Pucciniomycotina

Abstract

More than 8 % of all described Fungi belong to subphylum Pucciniomycotina, the basal lineage of Basidiomycota. Pucciniomycotina is well supported as monophyletic, as are eight of its nine classes, the exception being Agaricostilbomycetes. All members of the subphylum thus far studied have simple septal pores lacking dolipore swellings or septal pore caps and layered spindle pole bodies. Fungi belonging to Pucciniomycotina are found in a diversity of habitats, with the majority found in association with plants, predominantly as phytopathogens but also as asymptomatic members of the phylloplane and mycorrhizal symbionts of orchids. Life cycles range from simple teliosporic yeasts to the elaborate five spore-stage life cycles found in the biotrophic rust fungi, Pucciniales. The number of species and lineages of Pucciniomycotina continues to rise, and it is predicted that much diversity within this group remains to be discovered.

Full text

10 Pucciniomycotina
M. CATHERINE AIME
1
,MERJE TOOME
1
,DAVID J. MCLAUGHLIN
2
CONTENTS
I. Introduction ................................. 271
II. Systematics of Pucciniomycotina .......... 273
III. Diversity ..................................... 276
A. Ecological Diversity ...................... 276
B. Life Cycles. . . . . . . . . . . ...................... 278
C. Morphological and Genomic Diversity . . 278
D. Species Discovery and Diversity . . . . . . . . . 283
IV. Classification ................................ 283
A. Agaricostilbomycetes . . . . . . . . . ............ 284
B. Atractiellomycetes . . ...................... 285
C. Classiculomycetes . . ...................... 285
D. Cryptomycocolacomycetes . . . ............ 286
E. Cystobasidiomycetes. . . . . . . . . . ............ 286
F. Microbotryomycetes ...................... 287
G. Mixiomycetes . . . . . . . ...................... 288
H. Pucciniomycetes. . . . ...................... 288
I. Tritirachiomycetes . . ...................... 289
V. Culturing..................................... 290
VI. Conclusion ................................... 290
References. . . . . . . . ............................ 290
I. Introduction
More than 8,400 species of Pucciniomycotina
have been described (Table 10.1), or more than
8 % of all described Fungi (at 98,998 spp.) (Kirk
et al. 2008). Pucciniomycotina is the sister to
the Ustilaginomycotina and Agaricomycotina,
forming the basal lineage of Basidiomycota. All
members of the subphylum thus far studied
have simple septal pores lacking dolipores
(septal pore swellings) and septal pore caps,
which, along with predominant cell wall sugars
(mannose, Prillinger et al. 1993) and disclike
spindle pole bodies (McLaughlin et al. 1995;
Wells 1994), distinguishes them from most
other Basidiomycota. Although some Ustilagi-
nomycotina species appear to have simple
septal pores (e.g., Lutzoni et al. 2004), these
are reportedly associated with membranous
plates that are continuous with the plasma
membrane (Bauer et al. 2006). While the
position of Pucciniomycotina and the mono-
phyly of eight of the nine classes have
been established, deeper level phylogenetic
relationships within the subphylum have yet
to be resolved (Fig. 10.1).
Fungi belonging to Pucciniomycotina
are found in a diversity of habitats, including
specialized niches that are historically
undersampled for Fungi. Ecologically, most
discovered species are plant associates,
predominantly phytopathogens but also
including asymptomatic members of the
phylloplane and species that form mycorrhizal
associations with orchids. Others are insect and
fungal pathogens, and a few are presumably
saprobic. Pucciniomycotina species have been
recovered from soils, freshwater and marine
habitats, and the Arctic and tropical environ-
ments. They are shown to have an array of life
cycles, ranging from simple teliosporic yeasts
(Fig. 10.2)to the elaborate five-stage life cycles
of the biotrophic rust fungi (Fig. 10.3), often
regarded as the most complex organisms
in Kingdom Fungi (Lutzoni et al. 2004). The
number of new species and new lineages of
Pucciniomycotina continues to rise, and it is
predicted that much diversity within this
group remains to be discovered.
1
Department of Botany and Plant Pathology, Purdue Univer-
sity, West Lafayette, IN 47907, USA; e-mail: maime@purdue.
edu;
2
Department of Plant Biology, University of Minnesota, St.
Paul, MN 55108, USA
Systematics and Evolution, 2
nd
Edition
The Mycota VII Part A
D.J. McLaughlin and J.W. Spatafora (Eds.)
©Springer-Verlag Berlin Heidelberg 2014

Table 10.1 Pucciniomycotina: classes, orders, families, and number of species
Class Order Family
No.
spp.
Agaricostilbomycetes
R. Bauer et al.
a
75 spp.
Agaricostilbales Oberw. & R. Bauer Agaricostilbaceae Oberw. & R. Bauer 30
Chionosphaeraceae Oberw. &
Bandoni
34
Kondoaceae R. Bauer et al.
a
6
Spiculogloeales R. Bauer et al.
a
Spiculogloeaceae Denchev 5
Atractiellomycetes
R. Bauer et al.
a
44 spp.
Atractiellales Oberw. & Bandoni
Incertae sedis
Hoehnelomycetaceae Ju
¨lich
Phleogenaceae Ga
¨um.
38
1
Saccoblastiaceae Ju
¨lich 2
3
Classiculomycetes R. Bauer
et al.
a
2 spp.
Classiculales R. Bauer, Begerow,
Oberw. & Marvanova
´
Classiculaceae R. Bauer, Begerow,
Oberw. & Marvanova
´
2
Cryptomycocolacomycetes
R. Bauer et al.
a
2 spp.
Cryptomycocolacales Oberw. &
R. Bauer
Cryptomycocolacaceae Oberw. &
R. Bauer
2
Cystobasidiomycetes
R. Bauer et al.
a
43 spp.
Cystobasidiales R. Bauer et al.
a
Cystobasidiaceae Gum. 11
Erythrobasidiales R. Bauer et al.
a
Erythrobasidiaceae Denchev 11
Naohideales R. Bauer et al.
a
Incertae sedis
Naohideaceae Denchev 1
20
Microbotryomycetes
R. Bauer et al.
a
227 spp.
Heterogastridiales Oberw. &
R. Bauer
Heterogastridiaceae Oberw. &
R. Bauer
7
Kriegeriales Toome & Aime
Leucosporidiales J.P. Samp.
M. Weiss & R. Bauer
Kriegeriaceae Toome & Aime
Camptobasidiaceae R.T. Moore
Leucosporidiaceae Ju
¨lich
9
5
15
Microbotryales R. Bauer & Oberw. Microbotryaceae R.T. Moore 105
Ustilentylomataceae R. Bauer &
Oberw.
11
Sporidiobolales Doweld
Incertae sedis
Sporidiobolaceae R.T. Moore 37
39
Mixiomycetes
R. Bauer et al.
a
1 sp.
Mixiales R. Bauer et al.
a
Mixiaceae C.L. Kramer 1
Pucciniomycetes
R. Bauer et al.
a
8016 spp.
Helicobasidiales R. Bauer et al.
a
Helicobasidiaceae P.M. Kirk 17
Pachnocybales Bauer et al. Pachnocybaceae Oberw. & R. Bauer 1
Platygloeales R.T. Moore Eocronartiaceae Ju
¨lich 9
Platygloeaceae Racib. 6
Pucciniales Clem. & Shear Chaconiaceae Cummins & Y. Hirats. 75
Coleosporiaceae Dietel 313
Melampsoraceae Dietel 90
Mikronegeriaceae Cummins &
Y. Hirats.
13
Phakopsoraceae Cummins &
Y. Hirats.
205
Phragmidiaceae Corda 164
Pileolariaceae Cummins & Y. Hirats. 34
Pucciniaceae Chevall. 6,095
Raveneliaceae Leppik 323
Uncolaceae Buritica
´3
Uropyxidaceae Cummins & Y. Hirats. 143
Septobasidiales Couch ex Donk
Incertae sedis
Incertae sedis
Septobasidiaceae Racib.
340
179
6
Tritirachiomycetes Aime &
Schell
6 spp.
Tritirachiales Aime & Schell Tritirachiaceae Aime & Schell 6
Numbers are approximate estimates from Kirk et al. (2008), Kurtzman et al. (2011), and newly published papers cited in text
a
R. Bauer, Begerow, J. P. Samp., M. Weiss & Oberw.
272 M.C. Aime et al.

