplasmic microtubule, V vac-
through zoospore. (b) Detail of kinetosomal region and uole, open arrow amorphous perikinetosomal material
side body complex. N nucleus, Nu nucleolus, Nc nuclear
body, nine electron-dense props extend inward semicircle of amorphous material immediately
to the axoneme or kinetosome. In all genera below the organizing center is part of a flagellar
except Coelomomyces a nonkinetosomal cen- apparatus that connects with the mitochon-
triole is present alongside the nucleus and is drion. The nuclear cap is composed of a dense
attached to the functional kinetosome by an cluster of dormant 80S ribosomes surrounded
electron-opaque bridge. A cap of electron- by double membranes, the outermost of which
dense amorphous material surrounds the top is continuous with the nuclear membrane
of the functional kinetosome and extends down (Jaworski and Stumhofer 1984).
along the sides of the cartwheel region. In all
genera cytoplasmic microtubules arise from the
2. Microbody–Lipid Globule Complex
amorphous material at the extreme proximal
end of the functional kinetosome and pass up Powell (1978) separated the type 4 MLC of
and around the periphery of the nucleus and Blastocladiomycota into two subtypes. Subtype
nuclear cap and into the cytoplasm (Figs. 7.7, 4A contains a single large mitochondrion that
7.8, 7.9, and 7.10). It has been suggested that extends primarily along one side of the nucleus
this area is a so-called organizing center for and nuclear cap and includes motile cells of B.
kinetosome-related microtubule formation emersonii (Fig. 7.7a, b), C. punctatus (Fig. 7.9),
(Dewel and Dewel 1990; Fuller and Calhoun and P. maydis (Fig. 7.10). In B. emersonii and C.
1968). In cross sections distal to the kinetosome punctatus a cluster of lipid globules is located
the cytoplasmic microtubules typically occur in external to the long side of the mitochondrion
nine groups of three (triplets). The conical and internal to a microbody, which is distended
shape of the nucleus and nuclear cap is thought or completely penetrated by the rounded lipid
to be maintained by this basketlike arrange- globules. MLC subtype 4B occurs in motile cells
ment of cytoplasmic microtubules. The ring or of A. macrogynus (Fig. 7.8a, b) and Allomyces
Vms
Gl
T
T
L
B Pb
Nc
L
Mb Av
V
N
V
M
Nu
M
K
N
Vms
P
F Nkc
Fig. 7.9 Coelomomyces punctatus. Interpretive draw- K

ing of median longitudinal section through meios- F
pore showing ultrastructural details based primarily
on Martin (1971). Av adhesion vesicle, B backing
membrane (contrasted with microbody to show tubu- Fig. 7.10 Physoderma maydis. Interpretive drawing of
lar network), Glgammalike body, K functional kinet- median longitudinal section through meiospore
osome, L lipid globule, M mitochondrion, Mb showing ultrastructural details based primarily on
microbody, N nucleus, Nc nuclear cap, P prop, F Olson and Lange (1978) and Lange and Olson (1980).
flagellum, Pb paracrystalline body, T cytoplasmic F flagellum, K functional kinetosome, L lipid globule, M
microtubule, V vacuole, open arrow perikinetosomal mitochondrion, N nucleus, Nc nuclear cap, Nkc nonki-
striations netosomal centriole, Nu nucleolus, T cytoplasmic
microtubule, V vacuole, Vms vesicular–microbody sys-
tem, open arrow perikinetosomal striations
neo-moniliformis (Fuller and Olson 1971;
Olson 1980) and is unlike other blastocladian
genera in having components that are highly contain multiple mitochondria but lack an
divided and less closely associated. Numerous organized MLC (Lingle and Barstow 1983).
rounded mitochondria are present in zoospores The outermost component of the MLC in sub-
of A. macrogynus, and many are partially types 4A and 4B is a backing membrane that is
embedded in the nuclear cap. A larger cup- usually continuous at several points with the
shaped mitochondrion partially surrounds the outer membrane of the nuclear cap. The motile
functional kinetosome and is the main compo- cells of P. maydis have a modified subtype 4A
nent of a reduced and poorly organized MLC MLC in which the number of lipid globules may
that contains several microbodies, a small num- be reduced to one, and a vesicular-microbody
ber of lipid globules, and additional mitochon- system is present in place of a discrete backing
dria. Motile cells of Blastocladia ramosa membrane and microbody.
3. Flagellar Apparatus 4. Cytoplasmic Inclusions

