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Fungal Diversity
https://doi.org/10.1007/s13225-021-00497-3
REVIEW
Species diversity of Basidiomycota
Mao‑QiangHe1· Rui‑LinZhao1,2· Dong‑MeiLiu3· TeodorT.Denchev4· DominikBegerow5· AndreyYurkov6·
MartinKemler5· AnaM.Millanes7· MatsWedin8· A.R.McTaggart9· RogerG.Shivas10· BartBuyck11· JieChen12·
AlfredoVizzini13· ViktorPapp14· IvanV.Zmitrovich15· NaveedDavoodian16· KevinD.Hyde17,18,19
Received: 8 September 2021 / Accepted: 27 December 2021
© The Author(s) under exclusive licence to Mushroom Research Foundation 2022
Abstract
Fungi are eukaryotes that play essential roles in ecosystems. Among fungi, Basidiomycota is one of the major phyla with
more than 40,000 described species. We review species diversity of Basidiomycota from five groups with different lifestyles
or habitats: saprobic in grass/forest litter, wood-decaying, yeast-like, ectomycorrhizal, and plant parasitic. Case studies of
Agaricus, Cantharellus, Ganoderma, Gyroporus, Russula, Tricholoma, and groups of lichenicolous yeast-like fungi, rust
fungi, and smut fungi are used to determine trends in discovery of biodiversity. In each case study, the number of new species
published during 2009–2020 is analysed to determine the rate of discovery. Publication rates differ between taxa and reflect
different states of progress for species discovery in different genera. The results showed that lichenicolous yeast-like taxa
had the highest publication rate for new species in the past two decades, and it is likely this trend will continue in the next
decade. The species discovery rate of plant parasitic basidiomycetes was low in the past ten years, and remained constant
in the past 50years. We also found that the establishment of comprehensive and robust taxonomic systems based on a joint
global initiative by mycologists could promote and standardize the recognition of taxa. We estimated that more than 54,000
species of Basidiomycota will be discovered by 2030, and estimate a total of 1.4–4.2 million species of Basidiomycota glob-
ally. These numbers illustrate a huge gap between the described and yet unknown diversity in Basidiomycota.
Keywords Biodiversity· Fungi· Species number· Taxonomy
Introduction
The number of species are there on Earth was listed in the
top 125 scientific questions in 2005 that remains unanswered
(Kennedy and Norman 2005; https:// www. scien cemag. org/
colle ctions/ 125- quest ions- explo ration- and- disco very; Hyde
etal. 2020a, b). Fungi constitute a diverse kingdom of eukar-
yotes, estimated to represent 2.2 million species or possibly
up to 13.2 million species (Hawksworth and Lücking 2017;
Willis 2018; Wu etal. 2019; Antonelli etal. 2020). Fungi
are essential in ecosystems as they decompose and recycle
nutrients by breaking down complex organic compounds to
simple molecules. Some are symbiotic with plants or with
algae forming lichens, and some are parasites of plants, ani-
mals or other organisms.
Basidiomycota R.T. Moore 1980 is a lineage of Fungi
(Zhao etal. 2017a; Tedersoo etal. 2018). There are clades
in Basidiomycota supported by modern systematic studies
that correspond to the four subphyla viz. Agaricomycotina
Doweld 2001, Pucciniomycotina R. Bauer, Begerow, J.P.
Samp., M. Weiss & Oberw. 2006, Ustilaginomycotina Dow-
eld 2001 and Wallemiomycotina Doweld 2014 (Zhao etal.
2017a; Tedersoo etal. 2018; He etal. 2019; Wijayawardene
etal. 2020). These linegaes comprise most well-known phe-
notypic groups which are the mushrooms and puffballs in
Agaricomycotina, the rust fungi in Pucciniomycotina, and
the smut fungi in Ustilaginomycotina. The phylum Basidi-
omycota also includes a broad range of dimorphic fungi,
which switch between a yeast phase and and a filamentous
phase, along their life-cycle (Boekhout etal. 2021).
Molecular phylogenetic approaches have revolu-
tionised fungal taxonomy of Basidiomycota in the last
decades (Lücking etal. 2021). These advances have
greatly enhanced our knowledge of species diversity in
Basidiomycota. Based on evidence from molecular data,
Handling Editor: Antonio Roberto Gomes de Farias.
* Rui-Lin Zhao
zhaorl@im.ac.cn
Extended author information available on the last page of the article
Fungal Diversity
1 3
numerous new taxa have been discovered in the past ten
years. Besides new taxon discovery, many species identi-
fied only by morphology in the past have been reclassified
as novel taxa in the molecular era. Some examples from
China are (i) the cultivated medicinal mushroom “Lin-
zhi”, first identified as the European species Ganoderma
lucidum (Patouillard 1907), which is now recognized as
G. lingzhi (Cao etal. 2012); (ii) the enoki mushroom, for-
merly the European species Flammulina velutipes, pres-
ently F. filiformis (Wang etal. 2018); and (iii) the black
fungus, formerly Auricularia auricula-judae, presently A.
heimuer (Wu etal. 2014).
Molecular analyses aid in discovery of morphologically
indistinguishable cryptic species in basidiomycetes, includ-
ing species of Tricholoma (Carriconde etal. 2008; Jargeat
etal. 2010; Heilmann-Clausen etal. 2017; Yang etal. 2017),
polypores (Carlsen etal. 2011; Korhonen etal. 2018; Pei-
ntner etal. 2019), boletes (Sato etal. 2007), and yeasts
(Boekhout etal. 2021). The number of fungi might be up to
11-fold greater than currently known if cryptic speciation is
considered (Hawksworth and Rossman 1997; Hawksworth
and Lücking 2017).
The number of fungal species has been estimated in
different ways (Blackwell 2011; Hawksworth and Lükc-
ing 2017). Wu etal. (2019) estimated that there could be
11.7–13.2 million species of fungi worldwide based on
environmental DNA sequence data. A plant-to-fungus ratio
calculated from known plant and macrofungal associations
predicted between 53,000 and 110,000 macrofungal species
worldwide (including macrofungi in Ascomycota; Mueller
etal. 2007). Aptroot and Luecking (2016) used grid-based
approaches to estimate there could be 800 species of Try-
petheliaceae (Dothideomycetes: Ascomycota) which is
a lichenized group restricted to tropical forest and savan-
nah ecosystems. De Meeus and Renaud (2002) predicted
up to 25,000 species of Basidiomycota, but no method was
indicated.
Available estimates of extant species in Basidiomycota
vary because different criteria have been used. The number
of described species is feasible and has already been sug-
gested in several global team works. The number of Basidi-
omycota was mentioned as 31,515 in Ainsworth & Bisby’s
Dictionary of the Fungi (Kirk etal. 2008). Ten years later,
a detailed systematic study recognized more than 36,000
extant species in Basidiomycota (Begerow etal. 2018). The
number increased to 41,270 according to the latest outline
of Basidiomycota (He etal. 2019).
In this paper, we give overviews for particular groups of
basidiomycetes, focusing on species diversity and the pro-
gress in discovering new species during the past two dec-
ades. Using these results, we estimate how many species will
be described in the next decades. Furthermore, we estimate
the species number in Basidiomycota worldwide.
Methods ofspecies number estimation
Families of Basidiomycota were divided into five main
groups: grass/forest-litter saprobic, wood-decaying, yeast-
like, ectomycorrhizal, and plant parasitic taxa. These
groups could account for 88% of the known basidiomy-
cetes (Põlme etal. 2020).
Nine case studies were selected to represent basidiomy-
cetes within these five groups.
The new species publication rate was calculated by the
formula “
𝛼
= (A/B)/12” where “A” is the new species num-
ber published during 2009 to 2020, and “B” is the estimated
species number in 2008 (Kirk etal. 2008).
We extrapolated the publication rate from the nine case
studies to ecologically similar groups of Basidiomycota
based on the current taxonomic system of Basidiomycota
at the family rank (He etal. 2019). Assuming the con-
stant publication rate in the next ten years, we estimated
the number of species in each family by
N= A×(
1
+
𝛼
)y
,
where A is the number of recognized species in 2020,
y
is the number of year and
𝛼
is the publication rate.
The estimated species number of each order is listed
in Table11.
Finally, the described species are estimated by different
publication rates of each studied group of Basidiomycota.
Case studies
Grass/forest‑litter saprobic basidiomycetes
AGARICUS
Agaricus (Agaricaceae, Agaricales) are saprobic fungi
characterized by fruitbodies with an annulate stipe and
free lamellae that produce dark brown spore prints. They
are solitary or gregarious in various habitats, such as in
forests, gardens, on roadsides, pastures, manure heaps, or
decaying organic matter from sea level up to the vegeta-
tion limit in mountainous areas (Cappelli 1984). Agaricus
occurred around 66 million years ago (Mya) in the tropics
and was dispersed to other areas worldwide (Zhao etal.
2011, 2016a, b; He etal. 2017). The distribution range
extends to all continents except Antarctica (Parra 2008;
Zhao etal. 2011). Certain species of Agaricus are favored
by people for their nutritional and medicinal properties,
such as A. bisporus (J.E. Lange) Imbach, the button mush-
room, which is the most cultivated species in the world.
Similarly, A. subrufescens Peck is famous for its antioxi-
dant activities (Llarena-Hernández etal. 2017). Several
other Agaricus species are collected as wild edible mush-
rooms, for example, A. campestris L.: Fr., A. augustus Fr.
Fungal Diversity
1 3
and A. arvensis Schaeff (Li etal. 2021). However, species
belonging to the A. sect. Xanthodermatei may cause mild
digestive upsets, but without serious risks of fatal conse-
quences (Parra 2008; Boxshall etal. 2021).
Agaricus has a long history of taxonomic research.
Numerous monographs have been published from dif-
ferent areas mainly based on morphology, and mostly
from temperate areas, such as those from Europe (Möller
1950; Pilát 1951; Konrad and Maublanc 1952; Kühner
and Romagnesi 1953; Wasser 1980; Cappelli 1984; Parra
2008); from America (Kerrigan 1986; Singer 1986). The
most referred monographs on tropical Agaricus are those
of Heinemann (Heinemann 1956, 1978, 1980), in which
descriptions and classifications of tropical species has
been largely based on traditional systematics of temper-
ate species.
Until the year 2000, taxonomic classification did not
reflect molecular phylogeny of species, and their evolu-
tionary histories had not been studied (Callac and Chen
2018). In the last decade, due to the development of
molecular approaches, knowledge of the diversity of Aga-
ricus has improved. The first molecular study by Mitchell
and Bresinsky (1999) was soon to be followed by other
researchers (Challen etal. 2003; Geml etal. 2004; Kerri-
gan etal. 2005, 2008). Eight temperate sections have been
widely accepted in A. subg. Agaricus: Agaricus, Arvenses,
Bivelares, Chitonioides, Minores, Sanguinolenti, Spissi-
caules and Xanthodermatei. The structure of the annulus
(superous vs. inferous; simple vs. double or two layered),
odour, discoloration of context when cut or rubbed and
Schäffer reaction (aniline × nitrogen acid) are the major
criteria for infrageneric classification. The first mono-
graphs to use molecular data are those of Parra (2013)
and Kerrigan (2016), which documented the most com-
prehensive information of temperate species from Europe
and North America.
Generally, Agaricus species living in tropical or subtropi-
cal areas are much less well-studied than taxa in temper-
ate areas. Heinemann (1978, 1980) proposed Lanagaricus
Heinem. and Conioagaricus Heinem. as two predominantly
subtropical and tropical subgenera, which indicated that
the diversity of Agaricus from the tropics would be differ-
ent from those of temperate areas. ITS-based phylogenetic
studies revealed 11 new phylogenetic clades from tropical
areas, with more clades than from temperate areas (Zhao
etal. 2011). As a result of phylogenetic studies, Lanagaricus
became a heterotypic synonym of the subgenus Pseudochi-
tonia; sections Trisulphurati and Laeticolores, which were
placed in A. subgenus Lanagaricus by Heinemann (1956),
were placed in the subgenera Pseudochitonia and Minores,
respectively in systematic studies of Zhao etal. (2016a, b)
and Chen etal. (2017).
During the last decade, the taxonomy of Agaricus has
developed due to the application of multigene molecular
phylogenies, especially using divergence time estimates as
additional criteria, which proved to be a useful method to
rank and name monophyletic clades (Zhao etal. 2016a, b).
A new classification system for Agaricus considering stem
age as a criterion for standardizing taxonomic ranks was
proposed by Zhao etal. (2016a, b). The new system is com-
posed of 5 subgenera and 20 sections. Using the same crite-
ria, one more subgenus and four sections were described in
later phylogenetic studies (Chen etal. 2017; He etal. 2018a;
Parra etal. 2018).
