The evolution of species concepts and
species recognition criteria in plant
pathogenic fungi
Lei Cai, Tatiana Giraud, Ning Zhang,
Dominik Begerow, Guohong Cai & Roger
G. Shivas
Fungal Diversity
An International Journal of
Mycology
ISSN 1560-2745
Fungal Diversity
DOI 10.1007/
s13225-011-0127-8
1 23
Your article is protected by copyright and
all rights are held exclusively by Kevin D.
Hyde. This e-offprint is for personal use only
and shall not be self-archived in electronic
repositories. If you wish to self-archive your
work, please use the accepted author’s
version for posting to your own website or
your institution’s repository. You may further
deposit the accepted author’s version on
a funder’s repository at a funder’s request,
provided it is not made publicly available until
12 months after publication.
1 23
Author's personal copy
Fungal Diversity
DOI 10.1007/s13225-011-0127-8
REVIEW
The evolution of species concepts and species recognition
criteria in plant pathogenic fungi
Lei Cai & Tatiana Giraud & Ning Zhang &
Dominik Begerow & Guohong Cai & Roger G. Shivas
Received: 27 June 2011 / Accepted: 25 July 2011
# Kevin D. Hyde 2011
Abstract In this paper, we review historical and contemporary species concepts and species recognition criteria for
plant pathogenic fungi. Previous incongruent and unstable
classification based on subjective and changing criteria
have led to some confusion, especially amongst plant
pathologists. The goal of systematics is to provide an
informative and robust framework that stands the test of
time. The taxonomic histories of Cercospora, Colletotrichum,
Fusarium, as well as the rust and smut fungi, are used as
examples, to show how concepts and criteria used to delimit
and recognize species have changed. Through these examples
we compare the Genealogical Concordance Phylogenetic
L. Cai (*)
State Key Laboratory of Mycology, Institute of Microbiology,
Chinese Academy of Sciences,
West Bei Cheng Rd,
Beijing 100101, People’s Republic of China
e-mail: mrcailei@gmail.com
T. Giraud
Ecologie, Systématique et Evolution,
Bâtiment 360, Université Paris-Sud,
91405 Orsay cedex, France
N. Zhang : G. Cai
Department of Plant Biology and Pathology, Rutgers,
The State University of New Jersey,
59 Dudley Road, Foran Hall 201,
New Brunswick, NJ 08901, USA
D. Begerow
Ruhr-Universität Bochum,
Geobotanik ND03/174, Universitätsstr. 150,
44801 Bochum, Germany
R. G. Shivas
Plant Pathology Herbarium, Agri-Science Queensland,
40 Boggo Road,
Dutton Park, Qld 4102, Australia
Species Recognition, an extension of the Phylogenetic
Species Criterion, with other species recognition criteria and
show that it provides a better discrimination for delimiting
species. A rapidly increasing number of cryptic species are
being discovered amongst plant pathogenic fungi using the
Genealogical Concordance Phylogenetic Species Recognition, and it is important to determine their host range, the
severity of diseases they cause and their biosecurity significance. With rapidly expanding global trade it has become
imperative that we develop effective and reliable protocols to
detect these previously unrecognized pathogens.
Keywords Cryptic species . Species complex .
Microbotryum . Pucciniomycotina . Ustilaginomycotina .
Speciation . Taxonomy
Introduction
Plant pathologists are regularly confronted with having to
choose a name for their pathogen of interest and mycologists often need to decide when to recognize a new species
or apply an existing name. Country specific inventories of
plant pathogenic fungi with accurate and accepted names
are essential for the development of effective biosecurity
and trade policies as well as a prerequisite for pest risk
assessments (Hyde et al. 2010). These inventories also
facilitate the early identification of invasive fungal pathogens and allow the timely application of appropriate disease
control measures (Rossman and Palm-Hernández 2008).
The accurate identification of a plant pathogen will in most
cases provide a species name, which may then be used to
unlock all of our collective knowledge about the organism.
This knowledge may include its evolutionary history, life
cycle, distribution, host range, resistance to drugs, economic
Author's personal copy
Fungal Diversity
and biosecurity importance as well as control measures
(Rossman and Palm-Hernández 2008). Over time, our
understanding about how to identify plant pathogenic fungal
species has undergone several revolutionary changes.
The criteria used to delimit and identify species, as
applied to plant pathogenic fungi, have changed over time,
most recently due to the rapid development of molecular
tools. The different criteria that allow the delimitation of
species may be classified as morphological, physiological,
intersterility, host specificity, and phylogenetic. All of these
species recognition criteria attempt to identify evolutionary
independent lineages (Taylor et al. 2000). The morphological and phylogenetic criteria can further be used to
unravel evolutionary relationships between species and
arrive at a natural classification. The classification of plant
pathogenic fungal species, together with the associated
taxonomic nomenclature, as currently defined by the
International Code of Botanical Nomenclature, is fundamentally important for plant pathologists and mycologists
in all fields (Rossman and Palm-Hernández 2008; Hyde et
al. 2010).
The choice and justification of species criteria to identify
the 1.5 million fungal species estimated to populate the
world (Hawksworth 1991) or the ca 270,000 tropical plant
pathogenic fungi (Shivas and Hyde 1997), has significant
consequences for our understanding of emergent diseases
on plants and animals (Giraud et al. 2010), particularly
against a backdrop of global climate change (Chakraborty
and Newton 2011).
In this paper, we review the evolution of species
concepts and species recognition criteria in plant pathogenic
fungi, by using examples from some important groups,
namely, Cercospora, Colletotrichum, Fusarium, and the rust
and smut fungi. The taxonomic history of each group is
reviewed, with emphasis on the changing focus of criteria
used to recognize species. In particular, the utility of
Genealogical Concordance Phylogenetic Species Recognition in many fungal groups is compared with the other
species criteria. The practical implications of changing
criteria used to recognise species are discussed. We also
discuss the consequences that recent advances in our
understanding of fungal speciation have meant for developing robust species criteria, although more extensive
reviews on speciation and species recognition in fungi can
be found elsewhere (Giraud et al. 2008a; Kohn 2005;
Taylor et al. 2000).
Species concepts versus species criteria
The apparent diversity of concepts as to what constitutes a
species (De Queiroz 2007; Hey 2006) may lead one to
think that there is no general agreement amongst biologists
about what defines a species. This view stems from
confusion between the concept of a species, i.e. a description
of the kind of entity that constitutes a species, and the criteria
that delimit a particular species, i.e. practical standards for
the recognizing whether individuals should be considered
members of the same species. Many so-called “species
concepts” actually correspond to species criteria (De Queiroz
2007; Hey 2006; Taylor et al. 2000). The Biological
Species “Concept” for instance is most often meant to
emphasize the criterion of intersterility, the Morphological
Species “Concept” emphasizes the criterion of morphological divergence, the Ecological Species “Concept” emphasizes adaptation to a particular ecological niche, and the
Phylogenetic Species “Concept” emphasizes nucleotide
divergence between monophyletic lineages (Giraud et al.
2008a; Taylor et al. 2000). These species criteria correspond
to the different events that occurred during lineage
separation and divergence, rather than to fundamental
differences in what represents a species. To the contrary, it
has been argued that most modern biologists agree on a
common “species concept” or “species definition”, specifically segments of evolutionary lineages that have evolved
independently from one another (de Queiroz 1998).
Why are there conflicts over which species criteria we
adopt? There are three main reasons why species criteria
cannot be universal. Firstly, speciation is a temporally
extended process, and one that varies considerably in pace
for different types of organisms. Secondly, several modes of
speciation can occur, during which the phenomena used for
species recognition do not necessarily appear in the same
chronological order (Fig. 1). Thirdly, the characteristics of
certain organisms render some species criteria difficult to
apply (Giraud et al. 2008a). The most useful criteria for the
recognition of species in nature will depend on the type of
organism, its history of speciation and the degree of
achieved divergence. Searching for a single species criterion
applicable in all cases is fundamentally impossible (Giraud
et al. 2008a).
The most commonly used species criterion for fungi has
long been the Morphological Species Criterion. Recently
many cryptic species have been recognised using the
intersterility criterion, a derivative of the Biological Species
Criteria (Anderson and Ullrich 1978). Mayr (1963) defined
biological species as groups of actually or potentially
interbreeding natural populations which are reproductively
isolated from other such groups. A weakness of the intersterility criterion is that it cannot be applied to homothallic or
asexual fungi (Reynolds 1993; Taylor et al. 2000).
