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Short Communication
How many fungi make sclerotia?
Matthew E. SMITHa,*, Terry W. HENKELb, Jeffrey A. ROLLINSa
a
University of Florida, Department of Plant Pathology, Gainesville, FL 32611-0680, USA
Humboldt State University of Florida, Department of Biological Sciences, Arcata, CA 95521, USA
b
article info
abstract
Article history:
Most fungi produce some type of durable microscopic structure such as a spore that is
Received 25 April 2014
important for dispersal and/or survival under adverse conditions, but many species also
Revision received 23 July 2014
produce dense aggregations of tissue called sclerotia. These structures help fungi to survive
Accepted 28 July 2014
challenging conditions such as freezing, desiccation, microbial attack, or the absence of a
Available online -
host. During studies of hypogeous fungi we encountered morphologically distinct sclerotia
Corresponding editor:
in nature that were not linked with a known fungus. These observations suggested that
Dr. Jean Lodge
many unrelated fungi with diverse trophic modes may form sclerotia, but that these
structures have been overlooked. To identify the phylogenetic affiliations and trophic
Keywords:
modes of sclerotium-forming fungi, we conducted a literature review and sequenced DNA
Chemical defense
from fresh sclerotium collections. We found that sclerotium-forming fungi are ecologically
Ectomycorrhizal
diverse and phylogenetically dispersed among 85 genera in 20 orders of Dikarya, suggesting
Plant pathogens
that the ability to form sclerotia probably evolved 14 different times in fungi.
Saprotrophic
ª 2014 Elsevier Ltd and The British Mycological Society. All rights reserved.
Sclerotium
Fungi are among the most diverse lineages of eukaryotes with
an estimated 5.1 million species (Blackwell, 2011). They are the
principle saprotrophs in most terrestrial biomes and play
important ecological and economic roles as plant pathogens
and mutualists. Fungi are found in all terrestrial ecosystems
and they use a variety of strategies to colonize appropriate
substrata and survive unfavorable conditions (Blackwell,
2011). They have significant impacts on the biology of plants
because they are the most economically significant plant
pathogens, serve as mycorrhizal and endophytic symbionts,
and act as key players in nutrient cycles (Schumann, 1991;
Rodriguez et al., 2009; Hobbie and Hogberg, 2012). Two fungal phyla, Basidiomycota and Ascomycota, comprise the
subkingdom Dikarya, a diverse group with ca. 100,000
described species (James et al., 2006). Most Dikarya share key
features such as a hyphal thallus, non-flagellated cells, and
the production of spores (Stajich et al., 2009). However,
because of their cryptic lifestyles within environments such
as plants and soil, the ecology and evolutionary history of
many fungi remains poorly understood.
Almost all fungi produce some type of durable, quiescent
microscopic structure such as a spore that is important for
dispersal and/or survival under adverse conditions (Stajich
et al., 2009). However, some fungi also produce dense aggregations of fungal tissue called sclerotia (Willetts, 1971). These
persistent structures help fungi to survive challenging conditions such as freezing temperatures, desiccation, microbial
attack, or the long-term absence of a host (Townsend and
Willetts, 1954; Coley-Smith and Cooke, 1971). Sclerotia are
highly variable in their morphology (Fig 1). Some have a hard,
* Corresponding author. Tel.: þ1 352 273 2837; fax: þ1 352 392 6532.
E-mail address: [email protected] (M.E. Smith).
http://dx.doi.org/10.1016/j.funeco.2014.08.010
1754-5048/ª 2014 Elsevier Ltd and The British Mycological Society. All rights reserved.
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
2
M.E. Smith et al.
Fig 1 e Morphologically variable sclerotia found in soil, leaf litter, and decayed wood in natural forest habitats of North and
South America: (A) Ceriporia sp. (MES 332; Polyporales) from decayed wood on the forest floor in Pigsah National Forest,
North Carolina, USA; (B) Entoloma sp. (MES 347; Agaricales) from soil in a tropical rainforest dominated by leguminous
ectomycorrhizal trees, Guyana; (C) Cheilymenia sp. (MES 313; Pezizales) from soil in mixed woods near Cherryfield, Maine,
USA; (D) unknown species of Amylocorticiales (MCA 3949) from soil and leaf litter in a tropical rainforest in Guyana; (E)
Boletus sp. (MES 260; Boletales) from soil and leaf litter in angiosperm-dominated forest in Lexington, Massachusetts, USA.