Species diversity ofAgaricus
Asia, especially China and Thailand, is the region from
which most new species were described during the last dec-
ade. Large parts of the studies stem from international col-
laborations between European and Asian teams (Callac and
Chen 2018). In total, 119 new species were described from
Asia, representing 63% of the new species described world-
wide (Chen etal. 2012, 2015, 2016, 2017, 2019a; Zhao etal.
2012, 2013; Karunarathna etal. 2014; Li etal. 2014a, 2016;
Thongklang etal. 2014, 2016; Ariyawansa etal. 2015; Gui
etal. 2015; He and Zhao 2015; Liu etal. 2015a, 2020; Wang
etal. 2015b; Dai etal. 2016; Kaur etal. 2016; Zhao etal.
2016a, b; Zhou etal. 2016; He etal. 2017, 2018a,b; Hyde
etal. 2017; Zhang etal. 2017; Bashir etal. 2018; Mahdiza-
deh etal. 2018; Hussain and Sher 2019; Phookamsak etal.
2019; Zheng etal. 2019; Cao etal. 2021). Most of these new
species were from tropical or subtropical regions, which is
a good indication of the potential high species diversity in
other unexplored tropical areas.
Fourty two new species were published from the Ameri-
cas, which is the region with the most descriptions of new
species after Asia. Most contributions were from North
America, with a monograph on North American Agaricus
written by a senior mycologist and expert on Agaricus (Ker-
rigan 2016). Some new taxa were described from the Carib-
bean and South America (Drewinski etal. 2017; Parra etal.
2018).
Twenty new species were described from Europe (Parra
etal. 2011, 2014, 2015; Parra 2013; Mua etal. 2017; Parra
and Caballero 2017; Mahdizadeh etal. 2018). The majority
(20 species) are from the monograph of Parra (2013).
New species were also published from other areas. Seven
and three new species were described from Oceania and
Africa, respectively. Two of three species described from
Africa are also found in Asia (Zhao etal. 2012; Chen etal.
2017). Interestingly, the seven Agaricus species described
from Australia were of the sequestrate (secotioid) form with
an enclosed hymenium. Their phylogenetic analyses sug-
gested that climatic events in Australia could be correlated
Fungal Diversity
1 3
with the evolution of sequestrate forms (Lebel and Syme
2012; Lebel 2013). Ten species that are known species, but
as new combinations or new names are not accounted here.
Species, especially from tropical and subtropical regions
have been better studied and classified in recent years with
a comprehensive taxonomic system (Zhao etal. 2016a, b;
Chen etal. 2017; Parra etal. 2018; He etal. 2019). Previous
studies were preliminary steps to evaluate the species diver-
sity in these regions. Extensive sampling in under sampled
areas is necessary. Today, almost 600 species of Agaricus
are recognized, and this number will likely increase further,
since diversity studies in many regions are undergoing, such
as in Brazil, Caribbean regions, China, India, Mexico, and
Pakistan. On the other hand, numerous species appeared
to be widely distributed in different continents (based on
the morphology). However, among the hundreds of tropi-
cal collections, none are conspecific with temperate taxa
(with the exception of A. endoxanthus and A. subrufescens)
(Thongklang etal. 2014; Chen etal. 2016). That indicates
that many new cryptic species may be discovered during
such a process.
New species publication rate
According to Bas (1991), the number of extant Agaricus
species worldwide is close to 400. Zhao etal. (2011) rec-
ognized 386 species in the genus, including 183 that were
tropical species. With 189 new species described from
2010 to 2020, the number of species recognized today
exceeds 500 (Callac and Chen 2018; Chen etal. 2019a, b;
Hussain and Sher 2019; Phookamsak etal. 2019; Zheng
etal. 2019; Liu etal. 2020; Cao etal. 2021). In fact, among
the 189 newly described species, with the exception of A.
pachydermus (Lebel and Syme 2012), A. patialensis (Kaur
etal. 2016) and A. zelleri (Kerrigan 2016), ITS sequence
data is available for all taxa (Table1; Fig.1).
Wood‑decaying basidiomycetes
GANODERMA
Ganoderma is a large, worldwide distributed polypore
genus in the Basidiomycota that includes species causing
white rot on various tree species. Recent studies indicated
that Ganoderma emerged around 60 Mya (Zhu etal. 2015;
Tian etal. 2021). The first monograph of ganodermatoid
taxa was made by Patouillard (1889), in which he distin-
guished 29 Ganoderma species. A hundred years later,
more than two centuries of taxonomic work on this group
was summarized by Moncalvo and Ryvarden (1997), with
a thorough overview of Ganoderma species described
before the molecular era. Of the listed 217 Ganoderma
species (Ganoderma and Elfvingia were combined) in
their study, 148 species were accepted. The majority of
these species (ca. 65%) were represented only by one or
some few collections restricted to the type locality and
adjacent regions (Moncalvo and Ryvarden 1997). This
high rate of rare or poorly known species may have been
due to the varied morphology of Ganoderma fruitbod-
ies, and substandard identification keys based on some
arbitrarily chosen morpho-anatomical characteristics used
by different mycologists (e.g. Pegler and Young 1973;
Steyaert 1980; Moncalvo 2000; Ryvarden 2000; Smith
and Sivasithamparam 2003; Torres-Torres and Guzmán-
Dávalos 2012).
Table 1 Number of Agaricus
species published between 2009
and 2020
New species publication rate 0.0412 (190/384/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number 1 1 1 10 12 9 17 72 34 16 6 11
Fig. 1 Line chart of number of
new Agaricus species published
from 2009 to 2020
Fungal Diversity
1 3
Species diversity ofGanoderma
Although Ganoderma is a well-researched genus, differ-
ent morphology-based species concepts have resulted in
ambiguous species delimitation and identification sys-
tems (Moncalvo 2000). Since taxonomists have provided
scientific names for more than three hundred Ganoderma
species described solely on morphology, the re-discovery
of already named species is a real problem (Papp 2019).
In order to unlock the confused nomenclature and taxon-
omy in Ganoderma and clarify the geographical distribu-
tion range of the species, the use of barcoding sequences
seems to be necessary. Molecular phylogenetic studies have
shown that most of the examined Ganoderma species are
geographically restricted, in contrast to the earlier theories,
which assumed that these species have wide distributions
and largely unstructured populations (e.g., Moncalvo and
Buchanan 2008; Zhou etal. 2015; Loyd etal. 2018). Phy-
logenetic studies have also demonstrated that widely used
Ganoderma names have often been erroneously applied to
species described from other biogeographic zones. As an
example, Cabarroi-Hernández etal. (2019) found, that G.
weberianum (Bres. & Henn. ex Sacc.) Steyaert, a species
originally described from Samoa (Steyaert 1972) did not
occur in the Neotropics, and G. weberianum encompassed
at least two species, namely G. mexicanum Pat. and G. par-
vulum Murrill (Cabarroi-Hernández etal. 2019).
Ganoderma species are important wood-decaying fungi,
which grow as facultative parasites of trees, or live as sap-
robes on dead logs, stumps and roots. The host specificity
of Ganoderma species is highly variable, but many species
show striking host generalism (e.g. G. adspersum, G. appla-
natum, G. curtisii, G. philippi, G. resinaceum, G. zonatum)
(Luangharn etal. 2020). Although numerous Ganoderma
species have a wide host range, the study of Ganoderma spe-
cies occurring on different trees has recently yielded several
new species. As an example, based on a study of Gano-
derma basidiomes collected on Jacaranda mimosifolia in
South Africa (Crous etal. 2014; Coetzee etal. 2015), three
new Ganoderma species were described using nucleotide
sequence data. Two new Ganoderma species were found
by Xing etal. (2018) from the southeast coast of China on
living trees of Casuarina equisetifolia. Casuarina has been
reported as a host genus for Ganoderma casuarinicola (Xing
etal. 2018), but this species was later reported by Luangharn
etal. (2019) from Thailand, based on specimens collected on
Pinus kesiya. A recent study, multilocus phylogeny showed
that a bambusicolous species has long been incorrectly iden-
tified as G. neojaponicum Imazeki in Taiwan, and it is rather
a new undescribed species. The new species, G. bambusi-
cola is only known from southern Asia and grows on bam-
boo roots, while morphologically similar G. neojaponicum
occurs on roots or trunks of conifers in East Asia (Wu etal.
2020). The above examples demonstrate that although most
Ganoderma species are not host-specific, the host trees and
geographical distribution may play an important role in spe-
cies segregation.
Currently, more than 60,000 tree species are known to
science, from which nearly 58% are single country endem-
ics (Beech etal. 2017). Most of these species are known
from Australia, Brazil, China, Madagascar, and the largest
number of trees is found in the Neotropic biome, followed
by the Indo-Malay and the Afrotropic biomes (Beech etal.
2017). Although Ganoderma occurs in all forested eco-
systems, tropical and sub-tropical regions appear to be the
center of its biodiversity. We estimate that nearly 500 species
of Ganoderma occur globally, of which less than 40% are
currently known. Considering this, approximately 300 spe-
cies await discovery. The vast majority of these will likely
be discovered in biodiversity hotspots.
New species publication rate
Different morphology-based species concepts have resulted
in ambiguous species delimitation and identification sys-
tems in the genus, however, due to the rapid adoption of
molecular genetic methods, our understanding of the genetic
variability within the genus improved significantly over the
last two decades (Papp 2019). Therefore, species bounda-
ries in Ganoderma can be re-evaluated based on barcoding
sequences, and molecular systematics has been shown to
be a valuable tool in current taxonomy (Hapuarachchi etal.
2019). As a result of extensive taxonomic studies on Gano-
derma mostly performed by phylogenetic methods, 39 new
species were revealed in the past 20years from Africa (Cam-
eroon, Ghana, South Africa), Asia (China, India, Indonesia,
Japan, Laos, Thailand), Central America and the Caribbean
(Martinique, Mexico) and South America (Colombia, Ecua-
dor, French Guiana, Venezuela) (Hapuarachchi etal. 2018,
2019; Liu etal. 2019; Luangharn etal. 2019; Papp 2019;
Tchotet Tchoumi etal. 2019; Ye etal. 2019; Wu etal. 2020;
Ryvarden 2020). Currently only 64 Ganoderma species
are represented by DNA sequence data (Jayawardena etal.
2020). However, based on sequences deposited in GenBank
(Sayers etal. 2020) and UNITE (Nilsson etal. 2019), the
species number of Ganoderma is presumably much higher.
Considering the morphology-based observations and the
phylogenetic results, He etal. (2019) estimated there are
presently 180 extant species in the genus.
Ganoderma has a cosmopolitan distribution, but most of
the species are known from tropical and sub-tropical regions.
Although, more than 20 Ganoderma species have been
described from Europe (Moncalvo and Ryvarden 1997), only
five well separated clades are confirmed by phylogenetic
methods (Beck etal. 2020). Further studies are needed to
clarify the species boundaries in the G. lucidum complex
Fungal Diversity
1 3
(incl. three morphospecies) and the G. resinaceum lineage
(incl. two genotypes within one morphospecies) (Papp etal.
2017; Náplavová etal. 2020). In order to clarify the laccate
Ganoderma species present in the United States, more than
500 collections were studied by Loyd etal. (2018), who
revealed 12 species using molecular phylogenetic techniques
combined with morphological examination. Together with
the five additional non-laccate species listed by Zhou etal.
(2016), a total of 17 Ganoderma species are currently known
from the United States. The genus shows a much higher
diversity in Asia. As an example, Luangharn etal. (2020)
reported 23 Ganoderma species only from the Greater
Mekong Subregion, out of which three species were new
to science. In recent years the genus has been intensively
studied in Asia and several new species have been described
especially from China (e.g., Cao etal. 2012; Cao and Yuan
2013; Li etal. 2015, 2016; Xing etal. 2018; Hapuarachchi
etal. 2018; Liu etal. 2019; Ye etal. 2019). However, the
taxonomic position of many previously described species
has not yet been settled (e.g., Moncalvo and Ryvarden 1997;
Wu and Dai 2005; Papp 2016). However, more species can
be expected in the future, especially from the tropical parts
of Asia, and many more new species are expected to be
found from wooded areas of Africa, Australia, and as well
as Central and South America (Table2; Fig.2).
Although, no DNA sequence data are available for the
majority of currently accepted Ganoderma species (He
etal. 2019; Jayawardena etal. 2020), several unidentified
or mislabelled sequences are deposited at public databases,
which represents distinct Ganoderma lineages (Papp etal.
2017). In order to estimate the global species richness in
Ganoderma, an OTU (operational taxonomic unit; Blax-
ter etal. 2005) abundance dataset was used. ITS sequence
data was retrieved from the UNITE database (Nilsson etal.