II. Systematics of Pucciniomycotina
Most early treatments of basidiomycetes recog-
nized one main division in the group, between
those species that formed holobasidia (homo-
basidiomycetes) and those with phragmobasi-
dia (heterobasidiomycetes). However, analyses
of 5S ribosomal RNA sequences by Walker
and Doolittle (Walker and Doolittle 1982)
divided Basidiomycota into two groups, not
by any traditional characters but by whether
they possessed simple pores or dolipores.
Agaricoslbum hyphaenes
Bensingtonia yuccicola
Sporobolomyces linderae
Mixia osmundae
Trirachium oryzae
Trirachium roseum
Sporobolomyces coprosmae
Bannoa sp.
Sakaguchia dacryoidea
Naohidea sebacea
Sphacelotheca polygoni-persicariae
Microbotryum violaceum
Leucosporidium scoi
Colacogloea peniophorae
Classicula fluitans
Jaculispora submersa
Cryptomycocolax abnormis
Helicogloea lagerheimii
Helicogloea variabilis
Platygloea vesta
Endocronarum harknessii
Helicobasidium mompa
Septobasidium canescens
Auricularia sp.
Coprinus comatus
Calocera cornea
Cryptococcus neoformans
Tillea goloskokovii
Cintraca limitata
Sporisorium reilianum
Ustanciosporium standleyanum
Tillearia anomala
Malassezia pachydermas
Leoa lubrica
Taphrina wiesneri
0.05 substuons/site
AGARICOMYCOTINA
USTILAGINOMYCOTINA
ASCOMYCOTA
Atractiello mycetes
Agaricostilbomycetes
Mixiomycetes
Tritirachiomycetes
Cystobasidiomycetes
Microbotryomycetes
Classiculomycetes
Cryptomycocolacomycetes
Pucciniomycetes
//
*
*
*
**
*
*
*
*
*
*
*
*
*
*
*
*
*
*
PUCCINIOMYCOTINA
*
Fig. 10.1 Phylogenetic resolution of Pucciniomycotina
classes. Tree based on maximum likelihood analyses of
combined nuclear ribosomal small and large subunits
and translation elongation factor 1-alpha DNA
sequences. Ascomycota sequences included as out-
groups; representative Agaricomycotina and Ustilagi-
nomycotina sequences included to show monophyly of
Pucciniomycotina. Asterisk (*) denotes nodes that have
received strong (>80 %) support in the analyses of
Aime et al. (2006), Padamsee et al. (2012), and Schell
et al. (2011). Backbone resolution remains poor within
Pucciniomycotina. Figure adapted from Schell et al.
(2011)
Pucciniomycotina 273

Gottschalk and Blanz (Gottschalk and Blanz
1985) expanded that work by sampling a large
diversity of mostly basidiomycetous yeasts and
taking into account the 5S RNA secondary
structure in addition to sequence, again
showing a deep division of Basidiomycota
into two groups. Those with type A secondary
structure included members of the smut group
pro parte (p.p.) (including the anther smut
Microbotryum) and members of the heteroba-
sidiomycetes that had simple septal pores,
including members of Auriculariales p.p. and
Atractiellales p.p. (Gottschalk and Blanz 1985).
Species with type B secondary structure were
found in most of the smut groups excepting the
anther smuts, in heterobasidiomycetes with
dolipore septa, and in mushroom-forming
fungi (Gottschalk and Blanz 1985). The asco-
mycete Taphrina deformans was found to have
a 5S secondary structure of type A, while the
rust fungi, represented by four species in their
analyses, were reported to have type B
secondary structure (Gottschalk and Blanz
1984,1985). Cladistic analyses by these authors
of the representative 5S RNA sequences
provided evidence for a basal lineage of Basi-
diomycota that included many yeast-forming
fungi, phragmobasidiate fungi, and smutlike
fungi that could be distinguished from their
convergent cohorts by the absence of dolipore
septa. The group with type A secondary struc-
ture was initially referred to as the simple
Fig. 10.2 Life cycle of Rhodosporidium toruloides
(Sporidiobolales).A. A transversely septate basidium
arises from a teliospore and gives rise to spores. B. The
spores bud and persist as yeasts. C. Yeast cells of the
proper mating types fuse via a thin hyphal connection
to form a dikaryon. D. The dikaryon forms hyphae that
will eventually give rise to teliospores. Figure from
Aime et al. (2006), courtesy of D. Henk and reprinted
with permission of Mycologia. copyright The Mycolog-
ical Society of America
274 M.C. Aime et al.

septate basidiomycete lineage (e.g., Nishida
et al. 1995)or Atractiellales sensu lato (s.l.)
(Hawksworth et al. 1995).
Subsequent analyses of small subunit
ribosomal DNA (rDNA) sequence (18S rDNA)
data revealed the existence of three, rather than
two, major lineages of Basidiomycota (Swann
and Taylor 1993,1995). With the exception of
the rust fungi, those with a type B secondary
structure belonged to two lineages, Ustilagino-
mycetes (true smut fungi, now Ustilaginomyco-
tina) and Hymenomycetes (mushroom-
forming fungi and their relatives with dolipore
septa, now Agaricomycotina). The lineage
containing the simple septate basidiomycetes
with type A secondary structure and the rust
fungi were united in Urediniomycetes (now
Pucciniomycotina) (Swann and Taylor 1995).
receptive hyphae spermatium
on the other
side of larch
leaf aecia form
aecium
aeciospores
spread to
willow leaves
urediniospores
uredinium with urediniospores
telium with teliospores
basidium
basidiospores
spread to
larch leaves
spermogonia
+–
Fig. 10.3 Life cycle of a heteroecious macrocyclic rust
fungus, Melampsora larici-epitea. The cycle begins
with the germination of haploid basidiospores on new
leaves of the alternate or aecial host (e.g., larch), where
they form spermogonia. Spermogonia are haploid, pro-
ducing receptive hyphae and specialized spores called
spermatia. Fertilization occurs by the fusing of sperma-
tia or hyphae of two opposite mating types. Dikaryotic
hyphae form aecial sori containing long chains of
aeciospores. Aeciospores function as wind-
disseminated propagules that serve to colonize the pri-
mary or telial host (e.g., willow). Germinating aecio-
spores produce dikaryotic uredinia with urediniospores.
The uredinial stage is the cyclic asexual stage, capable
of continuously reinfecting the primary host under
favorable conditions. In general, only when the host
starts to prepare for dormancy is the fifth, or telial,
stage triggered. Teliospores form within telia that are
produced from the same mycelium that previously pro-
duced urediniospores. Karyogamy occurs in the telio-
spores, which often have thick cell walls and an
endogenous dormancy period, serving as the overwin-
tering stage. In the spring, teliospores act as probasidia
and germinate into basidia. Meiosis occurs within basi-
dia of the auricularioid phragmobasidium type, pro-
ducing four haploid basidiospores that are forcibly
discharged to a new aecial host, completing the life
cycle. Figure from Toome (2010)
Pucciniomycotina 275

