1 23

Fungal DiversityAn International Journal ofMycology ISSN 1560-2745 Fungal DiversityDOI 10.1007/s13225-011-0127-8

The evolution of species concepts andspecies recognition criteria in plantpathogenic fungi

Lei Cai, Tatiana Giraud, Ning Zhang,Dominik Begerow, Guohong Cai & RogerG. Shivas

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.

REVIEW

The evolution of species concepts and species recognitioncriteria 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 contem-porary species concepts and species recognition criteria forplant pathogenic fungi. Previous incongruent and unstableclassification based on subjective and changing criteriahave led to some confusion, especially amongst plantpathologists. The goal of systematics is to provide aninformative and robust framework that stands the test oftime. The taxonomic histories of Cercospora, Colletotrichum,Fusarium, as well as the rust and smut fungi, are used asexamples, to show how concepts and criteria used to delimitand recognize species have changed. Through these exampleswe compare the Genealogical Concordance Phylogenetic

Species Recognition, an extension of the PhylogeneticSpecies Criterion, with other species recognition criteria andshow that it provides a better discrimination for delimitingspecies. A rapidly increasing number of cryptic species arebeing discovered amongst plant pathogenic fungi using theGenealogical Concordance Phylogenetic Species Recogni-tion, and it is important to determine their host range, theseverity of diseases they cause and their biosecurity signif-icance. With rapidly expanding global trade it has becomeimperative that we develop effective and reliable protocols todetect these previously unrecognized pathogens.

Keywords Cryptic species . Species complex .

Microbotryum . Pucciniomycotina .Ustilaginomycotina .

Speciation . Taxonomy

Introduction

Plant pathologists are regularly confronted with having tochoose a name for their pathogen of interest and mycolo-gists often need to decide when to recognize a new speciesor apply an existing name. Country specific inventories ofplant pathogenic fungi with accurate and accepted namesare essential for the development of effective biosecurityand trade policies as well as a prerequisite for pest riskassessments (Hyde et al. 2010). These inventories alsofacilitate the early identification of invasive fungal patho-gens and allow the timely application of appropriate diseasecontrol measures (Rossman and Palm-Hernández 2008).The accurate identification of a plant pathogen will in mostcases provide a species name, which may then be used tounlock all of our collective knowledge about the organism.This knowledge may include its evolutionary history, lifecycle, distribution, host range, resistance to drugs, economic

L. Cai (*)State Key Laboratory of Mycology, Institute of Microbiology,Chinese Academy of Sciences,West Bei Cheng Rd,Beijing 100101, People’s Republic of Chinae-mail: mrcailei@gmail.com

T. GiraudEcologie, Systématique et Evolution,Bâtiment 360, Université Paris-Sud,91405 Orsay cedex, France

N. Zhang :G. CaiDepartment of Plant Biology and Pathology, Rutgers,The State University of New Jersey,59 Dudley Road, Foran Hall 201,New Brunswick, NJ 08901, USA

D. BegerowRuhr-Universität Bochum,Geobotanik ND03/174, Universitätsstr. 150,44801 Bochum, Germany

R. G. ShivasPlant Pathology Herbarium, Agri-Science Queensland,40 Boggo Road,Dutton Park, Qld 4102, Australia

Fungal DiversityDOI 10.1007/s13225-011-0127-8

Author's personal copy

and biosecurity importance as well as control measures(Rossman and Palm-Hernández 2008). Over time, ourunderstanding about how to identify plant pathogenic fungalspecies has undergone several revolutionary changes.

The criteria used to delimit and identify species, asapplied to plant pathogenic fungi, have changed over time,most recently due to the rapid development of moleculartools. The different criteria that allow the delimitation ofspecies may be classified as morphological, physiological,intersterility, host specificity, and phylogenetic. All of thesespecies recognition criteria attempt to identify evolutionaryindependent lineages (Taylor et al. 2000). The morpholog-ical and phylogenetic criteria can further be used tounravel evolutionary relationships between species andarrive at a natural classification. The classification of plantpathogenic fungal species, together with the associatedtaxonomic nomenclature, as currently defined by theInternational Code of Botanical Nomenclature, is funda-mentally important for plant pathologists and mycologistsin all fields (Rossman and Palm-Hernández 2008; Hyde etal. 2010).

The choice and justification of species criteria to identifythe 1.5 million fungal species estimated to populate theworld (Hawksworth 1991) or the ca 270,000 tropical plantpathogenic fungi (Shivas and Hyde 1997), has significantconsequences for our understanding of emergent diseaseson plants and animals (Giraud et al. 2010), particularlyagainst a backdrop of global climate change (Chakrabortyand Newton 2011).

In this paper, we review the evolution of speciesconcepts and species recognition criteria in plant pathogenicfungi, by using examples from some important groups,namely,Cercospora, Colletotrichum, Fusarium, and the rustand smut fungi. The taxonomic history of each group isreviewed, with emphasis on the changing focus of criteriaused to recognize species. In particular, the utility ofGenealogical Concordance Phylogenetic Species Recogni-tion in many fungal groups is compared with the otherspecies criteria. The practical implications of changingcriteria used to recognise species are discussed. We alsodiscuss the consequences that recent advances in ourunderstanding of fungal speciation have meant for devel-oping robust species criteria, although more extensivereviews on speciation and species recognition in fungi canbe 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 aspecies (De Queiroz 2007; Hey 2006) may lead one tothink that there is no general agreement amongst biologists

about what defines a species. This view stems fromconfusion between the concept of a species, i.e. a descriptionof the kind of entity that constitutes a species, and the criteriathat delimit a particular species, i.e. practical standards forthe recognizing whether individuals should be consideredmembers of the same species. Many so-called “speciesconcepts” actually correspond to species criteria (De Queiroz2007; Hey 2006; Taylor et al. 2000). The BiologicalSpecies “Concept” for instance is most often meant toemphasize the criterion of intersterility, the MorphologicalSpecies “Concept” emphasizes the criterion of morpholog-ical divergence, the Ecological Species “Concept” empha-sizes adaptation to a particular ecological niche, and thePhylogenetic Species “Concept” emphasizes nucleotidedivergence between monophyletic lineages (Giraud et al.2008a; Taylor et al. 2000). These species criteria correspondto the different events that occurred during lineageseparation and divergence, rather than to fundamentaldifferences in what represents a species. To the contrary, ithas been argued that most modern biologists agree on acommon “species concept” or “species definition”, specif-ically segments of evolutionary lineages that have evolvedindependently from one another (de Queiroz 1998).