2019). The dataset contained 2483 ITS sequences represent-
ing 160 phylogenetic species (OTUs) at a 98.5% similarity
threshold. The dataset was analyzed based on a Single-Indi-
vidual-Based rarefaction method in the EstimateS v9 pro-
gram (Colwell 2013). Based on the result of Chao1 estima-
tor, the estimation number is (1.9)2.7(4.2) times the extant
species. This indicate a global estimate for Ganoderma
of (342–)486(–756) species worldwide, 180 of which are
currently known. Therefore, the global species richness in
Ganoderma could be estimated at 2.7 × 180 ≈ 486 species.
Basidiomycetous yeasts andallied dimorphic taxa
inCystobasidiomycetes, Microbotryomycetes
andTremellomycetes
Basidiomycetous yeasts were among the first organisms to
be isolated and grown in culture from environmental plants
and air samples (e.g., Guillermond 1920; Stark 1921). The
ability to grow in a predominantly unicellular form appeared
independently in different lineages of Basidiomycota and
the ancestor of basidiomycetous yeasts occurred in Cysto-
basidiomycetes around 330 Mya (Nagy etal. 2014; Zhao
etal. 2017a). Identification of these species is based on a few
simple morphological characters, such as pigmentation, cell
shape and peculiarities of proliferation on artificial media.
With the development of microbiological methods, a few
important links between yeasts and basidiomycetous taxa
were made. The presence of ballistoconidia was observed
in the red yeast Sporobolomyces. Then, hyphae with clamp
connections, and smut-like teliospores were described in
the yeast genus Sporidiobolus (Nyland 1949). The mating
of sexually compatible yeasts and the discovery of mating
and a sexual state in Rhodotorula glutinis indicated a close
relationship between some yeasts and basidiomycetous fungi
(Banno 1963, 1967). Other teleomorphic basidiomycetous
genera have been described in yeasts, for example Auriculi-
buller, Curvibasidium, Cystofilobasidium, Leucosporidium,
Table 2 Number of new
Ganoderma species published
between 2009 and 2020
New species publication rate 0.0313 (30/80/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number131201442462
Fig. 2 Line chart of number of
new Ganoderma species pub-
lished from 2009 to 2020
Fungal Diversity
1 3
and Papiliotrema (reviewed in Kurtzman and Boekhout
2017).
Predominantly unicellular stages, or yeasts, occur in all
three sub-phyla of the phylum Basidiomycota: Agaricomy-
cotina, Pucciniomycotina, and Ustilaginomycotina (Hibbett
etal. 2007; Boekhout etal. 2011; Kurtzman and Boekhout
2017; Oberwinkler 2017). Many species alternate yeast and
hyphal stages throughout their life cycle and were termed
as “dimorphic” (Bandoni 1995). The term was introduced
by Brefeld in the 1880s to contrast the yeast stage of basidi-
omycetous fungi having also a dikaryotic hyphal phase from
the typical unicellular morphology of sexual ascomycetous
yeasts. In dimorphic taxa, the dikaryotic filamentous phase,
which forms the basidiomata, is a mycelium that originates
from the mating of two compatible strains, and has the
potential to form basidia and spores after meiosis. The dikar-
yotic mycelium grows in nature in association with another
fungus (including lichenized fungi) and gain nutrients com-
pletely or in parts from the host (Begerow etal. 2017). A
teleomorphic state has also been observed in laboratory
experiments in several yeast genera, for example Bullero-
myces, Curvibasidium, Leucosporidium, and Papiliotrema
(reviewed in Begerow etal. 2017). Two types of structures
responsible for host-parasite interactions were observed
in culture, namely, haustoria and colacosomes (reviewed
in Begerow etal. 2017). Interestingly, yeasts commonly
thought to be saprobes (e.g., Bullera, Cryptococcus, Dio-
szegia, Leucosporidium, Rhodotorula, and Sporobolomyces)
are also known to produce either of these structures. Poten-
tial hosts of sexual states of fungi known as basidiomycetous
yeasts are often not known, but they can be discovered in the
future, as in the case of Tremella yokohamensis (Malysheva
etal. 2015) and Phaeotremella foliacea (Spirin etal. 2018).
Basidiomycetous yeasts are common inhabitants of plant
surfaces, aquatic habitats and soils (Peter etal. 2017). The
role of saprobic asexual yeast states in successful propaga-
tion and vectoring was first recognized in plant parasites.
More recently, it has been convincingly demonstrated that
asexual species that are closely related to sexual myco-
parasites and lichenicolous fungi are widespread in nature
(reviewed in Peter etal. 2017; Begerow etal. 2017; Kacha-
lkin etal. 2019). Yeast and filamentous taxa have tradition-
ally been studied by different groups of researchers and
therefore the characteristics used have also been completely
different: physiology (biochemical characters) in yeasts, and
morphology (macro- and micromorphology) in filamentous
species (discussed in Begerow etal. 2017; Oberwinkler
2017). Integrated phylogenetic classifications (Liu etal.
2015a, b, c; Wang etal. 2015a) attempted to standardize
diagnostic characteristics in both phenotypic groups as much
as possible. Even if some groups are currently are known to
contain only or predominantly yeasts or filamentous stages, a
classification based on their life-stage is obviously artificial,
and here we will follow here integrated classifications as far
as possible.
The range of fungal hosts for the species with a known
filamentous phase in nature is very wide including both
basidio- and ascomycetes, but individual Tremellomycetes
are usually very host-specific. As examples, Tremella dac-
tylobasidia grows associated to the corticioid fungus Vuil-
leminia macrospora (Zamora 2009), Syzygospora lappon-
ica grows inside the hymenium of Ascocoryne sarcoides
(Kotiranta and Mietinen 2006), and there are a number of
lichenicolous Tremella species each growing on a different
genus or even species of lichenized ascomycetes (e.g., Mil-
lanes etal. 2014a, 2015; Zamora etal. 2016, 2018; Diederich
etal. 2018, 2020). Lichenicolous fungi with an assumed
dimorphic life-style, can be found among several clades of
the Tremellomycetes (Millanes etal. 2011; Liu etal. 2015a,
b, c), and the Cystobasidiomycetes, where lichen-inhabiting
species are represented only in the genera Chionosphaera,
Cyphobasidium and Microsporomyces (Diederich 1996;
Millanes etal. 2016a; Černajová and Škaloud 2019; Li etal.
2020a, b). The relatedness between fungi known as yeasts
and lichenicolous fungi was demonstrated by Diederich
(1996), who was the first to observe and illustrate unicel-
lular budding of spores which is also the first observations
of yeast-stages in lichenicolous representatives. Several
lichenicolous Tremellomycetes and Cystobasidiomycetes
have now been shown to be dimorphic, but the life cycle of
lichenicolous taxa is very poorly studied and understood.
The spectrum of hosts of lichen-associated taxa is most
likely much larger as suggested by recent observations of
yeasts not inducing symptoms in their lichen-hosts (Prill-
inger etal. 1997; Ekman 1999; Lindgren etal. 2015; Spri-
bille etal. 2016; Černajová and Škaloud 2019; Tuovinen
etal. 2019, 2021; Mark etal. 2020; Smith etal. 2020).
Yeasts detected or isolated from lichens include members
of classes Cystobasidiomycetes and Tremellomycetes. Both
groups comprise well-studied species of lichenicolous fungi,
traditionally considered parasites of lichens (Millanes etal.
2011; Oberwinkler 2017). Lichen-inhabiting yeasts are
included in the Cystobasidiales, Erythrobasidiales, and
Tremellales. Recently, a potential involvement of yeasts in
lichen symbiosis has been suggested as a third partner (Spri-
bille etal. 2016; Tuovinen etal. 2019) and this suggestion is
still under debate (Oberwinkler 2017; Begerow etal. 2017;
Lendemer etal. 2019; Mark etal. 2020; Hawksworth and
Grube 2020; Smith etal. 2020; Tagirzhanova etal. 2021).
Although interactions of different nature between lichenized
fungi and lichen-inhabiting yeasts are feasible, the specific-
ity of host-parasite associations and dispersal mechanisms
of yeast states needs to be clarified to prove the three-party
interactions. Consequently, here we use the terms ‘host’,
‘lichenicolous’ and ‘symptom’ without assuming parasit-
ism as the only possible relationship between the partners.
Fungal Diversity
1 3
Species diversity ofbasidiomycetous yeasts anddimorphic
taxa inCystobasidiomycetes, Microbotryomycetes
andTremellomycetes
The number of known basidiomycetous yeasts exceeded
1400 species in 2011 (Kurtzman etal. 2011) and is rap-
idly growing (Yurkov 2017). The most dynamic taxonomic
group is the class Tremellomycetes with 34 new genera, 385
species and 278 taxonomic combinations published in the
last 20years. The majority of these discoveries and changes
concern yeast-like taxa and the re-classification of the poly-
phyletic Bullera, Cryptococcus, and Trichosporon (Liu etal.
2015a, b, c; Li etal. 2020a, b), and the application of the
‘One fungus = One name’ principle to the classification of
sexual and asexual states in genera Bullera, Bulleribasidium,
Cryptococcus, Mrakia, and Papiliotrema (Liu etal. 2015a,
b, c). A total of 30 new genera, 127 species and 56 combina-
tions in Microbotryomycetes (excluding smuts) were pub-
lished. As in the previous case, the major changes in that
group concern the reclassification of previously polyphyl-
etic genera Bensingtonia, Rhodotorula, and Sporobolomyces
(Wang etal. 2015a) and unification of the classification of
anamorphic and teleomorphic taxa, e.g., Leucosporidium,
Rhodosporidium, and Sporidiobolus.
Taxonomic studies on Cystobasidiomycetes resulted
in ten new genera, 43 species and 39 combinations. As in
Microbotryomycetes, reclassification of members of genera
Rhodotorula and Sporobolomyces account for the majority
of taxonomic novelties (Yurkov etal. 2015a; Wang etal.
2015a). As a result of these recent major reclassification
events, several older teleomorphic generic names have been
resurrected and/or applied to clades containing also yeast
states, e.g. Carcinomyces, Colacogloea, Cystobasidium,
Heterocephalacria, Kriegeria, Naematelia, Phaeotremella,
and Rhynchogastrema.
Phylogenetic analyses convincingly demonstrated the
polyphyly of a few teleomorphic genera, such as Cystoba-
sidium (Millanes etal. 2016a) and Tremella (Millanes etal.
2011). Cystobasidium hypogymniicola and C. usneicola that
are distantly related to the type species of the genus Cysto-
basidium, were transferred into a new genus Cyphobasidium
(Millanes etal. 2016a). Liu etal. (2015a, b, c) suggested to
restrict the genus Tremella to the clade containing T. mes-
enterica and T. fuciformis and reclassified several clades
in Tremellomycetes. However, the placement of Tremella
s. l. clades 1–3 recognised by Millanes etal. (2011) and a
few sexual species remained unclear (Liu etal. 2015a, b,
c; Kachalkin etal. 2019; Li etal. 2020a, b). Twenty-two
Tremella species, of which 15 are not related to Tremella
s. s., have been described between 2015 and 2020. Not
only Cystobasidium and Tremella s. l., but also the genera
Sirobasidium and Syzygospora are highly polyphyletic. Syzy-
gospora was previously characterized by holobasidia and
passively released spores. Syzygospora s. s. has now been
restricted to S. alba and S. pallida (Filobasidiales, Tremel-
lomycetes), whereas other species have been transferred to
the genera Carcinomyces (C. effibulatus) in Tremellales,
Heterocephalacria (H. bachmannii, H. physciacearum, and
H. solida), and Piskurozyma (P. sorana) in Filobasidiales
(Liu etal. 2015a, b, c). Sirobasidium is characterized by
basidia arranged in linear chains (de Lagerheim and Paouil-
lard 1892). The phylogenetic position of the type species
of Sirobasidium, S. sanguineum, is unclear because there
is no sequence data available for this species, and thus it
has not been possible to re-delimit this genus (discussed in
Kachalkin etal. 2019).
A review of the geographic patterns of yeasts included
examples of organisms with broad and narrow distribution
ranges (Yurkov 2017). For instance, a few species of Vish-
niacozyma (e.g., V. victoriae, Tremellomycetes) are a good
example of ubiquitous plant-related species. The soil yeast
Saitozyma podzolica (Tremellomycetes) is another example
of a widespread species that is linked to a particular type of
habitat, moist, acid environments, including acid tropical
soils (Yurkov etal. 2012). Species of Naganishia can sus-
tain desiccation in deserts and cold environments (Buzzini
etal. 2018). Geographic distribution in mild climates in
opposite hemispheres and at complementary latitudes was
been reported for red-coloured yeasts of Phaffia (Yurkov
2017; David-Palma etal. 2020). A similar bipolar distribu-
tion showed psychrophilic yeasts in Arctic and Antarctic
regions, e.g., members of genera Glaciozyma and Nagan-
ishia (Tremellomycetes). Among yeasts predominantly
restricted to a particular type of substrate, Solicoccozyma
(Tremellomycetes) is a common member of soil communi-
ties (Yurkov 2018). Plant surfaces are often inhabited by
red-coloured Sporidiobolales (Microbotryomycetes), e.g.