Identities of illustrated sclerotia were determined based on ribosomal DNA sequence comparisons with GenBank. Scale
bars [ approximately 10 mm.
melanized rind enclosing compact, undifferentiated hyphae
while others lack a rind (Willetts, 1971). Some species make
round, determinate sclerotia but others have indeterminate
forms where the shape and size are influenced by resources
and environmental conditions (Chet and Henis, 1975). Some
sclerotia are produced inside of host tissues; Claviceps purpurea
produces sclerotia in grass florets after it has destroyed the
plant cells (Douhan et al., 2008) and Ophiocordyceps sinensis
colonizes caterpillars and transforms their tissues into a
sclerotium (Xing and Guo, 2008). In contrast, some fungi make
sclerotia that are spatially separated from hosts (e.g. Phymatotrichopsis omnivora forms sclerotia deep in soil e Lyda, 1984).
Sclerotia also range in size from “microsclerotia” <1 mm
across, as in the plant pathogen Macrophominia phaseolina
(Short and Wyllie, 1978), to the massive sclerotia of Polyporus
mylittae that reach over 40 cm in diameter (Macfarlane et al.,
1978). Sclerotia putatively serve a resource-storage and survival role in all sclerotium-forming fungi. However, some
fungi such as Sclerotinia sclerotiorum produce sexual fruiting
structures directly on sclerotia (Bolton et al., 2006) whereas
others such as Pteromyces flavus (¼Aspergillus flavus) produce
fruiting bodies within sclerotia (Horn et al., 2009). Still others,
such as Boletus rubropunctus, produce fruit bodies and sclerotia
at different times or in different places (Smith and Pfister,
2009).
Although sclerotia have been documented in several fungal lineages, sclerotium formation is primarily recognized as a
key life history trait in several necrotrophic plant pathogens
(e.g. Sclerotium rolfsii, Rhizoctonia solani, M. phaseolina, P. omnivora, S. sclerotiorum). Collectively, these devastating host generalist pathogens are responsible for hundreds of millions of
dollars in global crop losses annually (Aycock, 1966; Parmeter,
1971; Purdy, 1979; Mulrean et al., 1984). For example, S. sclerotiorum and S. rolfsii each attack >400 plant species, including
major crops such as peanuts, potatoes, and soybeans, and can
cause up to 100 % yield losses (Jenkins and Averre, 1986;
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
How many fungi make sclerotia?
Bowen et al., 1992; Cintas and Webster, 2001). For these and
other sclerotium-forming pathogens, survival is tightly linked
with sclerotium formation so sclerotia eradication is critical
for disease control (Coley-Smith and Cooke, 1971). Furthermore, the ecology of these fungi cannot be fully understood without understanding the biology of sclerotium
formation.
Although management of serious plant pathogens is an
important rationale for studying sclerotium formation, there
are nevertheless several other compelling reasons. First,
many sclerotia lie dormant in soil, leaf litter, or wood for
months, so they must survive attacks from a wide variety of
natural enemies, including bacteria, other fungi, and invertebrates (Willetts, 1971; Papavizas, 1977; Matsumoto and
Tajimi, 1985). The mechanisms that allow sclerotia to survive in soil despite ongoing biotic assault are not well known,
but evidence from well-studied species (e.g. S. sclerotiorum, C.
purpurea) suggests that most sclerotia contain biologically
active secondary metabolites (Morrall et al., 1978; Demain,
1999; Schardl et al., 2006; Ikewuchi and Ikewuchi, 2008;
Frisvad et al., 2014). Since different fungi use unique suites
of compounds for chemical defense and nutrient storage
(Antibus, 1989; Calvo et al., 2002; Li and Rollins, 2010; Zheng
et al., 2010), sclerotium-forming fungi are excellent targets
for the discovery of antibacterial, antifungal, and antiherbivore compounds. Secondly, many non-parasitic fungi
are known to form sclerotia, so it is likely that this life history
trait is ecologically important for many fungal species and not
just for plant pathogens (Chet and Henis, 1975).