Why are there conflicts over which species criteria weadopt? There are three main reasons why species criteriacannot be universal. Firstly, speciation is a temporallyextended process, and one that varies considerably in pacefor different types of organisms. Secondly, several modes ofspeciation can occur, during which the phenomena used forspecies recognition do not necessarily appear in the samechronological order (Fig. 1). Thirdly, the characteristics ofcertain organisms render some species criteria difficult toapply (Giraud et al. 2008a). The most useful criteria for therecognition of species in nature will depend on the type oforganism, its history of speciation and the degree ofachieved divergence. Searching for a single species criterionapplicable in all cases is fundamentally impossible (Giraudet al. 2008a).

The most commonly used species criterion for fungi haslong been the Morphological Species Criterion. Recentlymany cryptic species have been recognised using theintersterility criterion, a derivative of the Biological SpeciesCriteria (Anderson and Ullrich 1978). Mayr (1963) definedbiological species as groups of actually or potentiallyinterbreeding natural populations which are reproductivelyisolated from other such groups. Aweakness of the interste-rility criterion is that it cannot be applied to homothallic orasexual fungi (Reynolds 1993; Taylor et al. 2000).

The Phylogenetic Species Criterion has been responsiblefor a surge in the number of cryptic species recognized inrecent years (Schubert et al. 2007; Damm et al. 2009;Wulandari et al. 2009; Aveskamp et al. 2010; Summerell etal. 2010). The Phylogenetic Species Criterion relies on

Fungal Diversity

Author's personal copy

phylogenetic analysis of variable characters, usually DNAsequences of selected genes or genomes. PhylogeneticSpecies Criterion was originally defined as the smallestmonophyletic clade of organisms that share a derivedcharacter state (Cracraft 1983). A weakness with thisapproach is that single gene analyses, as compared towhole genome analyses, are dependent on the genes havingan evolutionary history that reflects that of the entirefungus, which is often not the case (Aguileta et al. 2008).Taylor et al. (2000) further developed a GenealogicalConcordance Phylogenetic Species Recognition, as anobjective way to define the limits of sexual species. TheGenealogical Concordance Phylogenetic Species Recognitionuses the phylogenetic concordance of multiple unlinked genesto indicate a lack of genetic exchange and thus evolutionaryindependence of lineages. Species have been identified withGenealogical Concordance Phylogenetic Species Recognitionthat cannot otherwise be recognized due to the lack ofdistinguishing morphological characters or incomplete inter-sterility. The Genealogical Concordance Phylogenetic SpeciesRecognition criterion has proved immensely useful in fungi,because it is more finely discriminating than the other criteriain many cases, or more convenient, e.g. with species that areunable to be crossed (Reynolds 1993; Taylor et al. 2000).Genealogical Concordance Phylogenetic Species Recogni-tion is currently more widely used for fungi than any otherorganisms, because fungi often have a simpler morphologyand it is difficult to demonstrate in vitro crosses for manyfungi (Dettman et al. 2003a; Fournier et al. 2005; Johnson etal. 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 Concor-dance Phylogenetic Species Recognition is better atrevealing cryptic species than the Biological SpeciesCriterion (intersterility criterion). Firstly, intersterility often

evolves slowly in allopatric divergences, in particular theprezygotic barriers most often tested in fungi (Coyne andOrr 1997; Le Gac and Giraud 2008). The divergence ofDNA sequences used under the Genealogical ConcordancePhylogenetic Species Recognition criterion may then occurbefore intersterility has evolved and thus be more useful todistinguish closely related sibling species. Among thenumerous complexes of sibling species recently uncoveredusing the Genealogical Concordance Phylogenetic SpeciesRecognition criterion, many in fact appear consistent withallopatric divergence, because the cryptic species occupynon-overlapping areas separated by geographic barriers(Taylor et al. 2006). This is the case for the speciescomplexes of the model organism Neurospora crassa(Dettman et al., 2003a, 2003b), the yeast Saccharomycesparadoxus, (Kuehne et al., 2007), the plant pathogenFusarium graminearum (O’Donnell et al., 2004), and themushrooms Schizophyllum commune (James et al. 1999)and Armillaria mellea (Anderson et al. 1980; Andersonet al. 1989).