In all members of the phylum there is a close A variety of inclusions have been reported in
association between the functional kinetosome the cytoplasm of various blastoclad motile cells,
and a completely or partially encircling mito- including concentric granules, vacuoles, adhe-
chondrion. The flagellar apparatus consists of sion vesicles, phosphate granules, gammalike
perikinetosomal structures (striations, rhizo- bodies, gamma bodies or granules, and para-
plasts, and fibrils) that appear to form connec- crystalline bodies. Inclusions that appear
tions between the functional kinetosome and homologous or analogous to gamma bodies or
mitochondrion. In motile cells of Sorochytrium gammalike bodies have been found in motile
milnesiopthora (Dewel and Dewel 1990), P. cells of all blastocladian genera. Gamma bodies
maydis (Lange and Olson 1980), and C. puncta- of B. emersonii are formed during zoosporo-
tus (Martin 1971) the amorphous band of mate- genesis by the coalescence of small granule-
rial surrounding the cartwheel portion of containing cisternae to form larger cisternae
functional kinetosome may be partially with many distinct granules (gammalike bod-
resolved in cross sections as a complete or ies) and a final aggregation stage that results in
partial circle of discrete electron-dense projec- a distinctive cup-shaped inclusion (Barstow
tions. In longitudinal sections the projections and Lovett 1975; Cantino and Truesdell 1971;
often appear as discrete striations, each a com- Lessie and Lovett 1968; Lovett 1975; Mills and
ponent of an inner electron-dense band and Cantino 1979). Mobilization or breakdown of
one or more outer diffuse bands (Figs. 7.7 and gamma bodies typically occurs shortly after the
7.8, open arrows). Thin fibrils are often beginning of zoospore encystment and results
observed connecting the inner and outer peri- in the vesiculation of the contents and the
kinetosomal striations and fanning out to con- translocation of vesicles to the cell surface.
nect with the surface of a mitochondrion or a Gamma bodies were once thought to function
membrane cisterna. Olson and Lange (1978) in the transport of chitin synthetase for cyst
referred to the striations as bridges, and pre- wall formation (Barstow and Pommerville
sumably they are homologous with the transi- 1980; Mills and Cantino 1981); however, later
tion fibers of Coelomomyces dodgei (Lucarotti studies failed to support this hypothesis (Dal-
and Federici 1984). The motile cells of A. ley and Sonneborn 1982; Hohn et al. 1984).
macrogynus (Fig. 7.8), A. neo-moniliformis Olson and Lange (1983) interpreted the
(Fuller and Olson 1971), B. emersonii gamma bodies in motile spores of Allomyces
(Fig. 7.7), Blastocladiella brittanica (Cantino as vesicle-generating structures that performed
and Truesdell 1971), and C. anguillulae (Olson multiple functions upon mobilization or break-
et al. 1978) contain a rhizoplast (also called a down, including (1) the formation of water-
striated or banded rootlet). The rhizoplast is a expulsion vacuoles to maintain osmotic bal-
bar- or ribbon-shaped structure composed of a ance during zoospore motility, (2) production
lateral series of equally spaced striae that is of vesicles that fuse to form axonemal and
located laterally and in close proximity to the plasma membranes during sporogenesis, and
cartwheel portion of the functional kinetosome. (3) formation of vesicles that appear to be
Double membranes in the form of sheets or involved in cyst wall creation. The widespread
cisternae believed to originate from the outer occurrence of gamma bodies in the Blastocla-
nuclear or nuclear cap membrane are impor- diomycota prompted Dewel and Dewel (1990)
tant components of the flagellar apparatus in to suggest that the gamma body should be con-
many, if not all, blastoclad genera (Figs. 7.7b, sidered a synapomorphy of the phylum. Adhe-
7.8b, 7.9). Powell (1983) has suggested that such sion vesicles are present in motile cells of
cisternae may function in signal reception and Coelomomyces and are distinguished from
transport between the cell surface and the fla- gamma particles by their fine granular back-
gellar apparatus. ground and indistinct fibrous core (Fig. 7.9).
The contents of adhesion vesicles are released intermediate arrangement is also observed in
to form an adhesive plate that attaches meios- natural isolates of A. javanicus, which Emer-
pores to the intersegmental membranes of son and Wilson hypothesized were hybrids of
copepods and zygotes to the cuticle of mos- A. arbusculus x A. macrogynus.
quito larvae (Federici and Lucarotti 1986; Trav- Emerson and Wilson further used cytology
land 1979). to verify the hybrid nature of the intermediate
F1 gametophytes. Comparison of natural iso-
A most unusual feature of both meiospores and lates suggested that A. arbusculus isolates were
gametes of Coelomomyces is the presence of one or a polyploid series with a base chromosome
more rod-shaped paracrystalline bodies that lie along- number of 8, with the most common haploid
side the axial components opposite the MLC (Fig. 7.9)
A similar structure has been reported in motile cells of
(gametophyte) chromosome number of 16,
Callimastix cyclopis (Manier and Loubes 1978; Vavra implying that most A. arbusculus sporophytes
and Joyon 1966) and various members of the Chytrio- are tetraploid. It was suggested that A. macro-
myces clade of Chytridiomycota (Barr and Hartmann gynus had a base chromosome number of 14,
1976; Picard et al. 2009; Taylor and Fuller 1981). The but the common chromosomal types used by
function of the paracrystalline body is unknown, but it
has been speculated that it plays a role in infection
Emerson and Wilson possessed 28 chromo-
(Madelin and Beckett 1972). somes. Artificially produced A. javanicus
would thus be expected to have 44 chromo-
somes before meiosis, and in crosses in which
haploid A. arbusculusA macrogynus fused, 44
VII. Genetics and Physiology chromosomes were observed, but only 1–5
bivalents were seen, indicating a lack of exten-
A. Hybridization sive homology between the chromosomes of
the two species. This lack of pairing explains
The phenomenon of hybridization is not exten- both the wide range of chromosome numbers
sively documented in fungi, and verified in the artificial hybrid F1 gametophytes
instances of interspecific hybridization are (improper segregation) and their low viability
rather rare (Brasier 2001; Schardl and Craven and agrees with the highly variable numbers of
2003). The classic work of Emerson and collea- chromosomes seen in A. javanicus wild isolates.
gues on hybridization between A. arbusculus However, it was unclear why A. javanicus wild
and A. macrogynus provides convincing evi- isolates had a variable but much lower (13–21)
dence for the existence of interspecific hybrids chromosome number than the artificial hybrids
in the wild, but very little work has been con- (20–44) (Emerson and Wilson 1954). It is also
ducted since the landmark paper by Emerson unclear whether the polyploid series within A.
and Wilson (1954). Emerson and Wilson’s work arbusculus and A. macrogynus are frequently
utilized clear differences between A. arbusculus generated by doubling or rarely generated and
and A. macrogynus in the arrangement of the actually represent different species. Evidence
pairs of male and female gametangia at hyphal that prolonged growth of A. macrogynus at
tips. Male gametangia (distinctively orange 35 C leads to a reduction in chromosome
from gamma-carotene) are terminal or epigy- number that can be restored by growth at
nous in A. macrogynus, while male gametangia 23 C (Borkhardt and Olson 1979; Olson and
are hypogynous in A. arbusculus. Using con- Borkhardt 1978) suggests that autopolyploidy
trolled crosses between the two species, Emer- by endomitosis could occur readily, but the
son and Wilson found that F1 sporophytes were absence of many bivalents in F1 hybrid meio-
readily obtained, but the viability of meiospores sis suggests, possibly, a more ancient origin.
produced by the sporophytes was greatly Olson and Borkhardt additionally showed that
reduced. Among the viable meiospores, the F1 when tetraploid resting sporangia are germi-
gametophyte generation displayed a range of nated and meiosis is blocked to induce the
gametangial arrangements, and putative generation of sporophytic colonies with
hybrids typically showed a mixture of epigy- increased ploidy, they are usually unstable
nous and hypogynous arrangements. This (Olson and Borkhardt 1978).
The highly selfing nature of Allomyces B. Mitosis