During investigations of hypogeous fungi, we encountered
morphologically variable sclerotia that were not clearly linked
with any known fungus (Fig 1). The wide variation in the
geography, microhabitats, and morphologies of these sclerotia suggested that the sclerotium-forming fungi were not
closely related and differed in their trophic modes. The
diversity of sclerotia encountered during random sampling
also suggested the possibility that many fungi form sclerotia
in nature but that these structures usually escape detection.
The discovery of these varied sclerotia generated several
questions. First, what are the identities of the unknown
sclerotium-forming fungi found in nature? Second, how many
unrelated lineages of fungi produce sclerotia? Third, besides
plant pathogens, what are the known ecological roles of the
sclerotium-forming fungi?
To answer these questions, we consulted the published
literature and studied sclerotia collected in nature. To identify
new sclerotium collections, we sequenced ribosomal DNA
(ITS, LSU, and/or SSU) using published protocols and compared these sequences with GenBank using BLAST searches
(Table 1) and preliminary phylogenetic analyses (data not
shown) (Altschul et al., 1990; Smith and Pfister, 2009; Tedersoo
and Smith, 2013). We also surveyed the literature to identify
sclerotium-forming fungi by querying Web of Science (www.
webofknowledge.com) and Google Scholar (http://scholar.
google.com/) with key words “sclerotia” and “sclerotium”. To
obtain a phylogenetic overview of sclerotium-forming fungi
(Fig 2), we created a database of sclerotium-producing genera
by recording one representative species and published reference for each genus reported to form sclerotia (Table 2). These
sclerotium-producing genera were then mapped onto a
3
schematic phylogeny based on Hibbett et al. (2007) with phylogenetic positions of new or revised orders inferred from
LoBuglio and Pfister (2010), Schoch et al. (2009a, 2009b), Binder
et al. (2010), Zhang et al. (2011), Toome et al. (2013), Boehm
et al. (2009), Campbell et al. (2009), and Padamsee et al.
(2012). All but two fungal species, Magnaporthe salvinii and
Verticilium dahliae, were easily resolved at the ordinal level
based on data from published references (Table 2) and Index
Fungorum (www.indexfungorum.org/).
We documented reports of sclerotium formation in species
from 85 fungal genera in at least 20 orders of Basidiomycota
and Ascomycota (Table 2, Fig 2). Since only one representative
sclerotium-forming species from each genus was recorded,
we cannot accurately estimate the number of sclerotiumforming species. However, we observed that many genera
with one sclerotium-forming species also contain others.
Also, despite our limited sampling of sclerotia, we found a
wide diversity of sclerotium-forming fungi in nature and
documented at least three genera for which sclerotium formation had not previously been reported, Ceriporia (Polyporales), Entoloma (Agaricales), and Cheilymenia (Pezizales), as
well as a sclerotium-forming fungus that could not be identified to genus (collection MCA3930, Table 1). These structures
were also found in a wide range of habitats from cool temperate forests in Maine (USA) to lowland tropical forests in
Guyana.
Although several review articles have discussed morphology, function, and diversity of sclerotia, the phylogenetic
relationships among the fungi involved were largely unresolved when these papers were published (Townsend and
Willetts, 1954; Coley-Smith and Cooke, 1971; Chet and Henis,
1975). When the affinities of the sclerotium-forming fungi are
viewed within the context of a molecular phylogeny, it is
obvious that sclerotium-forming fungi are widely dispersed
across the Dikarya. Although more detailed phylogenetic
analyses are needed to obtain a clear picture of the evolution
of sclerotium formation, we infer that the ability to make
sclerotia has probably evolved 14 different times within the
fungi (Fig 2). Our literature review and analysis of new collections also suggests that sclerotium formation is infrequent
or difficult to observe in some fungal orders (e.g. Dothidiales,
Helicobasidiales) but common and easy to observe in others
(e.g. Helotiales, Pezizales, Agaricales, Boletales).