Even in cases of sympatric speciation, certain mecha-nisms of reproductive isolation may allow intersterility toevolve much later than the divergence of DNA, againrendering the Genealogical Concordance PhylogeneticSpecies Recognition more finely discriminating than theBiological Species Criterion (Giraud et al. 2010; Giraudet al. 2008a, b; Le Gac and Giraud 2008). For manypathogenic fungi, sex must occur within the host aftermycelial development. This means that only individualsable to grow within the same host can mate. Adaptation toa new host can in these cases be sufficient to restrict geneflow in sympatry, without requiring active assortativemating, i.e. prezygotic intersterility (Giraud 2006; Giraudet al. 2006). In such cases, close species may remaininterfertile for some time, making in vitro crosses a poorcriterion for recognizing species. An example is provided

Fig. 1 Schematic divergence oftwo species, in two hypotheticalcases of respectively allopatricand sympatric speciation, withthe progressive appearenceof various criteria traditionnalyused to recognize species

Fungal Diversity

Author's personal copy

by the plant pathogenic genus Ascochyta, in which recentmultilocus phylogenetic analyses of a worldwide sampleof Ascochyta causing blights of chickpea, faba bean, lentil,and pea revealed that each of these hosted distinct species(Peever 2007). Experimental inoculations demonstratedthat infection was highly host specific, yet in vitro crossesshowed that the species were completely interfertile. Thehost specificity of these fungi may therefore constitute thesole reproductive barrier (Peever 2007), resulting insympatric speciation through the pleiotropic effect of hostadaptation (Giraud 2006; Giraud et al. 2006; Giraud et al.2010). More generally, there exist many close species ofascomycete pathogens that are sympatric but isolated byweak intersterilty barriers (Le Gac and Giraud 2008).

Some other pre-mating barriers to gene flow may allowgenetic divergence in sympatry without assortative matingand before intersterility evolves. For organisms dependingon biotic vectors, specialization of these vectors can preventcontact between two populations even if they lie close toone another, yielding ecological isolation, e.g. in theMicrobotryum violaceum complex of anther smut fungi,the insect vectors are different to some extent between hostspecies, which leads to a reduction in mating opportunitiesamong 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 promotepremating isolation, e.g. in the powdery mildew myco-parasite Ampelomyces, the phenology of the host plant ofthe parasitized fungus provides some reproductive isola-tion (Kiss et al. 2011). In addition, a high rate of selfingmay be efficient in limiting inter-specific matings as seenin some plants (Fishman and Wyatt, 1999). Selfing hasbeen proposed as a reproductive barrier in the anther smutfungus Microbotryum (Giraud et al. 2008b).

Evolution of species criteria in Cercospora

Members of the ascomycete genus Cercospora (Mycos-phaerellaceae, Capnodiales, Dothideomycetes) occurworld-wide and cause leaf spots on most dicot and monocotplant families, as well as some gymnosperms and ferns(Pollack 1987; Crous and Braun 2003). These fungi rankamong some of the most destructive of plant pathogens (To-Anun et al. 2011). Cercospora was first described byFresenius in Fuckel (1863) with C. apii as the type species.For many years, Cercospora was used for naming anycercosporoid fungus, i.e. a dematiaceous hyphomycete withfiliform conidia (Pons and Sutton 1988). As a result, itbecame one of the largest and most heterogeneous generaof hyphomycetes (Crous and Braun 2003). Chupp (1954)also adopted the broad morphological definition ofCercospora in his monograph.

Deighton (1967; 1973; 1976; 1979) tried to clarify thetaxonomy ofCercospora by segregating Cercospora speciesinto smaller and morphologically more similar units. ManyCercospora species were reclassified into Cercosporella,Cercosporidium, Paracercospora, Pseudocercospora, Pseu-docercosporella, Pseudocercosporidium, and other genera.Braun (1995) recognized close to 50 genera in theCercospora-complex. Members of Cercospora sensu strictoare 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 morpholog-ical criterion of Cercospora has been accepted by mosttaxonomists in the last 20 years (Hsieh and Goh 1990; Guoand Hsieh 1995; Crous and Braun 1996; Braun and Melnik1997; To-Anun et al. 2011).

While Cercospora was defined at genus level bymorphology until approximately two decades ago, speciesdefinition in this genus was based largely on hostassociation. Chupp (1954) considered species of Cercosporato be generally host specific and listed more than 1,900species names in his monograph. By 1987 more than 3,000names had been published in Cercospora (Pollack 1987).Crous and Braun (2003) challenged this concept of raisingnew names for morphologically indistinguishable Cerco-spora collections based on new host genera, when theyassigned 281 morphologically indistinguishable species tosynonymy under C. apii senso lato and recognized 659Cercospora species. The results of some earlier inoculationexperiments (Vestal 1933; Johnson and Valleau 1949; Fajola1978) and molecular sequence data (Crous et al. 2000;Goodwin et al. 2001) had also raised doubt about narrowhost specificity in the Cercospora complex. Using hostspecies as a basis for recognizing species of Cercospora alsofailed the pogo stick hypothesis of Crous and Groenewald(2005) formulated by observing some species of Mycos-phaerella, which proposed that host specific fungal plantpathogens often colonised non-host tissue or other substrates,forming fertile fruiting bodies.

In Cercospora, the application of the criterion ofintersterility was particularly limited because only a fewspecies in this genus have a known sexual stage (Chupp1954; Corlett 1991). Groenewald et al. (2006b) detected thetwo mating type genes in approximately even proportionsin C. beticola, C. zeae-maydis and C. zeina populations,and speculated that a sexual cycle may occur regularly inthese species. However, the actual sexual stage was notobserved.

The use of DNA sequence data and the adoption ofPhylogenetic Species Criterion have started to clarify someof the confusion in Cercospora taxonomy. The Cercosporacomplex has been shown to form a well-defined clade inthe Mycosphaerellaceae (Crous et al. 2009) supporting

Fungal Diversity

Author's personal copy

earlier molecular analyses (Stewart et al. 1999; Crous et al.2001; Goodwin et al. 2001). Furthermore, only species inthis group produce cercosporin, a phytotoxin that enhancesvirulence (Goodwin et al. 2001).