The Phylogenetic Species Criterion has been responsible
for a surge in the number of cryptic species recognized in
recent years (Schubert et al. 2007; Damm et al. 2009;
Wulandari et al. 2009; Aveskamp et al. 2010; Summerell et
al. 2010). The Phylogenetic Species Criterion relies on
Author's personal copy
Fungal Diversity
Fig. 1 Schematic divergence of
two species, in two hypothetical
cases of respectively allopatric
and sympatric speciation, with
the progressive appearence
of various criteria traditionnaly
used to recognize species
phylogenetic analysis of variable characters, usually DNA
sequences of selected genes or genomes. Phylogenetic
Species Criterion was originally defined as the smallest
monophyletic clade of organisms that share a derived
character state (Cracraft 1983). A weakness with this
approach is that single gene analyses, as compared to
whole genome analyses, are dependent on the genes having
an evolutionary history that reflects that of the entire
fungus, which is often not the case (Aguileta et al. 2008).
Taylor et al. (2000) further developed a Genealogical
Concordance Phylogenetic Species Recognition, as an
objective way to define the limits of sexual species. The
Genealogical Concordance Phylogenetic Species Recognition
uses the phylogenetic concordance of multiple unlinked genes
to indicate a lack of genetic exchange and thus evolutionary
independence of lineages. Species have been identified with
Genealogical Concordance Phylogenetic Species Recognition
that cannot otherwise be recognized due to the lack of
distinguishing morphological characters or incomplete intersterility. The Genealogical Concordance Phylogenetic Species
Recognition criterion has proved immensely useful in fungi,
because it is more finely discriminating than the other criteria
in many cases, or more convenient, e.g. with species that are
unable to be crossed (Reynolds 1993; Taylor et al. 2000).
Genealogical Concordance Phylogenetic Species Recognition is currently more widely used for fungi than any other
organisms, because fungi often have a simpler morphology
and it is difficult to demonstrate in vitro crosses for many
fungi (Dettman et al. 2003a; Fournier et al. 2005; Johnson et
al. 2005; Koufopanou et al. 2001; Le Gac et al. 2007a;
Pringle et al. 2005; Prihastuti et al. 2009; Glienke et al.
2011).
There are several reasons why the Genealogical Concordance Phylogenetic Species Recognition is better at
revealing cryptic species than the Biological Species
Criterion (intersterility criterion). Firstly, intersterility often
evolves slowly in allopatric divergences, in particular the
prezygotic barriers most often tested in fungi (Coyne and
Orr 1997; Le Gac and Giraud 2008). The divergence of
DNA sequences used under the Genealogical Concordance
Phylogenetic Species Recognition criterion may then occur
before intersterility has evolved and thus be more useful to
distinguish closely related sibling species. Among the
numerous complexes of sibling species recently uncovered
using the Genealogical Concordance Phylogenetic Species
Recognition criterion, many in fact appear consistent with
allopatric divergence, because the cryptic species occupy
non-overlapping areas separated by geographic barriers
(Taylor et al. 2006). This is the case for the species
complexes of the model organism Neurospora crassa
(Dettman et al., 2003a, 2003b), the yeast Saccharomyces
paradoxus, (Kuehne et al., 2007), the plant pathogen
Fusarium graminearum (O’Donnell et al., 2004), and the
mushrooms Schizophyllum commune (James et al. 1999)
and Armillaria mellea (Anderson et al. 1980; Anderson
et al. 1989).
Even in cases of sympatric speciation, certain mechanisms of reproductive isolation may allow intersterility to
evolve much later than the divergence of DNA, again
rendering the Genealogical Concordance Phylogenetic
Species Recognition more finely discriminating than the
Biological Species Criterion (Giraud et al. 2010; Giraud
et al. 2008a, b; Le Gac and Giraud 2008). For many
pathogenic fungi, sex must occur within the host after
mycelial development. This means that only individuals
able to grow within the same host can mate. Adaptation to
a new host can in these cases be sufficient to restrict gene
flow in sympatry, without requiring active assortative
mating, i.e. prezygotic intersterility (Giraud 2006; Giraud
et al. 2006). In such cases, close species may remain
interfertile for some time, making in vitro crosses a poor
criterion for recognizing species. An example is provided
Author's personal copy
Fungal Diversity
by the plant pathogenic genus Ascochyta, in which recent
multilocus phylogenetic analyses of a worldwide sample
of Ascochyta causing blights of chickpea, faba bean, lentil,
and pea revealed that each of these hosted distinct species
(Peever 2007). Experimental inoculations demonstrated
that infection was highly host specific, yet in vitro crosses
showed that the species were completely interfertile. The
host specificity of these fungi may therefore constitute the
sole reproductive barrier (Peever 2007), resulting in
sympatric speciation through the pleiotropic effect of host
adaptation (Giraud 2006; Giraud et al. 2006; Giraud et al.
2010). More generally, there exist many close species of
ascomycete pathogens that are sympatric but isolated by
weak intersterilty barriers (Le Gac and Giraud 2008).
Some other pre-mating barriers to gene flow may allow
genetic divergence in sympatry without assortative mating
and before intersterility evolves. For organisms depending
on biotic vectors, specialization of these vectors can prevent
contact between two populations even if they lie close to
one another, yielding ecological isolation, e.g. in the
Microbotryum violaceum complex of anther smut fungi,
the insect vectors are different to some extent between host
species, which leads to a reduction in mating opportunities
among strains from different plants (van Putten et al. 2007).
Another type of pre-mating barrier is allochrony, i.e.
differences in the time of reproduction may promote
premating isolation, e.g. in the powdery mildew mycoparasite Ampelomyces, the phenology of the host plant of
the parasitized fungus provides some reproductive isolation (Kiss et al. 2011). In addition, a high rate of selfing
may be efficient in limiting inter-specific matings as seen
in some plants (Fishman and Wyatt, 1999). Selfing has
been proposed as a reproductive barrier in the anther smut
fungus Microbotryum (Giraud et al. 2008b).
Evolution of species criteria in Cercospora
Members of the ascomycete genus Cercospora (Mycosphaerellaceae, Capnodiales, Dothideomycetes) occur
world-wide and cause leaf spots on most dicot and monocot
plant families, as well as some gymnosperms and ferns
(Pollack 1987; Crous and Braun 2003). These fungi rank
among some of the most destructive of plant pathogens (ToAnun et al. 2011). Cercospora was first described by
Fresenius in Fuckel (1863) with C. apii as the type species.
For many years, Cercospora was used for naming any
cercosporoid fungus, i.e. a dematiaceous hyphomycete with
filiform conidia (Pons and Sutton 1988). As a result, it
became one of the largest and most heterogeneous genera
of hyphomycetes (Crous and Braun 2003). Chupp (1954)
also adopted the broad morphological definition of
Cercospora in his monograph.
Deighton (1967; 1973; 1976; 1979) tried to clarify the
taxonomy of Cercospora by segregating Cercospora species
into smaller and morphologically more similar units. Many
Cercospora species were reclassified into Cercosporella,
Cercosporidium, Paracercospora, Pseudocercospora, Pseudocercosporella, Pseudocercosporidium, and other genera.
Braun (1995) recognized close to 50 genera in the
Cercospora-complex. Members of Cercospora sensu stricto
are currently recognized as having hyaline or subhyaline,
solitary (rarely catenate) conidia formed on pigmented
(rarely hyaline to subhyaline) conidiophores (Braun 1995,
Crous & Braun 2003, Crous et al. 2009). This morphological criterion of Cercospora has been accepted by most
taxonomists in the last 20 years (Hsieh and Goh 1990; Guo
and Hsieh 1995; Crous and Braun 1996; Braun and Melnik
1997; To-Anun et al. 2011).
While Cercospora was defined at genus level by
morphology until approximately two decades ago, species
definition in this genus was based largely on host
association. Chupp (1954) considered species of Cercospora
to be generally host specific and listed more than 1,900
species names in his monograph. By 1987 more than 3,000
names had been published in Cercospora (Pollack 1987).
Crous and Braun (2003) challenged this concept of raising
new names for morphologically indistinguishable Cercospora collections based on new host genera, when they
assigned 281 morphologically indistinguishable species to
synonymy under C. apii senso lato and recognized 659
Cercospora species. The results of some earlier inoculation
experiments (Vestal 1933; Johnson and Valleau 1949; Fajola
1978) and molecular sequence data (Crous et al. 2000;
Goodwin et al. 2001) had also raised doubt about narrow
host specificity in the Cercospora complex. Using host
species as a basis for recognizing species of Cercospora also
failed the pogo stick hypothesis of Crous and Groenewald
(2005) formulated by observing some species of Mycosphaerella, which proposed that host specific fungal plant
pathogens often colonised non-host tissue or other substrates,
forming fertile fruiting bodies.
In Cercospora, the application of the criterion of
intersterility was particularly limited because only a few
species in this genus have a known sexual stage (Chupp
1954; Corlett 1991). Groenewald et al. (2006b) detected the
two mating type genes in approximately even proportions
in C. beticola, C. zeae-maydis and C. zeina populations,
and speculated that a sexual cycle may occur regularly in
these species. However, the actual sexual stage was not
observed.