Rhodotorula and Sporobolomyces (Fonseca and Inácio
2006). Despite extensive sampling, a few species have been
so far obtained from a single region, being thus good candi-
dates for endemic species. For example, all three species of
the genus Carlosrosaea (Tremellomycetes) are known from
Brazilian bromeliads. Dimennazyma cistialbidi (Tremel-
lomycetes) has been isolated only from leaves of a single
Mediterranean plant, Cistus albidus in Portugal (Inácio etal.
2005). The lichenicolous species are in general widespread
and follow the geographical distribution of their lichen hosts.
Evidence suggests that speciation in investigated licheni-
colous Tremellomycetes and Cystobasidiomycetes is rather
driven by host selection rather than by geographical isola-
tion (Werth etal. 2013; Millanes etal. 2014b, 2015, 2016b;
Spribille etal. 2016; Diederich etal. 2020).
The number of species in the three classes is rapidly
growing, but it is often difficult to directly compare species
numbers reported across different studies. Detection, iden-
tification, and classification of yeasts have undergone major
Fungal Diversity
1 3
changes since the application of gene sequence analyses
and genome comparisons (Kurtzman and Boekhout 2017).
Phylogenetic analysis is leading to a major revision of yeast
systematics and redefinition of nearly all genera (Liu etal.
2015a, b, c; Wang etal. 2015a). In the absence of infor-
mation on hosts, ultrastructure and life-histories, which are
available for teleomorphic taxa, the bulk of solely asexual
yeasts has been taxonomically rearranged in phylogenetic
hypotheses (Oberwinkler 2017).
Application of ribosomal DNA sequencing for identifi-
cation of yeasts provided stable characters for recognition
of morphologically and physiologically indistinguishable
species. As a result of both sampling from the environment
and better species discrimination, the numbers of described
yeasts doubled in the period from 1998 to 2011 (Lachance
2006). Yeast species cited in earlier works were often iden-
tified by different techniques and criteria that may not be
as accurate as the current sequence-based approaches. The
same constraints, different sampling and isolation proto-
cols, and identification tools, make a direct comparison of
regional species richness values and yeast numbers in dif-
ferent substrates impossible. Another difficulty is that many
species are documented from only a limited number of
strains. Therefore, distribution range and association with a
particular substrate, host and vector are not known for many
of these fungi.
Recent phylogenetic analyses suggest that many clades
in Tremellomycetes, Microbotryomycetes and Cystobasidi-
omycetes are largely undersampled and represented only by
a few species and environmental sequences (e.g., Liu etal.
2015a, b, c; Mašínová etal. 2017; Kachalkin etal. 2019).
Public sequences in GenBank provide good overview of
potential new species. Known from very few isolates in cul-
ture collections, these yeasts await description, sometimes
for decades. A few Tremellomycetes have been isolated in
Portugal by Inácio etal. (2002) and re-sampled 20years later
(Kachalkin etal. 2019). The class Microbotryomycetes com-
prise a number of monotypic genera, which are character-
ized by a unique characteristic or phylogenetic position, for
example Heterogastridium, Kriegeria, Libkindia, Meredith-
blackwellia, Pseudoleucosporidium, Pycnopulvinus, Udeni-
ozyma, and Yunzhangia. The number of species in a few
more genera is growing slowly, notably in Camptobasidium,
Cryolevonia, Hamamotoa, Heitmania, Yamadamyces, and
Yurkovia. Many of these yeasts are slow-growing extremo-
philes, organisms thriving under conditions that are hard to
survive (Buzzini etal. 2018). Consequently, their isolation,
cultivation, characterization and preservation are extremely
difficult and their diversity is largely underestimated.
Gadanho etal. (2006) reported members of the tremel-
lomycete genera Goffeauzyma, Naganishia, Solicoccozyma,
Phaeotremella and the Microbotryomycetes genera Pseu-
dohyphozyma and Rhodotorula from an acidic pond of the
Iberian Pyrite Belt. The genus Goffeauzyma contains a clade
of yeasts from extreme acidic environments (Gadanho and
Sampaio 2009; Russo etal. 2010). Only a few fungal species
can survive temperatures of 55–60°C, and none of them are
yeasts, which usually grow between 20 and 25°C (Buzzini
etal. 2018). Among a few thermotolerant basidiomycetes,
human pathogens of the genus Cryptococcus (C. neofor-
mans species complex) in Tremellales and Trichosporonales
species Takashimella tepidaria and Vanrija thermophila
show a remarkable tolerance to elevated temperatures. Psy-
chrophilic and psychrotolerant species are more common
among basidiomycetous yeasts. The tremellomycete genera
Mrakia (Cystofilobasidiales), Naganishia (Filobasidiales),
Gelidatrema (Tremellales), Holtermanniella (Holtermanni-
ales) accommodate several prominent cold-adapted yeasts
(Buzzini etal. 2018). Members of the genus Cystobasidium
in Cystobasidiomycetes were also repeatedly isolated from
cold habitats. In Microbotryomycetes, several genera are
almost exclusively restricted to cold environments. Particu-
larly, the genera Leucosporidium (Leucosporidiales), and
members of the family Chrysozymaceae (e.g., Bannozyma,
Fellomyces, Hamamotoa) and order Kriegeriales (Campto-
basidium, Cryolevonia, Glaciozyma, Phenoliferia) show
strong affinity to low temperatures. Some of these yeasts
can be also isolated from mild climates (e.g., Yurkov etal.
2016, 2020). Nevertheless, many of them remain under-
sampled, probably because of the slow growth and com-
plicated culture handling. Extremophile yeasts may, there-
fore, represent a large proportion of undescribed diversity.
Also, knowing physiological preferences of yeast states is
important to obtain cultures of lichenicolous fungi and other
mycoparasites.
Sexual states of dimorphic basidiomycetes are not always
easy to spot in nature. Fruitbodies of witches' butter, Tre-
mella mesenterica and a few other jelly fungi are rather large
(up to 10–15cm) and brightly coloured. However, many
species of jelly fungi do not have such a remarkable outlook
being white, transparent, or dark-coloured, and producing
small basidiocarps that are hardly visible when dry (e.g.,
Pseudotremella moriformis, and Phaeotremella simplex).
Some other tremellalean species are intrahymenial parasites,
producing spores within the fruitbodies of their hosts, and
are only visible microscopically (e.g. Tremella giraffa, Tre-
mella protoparmaliae, and Syzygospora lapponica).
Ribosomal RNA sequencing helps largely when identi-
fying yeasts and dimorphic taxa. But molecular analyses
of mycoparasites and lichenicolous fungi is challenging
and may include cloning, design of specific primers and
meta-barcoding approaches. Due to the aforementioned
constraints, sequences of yeast stages largely outnum-
ber sequences of sexual species, as discussed in Liu etal.
(2015a, b, c) and Kachalkin etal. (2019). A combination
of two ribosomal DNA-barcodes provides usually reliable
Fungal Diversity
1 3
identification results, with the ITS region being, as a rule,
more variable than the LSU (Schoch etal. 2012). A few
lineages in the Tremellomycetes demonstrated the opposite
situation, in spite of the expected greater variability in the
ITS region, which is less constrained for mutations (Scor-
zetti etal. 2002). However, a growing number of available
sequences showed that species delimitation with ITS and
LSU is sometimes problematic. Studies that utilized multi-
locus sequence analyses (MLSA), mating experiments, and
genomic analyses revealed cryptic species and species com-
plexes. There are seven closely related species in the patho-
genic Cryptococcus species complex (Hagen etal. 2015)
and three species in the C. amylolentus species complex
(Passer etal. 2019). The available knowledge suggests that
the reliable identification of species in that genus can be
achieved by sequencing protein-coding genes (e.g., Passer
etal. 2019). An MLS analysis of the Papiliotrema flavescens
species complex demonstrated a limited utility of ITS and
LSU and additionally revealed two novel cryptic species in
the complex (Yurkov etal. 2015b). Nucleotide sequences
of type strains in Mrakia, Solicoccozyma, Saitozyma, and
Vishniacozyma allow a formal separation of species in these
genera. However, when other publicly available sequences
were considered, it was not always possible to set clear bor-
ders between closely related species (Scorzetti etal. 2002;
Yurkov etal. 2015b, 2020). Specifically, it is unlikely that
pairwise comparisons of nucleotide sequences of ITS and
LSU will always provide a reliable identification of yeasts
comprising the following species complexes, namely Mra-
kia gelida (with M. frigida and M. blollopis) Solicoccozyma
aeria (with S. phenolica and S. terrea), Saitozyma pod-
zolica, and Vishniacozyma victoriae (with V. carnescens
and V. tephrensis). There is a good chance that further, and
more detailed, studies will reveal cryptic diversity in other
clades and genera of Tremellomycetes. In Microbotryo-
mycetes, several species complexes are known, including
cold-adapted yeasts in Leucosporidium scottii and carotene-
producing red yeasts Rhodotorula glutinis. Species in the
Rhodotorula glutinis species complex were delimited using
a combination of nucleotide sequences analyses, MSP-PCR
fingerprinting, mating assays, and DNA-DNA hybridisa-
tion experiments (Gadanho and Sampaio 2002) and later
sequences of pheromone receptor genes (Coelho etal. 2011).
Similarly, the psychrotolerant yeasts Leucosporidium scottii,
L. creatinivorum, L. yakuticum were demonstrated to com-
prise a complex of closely related interbreeding species (de
García etal. 2015).
A large amount of overlooked diversity is probably also
hidden in several species complexes of lichenicolous and
mycoparasitic taxa. Millanes etal. (2014b) confirmed that
Biatoropsis usnearum included several independent line-
ages some of which were later described as species based
on molecular and morphological evidence (Millanes etal.
2016b; Diederich and Ertz 2020), and a few others remain
undescribed awaiting for thorough morphological charac-
terization. Other examples of species initially discovered as
‘cryptic’ that have been later characterized and described
based on morphological traits include Tremella cetrariel-
lae and Tremella tubulosae (Millanes etal. 2015; Diederich
etal. 2020). Several groups are known to include cryptic
diversity, notably Cyphobasidium spp. (Cystobasidiomy-
cetes), Phaeotremella foliacea, Tremella macrobasidiata
and Tremella mayrhoferi (Tremellomycetes) (Spribille etal.
2016; Zamora etal. 2009, 2016, 2018). Future analyses of
host-related, morphological, and molecular data will clarify
taxonomic status and diversity of these groups.
New species publication rate
The Dictionary of Fungi (Kirk etal. 2008) listed 14 species
in the class Cystobasidiomycetes, 208 species in Microbot-
ryomyctes, and 377 species in Tremellomycetes. Diversity
of fungi in Tremellomycetes and Cystobasidiomycetes have
substantially increased since then. In a breakdown of diver-
sity of species and genera described during the last ten years,
the most species-rich class is Tremellomycetes followed by
Microbotryomycetes and Cystobasidiomycetes (Table3,
Fig.3). The species numbers reflect problems of high-rank-
ing classification in these taxonomic groups. Nearly a half
of species described in Microbotryomycetes and Cystoba-
sidiomycetes could not be assigned to any taxonomic order
and are presently accommodated in incertae sedis genera. In
Tremellomycetes, the vast majority of taxonomic novelties
were described in the order Tremellales.
Ectomycorrhizal basidiomycetes
GYROPORUS
Gyroporus (Gyroporaceae, Boletales) is a genus of obli-
gately ectomycorrhizal, poroid mushrooms with represent-
atives on every major continent except Antarctica. The
genus comprises species with bright yellow spore prints,
clamp connections, and the unique condition of having
circumferentially (as opposed to longitudinally) arranged
stipe hyphae. Members of Gyroporus are mycorrhizal with
an array of plant species from several plant families includ-
ing Betulaceae, Fabaceae, Fagaceae, Myrtaceae, Pinaceae
and Phyllanthaceae. Gyroporus is a boletoid genus in the
largely gasteroid Sclerodermatineae (Binder 1999), a sub-
order of Boletales notable for exhibiting a diverse array of
morphologies and ecologies (Wilson etal. 2011). Gyro-
porus diverged from other lineages in Sclerodermatineae
around 61 Mya (Wilson etal. 2012). The iconic European
taxa Gyroporus castaneus and Gyroporus cyanescens have
been documented since the eighteenth century, classified
Fungal Diversity
1 3
at that time in Boletus (Bulliard 1787, 1788). Despite this
long history of formal documentation, many Gyroporus
species remain to be discovered and described. There are
about 35 recognized species (this includes some described
varieties not yet formally elevated to species status), which
historically have been mostly described from Eurasia,
Africa, and North America. The existence of globally
distributed semi-cryptic species complexes has hindered
progress on properly diagnosing and describing new spe-
cies. This is especially true for numerous nondescripts,
brown-colored species that are often mistakenly identified
as Gyroporus castaneus.