However, resolution of the relationship
between these three lineages of Basidiomycota
has been problematic with conventional molec-
ular systematics. Many studies, most relying on
rDNA sequence data, have recovered a topology
that places Pucciniomycotina as sister to the
other two subphyla, although these have been
weakly supported or unsupported (e.g., Bauer
et al. 2006; Lutzoni et al. 2004), whereas alter-
nate topologies, such as Ustilaginomycotina as
sister to the other two subphyla, have also been
recovered (Medina et al. 2011). In the higher-
level classification for Fungi proposed by the
Assembling the Fungal Tree of Life project, this
node remained unresolved (Hibbett et al. 2007).
However, recent analyses, based on 71 protein-
coding genes, have resolved the basal position
of Pucciniomycotina within Basidiomycota
(Padamsee et al. 2012). This topology is sup-
ported by studies of basidiomycete cell wall
carbohydrates, which in Pucciniomycotina,in
contrast to Agaricomycotina and Ustilagino-
mycotina, are predominantly of mannose and
lack xylose (Prillinger et al. 1993) and by the
septal pore and spindle pole body data dis-
cussed subsequently.
Molecular phylogenetic analyses fully
support Pucciniomycotina as monophyletic
and the monophyly of most of the classes
therein (e.g., Aime et al. 2006; Lutzoni et al.
2004; Schell et al. 2011). However, backbone
nodes within Pucciniomycotina have not been
resolved despite intensive sampling efforts that
included nearly the entire known generic diver-
sity (excluding that of the rust fungi) in the
subphylum (Aime et al. 2006); current research
is now focused on increased locus sampling.
Phylogenetic relationships within the subphy-
lum as currently understood are presented in
Fig. 10.1. The systematics of the lineages will be
discussed in the classification section.
III. Diversity
A. Ecological Diversity
Pucciniomycotina species play diverse ecological
roles, although these are incompletely known or
can only be inferred for a number of species and
lineages (Table 10.2). Plant associations domi-
nate and phytopathogens have arisen in several
classes (e.g., Pucciniomycetes, Microbotryomy-
cetes, Mixiomycetes). The rust fungi form both
the largest natural group of plant pathogens in
Fungi and the most speciose order in Puccinio-
mycotina (Table 10.1), comprising 95 % of the
subphylum and ca. 8 % of all described Fungi
(Kirk et al. 2008). Asymptomatic and presumably
saprobic phylloplane yeasts can be found in
Microbotryomycetes, Cystobasidiomycetes, and
Agaricostilbomycetes on hosts ranging from
lichens to Sphagnum mosses to vascular plants
(e.g., Ina
´cio et al. 2010; Kachalkin et al. 2008;
Sla
´vikova
´et al. 2009). The discovery that some
members of Atractiellomycetes form mycorrhi-
zae with neotropical orchids (Kottke et al. 2010)
makes this the basalmost lineage of mycorrhizal
associates in Basidiomycota since these sym-
bioses were previously known only from Agar-
icomycotina.
Mycoparasitism is observed or inferred
from culture characters (such as self-
parasitization), specialized subcellular charac-
ters (such as presence of colacosomes), or
mycophilic associations. Many mycoparasitic
species have been described from isolations
made from fungal fruiting bodies or co-isolated
with ascomycetous molds (e.g., Bauer et al.
2003; Beguin 2010; Kirschner et al. 2001), and
they are found to belong to several different
classes. Septobasidiales contains the only
entomopathogens, comprising species that are
symbiotic with scale insect colonies (Couch
1938), although the true nature of the
association may be more commensal than
truly parasitic (Henk and Vilgalys 2007).
Freshwater and marine yeasts can be found
primarily in Cystobasidiomycetes and some
Microbotryomycetes (Fell 1966; Sampaio 2004),
but they also include the enigmatic fungus
Reniforma strues, which was isolated from
biofilms in a wastewater treatment plant (Pore
and Sorenson 1990) and is placed incertae sedis
within Pucciniomycotina by rDNA sequences
(Aime et al. 2006). Classiculomycetes and Cyre-
nella elegans (Cystobasidiomycetes) are aquatic
hyphomycetes that share convergent characters
with other primarily ascomycetous aquatic fungi
(Bauer et al. 2003;Gochenaur1981).
276 M.C. Aime et al.

Table 10.2 Pucciniomycotina: Synopsis of key ecological and morphological characters by class
Class
Ecological
diversity
Asexual reproduction Sexual reproduction Subcellular characters
Yeast state Conidia Fruiting body Basidia Clamps
Septal pore
associations
Spindle pole
body Other features
Agaricostilbo-
mycetes
Mycoparasites,
saprobes
+ + (blasto-) Various—
stilboid,
pustulate
or none
Phragmo-, holo- +/Microbodies Multilayered
disc
Tremelloid
haustoria
Atractiellomycetes Saprobes, orchid
mycorrhiza
+ Stilboid,
resupinate
Phragmo- + Atractosomes,
microbodies
Multilayered
disc
Microscala/
symple-
chosomes
Classiculomycetes Aquatic,
mycoparasites
+ (triradiate) Phragmo-
w/subapically
swollen
sterigmata
+ Microbodies n/a Binucleate
tremelloid
haustoria
Cryptomyco-
colacomycetes
Mycoparasites (basidio-
spores
may form
yeast-like
buds)
+Holo-
(w/unique
development)
+ Microbodies,
pore plugs
Layered disc Colacosomes/
lenticular
bodies
Cystobasidio-
mycetes
Mycoparasites,
saprobes
+(+in
Cyrenella)
Holo-, phragmo- + Cystosome pore
plug
n/a Tremelloid
haustoria
Microbotryo-
mycetes
Phyto- or
mycoparasites,
saprobes
(aquatic)
+/+ Various—
pycnidioid,
sori
Phragmo- + Pulley-wheel-
shaped pore
plug,
microbodies
(Colacosiphon)
Subgloboid
with flat
internalized
layer
Colacosomes/
lenticular
bodies
Mixiomycetes Phytoparasite + ? Unknown n/a n/a n/a
Pucciniomycetes Obligate phyto-,
entomo- or
mycoparasites
(saprobe)
(+in Septo-
basidiales)
+ Various—
stilboid,
resupinate,
clavarioid,
sori
Phragmo-, holo- Pulley-wheel-
shaped pore
plug
Multilayered
disc
Microscala/
symple-
chosomes
Tritirachiomycetes Saprobes, human
pathogens,
mycoparasites
+Unknown Pore plug n/a n/a
Pucciniomycotina 277

Because of the microscopic or cryptic
nature of most of the fungi in Pucciniomyco-
tina, their presence and ecological roles may
have been overlooked in the past. For example,
sequences generated by environmental
sampling studies are providing data that sug-
gest the presence of unknown species of Puc-
ciniomycotina in soil rhizospheres (e.g., Porter
et al. (2008), as uncultured basidiomycete;
Stefani et al. (2010), as uncultured soil fungus),
anoxic deep-sea habitats (e.g., Bas et al. (2007),
as Urediniomycetes; Jebaraj et al. (2010), as
unnamed Pucciniomycotina), and Arctic ice
(D’Elia et al. 2009). In fact, extreme environ-
ments can harbor a diversity of psychrophilic
(e.g., Libkind et al. 2005; Libkind et al. 2010;
Turchetti et al. 2011), osmotolerant (e.g., Fell
1966), and toxicity-tolerant (e.g., Pohl et al.
2011) Pucciniomycotina yeasts, and such envir-
onments may prove to harbor additional
untapped diversity.
B. Life Cycles
A striking feature of Pucciniomycotina is the
predominance of asexual stages within most
lineages. Some lineages, in fact, are known
only from anamorphs, such as Tritirachiomy-
cetes and, potentially, Mixiomycetes
(Table 10.2). Perhaps another striking charac-
ter of Pucciniomycotina is the number of
unique developmental patterns and life cycles
that apparently arose in what might be thought
of as early experiments into basidiomycetiza-
tion, culminating in the elaborate life cycles in
Pucciniales wherein up to five different sporu-
lating stages can be produced on two unrelated
hosts (Fig. 10.3). Interestingly, the character of
heteroecism seems to have arisen only once in
Fungi outside of Pucciniomycetes in the unre-
lated chytrid genus Coelomomyces (Blastocla-
diales, Blastocladiomycetes) (Whisler et al.
1975; see James et al. 2014). The complexity of
the rust life cycle is perhaps why complete life
cycle data are missing for many of the species,
including emerging pathogens of great agricul-
tural significance such as Phakopsora pachyr-
hizi,Puccinia psidii, and Hemileia vastatrix.At
the other extreme are simple teliosporic yeasts,
such as found in Sporidiobolales (Fig. 10.2).
Other life cycles will be discussed within the
relevant sections to follow.
C. Morphological and Genomic Diversity
The morphological diversity in Pucciniomyco-
tina is immense. Table 10.2 presents some
salient morphological characters by class. A
diversity of sporulating forms is exhibited in
Pucciniomycotina species, ranging from
macrobasidiocarp formers to single-celled
yeasts (e.g., Fig. 10.4). To cite a few examples,
when present, basidiocarps may be stipitate-
capitate or stilboid, such as the fruiting bodies
of Agaricostilbum species, resupinate, as is
found in, for example, Septobasidium and Heli-
cobasidium species, sporodochial, as in Myco-
gloea species, or, rarely, clavarioid, as in
Eocronartium muscicola; others, such as
Pucciniales and Microbotryum species, form
spore-filled sori within their hosts.
As early basidiomycetes evolved, new
mechanisms for spore formation and dispersal
must have arisen, resulting in the amazing
variety of basidial morphologies present in
extant Pucciniomycotina (e.g., Figs. 10.5–11).
In Cystobasidiomycetes alone basidia may be
unicelled, phragmobasidia of the auricularioid
type (i.e., transversely septate), elongate
filamentous phragmobasidia, or two-celled
with budding basidiospores, and they may
germinate from probasidia, teliospores, or
directly from terminal hyphal cells. Mechan-
isms for producing and dispersing mitospores
are also diverse (e.g., Fig. 10.12). These may
reproduce, for example, by budding, ballistos-
poric discharge from stalklike condiophores,
or production of sessile conidia. Mitospores
may be single-celled, multicelled and coiled
(e.g., Hobsonia spp.), or resemble those of
Ingoldian fungi with filamentous appendages
adapted for water dispersal (e.g., C. elegans).
The anamorphic yeast Reniforma strues has
kidney-shaped cells that produce miniature
reniform buds (Pore and Sorenson 1990). One
unique spore developmental pattern is found
278 M.C. Aime et al.