Two examples of the application of GenealogicalConcordance Phylogenetic Species Recognition in theCercospora complex follow. Firstly, two phylogeneticallysupported species, C. apii and C beticola, were identifiedamong the 281 synonyms placed in C. apii sensu lato byCrous and Braun (2003), even though they were morpho-logically similar and capable of infecting the same hosts ininoculation experiments (Groenewald et al. 2005; Groenewaldet al. 2006a, b). Secondly, C. piaropi and C. rodmanii, whichboth infect the aquatic plant water hyacinth, were consideredto differ from each other by conidial morphology andvirulence (Tharp 1917). A multilocus DNA phylogeny didnot support the separation of these two species (Tessmannet al. 2001) and a more detailed study using a collection ofisolates showed that morphological characters also did notreliably separate them. Consequently C. rodmanii wasreduced to synonymy with C. piaropi.

The adoption of Genealogical Concordance PhylogeneticSpecies Recognition has profound implications for diseasecontrol and quarantine. For example, considering the 281synonyms in C. apii sensu lato as individual species maylead to unnecessary biosecurity measures and trade restric-tions, yet considering them as a single species may miss theopportunity to contain some diseases, e.g. those caused byC. beticola.

Evolution of species criteria in Colletotrichum

The ascomycete genus Colletotrichum (Glomerellaceae,Sordariomycetes) contains many well-known plant patho-gens that cause anthracnose and a range of diseasesworldwide 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 mostimportant plant pathogens as they cause latent or quiescentinfections at the pre-harvest and post-harvest stages (Sutton1992). The first report of Colletotrichum was by Tode(1790) in the genus Vermicularia, while the genus nameColletotrichum was introduced by Corda (1831). Colleto-trichum encompasses species with endophytic, epiphytic,saprobic and phytopathogenic lifestyles (Kumar and Hyde2004; Photita et al. 2001; 2003; 2005; Liu et al. 2007;Prihastuti et al. 2009), as well as human pathogens (Canoet al. 2004).

The taxonomy of many groups of plant pathogenicfungi, including Colletotrichum, has been based on hostassociation (von Arx 1957; Sutton 1980). If a pathogenicfungus 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 reliablyreflect evolutionary independence of the lineages ofColletotrichum and many other groups of fungi, as manypathogenic species have a facultative saprobic ability,with the exception perhaps of the obligate plantpathogenic fungi, e.g. rusts, smuts, downy and powderymildews (Cummins and Hiratsuka 2003; Vánky 2002,Yamaoka 2002).

The work done by mycologists during the 19th and early20th century resulted in numerous fungal names withspecific epithets based on the scientific names of the hostplant. These names cannot be ignored in modern systematicstudies and pose a huge challenge for modern researcherswho will need to determine whether these names representdistinct species or synonyms of other names (Hyde et al.2009a; Cai et al. 2009). Sutton (1992) suggested that “Inevery large genus like Colletotrichum there needs to be adegree of systematics catharsis resulting in a severereduction in the number of accepted species before anyreal advances in identification can be made”. Such anapproach was taken by von Arx (1957) who reduced thenumber of Colletotrichum species from several hundred to11 based on morphological characters, with many taxatreated as synonyms of C. gloeosporioides (ca. 600synonyms) or C. dematium (86 synonyms). Severaladditional species have been accepted since von Arx(1957), based on Morphological Species Criterion (Sutton,1980; 1992). Sutton (1980) also built a key that hasprovided a practical identification tool and standardreference for identifying species of Colletotrichum formany years. In the last 30 years, and until recently, thenumber of newly described species of Colletotrichum hassubstantially slowed down and species were defined bytheir distinguishable morphological characters.

Although the application of Morphological SpeciesCriterion has resulted in an important and revolutionaryprogress in Colletotrichum systematics, some flaws per-sisted. The species criteria of von Arx (1957) were verybroad, and most of his taxonomic treatments were based onliterature descriptions, that lead to considerable inaccuracyand generality. For example, the treatment of synonymizingca. 600 names to C. gloeosporioides has been questionable,as it contains a lot of physiologically and genetically distantlineages. Recent application of Genealogical ConcordancePhylogenetic Species Recognition in Colletotrichum hasrevealed that many distinct species exist in the C.gloeosporioides complex. Some of these have beenformally 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

Fungal Diversity

Author's personal copy

al. 2011). In the C. acutatum complex, 4 distinct lineageswere recognized and three of them have been assignedspecies names (Shivas and Tan 2009).

The application of Genealogical Concordance Phyloge-netic Species Recognition in Colletotrichum has had animportant impact on species discovery, plant breeding,disease control and biosecurity protocols, all of whichdepend on accurate pathogen identification. Identificationof a specimen as C. gloeosporioides sensu lato or C.dematium sensu lato has little practical value. The manyspecies hidden in the C. gloeosporioides complex willcertainly have different biosecurity significance. For exam-ple, the C. gloeosporioides complex on coffee berries hasbeen well characterized and several distinct genetic andphenotypic species have been established (Prihastuti et al.2009; Waller et al. 1993). Among these, C. kahawae is astrongly aggressive pathogen specific to coffee in Africa(Waller et al. 1993) and the application of strict quarantineprotocols is justified to prevent its spread to coffee growingregions on other continents where it is not present. On theother hand, C. asianum, C. fructicola and C. siamense areopportunistic pathogens of coffee berries (Prihastutiet al. 2009) and appear to have a wide host range andlittle biosecurity significance. Phoulivong et al. (2010)indicated that morphologically similar isolates from chilli,mango, papaya, rose apple and jujube comprised morethan one distinct species. Very little is known aboutwhether these records, and many other worldwide recordsof C. gloeosporioides sensu lato, represent saprobes,weak or opportunistic pathogens or severe pathogens (Hydeet al. 2010).