Species diversity ofGyroporus
Since Gyroporus species are described from fruitbodies, the
eventual description of all extant species via existing her-
barium specimens and further fieldwork is a tractable effort.
Also, metagenomic approaches may be a route to estimate
and corroborate species diversity. For example, in a study of
fungal internal transcribed spacer (ITS) sequences from soil
Table 3 New yeast species of Tremellomycetes, Microbotryomycetes and Cystobasidiomycetes published between 2009 and 2020
Taxon2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020 New species
publication rate
Tremellomycetes 12 14 17 19 14 7311512638 67 0.0557 (252/377/12)
Tremellales 11 8151611624 12 6316 54
Filobasidiales 111113 6
Trichosporonales122221325216
Holtermanniales1
Cystofilobasidiales313181
Cystobasidiomycetes 3142244149110.2679 (45/14/12)
Cystobasidiales2 22431325
Erythrobasidiales1 3
Microbotryomycetes 665413 7354320.0304 (76/208/12)
Heitmaniales 32
Heterogastridiales 1
Kriegeriales 12 11 2
Leucosporidiales 11111
Microbotryales 61 1
Rosettozymales 3
Sporidiobolales12327
Fig. 3 Line chart of new yeast
species of each order in Tremel-
lomycetes, Microbotryomycetes
and Cystobasidiomycetes pub-
lished between 2009 and 2020
Fungal Diversity
1 3
across Australia (Davoodian etal. 2020b), 19 species (opera-
tional taxonomic units based on ITS) of Gyroporus were
inferred from across the continent. Based on Davoodian
etal. (2018, 2019, 2020a), ten species of Gyroporus are
documented from Australia based on phylogenetic analysis
of atp6 and rpb2 DNA sequences and morphology (includ-
ing three species yet to be formally described). Considering
that ITS sequences can overestimate species diversity given
intragenomic variation among copies within some lineages
(e.g., Vydryakova etal. 2012; Lindner etal. 2013), it is pos-
sible that all species of Gyroporus from Australia are known
and the task of describing all species is easily achievable. If
not, it is possible that further collections are required from
areas where fieldwork has been infrequently conducted,
such as the Kimberly of Western Australia. Davoodian etal.
(2020b) inferred 1002 ITS operational taxonomic units for
the Boletales across Australia; assuming the diversity of
Australian Boletales is between half this number and 1000
species, describing all Australian Boletales is a potentially
achievable project with large teams of workers. By using
environmental metagenomics to acquire rough estimates of
species diversity throughout an area, in combination with
graphing species accumulation curves at various scales, the
discovery and eventual description of all species of Gyropo-
rus and other Boletales traditionally described from fleshy
basidiomes can be readily implemented across the globe.
New species publication rate
Given advances in phylogenetic systematic techniques, in
recent years there has been major activity around describing
new species of Gyroporus, which has aided in untangling the
species complexes and expanded the occurrence of novel
described species to Australia as well as South America
(e.g.Davoodian etal. 2018, 2019, 2020a; Magnago etal.
2018a, b; Table4; Fig.4). Based on the phylogenetic and
morphological diversity uncovered in these and other recent
studies, the number of species of Gyroporus is likely to be in
the range of 70–100. East Asia and Southeast Asia especially
appear to be the largest reservoir of undescribed Gyroporus
diversity (Davoodian etal. 2018, 2020a).
TRICHOLOMA
Tricholoma was established as a tribus within the genus
Agaricus (Fries 1821) and then erected as a distinct genus
by Staude (1857). Tricholoma now is the type and largest
genus of the conserved family Tricholomataceae (McNeill
etal. 2006) as recently circumscribed by Sánchez-García
etal. (2014) using molecular data. Over the years more than
1000 names (including species and infraspecific taxa; 1293
according to Index Fungorum, http:// www. index fungo rum.
org/, accessed on 27 Oct. 2020; 1350 according to Myco-
bank, https:// www. mycob ank. org/, accessed on 27 Oct.
2020, Robert etal. 1999; 1104 according to Catalogue of
Life, Roskov etal. 2020) have been published or combined
in the genus and many of these have since been transferred
to other genera, based on morphological and/or molecular
data (Singer 1986; Trudell 2012; Christensen and Heilmann-
Clausen 2013; Heilmann-Clausen etal. 2017; Reschke
etal. 2018). Currently, about 250 species are recognized in
Tricholoma s. s. worldwide (Kirk etal. 2008; Ovrebo and
Hughes 2018; Reschke etal. 2018; He etal. 2019; Ovrebo
etal. 2019; Xu etal. 2020). This genus diverged from its
saprotrophic sister genera Dermoloma and Pseudotricho-
loma and began diversification during the late Eocene, 61
(36–92) Mya, possibly with Pinaceae as ectomycorrhizal
hosts (Sánchez-García 2016; Sánchez-García and Matheny
2017), favored by cooling temperatures and the expansion
Table 4 Number of new
Gyroporus species published
per year between 2009 and 2020
New species publication rate 0.150 (18/10/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number000110012733
Fig. 4 Line chart of new Gyro-
porus species described per year
between 2009 and 2020
Fungal Diversity
1 3
of their host communities, as shown in other groups of
ECM fungi (Ryberg and Matheny 2012; Looney etal. 2016;
Sánchez-García 2016; Sánchez-García and Matheny 2017;
Sato and Toju 2019).
Tricholoma has been restricted to species with centrally
stipitate, fleshy fruitbodies with adnate-sinuate lamel-
lae (tricholomatoid habit), white spore-print and smooth,
hyaline, inamyloid spores (Gulden 1969; Bon 1984, 1991;
Singer 1986; Shanks 1997; Bessette etal. 2013; Christensen
and Heilmann-Clausen 2013; Heilmann-Clausen etal. 2017;
Reschke etal. 2018). Vizzini etal. (2020), using a novel
standardized method to test sporal amyloidity showed evi-
dence that in the tested European species of this genus, the
spores are amyloid. Tricholoma is widely accepted or sup-
posed to be an ectomycorrhizal (ECM) genus (Trappe 1962;
Garrido 1988; Molina etal. 1998; De Roman etal. 2005;
Agerer 1999, 2006; Zeller etal. 2007; Rinaldi etal. 2008;
Tedersoo etal. 2010; Ryberg and Matheny 2011; Chris-
tensen and Heilmann-Clausen 2013; Heilmann-Clausen
etal. 2017). However, the genus also encompasses some
species that form dual ectomycorrhizal/monotropoid or
ectomycorrhizal/pyroloid associations linking trees and
monotropoid or pyroloids mycoheterotrophic plants (Eri-
caceae) (Björkman 1960; Bidartondo and Bruns 2001, 2002;
Leake etal. 2004; Bidartondo 2005; Tedersoo etal. 2007;
Trudell 2012) or are associated with green or achlorophyl-
lic orchids (Jacquemyn etal. 2016; Pecoraro etal. 2018;
Schweiger 2018; Chen etal. 2019b). Tricholoma matsutake
was suspected to be parasitic on pine roots without forming
a fungal mantle (mycoclena) or a Hartig net (Masui 1927;
Ogawa 1975; Yamanaka etal. 2020). Yamada etal. (1999a,
b), Guerin-Laguette etal. (2004) and Endo etal. (2015),
however, demonstrated that T. matsutake form on roots of
seedlings, in field and invitro, true ectomycorrhizae with a
fungal mantle and a well-developed Hartig net. Tricholoma
matsutake can also behave as a root endophyte of arbuscular
mycorrhizal trees (Murata etal. 2013, 2014; Selosse etal.
2018). Tricholoma species form medium-distance explora-
tion types with uniformly shaped or differentiated rhizo-
morphs (Agerer 1999, 2006).
Species diversity ofTricholoma
Tricholoma species show a worldwide distribution (Teder-
soo etal. 2010; Christensen and Heilmann-Clausen 2013;
Heilmann-Clausen etal. 2017; Reschke etal. 2018), but
they seem to be the most common and diverse in temper-
ate and subtropical zones in both the southern and northern
hemisphere. The host plants are mainly trees belonging to
Pinaceae, Fagaceae, Betulaceae and Salicaceae (Trudell
2012; Bessette etal. 2013; Christensen and Heilmann-
Clausen 2013; Heilmann-Clausen etal. 2017; Reschke
etal. 2018) but some Tricholoma species are associated with
Eucalyptus (Myrtaceae) (Bougher 1996), Dryas (Rosaceae)
and Helianthemum (Cistaceae) (Christensen and Heilmann-
Clausen 2013), Ericaceae (subfamilies Monotropoideae and
Pyroloideae) (Leake etal. 2004; Bidartondo 2005; Teder-
soo etal. 2007; Trudell 2012) and Orchidaceae (Jacquemyn
etal. 2016). Some species prefer to fruitify in old and rather
unmanaged forests (Christensen and Heilmann-Clausen
2013; Dvořák etal. 2017) and can be used as indicators of
natural forests.
The diversity hotspot of Tricholoma species appears
to be the North American area, for which more than 100
accepted species have been reported (Trudell 2012; Bessette
etal. 2013; Trudell etal. 2017; Ovrebo and Hughes 2018;
Reschke etal. 2018). Sixty-three to 88 species are listed
from Europe (Bon 1984, 1991; Riva 1988, 1998, 2003;
Galli 2005; Kirby 2012; Christensen and Heilmann-Clausen
2013). Fifty-five species are reported from Turkey (Intini
etal. 2003, 2015; Sesli and Denchev 2008; Doğan and
Akata 2011; Vizzini etal. 2015; Şen etal. 2018; Şen and
Alli 2019; Haelewaters etal. 2020). About 50 species have
been reported from China (Deng etal. 2004; Deng and Yao
2005; Yu etal. 2006; Hosen etal. 2016; Yang etal. 2017;
Reschke etal. 2018; Xu etal. 2020). From other Asian areas,
there are scattered reports from Japan (Kawamura 1954;
Hongo 1959, 1968, 1974, 1983, 1988, 1991; Imazeki etal.
1988), Korea (Murata etal. 2008; Park etal. 2014),Viet-
nam (Kiet 1998), Laos (Wan etal. 2012), Thailand (Sanmee
etal. 2007), Malaysia (Corner 1994, who used a very broad
Tricholoma genus concept), Bhutan (Wan etal. 2012), India
(Tanti etal. 2011; Gogoi and Sarma 2012; Khaund and Joshi
2013) and Nepal (Adhikari 2014). Reports from other parts
of the world are those from Australia (Bougher 1996) and
New Zealand (Stevenson 1964; Orlovich and Cairney 2004),
North Africa (Maire 1915; Malençon and Bertault 1975;
Kytövuori 1988; Ota etal. 2012; Benazza-Bouregba etal.
2016), Central America (Costa Rica, Ovrebo etal. 2019) and
South America (Horak 1964; Singer 1954, 1966).
Several Tricholoma species seem to have a circumboreal
distribution in Asia, Europe and North America: e.g. T. albo-
brunneum, T. cingulatum, T. matsutake, T. roseoacerbum,
T. vaccinum (Heilmann-Clausen etal. 2017; Trudell etal.
2017; Reschke etal. 2018). Some species (~ 20%, Sánchez-
García 2016; Sánchez-García and Matheny 2017) show an
extreme host specificity and may be restricted to a single
host genus or species, such as T. diemii and T. patagonicum
with Nothofagus dombeyi, T. albobrunneum and T. imbrica-
tum with Pinus spp., T. cingulatum with Salix spp., T. popu-
linum with Populus spp., T. dulciolens and T. inamoenum
with Picea spp., T. quercetorum with Quercus spp. (Singer
1954; Grubisha etal. 2012; Christensen and Heilmann-
Clausen 2013; Reschke etal. 2018); many other species such
as T. argyraceum, T. scalpturatum, and T. sulphureum are
reported in association with various hosts (Bon 1984, 1991;
Fungal Diversity
1 3
Riva 1988, 2003; Molina etal. 1998; Galli 2005; Carriconde
etal. 2008; Jargeat etal. 2010; Christensen and Heilmann-
Clausen 2013; Sánchez-García and Matheny 2017; Reschke
etal. 2018).