The use of DNA sequence data and the adoption of
Phylogenetic Species Criterion have started to clarify some
of the confusion in Cercospora taxonomy. The Cercospora
complex has been shown to form a well-defined clade in
the Mycosphaerellaceae (Crous et al. 2009) supporting
Author's personal copy
Fungal Diversity
earlier molecular analyses (Stewart et al. 1999; Crous et al.
2001; Goodwin et al. 2001). Furthermore, only species in
this group produce cercosporin, a phytotoxin that enhances
virulence (Goodwin et al. 2001).
Two examples of the application of Genealogical
Concordance Phylogenetic Species Recognition in the
Cercospora complex follow. Firstly, two phylogenetically
supported species, C. apii and C beticola, were identified
among the 281 synonyms placed in C. apii sensu lato by
Crous and Braun (2003), even though they were morphologically similar and capable of infecting the same hosts in
inoculation experiments (Groenewald et al. 2005; Groenewald
et al. 2006a, b). Secondly, C. piaropi and C. rodmanii, which
both infect the aquatic plant water hyacinth, were considered
to differ from each other by conidial morphology and
virulence (Tharp 1917). A multilocus DNA phylogeny did
not support the separation of these two species (Tessmann
et al. 2001) and a more detailed study using a collection of
isolates showed that morphological characters also did not
reliably separate them. Consequently C. rodmanii was
reduced to synonymy with C. piaropi.
The adoption of Genealogical Concordance Phylogenetic
Species Recognition has profound implications for disease
control and quarantine. For example, considering the 281
synonyms in C. apii sensu lato as individual species may
lead to unnecessary biosecurity measures and trade restrictions, yet considering them as a single species may miss the
opportunity to contain some diseases, e.g. those caused by
C. beticola.
Evolution of species criteria in Colletotrichum
The ascomycete genus Colletotrichum (Glomerellaceae,
Sordariomycetes) contains many well-known plant pathogens that cause anthracnose and a range of diseases
worldwide on economic crops and ornamental plants
(Crouch & Beirn 2009, Crouch et al. 2009, Damm et al.
2009, Hyde et al. 2009a, b). They are amongst the most
important plant pathogens as they cause latent or quiescent
infections at the pre-harvest and post-harvest stages (Sutton
1992). The first report of Colletotrichum was by Tode
(1790) in the genus Vermicularia, while the genus name
Colletotrichum was introduced by Corda (1831). Colletotrichum encompasses species with endophytic, epiphytic,
saprobic and phytopathogenic lifestyles (Kumar and Hyde
2004; Photita et al. 2001; 2003; 2005; Liu et al. 2007;
Prihastuti et al. 2009), as well as human pathogens (Cano
et al. 2004).
The taxonomy of many groups of plant pathogenic
fungi, including Colletotrichum, has been based on host
association (von Arx 1957; Sutton 1980). If a pathogenic
fungus was found on a host from which no records of that
pathogen were known, it was described as a new species
(von Arx 1957). This species criterion has failed to reliably
reflect evolutionary independence of the lineages of
Colletotrichum and many other groups of fungi, as many
pathogenic species have a facultative saprobic ability,
with the exception perhaps of the obligate plant
pathogenic fungi, e.g. rusts, smuts, downy and powdery
mildews (Cummins and Hiratsuka 2003; Vánky 2002,
Yamaoka 2002).
The work done by mycologists during the 19th and early
th
20 century resulted in numerous fungal names with
specific epithets based on the scientific names of the host
plant. These names cannot be ignored in modern systematic
studies and pose a huge challenge for modern researchers
who will need to determine whether these names represent
distinct species or synonyms of other names (Hyde et al.
2009a; Cai et al. 2009). Sutton (1992) suggested that “In
every large genus like Colletotrichum there needs to be a
degree of systematics catharsis resulting in a severe
reduction in the number of accepted species before any
real advances in identification can be made”. Such an
approach was taken by von Arx (1957) who reduced the
number of Colletotrichum species from several hundred to
11 based on morphological characters, with many taxa
treated as synonyms of C. gloeosporioides (ca. 600
synonyms) or C. dematium (86 synonyms). Several
additional species have been accepted since von Arx
(1957), based on Morphological Species Criterion (Sutton,
1980; 1992). Sutton (1980) also built a key that has
provided a practical identification tool and standard
reference for identifying species of Colletotrichum for
many years. In the last 30 years, and until recently, the
number of newly described species of Colletotrichum has
substantially slowed down and species were defined by
their distinguishable morphological characters.
Although the application of Morphological Species
Criterion has resulted in an important and revolutionary
progress in Colletotrichum systematics, some flaws persisted. The species criteria of von Arx (1957) were very
broad, and most of his taxonomic treatments were based on
literature descriptions, that lead to considerable inaccuracy
and generality. For example, the treatment of synonymizing
ca. 600 names to C. gloeosporioides has been questionable,
as it contains a lot of physiologically and genetically distant
lineages. Recent application of Genealogical Concordance
Phylogenetic Species Recognition in Colletotrichum has
revealed that many distinct species exist in the C.
gloeosporioides complex. Some of these have been
formally described, such as C. asianum, C. siamense, C.
fructicola, and C. cordylinicola (Prihastuti et al. 2009;
Phoulivong et al. 2010), while others have been typified,
including C. gloeosporioides sensu stricto, C. horii and C.
musae (Cannon et al. 2008; Weir and Johnston 2010; Su et
Author's personal copy
Fungal Diversity
al. 2011). In the C. acutatum complex, 4 distinct lineages
were recognized and three of them have been assigned
species names (Shivas and Tan 2009).
The application of Genealogical Concordance Phylogenetic Species Recognition in Colletotrichum has had an
important impact on species discovery, plant breeding,
disease control and biosecurity protocols, all of which
depend on accurate pathogen identification. Identification
of a specimen as C. gloeosporioides sensu lato or C.
dematium sensu lato has little practical value. The many
species hidden in the C. gloeosporioides complex will
certainly have different biosecurity significance. For example, the C. gloeosporioides complex on coffee berries has
been well characterized and several distinct genetic and
phenotypic species have been established (Prihastuti et al.
2009; Waller et al. 1993). Among these, C. kahawae is a
strongly aggressive pathogen specific to coffee in Africa
(Waller et al. 1993) and the application of strict quarantine
protocols is justified to prevent its spread to coffee growing
regions on other continents where it is not present. On the
other hand, C. asianum, C. fructicola and C. siamense are
opportunistic pathogens of coffee berries (Prihastuti
et al. 2009) and appear to have a wide host range and
little biosecurity significance. Phoulivong et al. (2010)
indicated that morphologically similar isolates from chilli,
mango, papaya, rose apple and jujube comprised more
than one distinct species. Very little is known about
whether these records, and many other worldwide records
of C. gloeosporioides sensu lato, represent saprobes,
weak or opportunistic pathogens or severe pathogens (Hyde
et al. 2010).
Evolution of species criteria in Fusarium
The ascomycete genus Fusarium (Nectriaceae, Hypocreales, Sordariomycetes) represents a large group of
ascomycetes ubiquitously distributed in soil and in association with plants. Although most members are saprobic,
Fusarium is better known for its toxigenic and plant
pathogenic species, which significantly impact agriculture
(Marasas et al. 1984). Fusarium produces secondary
metabolites, such as fumonisins, trichothecenes and zearalenone, which are toxins that threaten food safety and
human health. Recently, Fusarium species also have
emerged as opportunistic human pathogens causing ocular
or systemic infections (Dignani and Anaissie 2004; Zhang
et al. 2006).
Fusarium was first described by Link (1809) as species
with fusiform spores borne on a stroma. This asexual genus
was validated by Fries (1821) in terms of the IBCN. With
increased knowledge of fungal morphological identification, the presence of fusoid macroconidia with a basal foot
cell became accepted as the key character of the genus
instead of the presence of a stroma (Booth 1971). The
teleomorphs of Fusarium, when known, belong to either
Haematonectria or Gibberella.
The history of the taxonomy of Fusarium has been
unstable. In the first century after the genus was established, over 1,000 species were defined on the basis of
superficial observations, often based on host association
(Toussoun and Nelson 1975). Wollenweber and Reinking
(1935) in their monograph Die Fusarien reduced the genus
to 142 species, varieties and forms in 16 sections. Based
solely on morphological characters, Snyder and Hansen
(1941; 1945) further reduced Fusarium to nine species.
Successor taxonomists conducted revisions based on either
the Wollenweber and Reinking system, e.g. Booth (1971),
or the Snyder and Hansen system, e.g. Nelson et al.