Evolution of species criteria in Fusarium

The ascomycete genus Fusarium (Nectriaceae, Hypo-creales, Sordariomycetes) represents a large group ofascomycetes ubiquitously distributed in soil and in associ-ation with plants. Although most members are saprobic,Fusarium is better known for its toxigenic and plantpathogenic species, which significantly impact agriculture(Marasas et al. 1984). Fusarium produces secondarymetabolites, such as fumonisins, trichothecenes and zear-alenone, which are toxins that threaten food safety andhuman health. Recently, Fusarium species also haveemerged as opportunistic human pathogens causing ocularor systemic infections (Dignani and Anaissie 2004; Zhanget al. 2006).

Fusarium was first described by Link (1809) as specieswith fusiform spores borne on a stroma. This asexual genuswas validated by Fries (1821) in terms of the IBCN. Withincreased knowledge of fungal morphological identifica-tion, the presence of fusoid macroconidia with a basal foot

cell became accepted as the key character of the genusinstead of the presence of a stroma (Booth 1971). Theteleomorphs of Fusarium, when known, belong to eitherHaematonectria or Gibberella.

The history of the taxonomy of Fusarium has beenunstable. In the first century after the genus was estab-lished, over 1,000 species were defined on the basis ofsuperficial observations, often based on host association(Toussoun and Nelson 1975). Wollenweber and Reinking(1935) in their monograph Die Fusarien reduced the genusto 142 species, varieties and forms in 16 sections. Basedsolely on morphological characters, Snyder and Hansen(1941; 1945) further reduced Fusarium to nine species.Successor taxonomists conducted revisions based on eitherthe 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 speciesnames according to the Dictionary of The Fungi (Kirk etal. 2008). The frequent conflicts and instability inFusarium systematics have resulted from the absence ofclear morphological characters to separate species as wellas the existence of phenotypic variation in cultures(Geiser et al. 2004).

The root of the problem in Fusarium systematics lies inthe use of the Morphological Species Criterion as adoptedin traditional fungal taxonomy. As with many other fungi,Fusarium taxonomy was mostly based on the Morpholog-ical Species Criterion until two decades ago, whenMorphological Species Criterion and Phylogenetic SpeciesCriterion were applied (Summerell et al. 2010). Intersterilitybarriers have been detected in some Fusarium groups basedon crossing experiments, e.g. the genetically distinct matingpopulations in the F. solani species complex (Matuo andSnyder 1973). Clearly, the Biological Species Criterioncannot be applied to the majority of Fusarium lineages,which are homothallic or apparently asexual (Taylor et al.1999). Nonetheless, the BSC enabled reliable identificationfor some sexual species of Fusarium, especially for those inthe Gibberella fujikuroi and F. solani species complexes(Leslie and Summerell 2006; Kvas et al. 2009).

For species of Fusarium for which sexual reproductionis difficult to induce in vitro, the Phylogenetic SpeciesCriterion (including the Genealogical Concordance Phylo-genetic Species Recognition) has proven to be highlyinformative. Several studies have shown that PhylogeneticSpecies Criterion and Biological Species Criterion arecongruent, although the Biological Species Criterionappears more finely discriminating than the MorphologicalSpecies Criterion, particularly in Fusarium (O’Donnell2000; O’Donnell et al. 1998; Zhang et al. 2006). Distinctlineages recognized by the Phylogenetic Species Criterioncan be used as a guide for finding diagnostic morphological

Fungal Diversity

Author's personal copy

or ecological differences among fungal species, whichotherwise did not appear obvious. For example, phyloge-netic analyses have revealed the existence of cryptic speciesin F. graminearum, occurring in different parts of the world,resulting in the description of 13 new species (O’Donnellet al. 2000; Starkey et al. 2007; Kvas et al. 2009). Themost frequently used gene for species recognition andphylogenetic analysis in Fusarium is the translationelongation factor 1 α gene (EF-1α). Other useful lociinclude the internal transcribed spacer (ITS) region of therRNA 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 PhylogeneticSpecies Criterion-based systematics in Fusarium can beseen in soybean sudden death syndrome (Rupe 1989), adisease occurring throughout the world. Previously, thecausal agent was referred to as F. solani f. sp. glycines orFusarium solani sensu lato (Gao et al. 2004). Multiple genesequence analyses revealed a diversity of cryptic taxa,leading to the recognition of four different species ofFusarium as causes of this disease. Those isolates known tocause soybean sudden death syndrome in North Americahave been segregated as Fusarium virgulifore, while threerelated but different species of Fusarium are associatedwith this disease in South America (Aoki et al. 2005).Studies based on experimental crosses further confirmedthe distinction of these phylogenetic species (Covert et al.2007). The intersterility and allopatry of these crypticspecies were discovered only after their existence wasrevealed using phylogenetic analyses. The geographical andgenetic information associated with these newly recognizedspecies will enable the development of precise controlstrategies and the formulation of appropriate biosecuritypolicies.

Evolution of species criteria in rust and smut fungi

The rust and smut fungi belong to the subphyla Puccinio-mycotina and Ustilaginomycotina respectively, in thephylum Basidiomycota (Hibbett et al. 2007). At the specieslevel there are almost 7,000 species of rust fungi in 163genera (Kirk et al. 2001) and about 1,675 smut fungi in 95genera (Vánky, pers. comm.), which collectively accountfor about 10% of all known fungi. The rust and smut fungiboth contain many economically and agriculturally impor-tant species and their profound influence on human historyis well documented (Carefoot and Sprott 1967).

The traditional definition of the rust and smut life formwas the presence of teliospores that germinate to producebasidia and these fungi were classified together in theTeliomycetes (Jülich, 1981). However ultrastructural andmolecular studies have shown that the rust and smut fungi

are only distantly related with separate monophyleticorigins (Bauer et al. 1997; Begerow et al. 1997). Further-more, the rust fungi have a pleomorphic life cycle with upto five spore states (spermatia, aeciospores, urediniospores,teliospores and basidiospores) which differentiates themfrom the smut fungi that mostly produce two types ofspores (teliospores and basidiospores).