Species identification and section recognition within
Tricholoma traditionally relied on morphological features
such as pileus colour, structure of the pileipellis, presence/
absence of clamp-connections, presence/absence of hyme-
nial cystidia, size and shape of the basidiospores (Bon 1984,
1991; Singer 1986; Riva 1988, 1998, 2003; Shanks 1997;
Kirby 2012; Trudell 2012; Bessette etal. 2013; Christensen
and Heilmann-Clausen 2013). Such morphological delimit-
ing characters were supported as useful and phylogenetically
informative by molecular analyses (e.g., Heilmann-Clausen
etal. 2017; Reschke etal. 2018). The nrITS region is still the
most widely used molecular marker in species delimitation
within Tricholoma and it has been found to be a suitable bar-
code (Comandini etal. 2004; Carriconde etal. 2008; Mou-
hamadou etal. 2008; Jargeat etal. 2010; Heilmann-Clausen
etal. 2017; Trudell etal. 2017; Reschke etal. 2018; Ovrebo
etal. 2019; Xu etal 2020), but see the caveats in Badotti
etal. (2017). Other markers, such as the V6 and V9 domains
of the mitochondrial SSU-rDNA (Mouhamadou etal. 2008),
the 5' part of the mitochondrial cox1 gene (Moukha etal.
2013), the gpd gene (Jargeat etal 2010; Ota etal. 2012),
megB1 region (Ota etal. 2012) and the tef gene (Jargeat etal
2010; Ota etal. 2012) were used coupled or not to nrITS. In
particular, sections Genuina, Caligata, Contextocutis, Seri-
cella, Terrea and Tricholoma are in urgent need of further
phylogenetic studies because T. equestre s.l., T. sulphureum
s.l., T. viridilutescens/sejunctum, T caligatum group, and T.
scalpturatum/argyraceum are species complexes showing
considerable cryptic diversity (Kytövuori 1988; Kalamees
2001; Carriconde etal. 2008; Jargeat etal. 2010; Moukha
etal. 2013; Heilmann-Clausen etal. 2017; Trudell etal.
2017; Reschke etal. 2018).
The knowledge of the diversity and distribution of Tricho-
loma species on a global scale is generally still unsatisfac-
tory and patchy. Species diversity of Tricholoma species
appears quite well-studied in Europe (above all in the north-
western part), and important recent monographic works in
Europe are those of Gulden (1969), Bon (1984, 1991), Riva
(1988, 1998, 2003), Noordeloos and Christensen (1999),
Galli (2005), Christensen and Heilmann-Clausen 2008,
2012, 2013; Kirby 2012 and Heilmann-Clausen etal. (2017).
Heilmann-Clausen etal. (2017) provided the first compre-
hensive molecular analysis (only ITS based) of the genus,
focused on northern European species. Molecular works
focused only on sections or species complexes are those
by Carriconde etal. (2008), Mouhamadou etal. (2008),
Moukha etal. (2013), Jargeat etal. (2010). Reschke etal.
(2018) is the first molecular analysis combining Tricholoma
collections from Europe, North America and Asia.
An estimate of total fungal diversity in Europe based
on the ideal 6:1 ratio of fungi/vascular plants proposed by
Hawksworth (1991, 2001) would suggest that, in general, the
fungal diversity in Europe is well investigated (over 75,000
fungal species/over 12,500 plant species, 6:1 ratio, Senn-
Irlet etal. 2007).
Despite being the area for which the highest number of
species (100) has currently been surveyed, in North America
the genus Tricholoma historically has received relatively lit-
tle attention. Compared to the situation in Europe, North
American Tricholoma species are poorly known and nearly
all groups/sections are in need of additional study (Trudell
2012; Reschke etal. 2018). The over 60 Tricholoma species
described by Peck in the late 1800s and early 1900s (e.g.,
Peck 1875, 1891, 1900, 1904, 1912), and those described
by Murrill in the first half of the 1900’s (e.g., Murrill 1913,
1938, 1942, 1945, 1949) are still difficult to interpret and
many of them were later transferred to other genera. The
studies by Kauffman (1918), Smith (1942), Hesler (1958)
and Bigelow (1979) were not carried out in a monographic
perspective. Then, the most important contributions were
those by Ovrebo (1973, 1980, 1986, 1989), Ovrebo and
Tylutki (1975), Ovrebo and Smith (1979), Ovrebo and
Hughes (2018), mainly focused on Pacific Northwest and
the Great Lakes region and often interpreting some of Peck’s
species concepts; by Shanks (1994, 1996, 1997) mainly on
Tricholoma species from California; Bessette etal. (2013),
with the first comprehensive monograph on North American
Tricholoma spp.; Trudell etal. (2017), Ovrebo and Hughes
2018 and Reschke etal. (2018) using molecular markers.
Additional studies are needed to deepen the knowledge
concerning the diversity and taxonomy of Tricholoma spp.
in North America. Bates etal. (2018) reported for North
America a 1.9:1 ratio (44,000 fungal species/23,000 plants).
China, albeit with only 50 species listed, is the Asian
area with the greatest diversity of Tricholoma species (Deng
etal. 2004; Deng and Yao 2005; Yu etal. 2006; Hosen etal.
2016; Yang etal. 2017; Reschke etal. 2018; Xu etal. 2020).
Scarce and scattered is the knowledge about the presence
of Tricholoma species in adjacent Asian countries due to
the lack of modern comprehensive treatments (Reschke
etal. 2018). The knowledge of Tricholoma in China is still
limited, as relatively few studies have been devoted to this
topic. Deng etal. (2004) provided an annotated checklist
of Tricholoma from China (40 species) and Deng and Yao
(2005) made revision of some Tricholoma species reported
from China. Since then, 12 new species were described from
China (Yu etal. 2006; Hosen etal. 2016; Yang etal. 2017;
Reschke etal. 2018; Xu etal. 2020). As one of 17 megad-
iverse countries (Noss 1990), China is a hotspot extremely
rich in biodiversity and endemism, and its Flora consists
of about 35,000 plant species (Ministry of Environmental
Protection of China (EMP), 2011; Volis 2018), while, on the
Fungal Diversity
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contrary, the database for the Checklist of Fungi in China
currently contains around 27,900 fungal species (Fang etal.
2018; Institute of Microbiology, Chinese Academy of Sci-
ences 2018), with a 0.8:1 ratio. Focusing on a smaller area,
Northern Yunnan in southwest China is part of one of the 25
world biodiversity hotspots of the world (Myers etal. 2000).
About 15,000 seed plant species and 7,000 fungal species
are reported from Yunnan (Yang etal. 2004), which leads
to a 0.46/1 ratio (7000/15,000), a ratio very far from the
ideal 6:1 ratio proposed by Hawksworth (1991, 2001) (but
see also Tedersoo etal. 2014 and Hawksworth and Lücking
2017 for a reassessment of diversity ratios).
The 250 Tricholoma species so far recognized world-
wide are an underrepresentation of the actual biodiversity
of the genus. Cryptic speciation occurrence revealed in some
Tricholoma species by molecular analyses (e.g. Carriconde
etal. 2008; Jargeat etal. 2010; Heilmann-Clausen etal.
2017; Yang etal. 2017) does not facilitate the assessment of
specific diversity (Hawksworth and Rossman 1997; Hawks-
worth and Lücking 2017). Based on studies of selected fun-
gal complexes available, it was suggested that, in general, the
number of known fungi might rise by a factor of five (Hawk-
sworth and Rossman 1997) or more (up to eleven according
to Hawksworth and Lücking 2017) for cryptic speciation.
The application of multiple genetic markers will allow to
untangle the species complexes.
The status of many species described from North Amer-
ica is unclear. The application of taxa originally described
from Europe on American specimens must be redefined for
many species. As said by Trudell (2012), “For now, a bigger
issue comes from not knowing whether the North American
fungi to which European names have been applied really
do belong to the same species. Few, if any, mycologists
have spent enough time on both continents to have firsthand
comparative knowledge of large numbers of their respective
fungi and few critical studies have been done to evaluate our
use of European names.
The number of Tricholoma species recorded in North
America and Asia is scarce compared to those in Europe,
considering the extension of these geographical areas and
the fact that in Asia and America there is the greatest diver-
sity of Pinaceae and Fagaceae (the two most important
host families for Tricholoma species) at genus and species
level (Nixon 2006; Kremer etal. 2007; Eckenwalder 2009;
Cannon etal. 2018; Farjon 2018). Most Tricholoma species
are able to form ECM associations with a wide range of
host trees, and, probably, this generalist attitude may have
allowed them to explore and adapt to new environmental
niches, and consequently increasing their rate of diversifica-
tion (Sánchez-García 2016; Sánchez-García and Matheny
2017). As it was generally pointed out by Tedersoo etal.
(2014), ectomycorrhizal species richness is strongly related
to the richness of host plant species.
Further research is needed to increase the knowledge
concerning the taxonomy, diversity and phylogeography of
Tricholoma species worldwide. A careful sampling strat-
egy of North American and Asian areas will be crucial, but
also Australia, New Zealand and South America should be
included. Biodiversity analyses will also have to take into
account the ongoing outputs from the metabarcoding meth-
ods (Tedersoo etal. 2014; Hawksworth and Lücking 2017;
Khan etal. 2020).
New species publication rate
The number of described fungal species accelerated in
the last decade (2009–2020) after the advent of molecular
approaches to species delimitation (Hawksworth and Lück-
ing 2017). Apart from some intraspecific taxa [e.g., T. sul-
phureum var. nigrescens (Gillet) Deparis (Deparis 2013,
T. virgatum var. fulvoumbonatum Seslı, Contu and Vizzini
(Vizzini etal. 2015), T. sulphureum var. inolens Chiarello
& Battistin (Chiarello and Battistin 2018), T. viridifucatum
var. etruriae Raumi, Martolini, Matteini and Pierotti (Raumi
Table 5 Number of new
Tricholoma species published
between 2009 and 2020
New species publication rate 0.0133 (32/200/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number211110126737
Fig. 5 Line chart of the number
of new Tricholoma species pub-
lished from 2009 to 2020
Fungal Diversity
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etal. 2019)], a nom. inval., T. grave (Bessette etal. 2013)
and four nomina nova published by Blanco-Dios (2020) for
replacing four Malaysian taxa whose names are preoccupied
(Corner 1994), 26 new species were established between
2010 and 2020 (see Table5), constituting 10% of the spe-
cies currently recognized in Tricholoma (about 250, Kirk
etal. 2008; Ovrebo and Hughes 2018; Reschke etal. 2018;
He etal. 2019; Ovrebo etal. 2019; Xu etal. 2020). Eleven
were described from Asia (China), eight from Europe, three
from Central America (Costa Rica), two from Turkey, and
two from North America (USA and Mexico); 20 of which
have been described in the last 4years (Fig.5).
RUSSULA
Russula is the type genus of the russuloid clade or the order
Russulales, and the ancestor of Russulales diverged during
late Jurassic (170–180 Mya) (Zhao etal. 2017a, b; Varga
etal. 2019). In taxonomic study, it is a very old genus, dating
back to the end of the eighteenth century (Persoon 1796),
probably because it is so prominently present in most habi-
tats, so extremely diverse and also very well characterizable
both in the field and under the microscope. Consequently, it
has attracted the interest of many professional and amateur
mycologists and is undoubtedly one of the most frequently
monographed genera of larger mushrooms (see Fig.6).
Fig. 6 European Russula
described in the past two centu-
ries (1793–2003) by European
mycologists with indication of
the most important published
genus monographs or other
major contributions by profes-
sional (in red) and amateur (in
green) mycologists
Fig. 7 American Russula described in the past two centuries (1872–2006) by American mycologists with indication of the most important pub-
lished genus monographs or other major contributions by professional (in red) and amateur (in green) mycologists
Fig. 8 Species number of Russula from 1860 to 2005 (416 species in
total including 329 species from USA and 87 species from Europe)
Fungal Diversity
1 3
Most of the traditional complex infrageneric classifica-
tion of the genus has been laid out in these European mono-
graphs, especially those written in more recent years by emi-
nent amateur mycologists (Romagnesi 1967, 1987; Sarnari
1998, 2005; Bon 1988). In Europe, this amateur community
represents in Europe the major source of expertise in the
genus since the 1960s.
In other parts of the world, the diversity of the genus has
been largely neglected as was the case for most of the other
macrofungi, with two notable exceptions though: The United
States of America and Central Africa. The exploration and
description of the existing Russula diversity in North Amer-
ica started approximately a century later compared to Europe
(see Figs.7, 8), essentially with the studies of Peck (see
Adamčík etal. 2018). However, the clear gap between pro-
fessional and amateur mycologists in America was respon-
sible for the sudden arrest of local Russula research once the
professional expertise had vanished, leaving this continent
at the beginning of the twenty-first century with an aston-
ishing number of 329 different endemic Russula that had
been described (in addition to an estimated number of 87
European Russula that had been reported from the area) but
that quasi nobody in America was able to identify any more.