(1983). This resulted in many taxonomic incongruences.
Currently, there are over 100 valid Fusarium species
names according to the Dictionary of The Fungi (Kirk et
al. 2008). The frequent conflicts and instability in
Fusarium systematics have resulted from the absence of
clear morphological characters to separate species as well
as the existence of phenotypic variation in cultures
(Geiser et al. 2004).
The root of the problem in Fusarium systematics lies in
the use of the Morphological Species Criterion as adopted
in traditional fungal taxonomy. As with many other fungi,
Fusarium taxonomy was mostly based on the Morphological Species Criterion until two decades ago, when
Morphological Species Criterion and Phylogenetic Species
Criterion were applied (Summerell et al. 2010). Intersterility
barriers have been detected in some Fusarium groups based
on crossing experiments, e.g. the genetically distinct mating
populations in the F. solani species complex (Matuo and
Snyder 1973). Clearly, the Biological Species Criterion
cannot be applied to the majority of Fusarium lineages,
which are homothallic or apparently asexual (Taylor et al.
1999). Nonetheless, the BSC enabled reliable identification
for some sexual species of Fusarium, especially for those in
the Gibberella fujikuroi and F. solani species complexes
(Leslie and Summerell 2006; Kvas et al. 2009).
For species of Fusarium for which sexual reproduction
is difficult to induce in vitro, the Phylogenetic Species
Criterion (including the Genealogical Concordance Phylogenetic Species Recognition) has proven to be highly
informative. Several studies have shown that Phylogenetic
Species Criterion and Biological Species Criterion are
congruent, although the Biological Species Criterion
appears more finely discriminating than the Morphological
Species Criterion, particularly in Fusarium (O’Donnell
2000; O’Donnell et al. 1998; Zhang et al. 2006). Distinct
lineages recognized by the Phylogenetic Species Criterion
can be used as a guide for finding diagnostic morphological
Author's personal copy
Fungal Diversity
or ecological differences among fungal species, which
otherwise did not appear obvious. For example, phylogenetic analyses have revealed the existence of cryptic species
in F. graminearum, occurring in different parts of the world,
resulting in the description of 13 new species (O’Donnell
et al. 2000; Starkey et al. 2007; Kvas et al. 2009). The
most frequently used gene for species recognition and
phylogenetic analysis in Fusarium is the translation
elongation factor 1 α gene (EF-1α). Other useful loci
include the internal transcribed spacer (ITS) region of the
rRNA gene repeat and β-tubulin gene (Geiser et al. 2004;
Summerell et al. 2010; Park et al. 2011).
An example of the benefits of modern Phylogenetic
Species Criterion-based systematics in Fusarium can be
seen in soybean sudden death syndrome (Rupe 1989), a
disease occurring throughout the world. Previously, the
causal agent was referred to as F. solani f. sp. glycines or
Fusarium solani sensu lato (Gao et al. 2004). Multiple gene
sequence analyses revealed a diversity of cryptic taxa,
leading to the recognition of four different species of
Fusarium as causes of this disease. Those isolates known to
cause soybean sudden death syndrome in North America
have been segregated as Fusarium virgulifore, while three
related but different species of Fusarium are associated
with this disease in South America (Aoki et al. 2005).
Studies based on experimental crosses further confirmed
the distinction of these phylogenetic species (Covert et al.
2007). The intersterility and allopatry of these cryptic
species were discovered only after their existence was
revealed using phylogenetic analyses. The geographical and
genetic information associated with these newly recognized
species will enable the development of precise control
strategies and the formulation of appropriate biosecurity
policies.
Evolution of species criteria in rust and smut fungi
The rust and smut fungi belong to the subphyla Pucciniomycotina and Ustilaginomycotina respectively, in the
phylum Basidiomycota (Hibbett et al. 2007). At the species
level there are almost 7,000 species of rust fungi in 163
genera (Kirk et al. 2001) and about 1,675 smut fungi in 95
genera (Vánky, pers. comm.), which collectively account
for about 10% of all known fungi. The rust and smut fungi
both contain many economically and agriculturally important species and their profound influence on human history
is well documented (Carefoot and Sprott 1967).
The traditional definition of the rust and smut life form
was the presence of teliospores that germinate to produce
basidia and these fungi were classified together in the
Teliomycetes (Jülich, 1981). However ultrastructural and
molecular studies have shown that the rust and smut fungi
are only distantly related with separate monophyletic
origins (Bauer et al. 1997; Begerow et al. 1997). Furthermore, the rust fungi have a pleomorphic life cycle with up
to five spore states (spermatia, aeciospores, urediniospores,
teliospores and basidiospores) which differentiates them
from the smut fungi that mostly produce two types of
spores (teliospores and basidiospores).
Rust and smut fungi are essentially obligate plant
pathogens, although the smut fungi may have a short stage
of saprobic growth on non-living substrates, and about 30
rusts have been cultivated on artificial media (Yamaoka
2002). The classification of rust and smut species has been
traditionally based on both Morphological Species
Criterion, with emphasis on sori and spore stages, as well
as on Ecological Species Criterion, with emphasis on
pathogenicity on specific hosts (Vánky 2002, Cummins
and Hiratsuka 2003). Consequently these groups have been
relatively stable, and easily classified and identified using
morphology and host associations for over 200 years. The
recent application of molecular phylogenetic analyses to the
rust and smut fungi has mostly supported previous
classifications at the level of genus (Maier et al. 2003;
Bauer et al. 2006; Aime et al. 2006; Begerow et al. 2006).
In contrast, higher taxonomic ranks have been shuffled in
part. While the Pucciniales (rust fungi) are monophyletic,
the smut fungi in the traditional sense correspond to at least
two phylogenetically distant clades. Those smut fungi in
the Ustilaginomycotina cluster together with other plant
pathogens of the Exobasidiales, Microstromatales as well
as human pathogens of Malassezia (Begerow et al. 2000;
Begerow et al. 2006). The smut fungi in the Microbotryales
cluster together with other plant pathogens and mycoparasites in the Microbotryomycetes in the Pucciniommycotina
(Bauer et al. 2006). Ultrastructural characters and cell wall
compounds have subsequently supported these modern
classifications (Bauer et al. 1997; 2006).
Early species descriptions of rust and smut fungi were
usually based on morphology and separation of the two
groups was not always clear. The earliest descriptions of
rust fungi date back to Micheli (1729) and Persoon
(1801), and smut fungi to Tillet (1755) and Prévost
(1807). They were followed by detailed studies on their
life cycle including teliospore formation and germination
(de Bary 1853; Tulasne and Tulasne 1847). Interestingly,
most of these early treatments included quite comprehensive studies comprising morphological, physiological and
systematic aspects. Most of the early species lists included
information about host species and the lists were even
organized according to host (Fischer von Waldheim 1869).
It is commonly accepted that rust and smut species are
each restricted to a family or even a narrower plant taxon
and there are many examples describing the rust or smut
species of a given plant family (Vánky 2006; Vánky and
Author's personal copy
Fungal Diversity
Lutz 2007) or a given host genus (Bauer et al. 1999;
Vánky 2003). Several genera of heteroecious rust fungi on
the other hand need two different hosts to complete their
life cycle, which may be from completely different plant
families.
Considering that over 8,000 species of rust and smut
fungi are known, there has been little application of DNA
sequence data to identify rust and smut fungi in terms of
the Genealogical Concordance Phylogenetic Species
Recognition. This is certainly because the morphological
characteristics of rust and smut fungi have appeared
stable and reliable, allowing confident identification of
species that are supported, in most cases, by narrow host
ranges. However complexes composed of closely related
reproductively isolated cryptic species are still common
in the rust fungi (Gaümann 1959) and also some groups
of smut fungi. Consequently, molecular studies have been
used to resolve phylogenetic relationships between morphologically similar taxa of rust and smut fungi. For
example, the host-specificity, morphology and DNA
sequence data of two microcyclic rusts species Puccinia
melampodii and P. xanthii (Seier et al. 2009) lead to the
establishment of a new morphospecies, P. xanthii var.
parthenii-hysterophorae, to accommodate records of P.
melampodii associated with the host Parthenium hysterophus. Another example is Karnal bunt of wheat, caused
by the smut fungus Tilletia indica, an important pathogen
absent from Australia. ITS sequence data have been used
to separate it from morphologically similar species that
may also occur as contaminants in consignments of wheat
seed (Levy et al. 2001, Pascoe et al. 2005). Overall, the
application of Phylogenetic Species Criterion supported
Morphological Species Criterion in many of the genera of
smut fungi (Hendrichs et al. 2005; Begerow et al. 2000;
Castlebury et al. 2005) and only recently the large
Ustilago / Sporisorium / Macalpinomyces species complex
has been substantially resolved using a phylogeny derived
from molecular data that reflected morphological synapomorphies and host associations (Stoll et al. 2003,
2005; McTaggart 2010).