Rust and smut fungi are essentially obligate plantpathogens, although the smut fungi may have a short stageof saprobic growth on non-living substrates, and about 30rusts have been cultivated on artificial media (Yamaoka2002). The classification of rust and smut species has beentraditionally based on both Morphological SpeciesCriterion, with emphasis on sori and spore stages, as wellas on Ecological Species Criterion, with emphasis onpathogenicity on specific hosts (Vánky 2002, Cumminsand Hiratsuka 2003). Consequently these groups have beenrelatively stable, and easily classified and identified usingmorphology and host associations for over 200 years. Therecent application of molecular phylogenetic analyses to therust and smut fungi has mostly supported previousclassifications 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 inpart. While the Pucciniales (rust fungi) are monophyletic,the smut fungi in the traditional sense correspond to at leasttwo phylogenetically distant clades. Those smut fungi inthe Ustilaginomycotina cluster together with other plantpathogens of the Exobasidiales, Microstromatales as wellas human pathogens of Malassezia (Begerow et al. 2000;Begerow et al. 2006). The smut fungi in the Microbotryalescluster together with other plant pathogens and mycopar-asites in the Microbotryomycetes in the Pucciniommycotina(Bauer et al. 2006). Ultrastructural characters and cell wallcompounds have subsequently supported these modernclassifications (Bauer et al. 1997; 2006).

Early species descriptions of rust and smut fungi wereusually based on morphology and separation of the twogroups was not always clear. The earliest descriptions ofrust 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 theirlife cycle including teliospore formation and germination(de Bary 1853; Tulasne and Tulasne 1847). Interestingly,most of these early treatments included quite comprehen-sive studies comprising morphological, physiological andsystematic aspects. Most of the early species lists includedinformation about host species and the lists were evenorganized according to host (Fischer von Waldheim 1869).It is commonly accepted that rust and smut species areeach restricted to a family or even a narrower plant taxonand there are many examples describing the rust or smutspecies of a given plant family (Vánky 2006; Vánky and

Fungal Diversity

Author's personal copy

Lutz 2007) or a given host genus (Bauer et al. 1999;Vánky 2003). Several genera of heteroecious rust fungi onthe other hand need two different hosts to complete theirlife cycle, which may be from completely different plantfamilies.

Considering that over 8,000 species of rust and smutfungi are known, there has been little application of DNAsequence data to identify rust and smut fungi in terms ofthe Genealogical Concordance Phylogenetic SpeciesRecognition. This is certainly because the morphologicalcharacteristics of rust and smut fungi have appearedstable and reliable, allowing confident identification ofspecies that are supported, in most cases, by narrow hostranges. However complexes composed of closely relatedreproductively isolated cryptic species are still commonin the rust fungi (Gaümann 1959) and also some groupsof smut fungi. Consequently, molecular studies have beenused to resolve phylogenetic relationships between mor-phologically similar taxa of rust and smut fungi. Forexample, the host-specificity, morphology and DNAsequence data of two microcyclic rusts species Pucciniamelampodii and P. xanthii (Seier et al. 2009) lead to theestablishment of a new morphospecies, P. xanthii var.parthenii-hysterophorae, to accommodate records of P.melampodii associated with the host Parthenium hyster-ophus. Another example is Karnal bunt of wheat, causedby the smut fungus Tilletia indica, an important pathogenabsent from Australia. ITS sequence data have been usedto separate it from morphologically similar species thatmay also occur as contaminants in consignments of wheatseed (Levy et al. 2001, Pascoe et al. 2005). Overall, theapplication of Phylogenetic Species Criterion supportedMorphological Species Criterion in many of the genera ofsmut fungi (Hendrichs et al. 2005; Begerow et al. 2000;Castlebury et al. 2005) and only recently the largeUstilago / Sporisorium / Macalpinomyces species complexhas been substantially resolved using a phylogeny derivedfrom molecular data that reflected morphological syna-pomorphies and host associations (Stoll et al. 2003,2005; McTaggart 2010).

As one of the best studied models, Microbotryumhas provided a good example of the utility of thePhylogenetic Species Criterion. A narrow species crite-rion based on host use (Zillig 1921; Liro 1924; Baker1947) long contrasted with a broad Morphological SpeciesCriterion species criterion, the latter defining a singlespecies, Microbotryum violaceum, considered as the patho-gen responsible for almost all anther smuts of Caryo-phyllaceae (Perlin 1996). Population genetics studies(Bucheli et al. 2000) and the use of the GenealogicalConcordance Phylogenetic Species Recognition (Le Gacet al. 2007a) revealed an absence of gene flow and an ancientdifferentiation between populations of Microbotryum found

on different host plants, which were confirmed by ITSphylogenies as distinct species on different hosts (Lutz et al.2005, 2008). As in other fungal species, the BiologicalSpecies Criterion was less discriminating (Le Gac et al.2007b), with little evidence of assortative mating in the formof conjugation initiation in vitro, although hybrid inviabilityand sterility was observed between the cryptic species (LeGac et al. 2007b; de Vienne et al. 2009a). Cross-inoculationstudies also appeared less discriminating in vitro than hostspecificity seen in the field (de Vienne et al. 2009b; Gladieuxet al. 2011). The studies highlight the value of GenealogicalConcordance Phylogenetic Species Recognition to validatePhylogenetic Species Criterion and Morphological SpeciesCriterion that have practical application in the field ofplant pathology.