The sclerotium-forming fungi also represent an extremely
wide trophic diversity. As expected, many sclerotium-forming
fungi are plant pathogens (25 genera) but many other
sclerotium-forming fungi are ectomycorrhizal (11 genera) or
saprotrophic (30 genera). The saprotrophs include specialists
on distinct substrata such as wood (Pleurotus), humus (Agrocybe), and dung (Cheilymenia). A few genera are also insect
pathogens (Ophiocordyceps), ericoid mycorrhizal (Phialocephala), animal pathogens (some Aspergillus), mycoparasites
(Laetisaria), or lichenicolous (Leucogyrophana) (Table 2). Two
genera (Trechispora, Fibulorhizoctonia) contain putative saprotrophs whose sclerotia are tended by termites in an unusual
symbiotic relationship that is analogous to brood parasitism
(Matsuura and Yashiro, 2010). Several sclerotium-forming
fungi, such as Helicobasidium purpureum (plant parasite/
mycoparasite) and Athelia arachnoidea (plant pathogen/
lichenicolous), have complex lifecycles that appear to involve
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
4
Genus of
sclerotiumforming
fungus
Cheilymenia
Unknown Genus
Inferred
ecology
Saprobe
?
Substrate
Order
Soil
Pezizales
Soil
Phylum
Ascoe
Collection
Collector and
number
collection
and herbarium
date
MES-313
(FLAS-F-58920)
ME Smith,
3-Aug-09
Amylocorticiales (?) Basidioe
MCA3930
(FLAS-F-58921)
ME Smith,
15-May-10
Morphology
Collection
location
Brown, rounded Mixed forest near
to irregular
Tunk Lake, outside
Cherryfield, Maine,
USA
Tan, rounded
Dicymbe forest in
the Pakaraima
Mnts., Guyana
Entoloma
Ectomycorrhizal
Soil and
leaf litter
Agaricales
Basidioe
MES-347
(FLAS-F-58922)
ME Smith,
18-Dec-09
Orange, round
Ceriporia
Saprobe
Decayed
wood
Polyporales
Basidioe
MES-332
(FLAS-F-58923)
ME Smith,
24-Oct-09
Tan to cream,
irregular
Boletus
Ectomycorrhizal
Soil and
leaf litter
Boletales
Basidioe
MES-260 (FH)
ME Smith,
19-Aug-08
Orange, lobed
Most informative
BLAST match
DQ220321 Cheilymenia
crucipila
(717/734 e 98 %),
LSU region
DQ144610 Amyloathelia
crassiuscula
(865/1023 e 85 %), ITS
and LSU regions
Mixed forest with
JF908003 Entoloma
Dicymbe, Pakaraima
platyphylloides
Mnts., Guyana
(603/644 e 94 %),
ITS region
Mixed forest,
JX644048 Ceriporia
Pisgah National Forest, purpurea
near Marion,
(677/704 e 96 %),
North Carolina, USA
LSU region
Angiosperm-dominated EU569236 Boletus sp.
woods, Arlington Great (779/808 e 96 %),
ITS region
Meadows, Arlington,
Massachusetts, USA
GenBank
KJ720887 (SSU),
KJ720888 (LSU)
KJ720886
(ITS, LSU)
KJ720892 (LSU),
KJ720893 (ITS)
KJ720890 (SSU),
KJ720891 (LSU),
KJ720889 (ITS)
FJ480429 (ITS)
M.E. Smith et al.
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
Table 1 e Collecting data, molecular data, and phylogenetic affiliations of new sclerotia specimens collected in soil, leaf litter, and wood
How many fungi make sclerotia?