allows for the rapid stabilization and fertility
of hybrids in the F2 and F3 generations as each Mitosis in the Blastocladiomycota has been well
haploid chromosome of viable F1 hybrids characterized using a combination of light and
would find an identical homologous chromo- electron microscopy, and several innovations
some to pair with following the fusion of genet- have been developed to study the process in
ically identical selfed male and female gametes. the group. The process of nuclear division was
Thus, selfing may have facilitated the recovery often described as a part of a larger description
of natural hybrids in Allomyces. Phylogenetic of the development of hyphal, zoosporangial, or
analyses have now begun to shed light on the gametangial development from germinating
relationships between these hybridizing species zoospores at a time when Allomyces and Blas-
of section Euallomyces. Neither A. arbusculus tocladiella were still considered model organ-
nor A. macrogynus seems to be monophyletic isms in genetics. Kniep (1930) observed that,
(Porter et al. 2011). Thus, the simple designa- although hyphal nuclei of Allomyces are large
tions used to designate the species based on compared with other fungi, they were difficult
gametangial arrangements seem to be artificial, subjects for the study of mitosis. Another early
and the extensive morphological variation and light-microscopy study described nuclear
polyploid series must be reevaluated by a com- behavior in detail for A. arbusculus (Hatch
bined study of chromosomes, phylogenies, and 1935). Hatch described the development of ger-
crosses. minating spores into coenocytic multinucleate
Experimental hybridization has also been hyphae that in turn develop into either a game-
conducted in Coelomomyces, between C. dodgei tophyte bearing gametangia or into a sporo-
and C. punctatus (Federici 1979, 1982). Utiliz- phyte bearing zoosporangia. The nuclear
ing the orange pigment of male gametangia and count at the start of septation, when the first
a common gametophyte host, the copepod septum forms on a hypha, delimiting the apical
Cyclops vernalis, Federici fused isogamous female gametangium, and the second septum
gametes of opposite mating type between the that forms further behind on the hypha, deli-
two species and then demonstrated that the miting the male gametangium, showed roughly
hybrids could infect a common mosquito host equal numbers of nuclei in each gametangium.
(either Anopheles freeborni or Anopheles quad- At the end of gametangial differentiation a two-
rimaculatus), proliferate as a sporophyte, and fold increase in the number of nuclei in the
produce meiosporangia. The resting sporangia male gametangium was observed as a result of
produced by the hybrid sporophytes displayed repeated nuclear divisions. It was also observed
a wide range of characteristics but were mostly that mitotic divisions were not synchronous,
similar to one or the other parental species. The and drawings of actively dividing nuclei with a
resting sporangia dehisced and released meios- spindle as well as anaphase and telophase chro-
pores that encysted on the copepod host; how- mosome configurations were provided. Though
ever, no gametophytes were ever produced. nuclei in the female gametangium were about
These results demonstrate that the germination twice the size of nuclei in the male gametan-
and growth of the haploid gametophyte is the gium, both gametes contain only six chromo-
most disrupted phase among hybrids of both somes. Hatch (1935) suggested that the size
Coelomomyces and Allomyces, as predicted by difference between male and female nuclei
genetics. These studies also produce a working may be related to maintaining a particular
model for testing biological species; however, nuclear-plasma ratio, though how this was
most of the crossing manipulations are related to an increased number of mitotic divi-
extremely laborious. sions in the male gametangium could not be
explained. Another light-microscopy study by (10–10 to 10–5 M) (Carlile and Machlis 1965).
Wilson and Flanagan (1968) followed mitosis Sirenin was the first fungal hormone to be
in resistant sporangia and hyphae in chemically characterized and shown to be a
Brachyallomyces strains and noted that somatic bicyclic sequiterpenediol (Machlis 1968). Pom-
nuclei were smaller than those in resistant spor- merville has also provided evidence that male
angia. gametes produce a hormone, though the swim-
Either closed mitosis or partially open ming ability of female gametes is much reduced
mitosis has been shown in fungi. So far, only compared to those of males (Pommerville 1977,
closed mitosis, or intranuclear division, has 1978).
been described in blastoclads. In closed mitosis
the nuclear membrane remains intact or largely
intact and the spindle forms inside the nucleus D. Substrate Utilization and Respiration
(DeSouza and Osmani 2007; Heath 1980). A
persistent nuclear membrane during somatic Completely defined media have been constructed
mitosis has been demonstrated in Allomyces for studying nutrition in Allomyces (Ingraham
spp. (Olson 1984), C. anguillulae (Ichida and and Emerson 1954). Growth on glucose, maltose,
Fuller 1968), and Coelomomyces indicus (Made- and starch as a sole carbon source has been
lin and Beckett 1972). Lessie and Lovett (1968) shown for Allomyces (Ingraham and Emerson
reported intranuclear mitosis in B. emersonii 1954), C. anguillulae (Nolan 1970), and B. pring-
comprised of a typical microtubular spindle sheimii (Crasemann 1957; Emerson and Cantino
apparatus and paired but unequal extranuclear 1948; Gleason and Gordon 1989). Nitrogen utili-
centrioles at each pole. zation varies among taxa, with Allomyces capable
of using inorganic nitrogen and Blastocladiella
and Catenaria using only organic sources (Bar-
ner and Cantino 1952). An absolute requirement
C. Taxis for an organic source of sulfur in the medium has
also been demonstrated for the saprotrophic
Taxis refers to the ability of motile cells or genera (Cantino and Turian 1959; Nolan 1969).
organisms to move across a gradient in a Nutritional studies have facilitated the isolation
directed manner. Such behavior is clearly of auxotrophic mutants; however, many mutants
advantageous for zoospores and gametes of reported in the literature have apparently been
blastoclads as they disperse to find a new food unstable or displayed non-Mendelian inheritance
source or mate. Both phototaxis and chemo- due to ploidy (Olson 1984).
taxis have been well documented in blastoclads. The obligately biotrophic parasites have
Positive phototaxis toward light was demon- been nearly impossible to isolate into pure
strated in both Allomyces spp. (Olson 1984; culture. Numerous methods employing a
Robertson 1972) and Coelomomyces (Martin “shotgun” approach have been tried for the
1970). Positive phototaxis may provide a mech- growth of Coelomomyces, which would have
anism by which gametes or zoospores may clear benefits for biocontrol (Bland 1985;
emerge from sediments. The attraction of zoos- Nolan 1985). Several media, such as BHM
pores of Allomyces to cellulose and chitin irre- (comprised of brain-heart infusion, mosquito
spective of light has been shown (Mitchell and larval extract, fetal bovine serum, and corn
Deacon 1986), as has positive chemotaxis stunt spiroplasma media, to name a few ingre-
toward several amino acids (Machlis 1969; dients!), have supported the growth of Coelo-
Stumm et al. 1976). momyces, including the production of inviable
Chemotaxis during mating should facilitate sporangia (Bland 1985; Castillo and Roberts
motile gametes seeking a compatible partner. 1980). Key to the successful deployment of Coe-
The diffusible hormone sirenin is produced by lomomyces inoculum as a biocontrol agent will
female gametes of Allomyces (Machlis 1958a, b) be the in vitro culture of the gametophyte stage
and has activity at very low concentrations from copepods, needed to produce infective
zygotes. Alternatively, the development of spe- (Ribichich et al. 2005). Our knowledge of fungal
cies such as Coelomomyces iliensis var. iliensis mitochondrial genomes is similarly biased, but
whose sporophyte stage makes asexual diploid mitochondrial genomes of the basal fungal
zoospores that can reinfect the mosquito host lineages are better represented. Two Blastocla-
should be pursued. Among the plant parasitic diomycota mitochondrial genomes have been
genera, the algal parasite Paraphysoderma is completed for A. macrogynus and B. emersonii
the only one that can be grown in vitro (Hoff- (Paquin and Lang 1996; Tambor et al. 2008).
man et al. 2008). This observation suggests Mitochondrial chromosomes (mtDNA)
inroads to cultivating Physoderma may be usually encode proteins involved in the electron
found by careful study of the nutritional transport chain, adenosine triphosphate (ATP)
requirements of the former. synthesis, structural proteins, and proteins of
The genus Blastocladia has been shown to unknown function that may be found as open
be obligately fermentative and facultatively reading frames in introns (Griffiths 1996).
anaerobic using with at least one species, B. Though mitochondrial function is basically
ramosa, conforming to its observed niche of the same in all organisms, fungal mitochondrial
stagnant waters (Held et al. 1969). Blastocladia genomes may show great differences in size and
cultures responded positively to the addition of gene organization due to the presence of
CO2 to 20 %, suggesting they may be able to introns and size variation in intergenic spacer
convert CO2 into organic acids (Tabak and regions (Lang et al. 2007). The mitochondrial
Cooke 1968). Interestingly, electron micro- genomes examined so far in Blastocladiomy-
graphs of B. ramosa showed double-membrane cota have been shown by electron microscopy,
structures like mitochondria lacking any cristae restriction enzyme analysis, and sequencing to
in germlings (Held et al. 1969); however, with be circular, although more recently it has been
improved fixation techniques the single mito- shown that linear forms may also be present
chondrion of the zoospores of B. ramosa did in vivo for many fungi (Bendich 1993, 1996,
indeed have cristae but not as many as the 2010; Burger et al. 2003).
obligately aerobic genera (Lingle and Barstow
1983). Microaerophily, or improved develop- Allomyces macrogynus The first mtDNA physical
ment under low oxygen conditions, has been maps for the aquatic fungi were for A. macrogy-
suggested for other members of Blastocladia- nus (Borkhardt and Delius 1983; Borkhardt et al.
ceae: Allomyces reticulatus and Microallomyces 1988). The mitochondrial genome sequence for A.
dendroideus (Emerson and Robertson 1974). macrogynus confirmed its circular nature, total
size of 57,473 bp, and slightly enriched A+T
base content of 60.5 % (Paquin and Lang 1996).
E. Genomics All mitochondrial genes seemed to be transcribed
from the same DNA strand, similar to many other
Our knowledge of fungal genomes is biased
fungi (Paquin and Lang 1996).
toward mainly Ascomycota species, particu-
It has been hypothesized that the universal
larly model organisms and pathogenic species.
mitochondrial code is an ancestral trait in fungal
The only Blastocladiomycota genome in prog-
mitochondria (Paquin et al. 1997). Similar to
ress is for A. macrogynus ATCC38327,
sequenced by the Broad Institute’s Origins of plants and protists, A. macrogynus only uses the
Multicellularity project (Ruiz-Trillo et al. 2007). UGG codon for tryptophan (Paquin and Lang
Data on the expressed portion of Blastocladio- 1996). Other fungi that share this trait include
mycota genomes are available from EST pro- the blastoclad B. emersonii, the zygomycete Rhi-
jects such as through the Taxonomically Broad zopus stolonifer, the chytrids Spizellomyces,
EST Database (TBestDB) for A. macrogynus Monoblepharella, and Harpochytrium, and the
(submitted by B.F. Lang, University of Mon- basal Ascomycete fission yeast Schizosaccharo-
treal) and the National Center for Bioinformat- myces pombe (Massey and Garey 2007; Paquin
ics Information (NCBI) for B. emersonii et al. 1997; Tambor et al. 2008). In most other
fungi and animals, the UGA stop codon has been across the mitochondrial genome of A. macrogy-
reassigned to code for tryptophan. Additionally, nus. The intergenic spacer regions comprise
A. macrogynus uses the UAG and UAA stop 47.9 % of the mitochondrial genome in B. emer-
codons equally to signal termination (A. macro- sonii, compared with 22 % in A. macrogynus.
gynus does not use UGA), whereas most other
fungi uniquely or preferentially use UAA (Paquin
and Lang 1996). The only other organism known
to use both stop codons equally is Paramecium
VIII. Conclusions and Future
(Pritchard et al. 1990). Directions
What the blastoclads lack in species number