Conclusive remarks

Molecular DNA sequence data have recently been exten-sively employed in studying the systematics of plantpathogenic fungi. The advantage of using molecular datais that it provides a greater number of heritable charactersthat allow for convenient information sharing betweenlaboratories. Morphological characters, however, are proneto change under different environmental conditions. Inaddition, well-developed bioinformatics tools make analy-sis of data more objective and less controversial whenexamined by different scientists. The Biological SpeciesCriterion has proved useful in some fungal groups butoverall appears less convenient and less discriminating,although congruent, with the Genealogical ConcordancePhylogenetic Species Recognition.

The Genealogical Concordance Phylogenetic SpeciesRecognition has been widely accepted in fungal systematics.Multi-gene sequencing and phylogenetic analysis havebecome a routine procedure in identifying new fungalspecies, especially for those that lack distinctive morpho-logical characters. Consequently a rapidly increasing num-ber of cryptic species are being discovered amongst plantpathogenic fungi using the Genealogical ConcordancePhylogenetic Species Recognition and it is critical todetermine their host range, the severity of diseases theycause and their biosecurity significance. With rapidlyexpanding global trade it has become imperative that wedevelop effective and reliable protocols to detect thesepreviously unrecognized pathogens.

Based on Genealogical Concordance Phylogenetic Spe-cies Recognition, previously applied phenotypic charactersthat were used to define taxa need re-evaluation. Althoughthe recent molecular advances in multi-locus phylogeny hasbeen able to recognize stable and well-separated phyloge-netic species, there is still a long way to go before we can

Fungal Diversity

Author's personal copy

finally establish a natural classification system and speciesrecognition criteria for most fungi using DNA sequencedata. A major problem is that only a very small number ofspecies have been deposited in public culture collectionsand only a fraction of these have had some DNA fragmentsequenced. The number of ex-type strains that have beensequenced is even lower. Another potential problem is thatmost of the well-known plant pathogenic fungi weredescribed based on the Morphological Species Criterionand ex-type cultures are not available. It is inevitable thatPhylogenetic Species Criterion and Morphological SpeciesCriterion will still be used together to define species formany years.

Once robust species delimitation and classification isestablished, the development of high-throughput identifica-tion tools like barcoding should be a major improvementfor assignment of particular strains to species (Begerowet al. 2010). Together with well-curated databases andregularly updated regional species lists rapid molecularidentification is able to efficiently support not only quarantineregulations but the monitoring of new emerging diseasesas well.

Acknowledgements DrAlistairMcTaggart (Louisiana State University)is thanked for his helpful comments. Ms. Liu Fang is thanked fortechnical assistance. Lei Cai acknowledges grants CAS KSCX2-YW-Z-1026 and NSFC 31070020. Tatiana Giraud acknowledges the grantsANR 06-BLAN-0201 and ANR 07-BDIV-003. Parts of this chapter arederivatives of articles previously published (Giraud et al., 2008a;Gladieux et al., 2010). Roger Shivas acknowledges Chinese Academy ofSciences for the Visiting Professorship for Senior International Scientists(Grant No. 2010T2S12). Dominik Begerow acknowledges the grants BE2201/4-2 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) Assessingthe performance of single-copy genes for recovering robustphylogenies. Syst Biol 57:613–627

Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH,Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, SampaioJP, Bauer R, Weiß M, Oberwinkler F, Hibbett DS (2006) Anoverview of the higher-level classification of Pucciniomycotinabased on combined analyses of nuclear large and small subunitrDNA sequences. Mycologia 98:896–905

Anderson JB, Korhonen K, Ullrich RC (1980) Relationships betweenEuropean and North American biological species of Armillariamellea. Exp Mycol 4:87–95

Anderson JB, Bailey SS, Pukkia PJ (1989) Variation in ribosomalDNA among biological species of Armillaria, a genus of root-infecting fungi. Evolution 43:1652–1662

Anderson JB, Ullrich RC (1978) Biological species of Armillariamellea in North America. Mycologia 71:402–414

Aoki T, O’donnell K, Scandiani M (2005) Sudden death syndrome ofsoybean 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, CrousPW (2010) Highlights of the Didymellaceae: a polyphasicapproach to characterize Phoma and related pleosporaleangenera. Stud Mycol 65:1–60

Baker HG (1947) Infection of species of Melandrium by Ustilaoviolacea (Pers.) Fuckel and the transmission of the resultantdisease. Ann Bot 11:333–348

Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers ansststematics in smut fungi and allied taxa. Can J Bot 75:1273–1314

Bauer R, Vánky K, BegerowD, Oberwinkler F (1999) Ustilaginomyceteson Selaginella. Mycologia 91:475–484

Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) Thesimple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66

Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies onthe nuclear large subunit ribosomal DNA of smut fungi andrelated taxa. Can J Bot 75:2045–2056

Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placement ofustilaginomycetous anamorphs as deduced from nuclear LSUrDNA sequences. Mycol Res 104:53–60

Begerow D, Lutz M, Oberwinkler F (2002) Implications of molecularcharacters for the phylogeny of the genus Entyloma. Mycol Res106:1392–1399

Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis ofUstilaginomycotina based on multiple gene analyses andmorphological data. Mycologia 98:906–916

Begerow D, Nilsson H, Unterseher M, Maier W (2010) Currentstate and perspectives of fungal DNA barcoding and rapididentification procedures. Appl Microbiol Biotechnol 87:99–108

Booth C (1971) The Genus Fusarium. Commonwealth MycologicalInstitute, Kew, Surrey, England: 1-237.