As one of the best studied models, Microbotryum
has provided a good example of the utility of the
Phylogenetic Species Criterion. A narrow species criterion based on host use (Zillig 1921; Liro 1924; Baker
1947) long contrasted with a broad Morphological Species
Criterion species criterion, the latter defining a single
species, Microbotryum violaceum, considered as the pathogen responsible for almost all anther smuts of Caryophyllaceae (Perlin 1996). Population genetics studies
(Bucheli et al. 2000) and the use of the Genealogical
Concordance Phylogenetic Species Recognition (Le Gac
et al. 2007a) revealed an absence of gene flow and an ancient
differentiation between populations of Microbotryum found
on different host plants, which were confirmed by ITS
phylogenies as distinct species on different hosts (Lutz et al.
2005, 2008). As in other fungal species, the Biological
Species Criterion was less discriminating (Le Gac et al.
2007b), with little evidence of assortative mating in the form
of conjugation initiation in vitro, although hybrid inviability
and sterility was observed between the cryptic species (Le
Gac et al. 2007b; de Vienne et al. 2009a). Cross-inoculation
studies also appeared less discriminating in vitro than host
specificity seen in the field (de Vienne et al. 2009b; Gladieux
et al. 2011). The studies highlight the value of Genealogical
Concordance Phylogenetic Species Recognition to validate
Phylogenetic Species Criterion and Morphological Species
Criterion that have practical application in the field of
plant pathology.
Conclusive remarks
Molecular DNA sequence data have recently been extensively employed in studying the systematics of plant
pathogenic fungi. The advantage of using molecular data
is that it provides a greater number of heritable characters
that allow for convenient information sharing between
laboratories. Morphological characters, however, are prone
to change under different environmental conditions. In
addition, well-developed bioinformatics tools make analysis of data more objective and less controversial when
examined by different scientists. The Biological Species
Criterion has proved useful in some fungal groups but
overall appears less convenient and less discriminating,
although congruent, with the Genealogical Concordance
Phylogenetic Species Recognition.
The Genealogical Concordance Phylogenetic Species
Recognition has been widely accepted in fungal systematics.
Multi-gene sequencing and phylogenetic analysis have
become a routine procedure in identifying new fungal
species, especially for those that lack distinctive morphological characters. Consequently a rapidly increasing number of cryptic species are being discovered amongst plant
pathogenic fungi using the Genealogical Concordance
Phylogenetic Species Recognition and it is critical to
determine their host range, the severity of diseases they
cause and their biosecurity significance. With rapidly
expanding global trade it has become imperative that we
develop effective and reliable protocols to detect these
previously unrecognized pathogens.
Based on Genealogical Concordance Phylogenetic Species Recognition, previously applied phenotypic characters
that were used to define taxa need re-evaluation. Although
the recent molecular advances in multi-locus phylogeny has
been able to recognize stable and well-separated phylogenetic species, there is still a long way to go before we can
Author's personal copy
Fungal Diversity
finally establish a natural classification system and species
recognition criteria for most fungi using DNA sequence
data. A major problem is that only a very small number of
species have been deposited in public culture collections
and only a fraction of these have had some DNA fragment
sequenced. The number of ex-type strains that have been
sequenced is even lower. Another potential problem is that
most of the well-known plant pathogenic fungi were
described based on the Morphological Species Criterion
and ex-type cultures are not available. It is inevitable that
Phylogenetic Species Criterion and Morphological Species
Criterion will still be used together to define species for
many years.
Once robust species delimitation and classification is
established, the development of high-throughput identification tools like barcoding should be a major improvement
for assignment of particular strains to species (Begerow
et al. 2010). Together with well-curated databases and
regularly updated regional species lists rapid molecular
identification is able to efficiently support not only quarantine
regulations but the monitoring of new emerging diseases
as well.
Acknowledgements Dr Alistair McTaggart (Louisiana State University)
is thanked for his helpful comments. Ms. Liu Fang is thanked for
technical assistance. Lei Cai acknowledges grants CAS KSCX2-YW-Z1026 and NSFC 31070020. Tatiana Giraud acknowledges the grants
ANR 06-BLAN-0201 and ANR 07-BDIV-003. Parts of this chapter are
derivatives of articles previously published (Giraud et al., 2008a;
Gladieux et al., 2010). Roger Shivas acknowledges Chinese Academy of
Sciences for the Visiting Professorship for Senior International Scientists
(Grant No. 2010T2S12). Dominik Begerow acknowledges the grants BE
2201/4-2 and BE 2201/8-1 from DFG.
References
Aguileta G, Marthey S, Chiapello H, Lebrun M-H, Rodolphe F,
Fournier E, Gendrault-Jacquemard A, Giraud T (2008) Assessing
the performance of single-copy genes for recovering robust
phylogenies. Syst Biol 57:613–627
Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH,
Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio
JP, Bauer R, Weiß M, Oberwinkler F, Hibbett DS (2006) An
overview of the higher-level classification of Pucciniomycotina
based on combined analyses of nuclear large and small subunit
rDNA sequences. Mycologia 98:896–905
Anderson JB, Korhonen K, Ullrich RC (1980) Relationships between
European and North American biological species of Armillaria
mellea. Exp Mycol 4:87–95
Anderson JB, Bailey SS, Pukkia PJ (1989) Variation in ribosomal
DNA among biological species of Armillaria, a genus of rootinfecting fungi. Evolution 43:1652–1662
Anderson JB, Ullrich RC (1978) Biological species of Armillaria
mellea in North America. Mycologia 71:402–414
Aoki T, O’donnell K, Scandiani M (2005) Sudden death syndrome of
soybean in South America is caused by four species of Fusarium:
Fusarium brasiliense sp. nov., F. cuneirostrum sp. nov., F.
tucumaniae, and F. virguliforme. Mycoscience 46:162–183
Aveskamp MM, Gruyter J de, Woudenberg JHC, Verkley GJM, Crous
PW (2010) Highlights of the Didymellaceae: a polyphasic
approach to characterize Phoma and related pleosporalean
genera. Stud Mycol 65:1–60
Baker HG (1947) Infection of species of Melandrium by Ustilao
violacea (Pers.) Fuckel and the transmission of the resultant
disease. Ann Bot 11:333–348
Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers ans
ststematics in smut fungi and allied taxa. Can J Bot 75:1273–
1314
Bauer R, Vánky K, Begerow D, Oberwinkler F (1999) Ustilaginomycetes
on Selaginella. Mycologia 91:475–484
Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The
simple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66
Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on
the nuclear large subunit ribosomal DNA of smut fungi and
related taxa. Can J Bot 75:2045–2056
Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placement of
ustilaginomycetous anamorphs as deduced from nuclear LSU
rDNA sequences. Mycol Res 104:53–60
Begerow D, Lutz M, Oberwinkler F (2002) Implications of molecular
characters for the phylogeny of the genus Entyloma. Mycol Res
106:1392–1399
Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of
Ustilaginomycotina based on multiple gene analyses and
morphological data. Mycologia 98:906–916
Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current
state and perspectives of fungal DNA barcoding and rapid
identification procedures. Appl Microbiol Biotechnol 87:99–108
Booth C (1971) The Genus Fusarium. Commonwealth Mycological
Institute, Kew, Surrey, England: 1-237.
Braun U (1995) A monograph of Cercosporella, Ramularia and allied
genera (Phytopathogenic Hyphomycetes). Vol. 1. IHW-Verlag,
Eching bei, München: 1-333
Braun U, Melnik VA (1997) Cercosporoid fungi from Russia and
adjacent countries. Russian Academy of Sciences, Proceedings of
the Komarov Botanical Institute 20:1–112
Bucheli E, Gautschi B, Shykoff JA (2000) Host-specific differentiation in the anther smut fungus Microbotryum violaceum as
revealed by micosatellites. J Evol Biol 13:188–198
Cai L, Hyde KD, Taylor PWJ, Weir B, Waller J, Abang MM, Zhang
JZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG,
McKenzie EHC, Johnston PR (2009) A polyphasic approach for
studying Colletotrichum. Fungal Divers 39:183–204
Cannon PF, Buddie AG, Bridge PD (2008) The typification of
Colletotrichum gloeosporioides. Mycotaxon 104:189–204
Cano J, Guarro J, Gene J (2004) Molecular and morphological
identification of Colletotrichum species of clinical interest. J Clin
Microbiol 42:2450–2454
Carefoot GL, Sprott ER (1967) Famine on the wind. Rand McNally,
Chicago
Castlebury LA, Carris LM, Vánky K (2005) Phylogenetic analysis of
Tilletia and allied genera in order Tilletiales (Tstilaginomycetes;
Exobasidiomycetidae) based on large subunit nuclear rDNA
sequences. Mycologia 97:888–900
Chakraborty S, Newton AC (2011) Climate change, plant diseases and
food security: an overview. Plant Pathol 60:2–14
Chupp C (1954) A monograph of the fungus genus Cercospo Ithaca,
New York, author
Corda ACI (1831) Die Pilze Deutschlands (ed. J. Sturm). Deutschlands
Flora, 3. Abtheilung 3: 1-144
Corlett M (1991) An annotated list of the published names in
Mycosphaerella and Sphaerella. Mycol Mem 18:1–328
Covert SF, Aoki T, O’Donnell K, Starkey D, Holliday A, Geiser DM,
Cheung F, Town C, Strom A, Juba J, Scandiani M, Yang XB
(2007) Sexual reproduction in the soybean sudden death
Author's personal copy
Fungal Diversity
syndrome pathogen Fusarium tucumaniae. Fungal Genet Biol
44:799–807
Coyne J, Orr HA (1997) Patterns of speciation in Drosophila revisited.