Structural RNAs included the large and small they make up for in phylogenetic and ecological
mitochondrial-encoded rRNA genes (rnl and rns) and a diversity. They are the only group of fungi
set of 25 transfer RNAs (tRNAs). Protein-coding genes known to possess an alternation of haploid
include three ATPase subunits (atp6, apt8, and atp9), and diploid generations. This trait, unlike
apocytochrome b (cob), three subunits of the cytochrome
oxidase complex (cox1, cox2, and cox3), and seven sub- anisogamy, which evolved in the ancestor of
units of the NADH dehydrogenase complex (nad1, nad2, subgenus Euallomyces, seems to be ancestral
nad3, nad4, nad4L, nad5, and nad6). Generally, the to blastoclads. Does a life cycle alternating
observed mitochondrial gene content is typical of that between haploid and diploid generations sug-
found in other fungi (Paquin and Lang 1996). The pres- gest that blastoclads might be the first diverging
ence of introns in mitochondrial genes was observed in
the first mtDNA genome sequences of fungi, including A. branch in fungi and that they inherited this trait
macrogynus, and has important consequences for the from the most recent common ancestor of all
development of mtDNA genes for DNA barcoding fungi? The answer is, unfortunately, unclear
efforts. For example, hybridization studies of the A. because the phylogenetic placement of the
macrogynus cox1 gene suggest the presence of intronic group has yet to be definitively resolved, and
sequences (Borkhardt et al. 1988). The cox1 gene is now
known to contain 12 introns and has a total size of more the life cycles of the putative outgroups of fungi
than 11 kbp (Paquin and Lang 1996). are not completely known (Brown et al. 2009;
Jones et al. 2011). On the other hand, closed
mitosis, Golgi equivalents rather than a Golgi
Blastocladiella emersonii The physical map of apparatus, and true mycelial growth are char-
the B. emersonii mtDNA genome showed this to acteristics of blastoclads that are more similar
be the smallest mitochondrial genome of the zoo- to the more derived nonzoosporic fungi.
sporic fungi sequenced so far, with a circular
Variations in life cycles are common
throughout the group, and they have been
structure and a size of 36,503 bp and an enriched
used to define subgenera and species in Allo-
A+T base content of 64.9 % (Borkhardt and
myces and Blastocladiella. Yet all indications
Olson 1986; Tambor et al. 2008). All mtDNA
are that life cycle variants can occur within
genes use the universal translation code and are species and that species may hybridize readily
found in the same orientation (Tambor et al. and differ greatly in ploidy. Thus, it is no sur-
2008). However, B. emersonii mtDNA differs prise that phylogenetic analysis of Allomyces
from that of A. macrogynus in several ways. reveals serious problems with traditional spe-
First, B. emersonii has a smaller mtDNA genome cies concepts (Porter et al. 2011). All five of the
relative to A. macrogynus, caused by differences species of Allomyces in the phylogeny repre-
in the number and size of introns, intergenic sented by more than one strain were shown to
spacer regions, and double-hairpin DNA ele- be nonmonophyletic. In the phylogeny, roughly
ments (DHEs) (Paquin and Lang 1996; Tambor 12 terminal clades that are suggestive of species
et al. 2008). Specifically, the mitochondrial were observed, whereas only 9 names are cur-
genome of B. emersonii contains only 2 introns rently valid. Thus, in the minimal sampling
(both in the cox1 gene), compared with 28 introns employed, additional species must be
described. A major unanswered question is how species-specific in inoculation studies (Sparrow