within the monotypic Mixia osmundae, which
produces hundreds of exogenous, enteroblastic
spores at a time from a single saclike sporoge-
nous cell (Nishida et al. 1995). Although the life
cycle of this fungus remains to be fully
described, recent genomic studies have sug-
gested that the spores on these sporogenous
cells are likely mitotic (Toome et al. 2014).
A uniting feature of Pucciniomycotina is
the presence of simple septal pores that lack
dolipores and septal pore caps (parenthe-
somes) that otherwise characterize most Basi-
diomycota (Celio et al. 2006). The presence of
Woronin bodies in association with the septal
pore is characteristic of Pezizomycotina in the
Ascomycota. Although Woronin-like bodies
Fig. 10.4 Representatives of Pucciniomycotina. a. Jola
cf. javensis (Platygloeales) fruiting on Sematophyllum
swartzii (E. Frieders).b. Septobasidium burtii (Septo-
basidiales) fungal mat completely covering scale insects
(D. Henk). c. Eocronartium muscicola (Platygloeales)
fruiting on moss Climacium dendroides (E. Frieders). d.
Yeast and filamentous cells of Sporidiobolus pararoseus
(Sporidiobolales) (M.C. Aime). e. Cultures of two Spor-
idiobolus species in S. pararoseus clade (Sporidiobo-
lales) (M.C. Aime). f. Phragmidium sp. (Pucciniales)
on Rosa rubiginosa (M.C. Aime). Figure from Aime
et al. (2006) and reprinted with permission of Mycolo-
gia. copyright The Mycological Society of America
Pucciniomycotina 279

Figs. 10.5–10.13 Basidial and conidial morphology in
Pucciniomycotina. 5–11. Basidia. 5. Gasteroid auricu-
larioid basidium of Atractiella sp. with sessile basidios-
pores; differentiated probasidium absent (E. Swann,
ECS CR27); bar 10 mm. 6. Gasteroid basidium of Micro-
botryum reticulatum with teliospore, sessile basidios-
pores, and yeast stage (E. Swann, ECS 698); bar 5mm. 7.
Gasteroid auricularioid basidium of Agaricostilbum
pulcherrimum with multiple basidiospores on each
compartment (F. Oberwinkler, F219); bar 5mm. 8. Bal-
listosporic auricularioid basidium of Jola cf. javensis
with differentiated probasidium (P) (E. Frieders, EMF
004); bar 5mm. 9. Deciduous auricularioid metabasidia
of Kriegeria eriophori prior to basidiospore production
280 M.C. Aime et al.

have been reported in Agaricostilbomycetes
and Cryptomycocolacomycetes (Kirschner
et al. 2001; Oberwinkler and Bauer 1989,
1990), cytochemical data are needed to ascer-
tain whether these are homologous with the
similar structures in ascomycetes (Celio et al.
2006; Dhavale and Jedd 2007; Roberson et al.
2010). Additional septal pore features may be
diagnostic for some classes. For instance, pores
may be occluded by a pulley-wheel-shaped plug
associated with a zone of organelle exclusion
bounded by microbodies (e.g., Pucciniomy-
cetes) (Fig. 10.14) or by a cystosome, a more
or less cylindrical plug with a reticulate surface
(e.g., Cystobasidiomycetes; Sampaio et al.
1999), or distinctive pore-associated microbo-
dies may be present (e.g., Atractiellomycetes)
(Fig. 10.15).
Spindle pole bodies (SPBs), organelles that
organize microtubules during nuclear division,
and nuclear division characters have been
examined for many Pucciniomycotina (e.g.,
McLaughlin et al. 1995; Swann et al. 2001 and
references therein). All species in Pucciniomy-
cotina have layered discoid (although this may
verge on globoid) SPBs (Figs. 10.16, 17). SPB
morphology has not been studied in all classes,
but it seems to be a diagnostic character for at
least some (Celio et al. 2006) (Table 10.2). Dur-
ing nuclear division the SPB in many Puccinio-
mycotina is more or less internalized within
the nucleus, but in the Pucciniomycetes and
Atractiellomycetes it is inserted in a nuclear
pore (Figs. 10.16, 17). In Pucciniomycetes,
except for Pucciniales, and Atractiellomycetes
the SPB is surrounded by an endoplasmic retic-
ulum cap (Fig. 10.17), the loss of which seems
to be apomorphic in Pucciniales (Fig. 10.16).
One subcellular character that seems to be
synapomorphic for Atractiellomycetes is the
presence of membrane complexes called micro-
scala or symplechosomes (McLaughlin 1990;
Oberwinkler and Bauer 1989). These consist of
stacked cisternae of endoplasmic reticulum
that are regularly cross-linked by filaments
that may also connect them with mitochondria
(Fig. 10.18). Colacosomes (sometimes referred
to as lenticular bodies), subcellular organelles
associated with mycoparasitism that serve to
connect the hyphal cell of the host with that
of the parasite, are found in many species
(Bauer et al. 1997), especially in Cryptomycoco-
lacomycetes and Microbotryomycetes.
Tremelloid haustoria, named for the type
of haustoria formed by mycoparasitic Tremel-
lales (Agaricomycotina), can be found in many
mycoparasitic or presumed mycoparasitic
Pucciniomycotina, although it is not known
whether these structures are truly homologous
with those formed in Tremellales. Nonetheless,
in Classiculomycetes these haustorial cells are
binucleate, rather than uninucleate as in all
other studied species, and are thus diagnostic
for this class (Bauer et al. 2003). The production
of coenocytic hyphae in Mixiomycetes may be
synapomorphic for that lineage and is other-
wise rare in basidiomycetes. Another rare
character in Fungi is branch origin, involving
the breaking of the hyphal wall. However, this
pattern occurs in both Pucciniomycetes and
Atractiellomycetes (Fig. 10.19) and seems to
be diagnostic for these classes (Swann et al.
2001).
Whole-genome data are lacking for most
lineages of Pucciniomycotina. However,
genome sizes for those known range from as
small as 13 Mbp for Mixia osmundae to 415
Mbp for the rust fungus Uromyces fabae,one
of the largest known in Fungi (Eilam et al. 1994;
Grigoriev et al. 2012). Complete genome
sequence data have been released for represen-
tatives of three classes, Pucciniomycetes, Micro-
botryomycetes and Mixiomycetes – Puccinia
graminis f. sp. tritici,P. triticina,P. striiformis,
Figs. 10.5–10.13 (continued) (J.C. Double
´s in Double
´s
and McLaughlin 1992); bar 10 mm. 10. Gasteroid holo-
basidium of Pachnocybe ferruginea with apical basi-
diospores (Kleven and McLaughlin 1988); bar 2.5 mm.
11. Maturing ballistosporic auricularioid basidium of
Helicogloea intermedia with saccate lateral probasi-
dium (P) and an adjacent probasidium prior to meta-
basidium formation (J.C. Double
´s); bar 10 mm. 12,13.
Conidia and conidiophores. 12. Microconidia forma-
tion in Atractiella sp. (D.J. McLaughlin, DJM 969); bar
5mm. 13. Sympodial conidium formation in Jola cf.
javensis (D.J. McLaughlin, DJM 739); bar 5mm. 5,6,8,
9,11–13. Bright-field micrographs. 7,10. Scanning elec-
tron micrographs. Figures reproduced from Swann
et al. (2001); collection or culture number in parenth-
eses
◂
Pucciniomycotina 281

Cronartium quercuum,andMelampsora larici-
populina (Pucciniales), R. graminis,Sporobolo-
myces sp. (as S. roseus) (Sporidiobolales), and
Microbotryum violaceum (Microbotryales) and
Mixia osmundae (Mixiales) [Grigoriev et al.
(2012); Microbotryum violaceum Sequencing
Project, Broad Institute of Harvard and
MIT (http://www.broadinstitute.org/); Puccinia
Group Sequencing Project, Broad Institute of
Harvard and MIT (http://www.broadinstitute.
org/]. Comparative genomics of these fungi has
already impacted our understanding of
the molecular bases of obligate biotrophy
(Duplessis et al. 2011).
Fig. 10.14–10.19 Subcellular structure in Pucciniomy-
cotina. Transmission electron micrographs. 14,15. Sep-
tal pore structure. 14. Pulley-wheel-shaped plug (large
arrow) in septal pore of Eocronartium muscicola and
zone of ribosome exclusion surrounded by microbo-
dies (small arrows) (D.J. McLaughlin, DJM 757-5); bar
0.2 mm. 15. Septal pore of Helicogloea sp. with adjacent
microbodies (arrow) (R.J. Bandoni, RJB 6478-5); bar
0.2 mm. 16,17. Spindle pole bodies (SPB). 16. Early
meiotic metaphase I SPB of Puccinia malvacearum
inserted into a pore of the nuclear envelope (arrows).
Spindle (S) (K.L. O’Donnell, in O’Donnell and
McLaughlin 1981); bar 0.2 mm. 17. Early mitotic meta-
phase SPB of Helicobasidium purpureum with endo-
plasmic reticulum cap (C). Nuclear envelope (arrows);
spindle (S) (T.M. Bourett, CBS 324.47); bar 0.1 mm. 18.
Microscala in hypha of Helicogloea variabilis with rod-
lets cross-linking endoplasmic reticulum and mito-
chondria (M) (from McLaughlin 1990); bar 0.2 mm.
19. Break (arrows) in outer hyphal wall during branch
(B) initiation in Jola cf. javensis (D.J. McLaughlin, DJM
739 ps); bar 1mm. Figures reproduced from Swann
et al. (2001); collection or culture number provided in
parentheses
282 M.C. Aime et al.