5
Fig 2 e Simplified schematic phylogeny highlighting fungal lineages with sclerotium-forming fungi. Only members of the
Dikarya (Ascomycota and Basidiomycota) are shown because no sclerotium-forming fungi have been documented among
the early-diverging fungal lineages. Numbers adjacent to fungal orders indicate the number of genera containing at least
one sclerotium-forming species. Black circles indicate fungal orders for which all reports of sclerotium formation were
obtained from published sources whereas white circles indicate fungal orders for which a new record for sclerotium
formation is reported for at least one genus. The schematic phylogeny is based on Hibbett et al. (2007) with phylogenetic
positions of new or revised orders inferred from LoBuglio and Pfister (2010), Schoch et al. (2009a, 2009b), Binder et al. (2010),
Zhang et al. (2011), Toome et al. (2013), Boehm et al. (2009), Campbell et al. (2009), and Padamsee et al. (2012). The unresolved
phylogenetic positions of two sclerotium-forming Sordariomycetes, Magnaporthe salvinii and Verticilium dahliae, are
depicted with broken lines. To reduce the complexity of the figure, some known orders are not shown; asterisks highlight
areas of the tree where fungal orders not currently know to form sclerotia have been omitted.
multiple, distantly related host organisms. Still other genera,
such as the putative root endophyte Mattirolomyces and the
putative aphid symbiont Boletinellus, have uncertain trophic
modes (Brundrett and Kendrick, 1987; Kovacs et al., 2007).
Taken together, our observations suggest that sclerotium
formation is a more common life history trait among fungi
than previously recognized. The widespread occurrence of
this trait across the fungal phylogeny along with the diverse
trophic modes of sclerotium-forming fungi suggests that the
biology and evolution of sclerotium formation warrants
additional study. We expect that future research on sclerotium formation will find this feature to be even more widely
dispersed across the fungal phylogeny than detected here. We
suggest that sclerotium formation is analogous to highly
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
6
M.E. Smith et al.
Table 2 e Phylogenetic affiliations, trophic modes, and reference information for 85 genera of sclerotium-forming fungi,
including three genera that are reported to form sclerotia for the first time: dung-specialized saprobe Cheilymenia
(Pezizales), wood decaying Ceriporia (Polyporales), and putatively ectomycorrhizal Entoloma (Agaricales) (this genus
contains both saprotrophic and ectomycorrhizal species e Tedersoo and Smith, 2013). One sclerotium collection (MCA3930)
found in a tropical rainforest in Guyana putatively belongs to the order Amylocorticiales, but could not be identified to
genus based on DNA sequences and has an uncertain trophic mode
Genus
Species
Phylum
Lineage
Trophic role
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Saprobe, animal
pathogen
Saprobe
Plant pathogen
References
Macrophomina
Mycosphaerella
Capnobotryella
Scleroconidioma
Aspergillus
phaseolina
ligulicola
renispora
sphagnicola
flavus
A
A
A
A
A
Botryosphaeriales
Capnodiales
Capnodiales
Dothideales
Eurotiales
Papavizas, 1977
Blakeman and Hornby, 1966
Hambleton et al., 2003
Hambleton et al., 2003
Hedayati et al., 2007
Penecillium
Scleromitrula
sclerotigenum
shiraianum
A
A
Eurotiales
Helotiales
Botryotinia
Ciborinia
Ciboria
Dumontinia
Grovesinia
Kohninia
Martininia
Myriosclerotinia
Ovulinia
Redheadia
Sclerocrana
Sclerotinia
Septotinia
Streptotinia
Stromatinia
Acephala
Phialocephala
Claviceps
Ophiocordyceps
Cylindrocladium
Cenococcum
Verticillium
fuckelinia
erythronii
carunculoides
tuberosa
pyramidalis1
linnaeicola
panamaensis
denisii
azaleae
quercus
atra
sclerotiorum
podophyllina
arisaemae
gladioli
macrosclerotiorum
fortinii
purpurea
sinensis
crotalariae
geophilum
dahliae
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Saprobe
Plant pathogen
Plant pathogen
Plant pathogen
Saprobe
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Ectomycorrhizal
Ericoid mycorrhizal
Plant pathogen
Insect parasite
Plant pathogen
Ectomycorrhizal
Plant pathogen
Magnaporthe
salvinii2
A
Plant pathogen
Cintas and Webster, 2001
Morchella
Mattirolomyces
Cheilymenia
Pseudombrophila
Pyronema
Phymatotrichopsis
Wynnea
Coniothyrium
Alternaria
Paraleptosphaeria
Leptosphaeria
Colletotrichum
Sordaria
Rosellinia
crassipes
terfezioides
sp.