many good blastoclad species have and Griffin 1964), it may be that the species
been proposed and how many are in need of diversity in this group is much lower than the
revision. Modern mycology emphasizes a holis- list of taxonomically accepted names. Similar
tic view of fungal species that includes morpho- difficulties may arise in other parasitic genera,
logical, physiological, phylogenetic, and for example, Coelomomyces and Catenaria;
compatibility data (Cai et al. 2011; Taylor however, the phylogenetic diversity of Physo-
et al. 2000). derma (as measured by branch lengths in a
While species concepts in blastoclads must phylogeny) is much shallower than observed
be redefined, a concerted effort to enumerate in the Coelomomyces clade.
what are likely to be many undescribed species
should also be undertaken. The mere 180 species
named is obviously a gross underestimate of the References
true diversity, and future taxonomists of the
group will be required to document and describe Barner HD, Cantino EC (1952) Nutritional relation-
new species as they will inevitably be encoun- ships in a new species of Blastocladiella. Am J
tered. Discovery of these species will be facili- Bot 39:746–751
Barr DJS, Hartmann VE (1976) Zoospore ultrastructure
tated by DNA-based evidence emerging from of three Chytridium species and Rhizoclosmatium
sampling of environments likely to be rich in globosum. Can J Bot 54:2000–2013
blastoclads, such as suboxic sediments, periodi- Barstow WE, Lovett JS (1975) Formation of gamma-
cally inundated soils, and invertebrate hosts. particles during zoosporogenesis in Blastocladiella
How we apply species concepts and delimit taxa emersonii. Mycologia 67:518–529
Barstow WE, Pommerville J (1980) The ultrastructure
in early-diverging fungi is a question that has of cell wall formation and of gamma-particles dur-
largely been avoided, and there are very little ing encystment of Allomyces macrogynus zoos-
data to address the question. Several lines of pores. Arch Microbiol 128:179–189
evidence suggest major revisions are warranted. Bendich AJ (1993) Reaching for the ring: the study of
Firstly, hybridization and horizontal gene trans- mitochondrial genome structure. Curr Genet
24:279–290
fer are poorly documented phenomena in fungi, Bendich AJ (1996) Structural analysis of mitochondrial
but recent studies suggest that they may be as DNA molecules from Fungi and Plants using
common in fungi as in other eukaryotic groups moving pictures and pulsed-field gel elctrophor-
(Brasier 2001; Schardl and Craven 2003). Perhaps esis. J Mol Biol 255:564–588
the best example of hybridization in fungi comes Bendich AJ (2010) The end of the circle for yeast mito-
chondrial DNA. Mol Cell 39:831–832
from experimental and natural hybrids in the Bland CE (1985) Culture. In: Couch JN, Bland CE (eds)
species A. javanicus, the presumed hybrid of A. The genus Coelomomyces. Academic, Orlando, FL,
macrogynus and A. arbusculus. However, experi- pp 349–359
ments to characterize A. javanicus genetically Borkhardt B, Delius H (1983) Physical map of the mito-
have never been done, and the role of hybridiza- chondrial DNA from the phycomycete Allomyces
macrogynus including the position of the ribo-
tion in speciation has not been addressed in the somal RNA genes and of an intervening sequence
blastoclads. in the large rRNA gene. Curr Genet 7:327–333
The coevolution of host and pathogen has Borkhardt B, Olson LW (1979) Meiotic prophase in
likely driven diversification in blastoclads. In diploid and tetraploid strains of Allomyces macro-
the future, studies of host specificity must be gynus. Protoplasma 100:323–343
Borkhardt B, Olson LW (1986) The mitochondrial
integrated into studies of taxonomy and sys- genome of the aquatic phycomycete Blastocla-
tematics so that the simple assumption of one diella emersonii. Curr Genet 11:139–143
pathogen species per host species does not lead Borkhardt B, Brown TA, Thim P, Olson LW (1988) The
to erroneous classifications. Because most of mitochondrial genome of the aquatic phycomycete
the Physoderma species were named under the Allomyces macrogynus. Physical mapping and
mitochondrial DNA instability. Curr Genet
assumption that each host species had distinct 13:41–47
parasites, and there is evidence to suggest that Bowman BH, Taylor JW, Brownlee AG, Lee J, Lu SD,
the species of Physoderma are less than host- White TJ (1992) Molecular evolution of the fungi-
relationship of the Basidiomycetes, Ascomycetes, Chapman HC (1985) Ecology and use of Coelomomyces
and Chytridiomycetes. Mol Biol Evol 9:285–296 species in biological control: a review. In: Couch
Brasier CM (2001) Rapid evolution of introduced plant JN, Bland CE (eds) The genus Coelomomyces. Aca-
pathogens via interspecific hybridization. Biosci- demic, Orlando, FL, pp 361–368
ence 51:123–133 Chen MJ, Chen FZ, Yu Y, Ji J, Kong FX (2008) Genetic
Brown MW, Spiegel FW, Silberman JD (2009) Phylog- diversity of eukaryotic microorganisms in Lake
eny of the “forgotten” cellular slime mold, Fonti- Taihu, a large shallow subtropical lake in China.
cula alba, reveals a key evolutionary branch within Microb Ecol 56:572–583
Opisthokonta. Mol Biol Evol 26:2699–2709 Couch JN (1945) Observations on the genus Catenaria.
Bruns TD, White TJ, Taylor JW (1991) Fungal molecu- Mycologia 37:163–191
lar systematics. Annu Rev Ecol Syst 22:525–564 Couch JN, Bland CE (1985) The genus Coelomomyces.
Bruns TD, Vilgalys R, Barns SM, Gonzalez D, Hibbett Academic, New York
DS, Lane DJ, Simon L, Stickel S, Szaro TM, Weis- Couch JN, Whiffen AJ (1942) Observations on the
burg WG, Sogin ML (1992) Evolutionary relation- genus Blastocladiella. Am J Bot 29:582–591
ships within the Fungi: analyses of nuclear small Crasemann JM (1957) Comparative nutrition of two
subunit rRNA sequences. Mol Phylogenet Evol species of Blastocladia. Am J Bot 44:218–224
1:231–241 Dalley NE, Sonneborn DR (1982) Evidence that Blasto-
Bullerwell CE, Forget L, Lang BF (2003) Evolution of cladiella emersonii zoospore chitin synthetase is
monoblepharidalean fungi based on complete located at the plasma membrane. Biochim Biophys
mitochondrial genome sequences. Nucleic Acids Acta 686:65–76
Res 31:1614–1623 Dasgupta SN, John R (1988) A contribution to our
Burger G, Forget L, Zhu Y, Gray MW, Lang BF (2003) knowledge of the genus Blastocladia. Indian Phy-
Unique mitochondrial genome architecture in uni- topathol 41:521–547
cellular relatives of animals. Proc Natl Acad Sci Debaisieux P (1920) Coelomycidium simulii nov. gen.,
USA 100:892–897 nov. sp. et remarques sur l’Amoebidium des larves
Butler EJ (1911) On Allomyces, a new aquatic fungus. de Simulium. Cellule 30:249–271
Ann Bot 25:1023–1035 DeSouza CPC, Osmani SA (2007) Mitosis, not just open
Cai L, Giraud T, Zhang N, Begerow D, Cai GH, Shivas or closed. Eukaryot Cell 6:1521–1527
RG (2011) The evolution of species concepts and Dewel RA, Dewel WC (1990) The fine structure of the
species recognition criteria in plant pathogenic zoospore of Sorochytrium milnesiophthora. Can J
fungi. Fungal Divers 50:121–133 Bot 68:1968–1977
Cantino EC (1956) The relation between cellular metab- Dewel RA, Joines JD, Bond JJ (1985) A new chytridio-
olism and morphogenesis in Blastocladiella. mycete parasitizing the tardigrade Milnesium tar-
Mycologia 48:225–240 digradum. Can J Bot 63:1525–1534
Cantino EC, Horenstein EA (1954) Cytoplasmic Doweld AB (2001) Prosyllabus tracheophytorum. Ten-
exchange without gametic copulation in the water tamen systematis plantarum vascularium (Tra-
mold Blastocladiella emersonii. Am Nat 88:143–154 cheophyta). Geos, Moscow
Cantino EC, Hyatt MT (1953) Phenotypic “sex” deter- Emerson R (1938) A new life cycle involving cyst-