D. Species Discovery and Diversity
Approximately 8,416 species of Pucciniomyco-
tina have been described to date (Table 10.1),
the majority belonging to Pucciniales. A num-
ber of higher-level Pucciniomycotina lineages
are monotypic (e.g., Mixiomycetes, Naohi-
deales, Pachnocybaceae) or contain less than
ten described species (Tritirachiomycetes, Clas-
siculomycetes, Cryptomycocolacomycetes).
New species discovery continues at a high
rate. A recent study of the moldlike genus
Tritirachium reassigned these fungi to Pucci-
niomycotina, revealing several cryptic species
in the genus (Schell et al. 2011). New species
and genera have been recently described from
habitats not traditionally associated with
Pucciniomycotina, such as soil (e.g., Bauer
et al. 2009; Yurkov et al. 2011), beetle galleries
(e.g., Oberwinkler et al. 2006), and extreme or
toxic environments (e.g., Libkind et al. 2010;
Pohl et al. 2011). The phylloplane has continued
to be a rich source of species discovery, espe-
cially of yeasts in Microbotryomycetes (e.g.,
Golubev and Scorzetti 2010; Toome et al. 2013;
Vale
´rio et al. 2008).
Even within Pucciniales, whose members,
due to their importance in agriculture, have
been one of the better studied groups of
Fungi, new species discovery continues as
molecular systematic studies show that some
morphologically circumscribed species are, in
fact, composed of numerous, sometimes
unrelated, cryptic species. For example, in one
study, rust fungi morphologically assigned to
Melampsora epitea in the Pacific Northwest of
North America were found to belong to 14
different phylospecies, of which none seems to
have been previously described (Bennett et al.
2011), and investigations of the previously
monotypic genus Dasyspora revealed it to
contain at least 11 species within Central and
South America (Beenken et al. 2012).
IV. Classification
Pucciniomycotina contains 9 classes divided
into 20 orders and 37 families (Table 10.1).
The systematics and composition of the three
major lineages of Basidiomycota have been
rapidlyevolvingoverthelasttwodecades,
none more so than within Pucciniomycotina.
Before 2006 these fungi were known as
class Urediniomycetes, which comprised four
lineages (Swann and Taylor 1995). The appli-
cation of molecular systematics to fungal
studies has driven the expansion of Puccinio-
mycotina to now include many lineages of
fungi that had previously been placed within
other groups. Plesiomorphic characters, such
as that of a simple septal pore apparatus, led to
the original assignment of fungi in classes
Mixiomycetes and Tritirachiomycetes within
Ascomycota (Nishida et al. 1995;Schelletal.
2011). Another potentially plesiomorphic
character, that of phragmobasidia of the
auricularioid type (Fig. 10.11), led to the origi-
nal classification of most members of Platy-
gloeales in Auriculariales (Agaricomycotina).
Similarity in life cycles and morphology,
now known to be the result of convergent
evolution, led to the original classification of
Microbotryomycetes within the smut fungi
(Ustilaginomycotina).
Basidiomycetes with yeast states occur in
all three subphyla. Anamorphic yeasts under
previous versions of the International Code of
Botanical Nomenclature were treated sepa-
rately from teleomorphic species and assigned
to form genera principally based on carbon
assimilation tests (Kurtzman et al. 2011 and
references therein). Numerous molecular phy-
logenetic studies have highlighted the artificial-
ity of this system. For example, species of
Sporobolomyces occur across most of the
yeast-forming Pucciniomycotina classes; spe-
cies of Rhodotorula can be found in Ustilagi-
nomycotina and Pucciniomycotina (Sampaio
2004; Scorzetti et al. 2002). The type species
for both Rhodotorula (R. glutinus) and
Sporobolomyces (S. salmonicolor) are placed in
Sporidiobolales with molecular data (Scorzetti
et al. 2002). At the 2011 meeting of the Interna-
tional Botanical Congress changes were
adopted that will discontinue the use of a dual
nomenclature in Fungi (Hawksworth 2011).
One challenge for the future will be to
implement the changes now allowed under the
new Code and integrate the various clades of
Pucciniomycotina 283

Sporobolomyces and Rhodotorula and other
polyphyletic anamorphic yeast genera into a
phylogenetic classification.
A. Agaricostilbomycetes
The type genus Agaricostilbum was originally
described as an anamorphic member of the
Ascomycota and later transferred to the Auri-
culariales (Agaricomycotina) (Wright 1970;
Wright et al. 1981) before being allied in
Pucciniomycotina. Agaricostilbomycetes as
currently defined contains two orders,
Agaricostilbales and Spiculogloeales (Bauer
et al. 2006). The monophyly of both orders
has been demonstrated using molecular data
(e.g., Aime et al. 2006; Bauer et al. 2009), but
strong support for a monophyletic Agaricostil-
bomycetes as currently circumscribed is lack-
ing. Genera included in Agaricostilbales are
Agaricostilbum,Bensingtonia (anamorphic),
Chionosphaera,Cystobasidiopsis,Kondoa,
Kurtzmanomyces (anamorphic), Mycogloea p.
p., Sterigmatomyces (anamorphic), and Stil-
bum;Mycogloea p.p. and Spiculogloea are
assigned to Spiculogloeales; anamorphic Spor-
obolomyces yeasts are found in both orders
(Aime et al. 2006; Bauer et al. 2006 and refer-
ences therein; Bauer et al. 2009; Kurtzman et al.
2011). Mycogloea s.l. is not monophyletic
(Aime et al. 2006; Bauer et al. 2009), and sam-
pling of the type species, M. carnosa, is needed
to resolve the placement of this genus.
Together, the species of Agaricostilbomy-
cetes possess a wide array of ecological and
morphological variation. Most species are
believed to be either saprobic or mycoparasi-
tic.Agaricostilbum and Stilbum species are typ-
ically isolated from dead plant material (of
palms in the case of A. pulcherrimum), and
Cystobasidiopsis is known only from soil
(Bauer et al. 2009). However, there is evidence
for a mycoparasitic habit for many of the
species, and many could be mycoparasitic
rather than saprobic. For instance, the original
description of A. palmicola, the type species of
Agaricostilbum, notes that the fungus was
almost always found in association with an
ascomycetous Anthostoma-like fungus (Wright
1970). Chionosphaera,Mycogloea, and Kondoa
species are found similarly in association with
other fungi, and species of Spiculogloea are
known mycoparasites. Mycogloea and Spiculo-
gloea species also produce tremelloid hausto-
rial cells such as are commonly found in other
known mycoparasitic fungi, especially those in
Tremellales (Agaricomycotina) (Bauer et al.
2006). Species of Kurtzmanomyces seem to be
very rare and are known only from type
cultures (Kurtzman et al. 2011), in contrast to
A. pulcherrimum, which is pantropical in
distribution. Sterigmatomyces halophilus is
usually found in association with marine
environments, and both species of Sterigmato-
myces are osmotolerant (Fell 1966). The ecolog-
ical niche of many species, however, remains
unknown.
All species form a yeastlike stage, with
the exception of Cystobasidiopsis nirenbergiae
(Bauer et al. 2009), and, excepting C. nirenber-
giae, those with known teleomorphs are
dimorphic. With one exception (members of
the genus Chionosphaera), teleomorphic
species in Agaricostilbomycetes produce
phragmobasidia; species of Spiculogloea and
Kondoa are ballistosporic (Bauer et al. 2006),
and Kurtzmanomyces and Sterigmatomyces
species form ballistoconidia on a stalked
conidiophore, a character otherwise not found
in Pucciniomycotina (Kurtzman et al. 2011).
Stilboid basidiocarps are formed in three
genera (Agaricostilbum,Stilbum, and Chiono-
sphaera), and minute pustulate fruiting bodies
are formed by members of Mycogloea (Bandoni
1998). Basidia are formed directly from
probasidia on hyphae in Cystobasidiopsis
(Bauer et al. 2009).
The septal pore in Agaricostilbum species is
associated with microbodies containing
electron-dense material that has been suggested
to resemble the Woronin bodies of Ascomycota
(Oberwinkler and Bauer 1989). Additionally, in
studied members of the Agaricostilbaceae and
Chionosphaeraceae an unusual pattern of
mitosis has been documented wherein, in the
yeast phage, the nucleus divides in the parent
cell, rather than migrating into the bud prior
284 M.C. Aime et al.