Evolution 51:295–303
Cracraft J (1983) Species concepts and speciation analysis. In
Current Ornithology, Vol. 1, pp. 159–187. Plenum Press, New
York
Crouch JA, Beirn LA (2009) Anthracnose of cereals and grasses.
Fungal Divers 39:19–44
Crouch JA, Clarke BB, White JF, Hillman BI (2009) Systematic
analysis of falcate-spored graminicolous Colletotrichum and a
description of six new species from warm-season grasses.
Mycologia 101:717–732
Crous PW, Braun U (1996) Cercosporoid fungi from South Africa.
Mycotaxon 57:233–321
Crous PW, Braun U (2003) Mycosphaerella and its anamorphs: 1.
Names published in Cercospora and Passalora. CBS Biodiversity
Series 1: 1-571
Crous PW, Groenewald JZ (2005) Hosts, species and genotypes:
opinions versus data. Australas Plant Pathol 34:463–470
Crous PW, Aptroot A, Kang JC, Braun U, Wingfield MJ (2000) The
genus Mycosphaerella and its anamorphs. Stud Mycol 45:107–
121
Crous PW, Kang JC, Braun U (2001) A phylogenetic redefinition of
anamorph genera in Mycosphaerella based on ITS rDNA
sequence and morphology. Mycologia 93(6):1081–1101
Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Hunter GC,
Burgess TI, Andjic V, Barber PA, Groenewald JZ (2009)
Unravelling Mycosphaerella: do you believe in genera? Persoonia
23:99–118
Cummins GB, Hiratsuka Y (2003) Illustrated Genera of Rust Fungi.
3rd ed. APS Press. The American Phythopathological Society. St.
Paul, Minnesota
Damm U, Woudenberg JHC, Cannon PF, Crous PW (2009)
Colletotrichum species with curved conidia from herbaceous
hosts. Fungal Divers 39:45–87
de Bary HA (1853) Untersuchungen über die Brandpilze und die
durch sie verursachten Krankheiten der Pflanzen mit Rücksicht
auf das Getreide und andere Nutzpflanzen. Habilitationsschrift.
de Queiroz K (2007) Species concepts and species delimitation. Syst
Biol 56(6):879–886
de Queiroz K (1998) The general lineage concept of species, species
criteria, and the process of speciation: a conceptual unification
and terminological recommendations. In: Howard DJ, Berlocher
SH (eds) Endless forms: species and speciation. Oxford Univ.
Press, New York, pp 57–75
de Vienne DM, Refrégier G, Hood ME, Guigue A, Devier B, Vercken
E, Smadja C, Deseille A, Giraud T (2009a) Hybrid sterility and
inviability in the parasitic fungal species complex Microbotryum.
J Evol Biol 22:683–698
de Vienne D, Hood M, Giraud T (2009b) Phylogenetic determinants
of potential host shifts in fungal pathogens. J Evol Biol 22:2532–
2541
Deighton FC (1967) Studies on Cercospora and allied genera. II.
Passalora, Cercosporidium, and some species of Fusicladium on
Euphorbia. Mycological Papers 112:1–80
Deighton FC (1973) Studies on Cercospora and allied genera. IV.
Cercosporella Sacc., Pseudocercosporella gen. nov. and
Pseudocercosporidium gen. nov. Mycological Papers 133:1–
62
Deighton FC (1976) Studies on Cercospora and allied genera. VI.
Pseudocercospora Speg., Pantospora Cif. and Cercoseptoria.
Mycological Papers 140:1–168
Deighton FC (1979) Studies on Cercospora and allied genera.
VII. New species and redispositions. Mycological Papers
144:1–56
Dettman JR, Jacobson DJ, Taylor JW (2003a) A multilocus genealogical approach to phylogenetic species recognition in the model
eukaryote Neurospora. Evolution 57:2703–2720
Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003b)
Reproductive isolation and phylogenetic divergence in Neurospora:
comparing methods of species recognition in a model eukaryote.
Evolution 57:2721–2741
Dignani MC, Anaissie E (2004) Human fusariosis. Clin Microbiol
Infect 10:67–75
Fajola AO (1978) Cultural studies in Cercospora taxonomy: I.
Interrelationships between some species from Nigeria. Nova
Hedwigia 29:912–921
Fischer von Waldheim A (1869) Beiträge zur biologie und
Entwicklungsgeschichte der Ustilagineen. Jahrbuch für
wissenschaftliche Botanik 7:61–144
Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in
Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733
Fournier E, Giraud T, Albertini C, Brygoo Y (2005) Partition of
the Botrytis cinerea complex in France using multiple gene
genealogies. Mycologia 97:1251–1267
Fries E (1821) Systema mycologicum 1. Gryphiswaldae, Mauritius
Fuckel KWGL (1863) Fungi rhenani exiccati, Fasc. I–IV. Hedwigia
2:132–136
Gao X, Jackson TA, Lambert KN, Li S, Hartman GL, Niblack TL
(2004) Detection and quantification of Fusarium solani f. sp
glycines in soybean roots with real-time quantitative polymerase
chain reaction. Plant Disease 88:1372–1380
Gaümann E (1959) Die Rostpilze Mitteleuropas. Bücheler, Bern
Geiser DM, Jimenez-Gasco MD, Kang SC, Makalowska I, Veeraraghavan
N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004)
FUSARIUM-ID v. 1.0: A DNA sequence database for identifying
Fusarium. Eur J Plant Pathol 110:473–479
Giraud T (2006) Selection against migrant pathogens: the immigrant
inviability barrier in pathogens. Heredity 97:316–318
Giraud T, Villaréal LMMA, Austerlitz F, Gac ML, Lavigne C (2006)
Importance of the life cycle in host race formation and sympatric
speciation in parasites. Phytopathology 96:280–287
Giraud T, Refrégier G, de Vienne DM, Le Gac M, Hood ME (2008a)
Speciation in fungi. Fungal Genet Biol 45:791–802
Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME
(2008b) Mating system of the anther smut fungus, Microbotryum
violaceum. Eukaryotic Cell 7:765–775
Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence of
fungal plant diseases with ecological speciation. Trends Ecol
Evol 25:387–395
Gladieux P, Byrnes E, Fisher M, Aguileta G, Heitman J, GiraudT.
(2010) Epidemiology and evolution of fungal pathogens, in
plants and animals in T. M., ed. Genetics and Evolution of
Infectious Diseases. Elsevier
Gladieux P, Vercken E, Fontaine MC, Hood ME, Jonot O, Couloux A,
Giraud T (2011) Maintenance of fungal pathogen species that are
specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28:459–471
Glienke C, Pereira OL, Stringari D, Fabris J, Kava-Cordeiro V, GalliTerasawa L, Cunnington J, Shivas RG, Groenewald JZ, Crous
PW (2011) Endophytic and pathogenic Phyllosticta species, with
reference to those associated with Citrus Black Spot. Persoonia
26:47–56
Goodwin SB, Dunkle LD, Dunkle LD, Zismann VL (2001)
Phylogenetic analysis of Cercospora and Mycosphaerella based
on the internal transcribed spacer region of ribosomal DNA.
Phytopathology 91(7):648–658
Groenewald M, Groenewald JZ, Crous PW (2005) Distinct species
exist within the Cercospora apii morphotype. Phytopathology 95
(8):951–959
Author's personal copy
Fungal Diversity
Groenewald M, Groenewald JZ, Braun U, Crous PW (2006a) Host
range of Cercospora apii and C. beticola and description of C.
apiicola, a novel species from celery. Mycologia 98(2):275–285
Groenewald M, Groenewald JZ, Harrington TC, Abeln ECA, Crous
PW (2006b) Mating type gene analysis in apparently asexual
Cercospora species is suggestive of cryptic sex. Fungal Genet
Biol 43(12):813–825
Guo YL, Hsieh WH (1995) The genus Pseudocercospora in China.