mination in the life history of a new species of formation in Allomyces. Mycologia 30:120–132
Blastocladiella, B emersonii. Antonie Van Leeu- Emerson R (1941) An experimental study of the life
wenhoek 19:25–70 cycles and taxonomy of Allomyces. Lloydia 4:77–
Cantino EC, Truesdell LC (1970) Organization and fine 144
structure of side body and its lipid sac in zoospore Emerson R, Cantino EC (1948) The isolation, growth,
of Blastocladiella emersonii. Mycologia 62:548–567 and metabolism of Blastocladia in pure culture.
Cantino EC, Truesdell LC (1971) Cytoplasmic gamma- Am J Bot 35:157–171
like particles and other ultrastructural aspects of Emerson R, Robertson JA (1974) Two new members of
zoospores of Blastocladiella britannica. Trans Br Blastocladiaceae. I. Taxonomy, with an evaluation
Mycol Soc 56:169–179 of genera and interrelationships in family. Am J
Cantino EC, Turian GF (1959) Physiology and develop- Bot 61:303–317
ment of lower fungi (Phycomycetes). Annu Rev Emerson R, Wilson CM (1949) The significance of mei-
Microbiol 13:97–124 osis in Allomyces. Science 110:86–88
Carlile MJ, Machlis L (1965) Response of male gametes Emerson R, Wilson CM (1954) Interspecific hybrids
of Allomyces to sexual hormone sirenin. Am J Bot and the cytogenetics and cytotaxonomy of Euallo-
52:478–483 myces. Mycologia 46:393–434
Castillo JM, Roberts DW (1980) In vitro studies of Coelo- Federici BA (1979) Experimental hybridization of Coe-
momyces punctatus from Anopheles quadrimaculatus lomomyces dodgei and Coelomomyces punctatus.
and Cyclops vernalis. J Invertebr Pathol 35:144–157 Proc Natl Acad Sci USA 76:4425–4428
Federici BA (1982) Inviability of interspecific hybrids in Ryvarden L, Sampaio JP, Schussler A, Sugiyama
the Coelomomyces dodgei complex. Mycologia J, Thorn RG, Tibell L, Untereiner WA, Walker C,
74:555–562 Wang Z, Weir A, Weiss M, White MM, Winka K,
Federici BA, Lucarotti CJ (1986) Structure and behavior Yao YJ, Zhang N (2007) A higher-level phyloge-
of the meiospore of Coelomomyces dodgei during netic classification of the Fungi. Mycol Res
encystment on the copepod host, Acanthocyclops 111:509–547
vernalis. J Invertebr Pathol 48:259–268 Hill EP (1969) Fine structure of zoospores and cysts of
Fischer A (1892) Phycomycetes. Die Pilze Deutsch- Allomyces macrogynus. J Gen Microbiol 56:125–
lands, Oesterreichs und der Schweiz. 130
Kryptogamen-Fl 1:1–490 Hoffman Y, Aflalo C, Zarka A, Gutman J, James TY,
Förster H, Coffey MD, Elwood H, Sogin ML (1990) Boussiba S (2008) Isolation and characterization of
Sequence analysis of the small subunit ribosomal a novel chytrid species (phylum Blastocladiomy-
RNAs of three zoosporic fungi and implications cota), parasitic on the green alga Haematococcus.
for fungal evolution. Mycologia 82:306–312 Mycol Res 112:70–81
Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS, Hohn TM, Lovett JS, Bracker CE (1984) Characteriza-
Meyer AF, Longcore JE, Simmons DR, Schmidt SK tion of the major proteins in gamma particles,
(2009) Evidence that chytrids dominate fungal cytoplasmic organelles in Blastocladiella emerso-
communities in high-elevation soils. Proc Natl nii zoospores. J Bacteriol 158:253–263
Acad Sci USA 106:18315–18320 Horenstein EA, Cantino EC (1962) Dark-induced mor-
Fuller MS, Calhoun SA (1968) Microtubule-kinetosome phogenesis in synchronized cultures of Blastocla-
relationships in motile cells of Blastocladiales. Z diella britannica. J Bacteriol 84:37–45
Zellforsch Mikrosk Anat 87:526–533 Horgen PA, Meyer RJ, Franklin AL, Anderson JB, Filion
Fuller MS, Olson LW (1971) Zoospore of Allomyces. J WG (1985) Motile spores from resistant sporangia
Gen Microbiol 66:171–183 of Blastocladiella emersonii possess one-half the
Garcia R (1983) Mosquito management - ecological DNA of spores from ordinary colorless sporangia.
approaches. Environ Manage 7:73–78 Exp Mycol 9:70–73
Gleason FH, Gordon GLR (1989) Anaerobic growth and Ichida AA, Fuller MS (1968) Ultrastructure of mitosis in
fermentation in Blastocladia. Mycologia 81:811– the aquatic fungus Catenaria anguillulae. Mycolo-
815 gia 60:141–155
Gleason FH, Marano AV, Johnson P, Martin WW Ingraham JL, Emerson R (1954) Studies of the nutrition
(2010) Blastocladian parasites of invertebrates. and metabolism of the aquatic phycomycete, Allo-
Fungal Biol Rev 24:56–67 myces. Am J Bot 41:146–152
Griffiths AJF (1996) Mitochondrial inheritance in fila- James TY, Porter D, Leander CA, Vilgalys R, Longcore
mentous fungi. J Genet 75:403–414 JE (2000) Molecular phylogenetics of the Chytri-
Harder R, Sörgel G (1938) Über einen neuen plano- diomycota supports the utility of ultrastructural
isogamen Phycomyceten mit Generationswechel data in chytrid systematics. Can J Bot 78:336–350
und seine phylogenetische Bedeutung. Nachrich- James TY, Kauff F, Schoch C, Matheny PB, Hofstetter V,
ten Gesell Wiss Göttingen Fachgruppe VI (Biol) Cox C, Celio G, Gueidan C, Fraker E, Miadlikowska
3:119–127 J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE,
Hatch WR (1935) Gametogenesis in Allomyces arbus- Amtoft A, Stajich JE, Hosaka K, Sung G-H, John-
cula. Ann Bot 49:623–649 son D, O’Rourke B, Crockett M, Binder M, Curtis
Heath IB (1980) Variant mitoses in lower eukaryotes: JM, Slot JC, Wang Z, Wilson AW, Schüßler A,
indicators of the evolution of mitosis? Int Rev Longcore JE, O’Donnell K, Mozley-Standridge S,
Cytol 64:1–80 Porter D, Letcher PM, Powell MJ, Taylor JW,
Held AA, Emerson R, Fuller MS, Gleason FH (1969) White MM, Griffith GW, Davies DR, Humber RA,
Blastocladia and Aqualinderella – fermentative Morton JB, Sugiyama J, Rossman AY, Rogers JD,
water molds with high carbon dioxide optima. Pfister DH, Hewitt D, Hansen K, Hambleton S,
Science 165:706–709 Shoemaker RA, Kohlmeyer J, Volkmann-
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Can- Kohlmeyer B, Spotts RA, Serdani M, Crous PW,
non PF, Eriksson OE, Huhndorf S, James T, Kirk Hughes KW, Matsuura K, Langer E, Langer G,
PM, Lucking R, Lumbsch HT, Lutzoni F, Matheny Untereiner WA, Lücking R, Büdel B, Geiser DM,
PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr
CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime R, Hibbett D, Lutzoni F, McLaughlin D, Spatafora
MC, Aptroot A, Bauer R, Begerow D, Benny GL, J, Vilgalys R (2006a) Reconstructing the early evo-
Castlebury LA, Crous PW, Dai YC, Gams W, Geiser lution of the fungi using a six gene phylogeny.
DM, Griffith GW, Gueidan C, Hawksworth DL, Nature 443:818–822
Hestmark G, Hosaka K, Humber RA, Hyde KD, James TY, Letcher PM, Longcore JE, Mozley-Standridge
Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, SE, Porter D, Powell MJ, Griffith GW, Vilgalys R
Lichtwardt R, Longcore J, Miadlikowska J, Miller (2006b) A molecular phylogeny of the flagellated
A, Moncalvo JM, Mozley-Standridge S, Oberwink- fungi (Chytridiomycota) and description of a new
ler F, Parmasto E, Reeb V, Rogers JD, Roux C, phylum (Blastocladiomycota). Mycologia 98:860–871
James TY, Hoffman Y, Zarka A, Boussiba S (2011) diomycota) isolates from North America and
Paraphysoderma sedebokerense, gen. et sp. nov., Argentina. Mycol Res 112:759–782
an aplanosporic relative of Physoderma (Blastocla- Lingle WL, Barstow WE (1983) Ultrastructure of the
diomycota). MycoTaxon 118:177–180 zoospore of Blastocladia ramosa (Blastocladiales).
Jaworski AJ, Stumhofer P (1984) Dormant ribosomes in Can J Bot 61:3502–3513
Blastocladiella emersonii zoospores are arrested at Liu YJ, Hodson MC, Hall BD (2006) Loss of the flagel-
elongation. Exp Mycol 8:13–24 lum happened only once in the fungal lineage:
Johnson PTJ, Longcore JE, Stanton DE, Carnegie RB, phylogenetic structure of Kingdom Fungi inferred