to division (Frieders and McLaughlin 1996;
McLaughlin et al. 2004; Swann et al. 2001).
B. Atractiellomycetes
This class contains a single order, Atractiellales,
and fewer than 50 species in the genera
Atractiella,Basidiopycnis,Helicogloea, Hobso-
nia (anamorphic), Infundibura (anamorphic),
Leucogloea (anamorphic), Phleogena,Procero-
pycnis (anamorphic), and Saccoblastia.Atrac-
tiellales was originally erected to accommodate
a number of genera and species formerly placed
in Auriculariales (Agaricomycotina) and subse-
quently separated by the presence of simple
septal pores and 5S RNA secondary structure
(Gottschalk and Blanz 1985; Oberwinkler and
Bandoni 1982). As in Agaricostilbomycetes, stil-
boid fruiting bodies are formed in Atractiella
and Phleogena and basidia are phragmobasidia
of the auricularioid type. However, yeast states
are not known for these fungi, and anamorphic
states are typically conidial. In Hobsonia species
conidia are tightly coiled on short conidio-
phores, forming a minute sporodochium-like
fruiting body on dead vegetation (Martin 1959).
Ultrastructurally, members possess orga-
nelles termed microscala or symplechosomes
that have no known function but seem to be
synapomorphic for the class (Bauer et al. 2006;
McLaughlin 1990; Oberwinkler and Bauer 1989).
Perhaps the most intriguing Pucciniomycotina
discovery of recent years was that of the associa-
tion of three unidentified species of Atractiello-
mycetes with tropical orchids, confirmed by
transmission electron microscopy and molecu-
lar phylogenetics (Kottke et al. 2010). Prior to
this discovery, all Atractiellomycetes were pre-
sumed saprobic, and the basalmost mycorrhizal
formers known in Basidiomycota were to be
found within Auriculariales. The sampling area
of Kottke et al. (Kottke et al. 2010)waslimitedto
a tropical montane rainforest in southern
Ecuador; thus, it is unknown how widespread
this association is. Nonetheless, the find remains
significant for documenting the first known
instance of a plant mutualistic association
within Pucciniomycotina.
C. Classiculomycetes
This class contains a single order, Classiculales,
for which only two species are known, Classi-
cula fluitans (anamorph Naiadella fluitans)
and the hyphomycete Jaculispora submersa
(teleomorph unknown) (Hudson and Ingold
1960; Marvanova
´and Bandoni 1987). Morpho-
logical and sequence data clearly show that C.
fluitans and J. submersa form a separate lineage
in Pucciniomycotina (Aime et al. 2006; Bauer
et al. 2006). Both species are aquatic and are
associated with leaf litter in freshwater
habitats. Plant host preferences have been
tested for J. submersa and suggest an affinity
for oak leaves (Prokhorov and Bodyagin 2007).
Additionally, there is evidence that they may be
mycoparasitic; C. fluitans has been observed to
parasitize its own hyphae in culture, and both
species form tremelloid haustorial cells such
as are commonly found in other known
mycoparasitic fungi (Bauer et al. 2003).
In both C. fluitans and J. submersa the
septal pores are surrounded by microbodies
that are arranged in a circular pattern, such as
are also found in Pucciniales and a few other
members of Pucciniomycotina (Bauer et al.
2003). The combination of binucleate, tremel-
loid haustorial cells and pore-associated
microbodies, however, is unique to Classiculo-
mycetes. Both species are hyphal with hyaline
cells. Primary septa are formed in association
with nuclear division and have clamp connec-
tions; adventitious septa may also be formed
independently of nuclear division and are
clampless. Asexual reproduction takes place
via conidia that have two to three long fusiform
subapical appendages resembling the conidia of
other unrelated aquatic fungi (Marvanova
´and
Bandoni 1987), including the cystobasidiomy-
cete C. elegans. The sexual stage of C. fluitans
has been observed to occur only on the surface
of water. The basidia occur in clusters and have
auricularioid septation and subapically swollen
sterigmata, the last of which is unique in Puc-
ciniomycotina. Basidiospores are small and
fusiform, which is another convergent charac-
ter found in other unrelated aquatic fungi
(Bauer et al. 2003).
Pucciniomycotina 285

D. Cryptomycocolacomycetes
This is a small enigmatic class with two known
species, Cryptomycocolax abnormis (published
as C. abnorme) and Colacosiphon filiformis
(anamorphic) (Kirschner et al. 2001; Oberwink-
ler and Bauer 1990). Both species are appar-
ently rare, having been isolated only once
each from a parasitized ascomycete (C. abnor-
mis) and bark beetle galleries, where it was
found parasitizing a co-isolated ascomycete
(C. filiformis). Available DNA sequence data of
the nuclear ribosomal large subunit indicate
that these fungi form a separate class-level line-
age within Pucciniomycotina (Bauer et al.
2006). Unfortunately, type or other material of
either species could not be located for addi-
tional analyses, and thus phylogenetic resolu-
tion of this lineage will not be possible until
additional isolates are discovered.
Within Pucciniomycotina, the extremely
elongate holobasidia produced by C. abnormis
are unique.C. filiformis is described as mitos-
poric with elongate conidiophores (Kirschner
et al. 2001), although Bauer et al. (2006) indi-
cate that this species also produces elongate
basidia of the Cryptomycocolax type. Species
form hyaline hyphae that are clamped in Cryp-
tomycocolax; basidia are produced on the host
surface and undergo a unique developmental
pattern (Oberwinkler and Bauer 1990). Mem-
bers of Cryptomycocolacomycetes possess
mycoparasitic organelles termed colacosomes,
a character that is shared only with some
Microbotryomycetes. Microbodies interpreted
as Woronin-like bodies have been reported in
association with the septal pores of both species
(Kirschner et al. 2001; Oberwinkler and Bauer
1990); septal-pore-associated microbodies and
pore plugs are present on some, but not all,
septa of C. abnormis (Oberwinkler and Bauer
1990).
E. Cystobasidiomycetes
This is a small class of predominantly yeast-
like fungi. Genera include Bannoa,Cyrenella
(anamorphic), Cystobasidium,Erythrobasidium,
Naohidea,Occultifur, and Sakaguchia, as well
as several anamorphic yeasts currently placed
in Rhodotorula and Sporobolomyces (Aime
et al. 2006; Kurtzman et al. 2011), most of
which are, or presumably are, mycoparasitic.
For instance, C. elegans was isolated from a
mushroom that had been submerged in fresh-
water (Gochenaur 1981). Species of Cystobasi-
dium,Erythrobasidium,Naohidea, and
Occultifur have been isolated from ascomycete
or basidiomycete fruiting bodies. The number
of known species in this class has probably
tripled in the last decade, primarily because of
the discovery of new yeast species from extreme
habitats (e.g., Libkind et al. 2010; Pohl et al.
2011). As is also true of some Microbotryomy-
cetes, a number of species seem to be psychro-
philes (e.g., Libkind et al. 2008). The majority of
Cystobasidiomycetes genera (Bannoa,Cyre-
nella,Erythrobasidium,Naohidea, and Sakagu-
chia) are monotypic, and most of these are
known from single cultures or a single geo-
graphic locale, making it likely that a tremen-
dous amount of undiscovered diversity exists
within the class.
The variety of sexual state morphologies in
this group is unusual, although not all research-
ers have reached similar interpretations of the
structures involved, especially for Bannoa and
Erythrobasidium, for which the same reproduc-
tive cells have been described as basidial (e.g.,
Sugiyama and Suh 1993) or conidial (Bauer
et al. 2006). However, Kurtzman et al. (2011)
provide convincing evidence, including the
illustration of conjugation tubes and basidio-
spore germination, that these are indeed teleo-
morphic species. Bannoa and Erythrobasidium
species form holobasidia; Naohidea,Cystobasi-
dium,andOccultifur members form phragmo-
basidia of the auricularioid type, which
germinate from probasidia in the latter two but
not in Naohidea;andinSakaguchia dacryoidea
two- to four-celled basidia germinate from tel-
iospores produced on short hyphal stalks
(Kurtzman et al. 2011;Oberwinkler1990;
Sugiyama and Suh 1993;Yamadaetal.1994).
The bipolar multiallelic mating system of
Bannoa hahajimensis is unique within Pucci-
niomycotina (Kurtzman et al. 2011). C. elegans
is also unique among yeast species in produc-
ing subclavate tetraradiate conidia, which are
286 M.C. Aime et al.