Mycosystema Monographicum Series 2:1–388
Hawksworth DL (1991) The fungal dimension of biodiversity:
magnitude, significance, and conservation. Mycol Res 95:641–
655
Hendrichs M, Begerow D, Bauer R, Oberwinkler F (2005) The genus
Anthracoidea (Basidiomycota, Ustilaginales): A molecular
phylogenetic approach using LSU rDNA sequences. Mycol Res
109:31–40
Hey J (2006) On the failure of modern species concepts. Trends Ecol
Evol 21:447–450
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF,
Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R,
Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell
MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys
R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL,
Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM,
Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka
K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP,
Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller
A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F,
Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio
JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA,
Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao
Y-J, Zhang N (2007) A higher-level phylogenetic classification of
the Fungi. Mycol Res 111:509–547
Hsieh WH, Goh TK (1990) Cercospora species and similar fungi from
Taiwan. Maw Chang Book Company, Taiwan
Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H
(2009a) Colletotrichum: a catalogue of confusion. Fungal Divers
39:1–17
Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW, Damm U,
Goodwin PH, Chen H, Johnston PR, Jones EBG, Liu ZY,
McKenzie EHC, Moriwaki J, Noireung P, Pennycook SR,
Pfenning LH, Prihastuti H, Sato T, Shivas RG, Taylor PWJ, Tan
YP, Weir BS, Yang YL, Zhang JZ (2009b) Colletotrichum names in current use. Fungal Divers 39:147–182
Hyde KD, Chomnunti P, Crous PW, Groenewald JZ, Damm U, KoKo
TW, Shivas RG, Summerell BA, Tan YP (2010) A case for reinventory of Australia’s plant pathogens. Persoonia 25:50–60
James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence for
limited intercontinental gene flow in the cosmopolitan mushroom
Schizophyllum commune. Evolution 53:1665–1677
Johnson EM, Valleau WD (1949) Synonomy in some common species
of Cercospora. Phytopathology 39:763–770
Johnson JA, Harrington TC, Engelbrecht CJB (2005) Phylogeny and
taxonomy of the North American clade of the Ceratocystis
fimbriata complex. Mycologia 97:1067–1092
Jülich W (1981) Higher taxa of basidiomycetes. Bibliotheca
Mycologia 85:1–485
Kirk AM, Cannon PF, David JC, Stalpers JA (2001) Dictionary of the
Fungi, 9th edn. CABI Publishing, UK
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of
the Fungi. (10th ed.). CAB International
Kiss L, Pintye A, Kovács GM, Jankovics T, Fongtaine MC, Harvey N,
Xu X, Nicot PC, Bardin M, Shykoff JA, Giraud T (2011)
Temporal isolation explains host-related genetic differentiation in
a group of widespread mycoparasitic fungi. Mol Ecol 20:1492–
1507
Kohn LM (2005) Mechanisms of fungal speciation. Annu Rev
Phytopathol 43:279–308
Koufopanou V, Burt A, Szaro T, Taylor JW (2001) Gene genealogies,
cryptic species, and molecular evolution in the human pathogen
Coccidioides immitis and relatives (Ascomycota, Onygenales).
Mol Biol Evol 18:1246–1258
Kuehne HA, Murphy HA, Francis CA, Sniegowski PD (2007)
Allopatric divergence, secondary contact and genetic isolation
in wild yeast populations. Curr Biol 17:407–411
Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of
endophytic fungi from Tripterygium wilfordii. Fungal Divers
17:69–90
Kvas M, Marasas WFO, Wingfield BD, Wingfield MJ, Steenkamp ET
(2009) Diversity and evolution of Fusarium species in the
Gibberella fujikuroi complex. Fungal Divers 34:1–21
Le Gac M, Hood ME, Fournier E, Giraud T (2007a) Phylogenetic
evidence of host-specific cryptic species in the anther smut
fungus. Evolution 61:15–26
Le Gac M, Hood ME, Giraud T (2007b) Evolution of reproductive
isolation within a parasitic fungal complex. Evolution 61:1781–
1787
Le Gac M, Giraud T (2008) Existence of a pattern of reproductive
character displacement in Basidiomycota but not in Ascomycota.
J Evol Biol 21:761–772
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual.
Blackwell, Iowa
Levy L, Castlebury LA, Carris LM, Meyer RJ, Pimentel G (2001)
Internal transcribed spacer sequence-based phylogeny and polymerase chain reaction-restriction fragment length polymorphism
differentiation of Tilletia walkeri and T. indica. Phytopathology
91:935–940
Link HF (1809) Observationes in ordines plantarum naturales.
Dissertatio I. Gesellschaft der Naturforschenden Freunde Berlin,
Magazin der Neuesten Entdeckungen in der gesammten.
Naturkunde 3:3–42
Liro JL (1924) Die Ustilagineen Finnlands I. Ann Acad Sci Fenn A
17:1–636
Liu XY, Duan JX, Xie XM (2007) Colletotrichum yunnanense sp.
nov., a new endophytic species from Buxus sp. Mycotaxon
100:137–144
Lutz M, Göker M, Piatek M, Kemler M, Begerow D, Oberwinkler F
(2005) Anther smuts of Caryophyllaceae: molecular characters
indicate host-dependent species delimitation. Mycol Prog 4:225–
238
Lutz M, Piatek M, Kemler M, Chlebicki A, Oberwinkler F (2008)
Anther smuts of Caryophyllaceae: molecular analyses reveal
further new species. Mycol Res 112:1280–1296
Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny of
the rust fungi: an approach using nuclear large subunit ribosomal
DNA sequences. Can J Bot 81:12–23
Marasas WFO, Nelson PE, Toussoun TA (1984) Toxigenic Fusarium
species: identity and mycotoxicology. Pennsylvania State
University Press, University Park
Matuo T, Snyder WC (1973) Use of morphology and mating
populations in the identification of formae speciales in Fusarium
solani. Phytopathology 63:562–565
Mayr E (1963) Animal species and evolution. Harvard University
Press, Cambridge
McTaggart AR (2010) Systematics of the Ustilato-SporisoriumMacalpinomyces complex of smut fungi. PhD thesis. Queensland
University of Technology, Brisbane, Australia.
Micheli PA (1729) Nova plantarum genera. Firenze: Bernardo Paperini:
1-234
Nelson PE, Tousson TA, Marasas WFO (1983) Fusarium species: an
illustrated manual for identification. Pennylvania State University
Press, University Park
Author's personal copy
Fungal Diversity
O’Donnell K (2000) Molecular phylogeny of the Nectria
haematococca-Fusarium solani species complex. Mycologia
92:919–938
O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics
and phylogeography of the Gibberella fujikuroi species complex.
Mycologia 90:465–493
O’Donnell K, Kisler HC, Tacke BK, Casper HH (2000) Gene
genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the
fungus causing wheat scab. Proc Natl Acad Sci USA 97:7905–
7910
O’Donnell K, Ward TJ, Geiser DM, Corby Kistler H, Aoki T (2004)
Genealogical concordance between the mating type locus and
seven other nuclear genes supports formal recognition of nine
phylogenetically distinct species within the Fusarium graminearum
clade. Fungal Genet Biol 41:600–623
Park B, Park J, Cheong KC, Choi J, Jung K, Kim D, Lee YH, Ward
TJ, O’Donnell K, Geiser DM, Kang S (2011) Cyber infrastructure
for Fusarium: three integrated platforms supporting strain identification, phylogenetics, comparative genomics and knowledge
sharing. Nucleic Acids Res 39:D640–D646
Pascoe IG, Priest MJ, Shivas RG, Cunnington JH (2005) Spores of
Tilletia ehrhartae, a smut of Ehrharta calycina, are common
contaminants of Australian wheat grain, and a potential source of
confusion with Tilletia indica, the cause of Karnal bunt of wheat.
Plant Pathol 54:161–168
Peever T (2007) Role of host specificity in the speciation of Ascochyta
pathogens of cool season food legumes. Eur J Plant Pathol
119:119–126
Perlin MH (1996) Pathovars of Formae speziales of Microbotryum
violaceum differ in electrophoretic karyotype. Int J Plant Sci
157:447–452
Persoon CH (1801) Synopsis methodica fungorum. Apud Henricum
Dieterich, Gottingae, pp 1–708
Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic
fungi of wild banana (Musaacuminata) at Doi Suthep Pui
National Park, Thailand. Mycol Res 105:1508–1513
Photita W, Lumyong S, Lumyong P, McKenzieEHC HKD (2003)
Saprobic fungi on dead wild banana. Mycotaxon 85:345–356
Photita W, Taylor PWJ, Ford R, Hyde KD, Lumyong S (2005)
Morphological and molecular characterization of Colletotrichum
species from herbaceous plants in Thailand. Fungal Divers
18:117–133
Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K,
Chukeatirote E, Hyde KD (2010) Colletotrichum gloeosporioides
is not a common pathogen on tropical fruits. Fungal Divers
44:33–43
Pollack FG (1987) An annotated compilation of Cercospora names.