Shields JD, Preu ER (2006) Chytrid infections of from RNA polymerase II subunit genes. BMC Evol
Daphnia pulicaria: development, ecology, pathol- Biol 6:13
ogy and phylogeny of Polycaryum laeve. Freshw Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe
Biol 51:634–648 H, Lang BF (2009) Phylogenomic analyses predict
Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, sistergroup relationship of nucleariids and Fungi
Massana R, Richards TA (2011) Discovery of and paraphyly of zygomycetes with significant
novel intermediate forms redefines the fungal support. BMC Evol Biol 9:11
tree of life. Nature 474:200–234 Lovett JS (1975) Growth and differentiation of water
Karling JS (1950) The genus Physoderma. Lloydia mold Blastocladiella emersonii – cytodifferentia-
13:29–71 tion and role of ribonucleic acid and protein syn-
Karling JS (1965) Catenophlyctis, a new genus of Cate- thesis. Bacteriol Rev 39:345–404
nariaceae. Am J Bot 52:133–138 Lucarotti CJ (1987) Coelomomyces stegomyiae infection
Karling JS (1977) Chytridiomycetarum Iconographia. in adult Aedes aegypti. Mycologia 79:362–369
Lubrecht and Cramer, Monticello, NY Lucarotti CJ, Federici BA (1984) Ultrastructure of the
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) gametes of Coelomomyces dodgei Couch (Blastocla-
Dictionary of the Fungi, 10th edn. CABI Publish- diales, Chytridiomycetes). Protoplasma 121:77–86
ing, The Netherlands Machlis L (1958a) A study of sirenin, the chemotactic
Kniep H (1930) Über den Generationswechsel von Allo- sexual hormone from the watermold Allomyces.
myces. Zeitschrift für Botanik 22:433–441 Physiol Plant 11:845–854
Koch WJ (1956) Studies of the motile cells of chytrids. I. Machlis L (1958b) Evidence for a sexual hormone in
Electron microscope observations of the Allomyces. Physiol Plant 11:181–192
flagellum, blepharoplast and rhizoplast. Am J Bot Machlis L (1968) Response of male gametes of Allo-
43:811–819 myces to sexual hormone sirenin. Plant Physiol
Lang BF, O’Kelly C, Nerad T, Gray MW, Burger G 43:1319–1320
(2002) The closest unicellular relatives of animals. Machlis L (1969) Zoospore chemotaxis in the water
Curr Biol 12:1773–1778 mold Allomyces. Physiol Plant 22:126–139
Lang BF, Laforest M-J, Burger G (2007) Mitochondrial Madelin MF, Beckett A (1972) Production of planonts
introns: a critical view. Trends Genet 23:119–125 by thin-walled sporangia of fungus Coelomomyces
Lange L, Olson LW (1979) Uniflagellate phycomycete indicus – parasite of mosquitos. J Gen Microbiol
zoospore. Dansk Botanisk Arkiv 33:7–95 72:185–200
Lange L, Olson LW (1980) Transfer of the Physoderma- Manier JF, Loubes C (1978) Callimastix cyclopis Weis-
taceae from the Chytridiales to the Blastocladiales. senberg, 1912 (Phycomycetes, Blastocladiales) a
Trans Br Mycol Soc 74:449–457 parasite of Microcyclops claus, 1893 (Copepoda,
Lefèvre E, Bardot C, Noel C, Carrias JF, Viscogliosi E, Cyclopoida) from Tchad - ultrastructural features.
Amblard C, Sime-Ngando T (2007) Unveiling fun- Protistologica 14:493–501
gal zooflagellates as members of freshwater Manton I, Clarke B, Greenwood AD, Flint EA (1952)
picoeukaryotes: evidence from a molecular diver- Further observations on the structure of plant cilia
sity study in a deep meromictic lake. Environ by combination of visual and electron microscopy.
Microbiol 9:61–71 J Exp Bot 3:204–215
Lessie PE, Lovett JS (1968) Ultrastructural changes dur- Martin WW (1970) A morphological and cytological
ing sporangium formation and zoospore differen- study of Coelomomyces punctatus. M.Sc., Univer-
tiation in Blastocladiella emersonii. Am J Bot sity of North Carolina, Chapel Hill
55:220–236 Martin WW (1971) The ultrastructure of Coelomomyces
Letcher PM, Powell MJ, Churchill PF, Chambers JG punctatus zoospores. J Elisha Mitchell Sci Soc
(2006) Ultrastructural and molecular phylogenetic 87:209–221
delineation of a new order, the Rhizophydiales Martin WW (1975) A new species of Catenaria parasitic
(Chytridiomycota). Mycol Res 110:898–915 in midge eggs. Mycologia 67:264–272
Letcher PM, Velez CG, Barrantes ME, Powell MJ, Martin WW (1978) Two additional species of Catenaria
Churchill PF, Wakefield WS (2008) Ultrastructural (Chytridiomycetes, Blastocladiales) parasitic in
and molecular analyses of Rhizophydiales (Chytri- midge eggs. Mycologia 70:461–467
Martin WW (1987) Zoosporic parasites of aquatic Olson LW, Reichle R (1978b) Synaptonemal complex
insects: collection, identification, and culture. In: formation and meiosis in the resting sporangium
Fuller MS, Jaworski A (eds) Zoosporic fungi in of Blastocladiella emersonii. Protoplasma 97:261–
teaching and research. Southeastern, Athens, GA, 273
pp 137–142 Olson LW, Lange L, Reichle R (1978) Zoospore and
Massey SE, Garey JR (2007) A comparative genomics meiospore of aquatic phycomycete Catenaria
analysis of codon reassignments reveals a link with anguillulae. Protoplasma 94:53–71
mitochondrial proteome size and a mechanism of Paquin B, Lang BF (1996) The mitochondrial DNA of
genetic code change via suppressor tRNAs. J Mol Allomyces macrogynus: the complete genomic
Evol 64:399–410 sequence from an ancestral fungus. J Mol Biol
Matthews VD (1937) A new genus of the Blastocladia- 255:688–701
ceae. J Elisha Mitchell Sci Soc 53:191–195 Paquin B, Laforest MJ, Forget L, Roewer I, Wang Z,
McCrainie J (1942) Sexuality in Allomyces cystogenus. Longcore J, Lang BF (1997) The fungal mitochon-
Mycologia 34:209–213 drial genome project: evolution of fungal mito-
Mills GL, Cantino EC (1979) Trimodal formation of chondrial genomes and their gene expression.
microbodies and associated biochemical and cyto- Curr Genet 31:380–395
chemical changes during development in Blasto- Petersen HE (1909) Studier over Ferskvands-
cladiella emersonii. Exp Mycol 3:53–69 Phycomyceter. Bidrag til Kundskaben om de sub-
Mills GL, Cantino EC (1981) Chitosome-like vesicles merse Phykomyceters Biologi og Systematik, samt
from gamma-particles of Blastocladiella emersonii om deres Udbredelse i Danmark. Bot Tidskrift
synthesize chitin. Arch Microbiol 130:72–77 29:345–440
Mitchell RT, Deacon JW (1986) Selective accumulation of Picard KT, Letcher PM, Powell MJ (2009) Rhizidium
zoospores of chytridiomycetes and oomycetes on phycophilum, a new species in Chytridiales. Myco-
cellulose and chitin. Trans Br Mycol Soc 86:219–223 logia 101:696–706
Nagahama T, Sato H, Shimazu M, Sugiyama J (1995) Pommerville J (1977) Chemotaxis of Allomyces
Phylogenetic divergence of the entomophthora- gametes. Exp Cell Res 109:43–51
lean fungi: evidence from nuclear 18S ribosomal Pommerville J (1978) Analysis of gamete and zygote
RNA gene sequences. Mycologia 87:203–209 motility in Allomyces. Exp Cell Res 113:161–172
Nascimento CDA, Pires-Zottarelli CLA (2010) Blasto- Porter TM, Martin WM, James TY, Longcore JE, Glea-
cladiales e Spizellomycetales do Parque Estadual son F, Adler PH, Letcher PM, Vilgalys R (2011)
da Serra da Cantareira, São Paulo, Brasil. Revista Molecular phylogeny of the Blastocladiomycota
Brasileira de Botânica 33:693–704 (Fungi) based on nuclear ribosomal data. Fungal
Nolan RA (1969) Nutritional requirements for species Biol 115:381–392
of Allomyces. Mycologia 61:641–644 Powell MJ (1978) Phylogenetic implications of
Nolan RA (1970) Sulfur source and vitamin require- microbody-lipid globule complex in zoosporic
ments of aquatic phycomycete, Catenaria anguil- fungi. BioSyst 10:167–180
lulae. Mycologia 62:568–577 Powell MJ (1983) Localization of antimonate-mediated
Nolan RA (1985) Physiology and biochemistry. In: precipitates of cations in zoospores of Chytrio-
Couch JN, Bland CE (eds) The genus Coelomo- myces hyalinus. Exp Mycol 7:266–277
myces. Academic, Orlando, FL, pp 321–348 Powell MJ, Koch WJ (1977a) Morphological variations