The second part of the world for which Russula diversity
was fairly well-documented during the past century is tropi-
cal Africa (including Madagascar), where the mycological
exploration of larger mushrooms had its roots in the colonial
period. For Russula, apart from many smaller contributions,
the principal monographs were those published in the Fun-
gus flora of Central Africa series (https:// www. ffta- online.
org/) by Buyck (1993, 1994, 1997) and in the “Prodrôme a
une flore mycologique pour Madagascar et Dépendances”
series by Heim (1938), culminating in almost 200 hundred
different, well-illustrated and described Russula species and
their infraspecific taxa for tropical Africa at the beginning
of the twenty-first century.
Species diversity ofRussula
Russula has always been considered one of the most diverse
ectomycorrhizal mushroom genera, whereas older hand-
books estimated the total number of Russula species in the
world to be around 700–800 (Kirk etal. 2008), the most
recent estimates are higher. Looney etal. (2016) calculated
that the number of sequenced OTUs in the northern hemi-
sphere was already in excess of 1000, but Buyck (2012)
estimated on the basis of more than 10years of collecting in
North America that the number of North American Russula
alone was surely closer to 1500 than to the ca. 450 known
at present. The total number of Russula species in the world
has been estimated to be in excess of 3000 (He etal. 2019),
but could still be higher. These high estimates seem at least
supported by the fact that many newly published Russula
species are not known from environmental sequences, while
most of the continents are largely unexplored with excep-
tion of Europe and, to a lesser degree, also North America.
Indeed, unpublished results from inventories in little or
unexplored parts of the world such as Madagascar and New
Caledonia show that probably their entire Russula mycota
may be original as even morphologically similar species are
genetically distant from their closest relatives.
New species publication rate
During the past ten years the situation has changed pro-
foundly, and this time on all continents. The main game
changer has been the development of molecular tools at the
end of the twentieth century and their impact on species
descriptions and fungal phylogenies. Even for beginners,
Russula was always a very ‘easy’ genus to recognize in the
field, at least in Europe, but the genus was reputed extremely
difficult as to the recognition of the various individual spe-
cies because of the often-incredible variation in color and
other features, and this notwithstanding a rich array of
microscopic features compared to many other mushroom
genera. This morphological variability ultimately led to an
exaggerated multiplication of names at different nomenclatu-
ral ranks (species, variety or form) given to the same taxa by
different mycologists.
During the past decennium, the number of new Rus-
sula species published each year oscillated between 10 and
15, except for a few years when new species numbers sky-
rocketed. In 2011, for example, there were 88 new Russula
taxa published, 23 new species and many new varieties and
forms, all of them uniquely based on often rather insignifi-
cant morphological differences. The large majority of these
new taxa were described in a new Russula monography pub-
lished in Eastern Europe (Socha etal. 2011), others were
described by a French Russula expert with a prolific record
of new species and infraspecific taxa (Freund and Reumaux
2011). The year 2011 therefore resembles other years in the
past (e.g. Reumaux etal. 1996; Reumaux and Moenne-Loc-
coz 2003) when similar monographs were published with
many new species and infraspecific taxa entirely based on
subjective interpretations of sometimes minor morphologi-
cal differences. Nowadays, large monographic works that
introduce large numbers of new species in Russula purely
based on morphology are becoming increasingly rare in the
modern era of sequence data. Indeed, with the introduction
of ITS barcode sequences to characterize species most of
the subjectivity in species recognition shifted from mor-
phology to interpretation of nucleotide differences (Li etal.
2019a, b), especially since most new species are now often
described by young mycologists with hardly any experience
with morphological recognition of Russula species.
Fungal Diversity
1 3
More recently, there has been another sudden surge in
novel Russula names with the publication in 2017, 2018
and 2019 of respectively 78, 115 and 42 new Russula spe-
cies. This time, the explanation is entirely different from the
one in 2011 as no monograph or other major revision is the
origin of this avalanche of new names, but rather a purely
technical implication of previously published phylogenetic
results. Indeed, similarly to many other lineages of agaricoid
mushrooms, earlier molecular phylogenies (e.g. Miller etal.
2001; Lebel and Tonkin 2007) had suggested that several
secotioid to entirely hypogeous genera in Russulales were
possibly synonymous with older agaricoid genera, represent-
ing convergent evolutions toward similar morphologies in
unrelated terminal clades. The publication of new species
of ‘truffle-like’ Russula had started with a paper by Lebel
and Tonkin (2007) describing several novel species from
Australia supported by molecular sequence data. Massive
recombination of the known species of these secotioid to
hypogeous relatives into Russula followed only recently
with papers published by Lebel (2017) and Elliot and Trappe
(2018) (Table6; Fig.9).
CANTHARELLUS
Cantharellus, is the type genus of the cantharelloid clade
or the order Cantharellales. The ancestor of Cantharellus
occurred around late Jurassic (170–180 Mya) or earlier (280
Mya) (Zhao etal. 2017a, b; Varga etal. 2019). In taxonomy
study, it is a very old genus and the first published mention
of the name ‘Cantharel’ date back to the mid-eighteenth cen-
tury (Adanson 1763), The genus delimitation and system-
atic placement of Cantharellus has a very turbulent history
(Buyck etal. 2014), most likely due to the very poor diver-
sity of useful microscopic features for species recognition
and the very similar overall morphology shared with many
other mushroom genera. Of the 346 species described in
Cantharellus at the end of the twentieth century, the genus-
wide type revisions by Eyssartier (2001) demonstrated that
only 59 species were good members of Cantharellus; all
other names had been recombined in as many as 40 different
genera distributed over nine of the major clades in Agarico-
mycetes (Buyck etal. 2014).
Modern phylogenies have demonstrated that Cantharellus
belongs to one of the oldest mushroom-forming clades in
Basidiomycota (Zhao etal. 2017a, b). This might explain the
poor diversity of microscopic features (no spore ornamenta-
tions, lack of well-differentiated cystidia in any of their tis-
sues) and the important variation in some of these, such as
the instability of the number of spores produced per basid-
ium, or the absence or presence of clamp connections among
infrageneric clades. It is therefore not surprising that phylo-
genetic analyses of sequence data have profoundly impacted
species recognition that was, before the advent of molecular
tools, primarily based on field habit. Also, a correct genus
delimitation, in particular from its sister genus Craterellus,
was only possible after the introduction of molecular data
(Feibelman etal. 1994; Dahlman etal. 2000). Today, spe-
cies recognition in Cantharellus has primarily become a
matter of sequence data, although successful sequencing of
the typical fungal barcode (nr ITS) poses major problems
because of its unusual length (up to > 1500 base pairs) and
extreme variability, favoring the use of tef-1 sequences to
characterize species (Buyck and Hofstetter 2011).
Species diversity ofCantharellus
Contrary to many other ectomycorrhizal genera, such as
Russula, which are common in appropriate habitats on all
continents, the existing biodiversity of Cantharellus varies
Table 6 Number of new
Russula species published per
year between 2009 and 2020
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number 3 10 22 9 11 11 12 14 40 60 37 19
New species publication rate 0.0276 (248/750/12)
Fig. 9 Line chart of number of
new Russula species published
from 2009 to 2020
Fungal Diversity
1 3
greatly between continents (Buyck 2016) and reflects most
likely its different evolutionary history. Indeed, whereas
lower diversity in Europe may probably be explained by
recent glaciations, both South America and Australia seem
extremely poor in Cantharellus species, with only a hand-
ful of species known from either continent. This is in great
contrast with the extreme biodiversity of Cantharellus in
tropical Africa (including Madagascar), with already more
than 90 different species, and the steadily growing num-
ber of chanterelles that are described from North America
and Asia. Future biogeographic interpretations based on
broadly sampled, multi-marker phylogenies will hopefully
offer an appropriate explanation for the distribution pattern
of Cantharellus.
New species publication rate
During the past 10years the number of new Cantharellus
species has been constantly growing at a rate of five to 15
new species published every year, or a total of 90 new spe-
cies between 2010 and 2020. Compared to the 19 new Can-
tharellus species published between 2000 and 2009 (this
number does not account for infra-specific or infra-generic
taxa, nor for two species that have since been transferred
to Craterellus), this is a considerable progress, putting the
total number of accepted Cantharellus species now at 166 or
almost three times more than there were 20years ago. The
publication rate of new species is not expected to diminish
in the years to come as many undescribed taxa await descrip-
tion, particularly in Africa and Asia (Buyck 2016), justifying
a total biodiversity estimate for Cantharellus ranging from
250 to perhaps 300 species worldwide (Table7, Fig.10).
Plant parasitic basidiomycetes
RUST FUNGI
Rust fungi (Pucciniales) are amongst the most collected and
studied fungi, in part due to their impact to agriculture as
well as distinctive disease symptoms. Rust fungi are obli-
gate biotrophic pathogens of plants and the largest patho-
genic order in the Basidiomycota (Cummins and Hiratsuka
2003). Rust fungi are highly host-specific, yet their evolu-
tion has been driven by host jumps to unrelated plants, fol-
lowed by adaptive radiation and switches to proximal hosts
(van der Merwe etal. 2008; McTaggart etal. 2016; Aime
etal. 2018a; Aime and McTaggart 2021). The phenotypic
and genetic diversity of rust fungi is reflected across seven
suborders and 18 families (Aime and McTaggart 2021).
The starting point for binomial names of rust fungi is Syn-
opsis Methodica Fungorum (Persoon 1801). By the height
of the Agricultural Revolution in the 1850s, more than 1500
rust fungi had been named and described, mostly from
Europe and North America. Up to the end of the twentieth
century, revisionary studies of rust fungi were based on mor-
phology (Sydow and Sydow 1904, 1915) and/or host range
(Cummins 1937, 1940a, b, 1943a, b, 1945). Notable regional
revisions of rust fungi have been composed for Australia
(McAlpine 1906), Europe (Sydow and Sydow 1904, 1915;
Dietel 1928), Japan (Hiratsuka etal. 1992), New Zealand
(Cunningham 1931), North America (Arthur 1907–1931)
and South Africa (Doidge 1950).
The largest radiation of rust fungi is found in the Puccini-
aceae, whose members shared a most recent common ances-
tor between 15 and 65 Mya (McTaggart etal. 2016; Aime
etal. 2018a; Aime and McTaggart 2021). The evolutionary
success of the Pucciniaceae is evident by (i) their known
diversity that accounts for almost half of all rust fungi,
including almost 4000 species in Puccinia, (ii) their ability
to infect diverse and unrelated hosts, and (iii) multiple path-
ways of evolution to convergent hosts (Dixon etal. 2010).
There are a few plant families that do not host rust fungi,
notably the Dipterocarpaceae and Restionaceae. In Aus-
tralia, two of the largest and most diverse plant families,
Myrtaceae and Proteaceae, are hosts to very few rust fungi
(Walker 1983), with exceptions in the Pucciniaceae, namely,
Puccinia cygnorum (Shivas and Walker 1994) and Uredo
xanthostemonis on Myrtaceae, and Puccinia grevilleae
(McTaggart and Shivas 2008) and Uredo angiosperma on
Proteaceae.
Species diversity ofrust fungi
Approximately 320 genera of rust fungi have been described,
of which ~ 125 generic names are in current use. Genera
described before nomenclatural changes brought about by
1F1N were often based on a life cycle stage (asexual taxa),
which did not indicate evolutionary relationships between
taxa. Some examples of these asexual rust genera include
Campanulopsora, Canasta, Morispora (Yepes etal. 2007),
Malupa (Ono etal. 1992), Petersonia and Wardia (Cummins
and Hiratsuka 2003). Seven of the nine genera described
in the last decade are monotypic and from Asia, Australia
or South America, namely Austropuccinia (Beenken 2017),
Caetea (Yepes and de Carvalho 2012), Crossopsorella
Table 7 New species of
Cantharellus published between
2009 and 2020
New species publication rate 0.1153 (87/65/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number 3 2 7 10 4 17 8 15 6 4 4 7
Fungal Diversity
1 3
(Souza etal. 2018), Neopuccinia (Junior etal. 2019), Qua-
sipucciniastrum (Qi etal. 2019), Puccorchidium and Sphe-
norchidium (Beenken and Wood 2015). The two exceptions
are Neophysopella with 13 species (Ji etal. 2019) and Pelas-
toma with two species (Yepes etal. 2012). Three challenges
that currently face taxonomic resolution of rust fungi at
generic rank are (i) polyphyly of genera such as Puccinia,
Pucciniastrum and Ravenelia, (ii) generic placement of spe-
cies in asexual taxa, and (iii) taxonomic placement without
comparison to types (Aime and McTaggart 2021).