Mycol Mem 12:1–212
Pons N, Sutton BC (1988) Cercospora and similar fungi on yams
(Dioscorea spp.). Mycol Papers 160:1–78
Prévost IB (1807) Memoire sur la cause immédiate de la carie.
Montauban
Prihastuti H, Cai L, Chen H, Hyde KD (2009) Characterization of
Colletotrichum species associated with coffee berries in Chiang
Mai, Thailand. Fungal Divers 39:89–109
Pringle A, Baker DM, Platt JK, Wares JP, Latgé JP, Taylor JW (2005)
Cryptic speciation in the cosmopolitan and clonal human
pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–
1899
Reynolds DR (1993) The fungal holomorph: an overview. In:
Reynolds DR, Taylor JW (eds) The fungal Holomorph: Mitotic,
Meiotic and Pleomorphic Speciation in Fungal Systematics.
CAB International, Wallingford, pp 15–25
Rossman AY, Palm-Hernández ME (2008) Systematics of plant
pathogenic fungi: why it matters. Plant Dis 92:1376–1386
Rupe JC (1989) Frequency and pathogenicity of Fusarium solani
recovered from soybeans with Sudden-Death Syndrome. Plant
Dis 73:581–584
Seier MK, Morin L, van der Merwe M, Evans HC, Romero Á (2009)
Are the microcyclic rust species Puccinia melampodii and
Puccinia xanthii conspecific. Mycol Res 113:1271–1282
Shivas RG, Hyde KD (1997) Biodiversity of plant pathogenic fungi in
the tropics. In: Hyde KD (ed) Biodiversity of tropical microfungi.
Hong Kong University Press, Hong Kong, pp 47–56
Shivas RG, Tan YP (2009) A taxonomic re-assessment of
Colletotrichum acutatum, introducing C. fioriniae comb. et
stat. nov. and C. simmondsii sp. nov. Fungal Divers 39:111–
122
Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill
CF, Zalar P, de Hong GS, Crous PW (2007) Biodiversity in the
Cladosporium herbarum complex (Davidiellaceae, Capnodiales),
with standardisation of methods for Cladosporium taxonomy and
diagnostics. Stud Mycol 58:105–156
Snyder WC, Hansen HN (1941) The species concept in Fusarium with
reference to section Martiella. Am J Bot 28:738–742
Snyder WC, Hansen HN (1945) The species concept in Fusarium
with reference to Discolor and other sections. Am J Bot
32:657–666
Starkey DE, Ward TJ, Aoki T, Gale LR, Kisler HC (2007) Global
molecular surveillance reveals novel Fusarium head blight
species and trichothecene toxin diversity. Fungal Genet Biol
44:1191–1204
Stewart EL, Liu ZW, Crous PW, Szabo LJ (1999) Phylogenetic
relationships among some cercosporoid anamorphs of Mycosphaerella based on rDNA sequence analysis. Mycol Res
103:1491–1499
Stoll M, Piepenbring M, Begerow D, Oberwinkler F (2003) Molecular
phylogeny of Ustilago and Sporisorium species (Basidiomycota,
Ustilaginales) based on internal transcribed spacer (ITS)
sequences. Can J Bot 81:976–984
Stoll M, Begerow D, Oberwinkler F (2005) Molecular phylogeny of
Ustilago, Sporisorium, and related taxa based on combined
analyses of rDNA sequences. Mycol Res 109:342–356
Su YY, Noireung P, Liu F, Hyde KD, Moslem MA, Bahkalii AH, AbeElsalam KA, Cai L (2011) Epitypification of Colletotrichum
musae, the causative agent of banana anthracnose. Mycosciense.
doi:10.1007/s10267-011-0120-9
Summerell BA, Laurence MH, Liew ECY, Leslie JF (2010) Biogeography and phylogeography of Fusarium: a review. Fungal Divers
44:3–13
Sutton BC (1980) The coelomycetes. Commonwealth Mycological
Institute, Kew, pp 1–696
Sutton BC (1992) The genus Glomerella and its anamorph
Colletotrichum. In: Bailey JA, Jeger MJ (eds) Colletotrichum:
biology, pathology and control. CAB International, Wallingford,
pp 1–26
Taylor JW, Jacobson DJ, Fisher MC (1999) The evolution of asexual
fungi: Reproduction, speciation and classification. Annu Rev
Phytopathol 37:197–246
Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS,
Fisher MC (2000) Phylogenetic species recognition and species
concepts in fungi. Fungal Genet Biol 31:21–32
Taylor JW, Turber E, Townsend JP, Dettman JR, Jacobson D (2006)
Eukaryotic microbes, species recognition and the geographic
limits of species: examples from the kingdom Fungi. Phil Trans
R Soc B Biol Sci 361:1947–1963
Tessmann DJ, Charudattan R, Kistler HC, Rosskopf EN (2001) A
molecular characterization of Cercospora species pathogenic to
water hyacinth and emendation of C-piaropi. Mycologia 93
(2):323–334
Tharp BC (1917) Texas parasitic fungi. Mycologia 9:105–124
Author's personal copy
Fungal Diversity
Tillet M (1755) Dissertation sur la cause qui corrompt et noircit le bled
dans les épis; et sur les moyens de prévenir ces accidens.
Bordeaux
To-Anun C, Hidayat I, Meeboon J (2011) Genus Cercospora in
Thailand: taxonomy and phylogeny (with a dichotomous key to
species). Plant Pathology & Quarantine 1:11–87
Tode HJ (1790) Fungi Mecklenbergensis Selecti 1: 1-64
Toussoun TA, Nelson PE (1975) Variation and speciation in the
fusaria. Annu Rev Phytopathol 13:71–82
Tulasne LR, Tulasne C (1847) Mémoire sur les Ustilaginées
comparées aux Uredinées. Annales des Sciences Naturelles.
Botanique et Biologie Végétale 3:12–126
van Putten WH, Elzinga JA, Biere A (2007) Host fidelity of the
pollinator guilds of Silene dioica and Silene latifolia: possible
consequences for sympatric host race differentiation of a vectored
plant disease. Int J Plant Sci 168:421–434
Vánky K (2002) Illustrated Genera of Smut Fungi. APS Press,
Minnesota
Vánky K (2003) The smut fungi (ustilaginomycetes) of Sporobolus
(Poaceae). Fungal Divers 14:205–241
Vánky K (2006) The smut fungi (Ustilaginomycetes) of Restionaceae
s. lat. Mycol Balc 3:19–46
Vanky K, Lutz M (2007) Revision of some Thecaphora species
(Ustilaginomycotina) on Caryophyllaceae. Mycol Res 111:1207–
1219
Vestal EF (1933) Pathogenicity, host response and control of Cercospora
leaf spot of sugar beet. Iowa Agric Exp Stn Res Bull 168:43–72
von Arx JA (1957) Die Arten der Gattung Colletotrichum Cda.
Phytopathologische Zeitschrift 29:414–468
Waller JM, Bridge PD, Black R, Hakiza G (1993) Characterization of
the coffee berry disease pathogen. Colletotrichum kahawae sp.
nov. Mycol Res 97:989–994
Weir BS, Johnston PR (2010) Characterisation and neotypification of
Gloeosporium kaki Hori as Colletotrichum horii nom. nov.
Mycotaxon 111:209–219
Wollenweber HW, Reinking OA (1935) Die Fusarien, ihre Beschreiburg,
Schadwirkung, ud Bekampfung. Verlag Paul Parey, Berlin, pp 1–
335
Wulandari NF, To-anun C, Hyde KD, Duong LM, de Gruyter J,
Meffert JP, Groenewald JZ, Crous PW (2009) Phyllosticta
citriasiana sp. nov., the cause of Citrus tan spot of Citrus
maxima in Asia. Fungal Divers 34:23–39
Yamaoka Y (2002) Artificial culture of rust fungi. Yet-to-be-cultured
microorganisms and culture collections: 14-17 (in Japanese)
Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC,
Padhye AA, Geiser DM (2006) Members of the Fusarium solani
species complex that cause infections in both humans and plants
are common in the environment. J Clin Microbiol 44:2186–2190
Zillig H (1921) Über spezialisierte Formen beim Antherenbrand,
Ustilago violacea (Pers.) Tuck. Zentralbl Bakteriol II 53:33–74