dentata3
domesticum
omnivora
americana
glycines4
brassicae
orobanches
sclerotioides5
coccodes
sclerogenia
necatrix
A
A
A
A
A
A
A
A
A
A
A
A
A
A
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Helotiales
Hypocreales
Hypocreales
Hypocreales
Hysteriales
Hypocreomycetidae
incertae sedis
Sordariomycetidae
incertae sedis
Pezizales
Pezizales
Pezizales
Pezizales
Pezizales
Pezizales
Pezizales
Pleosporales
Pleosporales
Pleosporales
Pleosporales
Sordariales
Sordariales
Xylariales
Joshi et al., 1999
Schumacher and Holst-Jensen,
1997
Hsiang and Chastagner, 1992
Batra and Korf, 1959
Whetzel and Wolf, 1945
Uzuhashi et al., 2010
Grand and Menge, 1974
Holst-Jensen et al., 2004
Whetzel, 1942
Schumacher and Kohn, 1985
Weiss, 1940
Suto and Suyama, 2005
Samuels and Kohn, 1986
Kohn, 1979
Whetzel, 1945
Whetzel, 1945
Whetzel, 1945
€ nzenberger et al., 2009
Mu
Currah et al., 1993
Douhan et al., 2008
Xing and Guo, 2008
Roth et al., 1979
Douhan and Rizzo, 2005
Tjamos and Fravel, 1995
Saprobe
Root endophyte?
Saprobe
Saprobe
Saprobe
Plant pathogen
Saprobe
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Plant pathogen
Saprobe
Plant pathogen
Volk and Leonard, 1989
cs et al., 2007
Kova
Gloeocercospora
Leucocoprinus
Pleurotus
Coprinus
Cortinarius
Entoloma
Coprinopsis
Agrocybe
Hebeloma
Hypholoma
sorghi6
luteus
tuber-regium
lagopus
calochrous
sp.
sclerotiorum
arvalis
sacchariolens
tuberosum
A
B
B
B
B
B
B
B
B
B
Xylariales
Agaricales
Agariacles
Agaricales
Agaricales
Agaricales
Agaricales
Agaricales
Agaricales
Agaricales
Plant pathogen
Saprobe
Saprobe
Saprobe
Ectomycorrhizal
Ectomycorrhizal?
Saprobe
Saprobe
Ectomycorrhizal
Saprobe
This Study
Pfister, 1984
Moore, 1962
Marek et al., 2009
Pfister, 1979
Hartman and Sinclair, 1992
Tsuneda and Skoropad, 1977
de Gruyter et al., 2013
Gray et al., 2008
Blakeman and Hornby, 1966
Fields and Grear, 1966
rrez-Barranquero et al.,
Gutie
2012
Dean, 1968
Warcup and Talbot, 1962
Fasidi and Ekuere, 1993
Waters et al., 1975
Kernaghan, 2001
This Study
Keirle et al., 2004
Redhead and Kroeger, 1987
Ingleby et al., 1990
Redhead and Kroeger, 1987
Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
10.1016/j.funeco.2014.08.010
How many fungi make sclerotia?
7
Table 2 e (continued )
Genus
Species
Phylum
Lineage
Psilocybe
Stropharia
Collybia
Omphalia
Rimbachia
Typhula
Unknown Genus
Sclerotium
caerulescens
tuberosa
tuberosa
lapidescens
sp.7
incarnata
sp.
rolfsii8
B
B
B
B
B
B
B
B
Agaricales
Agaricales
Agaricales
Agaricales
Agaricales
Agaricales
Amylocorticiales
Amylocorticiales
Athelia
arachnoidea
B
Atheliales
Fibularhizoctonia
sp.