found in unrelated aquatic hyphomycetes,
making an aquatic habit likely for this species
(Kurtzman et al. 2011). These differ from the
aquatic conidia produced in Classiculomycetes
in shape and number of appendages. Mycopar-
asitic tremelloid haustorial cells are produced
by members of Cystobasidiales (Bauer et al.
2006). Ultrastructurally, septal pores of Cysto-
basidiales are occluded by a cystosome.
F. Microbotryomycetes
Microbotryomycetes are known for containing
the model genetic organism Microbotryum vio-
laceum and several ubiquitous red yeasts
including Sporidiobolus pararoseus. Three
members of Microbotryomycetes, the yeasts
Sporobolomyces sp. (as S. roseus) and Rhodotor-
ula graminis and the anther smut M. violaceum,
are the only Pucciniomycotina species outside
of Pucciniales to be whole-genome sequenced to
date [Grigoriev et al. (2012); Microbotryum vio-
laceum Sequencing Project, Broad Institute of
Harvard and MIT (http://www.broadinstitute.
org/)]. With more than 200 described species,
it is the second largest class in Pucciniomyco-
tina (Kirk et al. 2008) (Table 10.1). Five orders
and seven families have been described. Genera
include Atractocolax,Aurantiosporium,Bauer-
ago,Camptobasidium,Colacogloea,Curvibasi-
dium,Fulvisporium,Heterogastridium,
Kriegeria, Krieglsteinera, Leucosporidium p.p.,
Liroa,Mastigobasidium,Meredithblackwellia,
Microbotryum,Rhodosporidium,Sphace-
lotheca,Sporidiobolus,Ustilentyloma,Zunde-
liomyces, and Zymoxenogloea (anamorphic),
and numerous anamorphic yeasts placed in
Glaciozyma,Leucosporidiella,Rhodotorula,
and Sporobolomyces, including the type species
of Rhodotorula and Sporobolomyces (Aime
et al. 2006; Bauer et al. 2006; Toome et al. 2013;
Turchetti et al. 2011). A large percentage of the
described genera are monotypic (e.g., Atracto-
colax,Camptobasidium,Fulvisporium,Hetero-
gastridium,Krieglsteinera,Liroa,
Mastigobasidium,Meredithblackwellia, and
Zundeliomyces), which may be an indication of
an as yet undiscovered diversity.
Microbotryum species, often referred to as
the anther smuts, were originally classified
within Ustilaginomycotina, although numerous
lines of evidence now show that the smut syn-
drome, including an anamorphic yeast phase,
gasteroid basidia, pigmented teliospores, and
parasitism of plant reproductive parts, has
independently evolved at least twice within
Basidiomycota. Most phylogenetic analyses
recover Microbotryomycetes as a monophyletic
class (e.g., Aime 2006; Bauer et al. 2006), yet
the backbone within the class has not been
adequately resolved, and nearly 20 % of the
species now classified in Microbotryomycetes
have not been confidently placed to order or
family (Table 10.1).
Yeast stages of this group are increasingly
recovered in environmental samplings of phyl-
loplanes, soils, and extremely cold habitats with
concomitant new species discovery (e.g., Golu-
bev and Scorzetti 2010; Kachalkin et al. 2008;
Libkind et al. 2005; Toome et al. 2013; Turchetti
et al. 2011; Vale
´rio et al. 2008; Yurkov et al.
2011). The tractability of many of these organ-
isms in the laboratory has led to the develop-
ment of molecular biological and genomics
tools for studying genetics and gene function
in Microbotryomycetes that are lacking in other
Pucciniomycotina (e.g., Coelho et al. 2011;
Ianiri et al. 2011). The first studies to identify
mating type loci in Pucciniomycotina were con-
ducted with a member of Microbotryomycetes
(Coelho et al. 2008; Giraud et al. 2008).
Most teleomorphic species are dimorphic
with haploid yeast stages and phragmobasidi-
ate teleomorphs, with the exception of Curvi-
basidium (Bauer et al. 2006). Colacosomes,
subcellular organelles associated with myco-
parasitism, of similar appearance to those in
Cryptomycocolacomycetes, are found in many
species (Bauer et al. 1997), but otherwise there
is a tremendous diversity in morphology and
ecology within this class, which is discussed in
detail in Bauer et al. (2006) and Swann et al.
(2001). There is a range of fruiting morpholo-
gies from the simple teliosporic yeasts, e.g.,
Rhodosporidium (Fig. 10.2), to the pycnidioid
fruiting bodies of Heterogastridium species.
Ecologically, many are plant associates, either
as presumably saprobic yeasts on plant surfaces
or as pathogens of leaves (e.g., Kriegeria) and
plant anthers (e.g., Microbotryum). Heterogas-
tridium species are mycoparasites, and the
Pucciniomycotina 287

presence of colacosomes in most other genera
in Heterogastridiales would suggest a similar
habit for these. The yeast Camptobasidium
hydrophilum is aquatic (Marvanova
´and Sub-
erkropp 1990), and several Sporidiobolales
members are cosmopolitan, having been recov-
ered from many terrestrial and marine habitats
(e.g., Sampaio 2004).
G. Mixiomycetes
Mixia osmundae is the only species currently
known in Mixiomycetes. It was first described
as an ascomycete (Taphrina osmundae) and
remained classified within Ascomycota for
more than 80 years, primarily due to superficial
similarities between the sporogenous cells of
Mixia and the asci produced by some Ascomy-
cota. However, molecular and closer morpho-
logical studies of the sporogenous cells in the
1990s provided multiple lines of evidence that
Mixia belongs to Basidiomycota (Nishida et al.
1995). Later phylogenetic analyses of rDNA
sequences support its placement in Basidiomy-
cota and show clearly that it is a member of
Pucciniomycotina (Aime et al. 2006; Bauer et al.
2006) (Fig. 10.1).
The fungus is an intracellular parasite of
ferns in the genus Osmunda,in which it causes
small yellow to brown leaf spots. Mixia is
known from Osmunda regalis in Japan and
Taiwan and Osmunda cinnamomea in the
USA (Kramer 1958; Mix 1947; Nishida 1911;
Sugiyama and Katumoto 2008), but it is rarely
found, and many aspects of its biology are
unknown.
When growing within a host, Mixia forms
intercellular coenocytic hyphal cells, forming
large saclike, nonseptate, sporogenous cells on
the surface of the host epidermis. The produc-
tion of coenocytic hyphae is a rare condition in
Basidiomycota, and the sporogenous cells pro-
duced by Mixia are unique in the phylum.Spore
production is very unusual in that the spores are
formed on the surface of the sporogenous cell
simultaneously, creating a powdery layer on fern
leaves (Nishida et al. 1995). Genome sequencing
revealed that these spores are haploid and likely
produced via asexual reproduction (Toome et al.
2014). In culture, M. osmundae forms yeastlike
cells that reproduce by budding. Septal pore
ultrastructure has not yet been determined for
this fungus, likely due to the limited formation of
septa (Bauer et al. 2006).
H. Pucciniomycetes
Pucciniomycetes is a diverse class containing
the vast majority (ca. 8000; Kirk et al. 2008)of
Pucciniomycotina species. Before the availabil-
ity of DNA sequence data, Pucciniomycetes
were placed in various positions on the fungal
tree of life. For instance, based on some of their
structural characters (e.g., lack of clamp con-
nections) and parasitic life style, Pucciniales
and their relatives were often thought to repre-
sent an early diverging lineage of Basidiomy-
cota. Phylogenetic studies based on rDNA have
shown that rust fungi and their closest relatives
in Pucciniomycetes are a derived group within
the Pucciniomycotina (Aime et al. 2006). One
earlier name for this lineage is Urediniomyce-
tidae sensu Swann et al. (2001).
Almost all of the organisms in Pucciniomy-
cetes are parasites of plants, insects, or
other fungi. The class contains five orders
(Table 10.1), the most speciose of which, at ca.
7,800 species in ca. 150 genera (Kirk et al. 2008),
is Pucciniales, or rust fungi, named for the typi-
cally rusty coloration of their urediniospores.
Rust fungi are parasites of vascular plants with
highly complex life cycles requiring the produc-
tion of up to five different spore stages on two
different host plants (Cummins and Hiratsuka
2003) (Fig. 10.3). In Fungi true obligate bio-
trophs, i.e., organisms that completely depend
on a living host to complete their life cycle, are
rare, mainly comprising the powdery mildews
(Erysiphales, Ascomycota) and the rust fungi.
Species of Pucciniales cause some of the most
devastating plant diseases and therefore have
been studied in greater detail than other Puc-
ciniomycotina. However, their obligately bio-
trophic nature renders them recalcitrant
organisms for molecular studies. Thus, family
and generic concepts are predominantly
morphology-based, which has led to the recog-
nition of several artificial taxa. Comprehensive
phylogenetic treatments of the order include
Aime (2006), Maier et al. (2003), and Wingfield
288 M.C. Aime et al.