There are approximately 10,559 accepted names of rust
fungi at species rank (www. Index Fungo rum. org, accessed
Fig. 10 Line chart of number of new Cantharellus species published from 2009 to 2020
Fig. 11 Treemap of taxonomic placement at family and genus rank for 10,559 described species of rust fungi. Plotted using the Treemap pack-
age (Vitolo C. 2014. TreeMap, available at https:// github. com/ cvito lo/r_ treem ap) in R (R Core Team 2014)
Fungal Diversity
1 3
9th Nov. 2020) (Fig.11). This number was calculated by
querying 110 generic names of rust fungi and exclud-
ing names that were variants below species rank as well
as taxonomic or nomenclatural synonyms. The three most
speciose genera, Puccinia (3978 species), Aecidium (1455
species) and Uredo (1394 species), are polyphyletic (Aime
and McTaggart 2021).
New species of rust will certainly be found in isolated,
under-explored, biodiverse areas, as well as through dis-
covery of cryptic diversity in species complexes. For
example, species diversity of rust fungi has increased
through resolution of taxa in Chrysomyxa (Feau etal.
2011), Coleosporium (McTaggart and Aime 2018),
Dasyspora (Beenken etal. 2012), Endoraecium (McTag-
gart etal. 2015), Gymnosporangium (Zhao etal. 2016a, b),
Melampsora (Toome and Aime 2015; Zhao etal. 2017a),
Milesina (Bubner etal. 2019), Neophysopella (Chatasiri
and Ono 2008), Phakopsora (Beenken 2014; Maier etal.
2016), Phragmidium (Liu etal. 2018), Puccinia (Demers
etal. 2017; Liu and Hambleton 2010, 2013), Puccinias-
trum (Liang etal. 2006), Ravenelia (Ebinghaus and Bege-
row 2018; Ebinghaus etal. 2018, 2020) and Uromycladium
(Doungsa-ard etal. 2018) (Fig.12).
Fig. 12 Lollipop plot of the number of described species of Puccinia from 1800 to 2020. Made using ggplot (Wickham 2016) in R (R Core
Team 2014)
Table 8 Number of new species
of selected rust fungi published
in between 2009 and 2020
New species publication rate 0.0029 (228/6570/12)
Year 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number 14 26 14 23 12 17 25 12 15 34 10 26
Fungal Diversity
1 3
New species publication rate
We searched MycoBank.org (Robert etal. 2013) to calcu-
late the number of names described after 2009 in the largest
genera of rust fungi based on Fig.11, namely Aecidium,
Chrysomyxa, Dasyspora, Endoraecium, Gymnosporangium,
Melampsora, Milesina, Neophysopella, Phakopsora, Phrag-
midium, Puccinia, Pucciniastrum, Ravenelia, Uredo, Uro-
myces and Uromycladium (Table8; Fig.13).
We predict that the rate of discovery of new taxa of rust
fungi will decline in the future. The rigor with which rust
fungi were collected in the golden age of mycological dis-
covery (nineteenth and twentieth centuries) has declined.
This is illustrated in Fig.12 by the change in numbers of
species of Puccinia described since 1801. Further, the rate
of habitat loss bodes poorly for taxa that await discovery. We
estimate that the number of extant rust fungi on this planet
is ~ 10,000 species, which accounts for as yet unidentified
taxonomic synonymy.
SMUT FUNGI
Classically, smut fungi are characterized by a specific life
cycle that alternates between a dikaryotic, plant-parasitic
stage and a haploid, saprobic yeast phase. The most charac-
teristic trait of smut fungi is their thick-walled teliospores,
which often results in a sooty-like appearance of affected
plant parts. Only recently has it been realized that this group
of fungi, which is very well-characterized by its life cycle,
represents a phylogenetically, heterogenous group that has
evolved three times independently in Ustilaginomycotina,
Microbotryales (Pucciniomycotina), and Entorrhizomycota
(Begerow etal. 1997, 2014, 2018). Many taxa belonging to
these clades do not exhibit the classical smut fungal lifestyle.
In the Exobasidiomycetes (Ustilaginomycotina) deviations
from the canonical smut fungal life cycle are often observed.
Exobasidium species on Ericaceae or Microstroma species
on various tree species, for instance, do not produce teli-
ospores anymore, but produce basidia directly from their
hyphae through the stomata of their hosts (e.g., Begerow
etal. 2001, 2002). Additionally, phylogenetic studies have
shown that many lineages that are exclusively known as
yeasts are found in these groups and it is assumed that sev-
eral lineages have lost the ability to parasitize plants (Wang
etal. 2015c; Kijpornyongpan etal. 2018; Nasr etal. 2019).
Several genera of smut fungi consist exclusively of spe-
cies known only from their asexual states: Acaromyces, Fer-
eydounia, Golubevia, Jaminaea, Meira, Microbotryozyma,
Moniliella, Quambalaria, Robbauera, Sympodiomycopsis,
Tilletiopsis, and Violaceomyces. Many yeasts were classi-
fied in large asexual genera, e.g. Pseudozyma (asexual Usti-
laginaceae), Rhodotorula (asexual Microbotriales as well a
few Ustilaginales and Microstromatales species), and Til-
letiopsis (asexual Exobasidiomycetes) until re-classification
by Wang etal. (2015c, d). In Microstroma, Mycosarcoma,
Moesziomyces, and Ustilentyloma it was possible to link
independently discovered asexual and sexual states in sev-
eral instances. The correct placement of asexual species into
sexual genera is often hampered by the lack of sequences
derived from teleomorphs. It is likely that sexual parasitic
states of asexual species will be discovered among known
fungal species when sequenced.
Species diversity ofsmut fungi
Over 2000 species of smut fungi and related lineages are
currently known. By far the most species-rich are Ustilag-
inomycotina (1906 species), followed by Microbotryales
(128), and Entorrhizomycota (18). Smut fungi are found
mostly on herbaceous host plants, and some of the Exoba-
sidiomycetes (e.g. Exobasidium, Graphiola, Microstroma,
and Quambalaria) also occur on woody hosts. Smut fungi
have been observed worldwide, including Tilletia schencki-
ana on Deschampsia antarctica from the Kerguelen Islands
in the Antarctic region (Hennings 1906). The highest species
diversity has been reported from the Northern Hemisphere,
with most species in Europe and Asia. The available lit-
erature, monographs, and regional checklists suggest that
these estimates of diversity are highly biased towards the
northern Hemisphere, whereas other regions, especially in
the tropics, are yet to be surveyed. The most comprehensive
and still most up to date source concerning the diversity
and distribution of smut fungi is the world monograph by
Vánky (2011a).
Fig. 13 Line chart of new
species of selected rust fungi
published from 2009 to 2020
Fungal Diversity
1 3
Europe is the best studied continent (Vánky 1994), espe-
cially, Northern Europe (UK: Mordue and Ainsworth 1984;
Norway: Jørstad 1963; Sweden: Lindeberg 1959; Nannfeldt
1979; Finland: Liro 1924, 1938; Denmark: Rostrup 1890),
Central Europe (Belgium: Vanderweyen and Fraiture 2014;
Germany: Scholz and Scholz 1988; Klenke and Scholler
2015; Austria: Zwetko and Blanz 2004; Switzerland: Zogg
1986; Poland: Kochman and Majewski 1973; Hungary:
Vánky 1985), and the Carpathian Region (Vánky 1985).
Monographs or checklists of smut fungi in Southwestern,
Southern, and Southeastern Europe are published for France
(Viennot-Bourgin 1956), Iberian Peninsula (Almaraz 2002),
Italy (Ciferri 1938), Slovenia (Lutz and Vánky 2009), Cro-
atia (Ivić etal. 2013), Romania (Săvulescu 1957; Vánky
1985), and Bulgaria (Denchev 2001), and for Eastern
Europe: for the Baltic States (Ignatavičiūtė 1975, 2001),
European Russia (Karatygin and Azbukina 1989; Azbukina
and Karatygin 1995), and Ukraine (Savchenko and Heluta
2012). The distribution data for some of these countries are
outdated while the information about the western and south-
ern parts of the Balkan Peninsula and the Aegean Islands is
lacking.
For Asia, monographs or checklists of smut fungi are
published for Siberia and Russian Far East (Karatygin and
Azbukina 1989; Govorova 1990; Azbukina and Karatygin
1995; Azbukina etal. 1995), Middle Asia (Uzbekistan:
Ramazanova etal. 1987; and Kazakhstan: Schwarzman
1960), Transcaucasus (Azerbaijan: Ulyanishchev 1952),
Western Asia (Israel: Savchenko etal. 2015; Iran: Vánky
and Abbassi 2013), Indian Subcontinent (Ahmad etal. 1997;
Vánky 2007), Central and Eastern Asia (Mongolia: Braun
1999; China: Guo 2000, 2011; Korean Peninsula: Denchev
etal. 2007; Japan: Ito 1936; Kakishima 1982; Denchev etal.
2013a), Indo-China (Thailand: Shivas etal. 2007), and Pap-
uasia (Papua New Guinea: Shivas etal. 2001). Many regions
in Siberia, Middle Asia, Caucasus, Western and Central
Asia, Indo-China, Malesia, and Papuasia are understudied
or even unexplored.
In North America, monographs were published by Clin-
ton (1902, 1904, 1906), Zundel (1939), and Fischer (1953).
The smut fungi of Mexico are presented in Durán (1987).
Recently, a comprehensive monographic treatment of the
smut fungi of Greenland was published by Denchev etal.
(2020a). The largest gap of knowledge for this continent is
Canada from where only a few articles have been published
during the last 50years.
For Central and South America and the Caribbean, mono-
graphs or checklists of smut fungi are published for Costa
Rica (Piepenbring 1996), Panama (Piepenbring 2001), Cuba
(Piepenbring and Hernández 1998), Colombia (Molina-
Valero 1980; Piepenbring 2002a), Bolivia (Piepenbring
2002b), Brazil (Viegas 1944), and the Neotropics (Piepen-
bring 2003). A monographic treatment of the smut fungi of
Argentina was published by Hirschhorn (1986). Neverthe-
less, few collection trips focused on this group have been
carried out in this part of the world and the smut fungi of
Central and South America and the Caribbean continue to
be understudied.
In terms of the smut fungi, Africa is the least studied con-
tinent. There is a monograph of African smut fungi by Zam-
bettakis (1970, with a supplement in 1980), a monograph of
South African smut fungi (Zundel 1938), and checklists of
the smut fungi in Africa (Vánky etal. 2011), Ethiopia and
Eritrea (Vánky 2005), and Malawi, Zambia, and Zimbabwe
(Vánky and Vánky 2002).
For Australasia, there are monographs of the smut fungi
of Australia (Vánky and Shivas 2008) and New Zealand
(Vánky and McKenzie 2002). Australia is the continent from
where the highest number of smut fungi have been described
for the last few decades.
Compared to filamentous smuts, the number of discov-
ered yeast taxa in the Ustilaginomycotina is rather small and
currently about 50 species are recognized. No yeast-like taxa
are known from the Entorrhizomycota. Due to the limited
number of observations, geographic distribution patterns of
these yeast species are mostly unknown. Often these are also
recovered from geographic regions or ecosystems that do not
harbour known host species. For example, several asexual
species of Farysia, which parasitizes hosts belonging to the
Cyperaceae, were described from leaves of different plants
worldwide with no link to a sexual stage (Inácio etal. 2008;
Rush etal. 2020). Often these yeasts are found on the surface
of leaves (Fonseca and Inácio 2006; Kemler etal. 2017) and
some yeast taxa interact with plants in other ways than do
smut fungi. Several new Exobasidiomycetes yeasts (Enty-
loma, Golubevia, and Jamesdicksonia) for instance were iso-
lated from apples in different countries and were ultimately
linked to the postharvest disorder named “white haze”, an
intensive fungal growth on the apple fruit surface result-
ing in a compromised quality of the fruits (Boekhout etal.
2006; Richter etal. 2019). Fungi morphologically similar
to the asexual morphs of Ustilaginomycotina were also fre-
quently isolated from air, soils, or animal (including human)
samples (reviewed in Boekhout etal. 2011; Begerow etal.
2014, 2018). It is also worth mentioning that some yeast
states of smuts (e.g., Acaromyces, Meira, some members of
Microstromatales) are associated with insects or insect frass.
Whether these fungi performed a remarkable host-shift or
use the insects as vectors requires further studies.
Biased accounts of species diversity to a few regions
is a difficulty to estimate the exact number of smut fungi
throughout the world. As can be seen from the species
descriptions throughout the last decade, it is also clear that
a handful of researchers have described the majority of smut
fungi in this period. Further problems result from the fact
that the species concept in smut fungi have changed from a