B
Atheliales
Boletus
Leccinum
Hygrophoropsis
Leucogyrophana
Boletinellus
Gyrodon
Paxillus
Phlebopus
Pisolithus
Scleroderma
Austropaxillus
Ceratorhiza
Rhizoctonia
Corticium
Laetisaria
Marchandiomyces
Helicobasidium
rubropunctus
holopus
aurantiaca
lichenicola
meruloides
lividus
involutus
sudanicus
tinctorious
verrucosum
sp.
hydrophila9
solani10
botryohypochnoideum
arvalis
lignicola
purpureum
B
B
B
B
B
B
B
B
B
B
B
B
B
B
B
B
B
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Boletales
Cantharelalles
Cantharelalles
Corticiales
Corticiales
Corticiales
Helicobasidiales
Ceriporia
Lignosus
Polyporus
Wolfiporia
Trechispora
sp.
rhinocerus
mylittae
cocos11
sp.
B
B
B
B
B
Polyporales
Polyporales
Polyporales
Polyporales
Trechisporales
Trophic role
Saprobe
Saprobe
Saprobe
Saprobe
Saprobe (?)
Pathogen
?
Saprobe,
plant pathogen
Lichenicolous,
plant pathogen
Saprobe,
insect parasite
Ectomycorrhizal
Ectomycorrhizal
Saprobe
Lichenicolous
Insect symbiont?
Ectomycorrhizal
Ectomycorrhizal
Saprobe
Ectomycorrhizal
Ectomycorrhizal
Ectomycorrhizal
Plant pathogen
Plant pathogen
Saprobe
Mycoparasite
Lichenicolous
Plant pathogen,
mycoparasite
Saprobe
Saprobe
Saprobe
Saprobe
Saprobe,
insect parasite
References
Redhead and Kroeger, 1987
Redhead and Kroeger, 1987
Murrill, 1915
Saito et al., 1992
Warcup and Talbot, 1962
Matsumoto and Tajimi, 1985
This Study
Binder et al., 2010
Diederich and Lawrey, 2007
Matsuura, 2006
Smith and Pfister, 2009
Muller and Agerer, 1990
Antibus, 1989
Diederich and Lawrey, 2007
Cotter and Miller, 1985
Agerer et al, 1993
Fox, 1986
Thoen and Ducousso, 1990
Piche and Fortin, 1982
Ba and Thoen, 1990
Palfner, 2001
Xu et al., 2010
Cubeta and Vilgalys, 1997
Warcup and Talbot, 1962
Burdsall et al., 1980
Larsson, 2007
Lutz et al., 2004
This Study
Cui et al., 2011
Macfarlane et al., 1978
Weber, 1929
Matsuura and Yashiro, 2010
Synonyms ¼ 1Cristulariella pyramidalis, 2Sclerotium oryzae, 3Firmaria dentata, 4Dactuliochaeta glycines, 5Phoma scierotioides, 8Athelia rolfsii,
cocos.
Sexual stage ¼ 6Monographella, 9Ceratobasidium, 10Thanatephorus.
7
Reported as Leptoglossum sp.
8
Binder et al. (2010) showed A. rolfsii is not closely related to Athelia sensu stricto.
adaptive yet massively convergent traits in animals (e.g.
warning coloration, production of shells, flight/gliding) and
plants (e.g. thorns, succulents, C4 photosynthesis) but that the
hidden nature of the fungi has concealed the importance of
this trait. Lastly, we suspect that the sclerotium-forming fungi
contain a veritable treasure trove of interesting secondary
metabolites and we suggest that the sclerotium-forming fungi
should be prioritized for genome sequencing and closer
metabolomic and ecological study.
Acknowledgments
Funding for ME Smith was provided in part by University of
Florida’s Institute of Food and Agricultural Sciences (IFAS).
Collecting of sclerotia in New England was made possible via a
fellowship provided by the Harvard University Herbaria to ME
Smith. Collecting in Guyana was funded by National Science
11
Poria
Foundation grants DEB-0918591 (TW Henkel) and DEB-3331108
(R Vilgalys) with permits granted by the Guyana Environmental Protection Agency. MC Aime is acknowledged for her
help in photographing and processing sclerotia collection
MCA3930.
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Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/
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