et al. (2004). Descriptions of families and genera
can be found in Cummins and Hiratsuka (2003).
The remaining approximately 200 species
in the Pucciniomycetes are of little economic
importance. The largest among these is Septo-
basidiales [Auriculoscypha,Coccidiodictyon,
Johncouchia (anamorphic), Ordonia, Septoba-
sidium, and Uredinella], of which more than
150 species are known and which contains the
only entomopathogenic species in Pucciniomy-
cotina. Members of Septobasidiales parasitize
scale insects that feed on trees, forming dense
fungal mats that cover the insects on their hosts
(Couch 1938). The next two largest orders con-
tain species parasitic on mosses and ferns (Pla-
tygloeales, ca. 20 species in Eocronartium,
Herpobasidium,Jola,Insolibasidium, Platy-
gloea s.s., Platycarpa, and Ptechetelium)or
parasites that alternate between plant roots
and rust fungi (Helicobasidiales, ca. 17 species
of Helicobasidium, and its Tuberculina ana-
morph). Some species in Helicobasidiales have
been the focus of ecological studies to deter-
mine their potential as biocontrol agents
against rust fungi, but very little is known
about the other species in these orders. The
fifth order, Pachnocybales, contains a single
species, Pachnocybe ferruginea, which seems
to be a saprobe, having been repeatedly isolated
from creosoted telephone poles, and therefore
differs significantly from all other Pucciniomy-
cetes by having a nonparasitic habit.
The dikaryon is the dominant phase in
Pucciniomycetes, and only one of the orders,
Septobasidiales, is known to have a yeast stage.
However, production of asexual spores is often
well developed, especially among rust fungi.
Members of Pucciniomycetes lack clamp con-
nections (Bauer et al. 2006). Basidia are of the
auricularioid type, germinating from a proba-
sidium that, in the rust fungi, is a thick-walled
resting spore (i.e., teliospore). P. ferruginea is
again the exception for Pucciniomycetes in that
it produces holobasidia rather than phragmo-
basidia (Kropp and Corden 1986). Pucciniales
are heteroecious, i.e., they alternate between
two unrelated hosts during different stages of
their life cycle. Members of Helicobasidiales
also need to alternate between two hosts; the
dikaryon parasitizes plant stems and roots,
whereas the monokaryotic stage parasitizes
rust fungi in the Pucciniales (Lutz et al. 2004).
The most important ultrastructural charac-
ter of Pucciniomycetes is that of a simple septal
wall with a central pore that in many species
has a pulley-wheel-shaped plug (Swann et al.
2001), and the SPB is inserted into a pore of the
nuclear envelope (Bauer et al. 2006). In Septo-
basidiales and Pachnocybales, the presence of
microscala has also been reported (Swann et al.
2001).
I. Tritirachiomycetes
This class contains a single order, Tritira-
chiales, with six currently known Tritirachium
species. Until recently the genus Tritirachium
was placed in phylum Ascomycota, primarily
due to similarities in conidiophore morphology
with other mold species in subphylum Pezizo-
mycotina. However, multigene analyses based
on nuclear small and large subunits and trans-
lation elongation factor 1-alpha revealed that
most species currently placed in Tritirachium,
including the type species, belong to Puccinio-
mycotina (Schell et al. 2011).
All the members of Tritirachiomycetes are
anamorphic molds with no known teleo-
morphic stage. Species have been isolated
from dead plant roots, indoor environments,
and insects (Beguin 2010; Jebaraj et al. 2010;
Limber 1940; Schell et al. 2011). While the pre-
cise role of Tritirachium species in the environ-
ment is not known, there is strong evidence that
T. dependens is a potentially obligate parasite of
Penicillium and other ascomycetous species, on
which it depends for certain micronutrients
(Beguin 2010,asT. egenum). Two species, T.
oryzae and T. roseum, can be causal agents of
infections on human cornea and scalp (Moraes
et al. 2010; Rodrigues and Laibson 1975). There
is little information about the biology of Tritir-
achium species, and only those of potential
medical importance have been studied in
any detail. Although not originally identified
as such, environmental sequences of what
seem to be species of Tritirachium have been
Pucciniomycotina 289

generated from soil clones from a rhizosphere
in Canada in a study by Stefani et al. (2010) and
from minimally oxygenated deep waters of the
Arabian Sea reported by Jebaraj et al. (2010).
There is some overlapping of cultural and
morphological characteristics between the spe-
cies currently placed in Tritirachium; therefore,
morphological observations alone may not be
sufficient for diagnosing all members of this
genus at the species level. At the genus level,
Tritirachium species are hyphal in culture, pro-
ducing conidiophores that branch in a charac-
teristic zigzaglike pattern. Conidia are hyaline
and single-celled. Septal pores are uniperforate
with a small pore plug (Schell et al. 2011), but
little else is currently known of the subcellular
characters of these fungi.
V. Culturing
For the majority of Pucciniomycotina species
in Pucciniales, culturing on standard media is
not possible because these are obligate plant
pathogens. Nevertheless, various methods have
been developed to facilitate the multiplication
of rust fungi, and uredinial spore states can be
maintained on susceptible host plant tissue for
a number of species. A few species of rust fungi
have been successfully cultured from germinat-
ing basidiospores or hyphae from leaves; how-
ever, complex media are needed, and the
growth rate of such cultures is extremely slow
and limited (Kinloch and Dupper 1996; Mor-
icca and Ragazzi 2001).
Most other known members of Puccinio-
mycotina are culturable and grow well on stan-
dard nutrient sources, both in liquid and on
solid media. Those with forcible spore dis-
charge can be isolated via the spore fall method
by suspending the substrate (such as plant leaf)
above nutrient media with antibiotics (e.g.,
Toome et al. 2013). This method works well
for separating many mycoparasites from their
fungal hosts (e.g., Langer and Oberwinkler
1998). Gasteroid species, yeasts, and anther
smuts can be isolated via streak plating on
antibiotic media (e.g., Kurtzman and Fell
2004). Some halotolerant species, such as
Sterigmatomyces spp., can be isolated by expos-
ing air to media with high sodium (up to 20 %)
or glucose (up to 50 %) content (e.g., Fell 1966).
VI. Conclusion
Pucciniomycotina contains a diversity of fungi
that are united in possessing simple septal
pores that lack dolipores and septal pore caps.
Most, but not all, produce phragmobasidia,
and many have yeast states. Members now
united in Pucciniomycotina were previously
placed within Ascomycota and the other two
subphyla (Ustilaginomycotina and Agaricomy-
cotina) of Basidiomycota. More than 8 % of all
described Fungi belong to Pucciniomycotina,
whose members can be found in habitats
ranging from deep oceans and Arctic ice to
most terrestrial systems. Plant associations
dominate, and the majority of described
species are phytopathogens of vascular plants,
ferns, and mosses, but other members are
known as asymptomatic members of the phyl-
loplane, entomopathogens and mycoparasites,
or mycorrhizal symbionts of orchids. Life cycles
range from simple teliosporic yeasts to the elab-
orate life cycles found in the biotrophic rust
fungi. The description of new species of Pucci-
niomycotina has been steadily rising in the last
10 years, and it is predicted that much diversity
within this group remains to be discovered.
Acknowledgements Some of the figures were previ-
ously published in Swann et al. (2001), Aime et al.
(2006), and Toome (2010), and we would like to thank
the individuals who produced the original images,
including Drs. D. Henk, E.M. Frieders, J.C. Double
´s, E.
C. Swann, R.J. Bandoni, K. O’Donnell, and T.M. Bour-
ett. This work was supported in part by National Sci-
ence Foundation Grants DEB 0732968 and DEB-
0732550, Assembling the Fungal Tree of Life: Resolving
the Evolutionary History of the Fungi.
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