Olson LW (1974) Meiosis in the aquatic Phycomycete in a new species of Entophlyctis. I. Species concept.
Allomyces macrogynus. Comptes rendus des tra- Can J Bot 55:1668–1685
vaux du laboratoire Carlsberg 40:113–124 Powell MJ, Koch WJ (1977b) Morphological variations
Olson LW (1980) Allomyces neo-moniliformis gameto- in a new species of Entophlyctis. II. Influence of
genesis. The Cystogenes life cycle. Protoplasma growth-conditions on morphology. Can J Bot
105:87–106 55:1686–1695
Olson LW (1984) Allomyces – a different fungus. Opera Pritchard AE, Seilhammer JJ, Mahalingam R, Sable CL,
Bot 73:5–96 Venuti SE, Cummings DJ (1990) Nucleotide
Olson LW, Borkhardt B (1978) Polyploidy and its con- sequence of the mitochondrial genome of Parame-
trol in Allomyces macrogynus. Trans Br Mycol Soc cium. Nucleic Acids Res 18:173–180
71:65–76 Reichle RE, Fuller MS (1967) Fine structure of Blasto-
Olson LW, Lange L (1978) Meiospore of Physoderma cladiella emersonii zoospores. Am J Bot 54:81–92
maydis – causal agent of physoderma disease of Remy W, Taylor TN, Hass H (1994) Early Devonian
maize. Protoplasma 97:275–290 fungi – a Blastocladalean fungus with sexual repro-
Olson LW, Lange L (1983) The gamma body- a vesicle duction. Am J Bot 81:690–702
generating structure. Nord J Bot 3:673–680 Ribichich KF, Salem-Izacc SM, Georg RC, Vencio RZN,
Olson LW, Reichle R (1978a) Meiosis and diploidiza- Navarro LD, Gomes SL (2005) Gene discovery and
tion in the aquatic Phycomycete Catenaria angu- expression profile analysis through sequencing of
illulae. Trans Br Mycol Soc 70:423–437 expressed sequence tags from different develop-
mental stages of the chytridiomycete Blastocla- Tambor JHM, Ribichich KF, Gomes SL (2008) The
diella emersonii. Eukaryot Cell 4:455–464 mitochondrial view of Blastocladiella emersonii.
Robertson JA (1972) Phototaxis in a new Allomyces. Gene 424:33–39
Arch f Mikrobiol 85:259–266 Tanabe Y, O’Donnell K, Saikawa M, Sugiyama J (2000)
Ruiz-Trillo I, Burger G, Holland PWH, King N, Lang Molecular phylogeny of parasitic Zygomycota
BF, Roger AJ, Gray MW (2007) The origins of (Dimargaritales, Zoopagales) based on nuclear
multicellularity: a multi-taxon genome initiative. small subunit ribosomal DNA sequences. Mol
Trends Genet 23:113–118 Phylogenet Evol 16:253–262
Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Tanabe Y, Watanabe MM, Sugiyama J (2002) Are
Seasonal dynamics of previously unknown fungal Microsporidia really related to Fungi?: a reap-
lineages in tundra soils. Science 301:1359–1361 praisal based on additional gene sequences from
Schardl CL, Craven KD (2003) Interspecific hybridiza- basal fungi. Mycol Res 106:1380–1391
tion in plant-associated fungi and oomycetes: a Tanabe Y, Saikawa M, Watanabe MM, Sugiyama J
review. Mol Ecol 12:2861–2873 (2004) Molecular phylogeny of Zygomycota
Scherffel A (1925) Endophytische Phycomyceten- based on EF-1 and RPB1 sequences: limitations
Parasiten der Bacillariaceen und einege neue Mon- and utility of alternative markers to rDNA. Mol
adinen. Ein Beitrag zur Phylogenie der Oomyceten Phylogenet Evol 30:438–449
(Schröter). Archiv Protistenk 52:1–141 Tanabe Y, Watanabe MM, Sugiyama J (2005) Evolution-
Schroeter J (1893) Phycomycetes. Natürlichen Pflan- ary relationships among basal fungi (Chytridiomy-
zenfam 1:63–141 cota and Zygomycota): insights from molecular
Seif E, Leigh J, Liu Y, Roewer I, Forget L, Lang BF (2005) phylogenetics. J Gen Appl Microbiol 51:267–276
Comparative mitochondrial genomics in zygomy- Taylor JW, Fuller MS (1981) The Golgi apparatus, zoos-
cetes: bacteria-like RNase P RNAs, mobile elements porogenesis, and development of the zoospore
and a close source of the group I intron invasion in discharge apparatus of Chytridium confervae.
angiosperms. Nucleic Acids Res 33:734–744 Exp Mycol 5:35–59
Shaw DS, Cantino EC (1969) An albino mutant of Blas- Taylor TN, Remy W, Hass H (1994) Allomyces in the
tocladiella emersonii - comparative studies of zoo- Devonian. Nature 367:601–601
spore behaviour and fine structure. J Gen Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser
Microbiol 59:369–382 DM, Hibbett DS, Fisher MC (2000) Phylogenetic
Simmons DR, James TY, Meyer AF, Longcore JE (2009) species recognition and species concepts in fungi.
Lobulomycetales, a new order in the Chytridiomy- Fungal Genet Biol 31:21–32
cota. Mycol Res 113:450–460 Teter HE (1944) Isogamous sexuality in a new strain of
Singh KP, Jaiswal RK, Kumar N (2007) Catenaria angu- Allomyces. Mycologia 36:194–210
illulae Sorokin: a natural biocontrol agent of Travland LB (1979) Structures of the motile cells of Coe-
Meloidogyne graminicola causing root knot dis- lomomyces psorophorae and function of the zygote in
ease of rice (Oryza sativa L.). World J Microbiol encystment on a host. Can J Bot 57:1021–1035
Biotechnol 23:291–294 Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J,
Slapeta J, Moreira D, Lopez-Garcia P (2005) The extent Young JPW (2002) Evolution - Extensive fungal
of protist diversity: insights from molecular ecol- diversity in plant roots. Science 295:2051–2051
ogy of freshwater eukaryotes. Proc R Soc B Biol Sci Vavra J, Joyon L (1966) Etude sur la morphologie le
272:2073–2081 cycle evolutif et la position systematique de Calli-
Sparrow FK (1939) The entomogenous chytrid Myro- mastix cyclopis Weissenberg. Protistologica 2:5–15
phagus Thaxter. Mycologia 304:113–116 Whisler HC (1987) On the isolation and culture of water
Sparrow FK (1960) Aquatic phycomycetes. University molds: the Blastocladiales and Monoblepharidales.
of Michigan Press, Ann Arbor, MI In: Fuller MS, Jaworski A (eds) Zoosporic fungi in
Sparrow FK (1962) Urophlyctis and Physoderma. Trans teaching and research. Southeastern, Athens, GA,
Mycol Soc Jpn 3:16–18 pp 121–124
Sparrow FK (1965) Concerning Physoderma graminis. Willoughby LG (1959) A new species of Blastocladiella
Mycologia 57:624–627 from Great Britain. Trans Br Mycol Soc 42:287–291
Sparrow FK, Griffin JE (1964) Observation on chytri- Wilson CM (1952) Meiosis in Allomyces. Bull Torr Bot
diaceous parasites of phanerograms. XV. Host Club 79:139–160
range and species concepts studies in Physoderma. Wilson CM, Flanagan PW (1968) The life cycle and
Arch f Mikrobiol 40:275–282 cytology of Brachyallomyces. Can J Bot 46:1361–
Stumm C, Hermans JMH, Croes AF, Bucks JH (1976) 1367
Chemotaxis and transport of amino acids in Allo- Wolf FT (1941) A contribution to the life history and
myces arbuscula. Ant v Leeuwenhoek 42:203–209 geographic distribution of the genus Allomyces.
Tabak HH, Cooke WB (1968) Effects of gaseous envir- Mycologia 33:158–173
onments on growth and metabolism of fungi. Bot
Rev 34:126–252

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7 Blastocladiomycota

TIMOTHY Y. JAMES1, TERESITA M. PORTER2, W. WALLACE MARTIN3

Systematics and Evolution, 2nd Edition

rDNA operon clades and Blastocladiomycota

Catenaria spinosa (3)

Coelomomyces (4) + Coelomomycetaceae

Paraphysoderma sedebokerense (1)

V. Life Cycles B. Life Cycles of Allomyces

Gametangium Gametangium Gametangium Gametangium ♂ ♀

Planozygotes Planozygotes Planozygotes

Zoospores Meiospores Meiospores

Resistant Resistant Resistant

B. Generalized Structure of Motile Cells in distinguishing major clades, subclades, and

Surveys of ultrastructural characters in motile

Fig. 7.9 Coelomomyces punctatus. Interpretive draw- K

3. Flagellar Apparatus 4. Cytoplasmic Inclusions

The highly selfing nature of Allomyces B. Mitosis

What the blastoclads lack in species number

described. A major unanswered question is how species-specific in inoculation studies (Sparrow

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