Braun U (1995) A monograph of Cercosporella, Ramularia and alliedgenera (Phytopathogenic Hyphomycetes). Vol. 1. IHW-Verlag,Eching bei, München: 1-333

Braun U, Melnik VA (1997) Cercosporoid fungi from Russia andadjacent countries. Russian Academy of Sciences, Proceedings ofthe Komarov Botanical Institute 20:1–112

Bucheli E, Gautschi B, Shykoff JA (2000) Host-specific differentia-tion in the anther smut fungus Microbotryum violaceum asrevealed by micosatellites. J Evol Biol 13:188–198

Cai L, Hyde KD, Taylor PWJ, Weir B, Waller J, Abang MM, ZhangJZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG,McKenzie EHC, Johnston PR (2009) A polyphasic approach forstudying Colletotrichum. Fungal Divers 39:183–204

Cannon PF, Buddie AG, Bridge PD (2008) The typification ofColletotrichum gloeosporioides. Mycotaxon 104:189–204

Cano J, Guarro J, Gene J (2004) Molecular and morphologicalidentification of Colletotrichum species of clinical interest. J ClinMicrobiol 42:2450–2454

Carefoot GL, Sprott ER (1967) Famine on the wind. Rand McNally,Chicago

Castlebury LA, Carris LM, Vánky K (2005) Phylogenetic analysis ofTilletia and allied genera in order Tilletiales (Tstilaginomycetes;Exobasidiomycetidae) based on large subunit nuclear rDNAsequences. Mycologia 97:888–900

Chakraborty S, Newton AC (2011) Climate change, plant diseases andfood 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). DeutschlandsFlora, 3. Abtheilung 3: 1-144

Corlett M (1991) An annotated list of the published names inMycosphaerella 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

Fungal Diversity

Author's personal copy

syndrome pathogen Fusarium tucumaniae. Fungal Genet Biol44:799–807

Coyne J, Orr HA (1997) Patterns of speciation in Drosophila revisited.Evolution 51:295–303

Cracraft J (1983) Species concepts and speciation analysis. InCurrent Ornithology, Vol. 1, pp. 159–187. Plenum Press, NewYork

Crouch JA, Beirn LA (2009) Anthracnose of cereals and grasses.Fungal Divers 39:19–44

Crouch JA, Clarke BB, White JF, Hillman BI (2009) Systematicanalysis of falcate-spored graminicolous Colletotrichum and adescription 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 BiodiversitySeries 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) Thegenus Mycosphaerella and its anamorphs. Stud Mycol 45:107–121

Crous PW, Kang JC, Braun U (2001) A phylogenetic redefinition ofanamorph genera in Mycosphaerella based on ITS rDNAsequence 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? Persoonia23:99–118

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 herbaceoushosts. Fungal Divers 39:45–87

de Bary HA (1853) Untersuchungen über die Brandpilze und diedurch sie verursachten Krankheiten der Pflanzen mit Rücksichtauf das Getreide und andere Nutzpflanzen. Habilitationsschrift.

de Queiroz K (2007) Species concepts and species delimitation. SystBiol 56(6):879–886

de Queiroz K (1998) The general lineage concept of species, speciescriteria, and the process of speciation: a conceptual unificationand terminological recommendations. In: Howard DJ, BerlocherSH (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, VerckenE, Smadja C, Deseille A, Giraud T (2009a) Hybrid sterility andinviability in the parasitic fungal species complex Microbotryum.J Evol Biol 22:683–698

de Vienne D, Hood M, Giraud T (2009b) Phylogenetic determinantsof 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 onEuphorbia. Mycological Papers 112:1–80

Deighton FC (1973) Studies on Cercospora and allied genera. IV.Cercosporella Sacc., Pseudocercosporella gen. nov. andPseudocercosporidium 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 Papers144:1–56

Dettman JR, Jacobson DJ, Taylor JW (2003a) A multilocus genea-logical approach to phylogenetic species recognition in the modeleukaryote 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 MicrobiolInfect 10:67–75

Fajola AO (1978) Cultural studies in Cercospora taxonomy: I.Interrelationships between some species from Nigeria. NovaHedwigia 29:912–921

Fischer von Waldheim A (1869) Beiträge zur biologie undEntwicklungsgeschichte der Ustilagineen. Jahrbuch fürwissenschaftliche Botanik 7:61–144

Fishman L, Wyatt R (1999) Pollinator-mediated competition, repro-ductive character displacement, and the evolution of selfing inArenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733

Fournier E, Giraud T, Albertini C, Brygoo Y (2005) Partition ofthe Botrytis cinerea complex in France using multiple genegenealogies. Mycologia 97:1251–1267

Fries E (1821) Systema mycologicum 1. Gryphiswaldae, MauritiusFuckel KWGL (1863) Fungi rhenani exiccati, Fasc. I–IV. Hedwigia

2:132–136Gao X, Jackson TA, Lambert KN, Li S, Hartman GL, Niblack TL

(2004) Detection and quantification of Fusarium solani f. spglycines in soybean roots with real-time quantitative polymerasechain reaction. Plant Disease 88:1372–1380

Gaümann E (1959) Die Rostpilze Mitteleuropas. Bücheler, BernGeiser DM, Jimenez-GascoMD, 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 identifyingFusarium. Eur J Plant Pathol 110:473–479

Giraud T (2006) Selection against migrant pathogens: the immigrantinviability 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 sympatricspeciation 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, Microbotryumviolaceum. Eukaryotic Cell 7:765–775

Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence offungal plant diseases with ecological speciation. Trends EcolEvol 25:387–395

Gladieux P, Byrnes E, Fisher M, Aguileta G, Heitman J, GiraudT.(2010) Epidemiology and evolution of fungal pathogens, inplants and animals in T. M., ed. Genetics and Evolution ofInfectious Diseases. Elsevier

Gladieux P, Vercken E, Fontaine MC, Hood ME, Jonot O, Couloux A,Giraud T (2011) Maintenance of fungal pathogen species that arespecialized to different hosts: allopatric divergence and introgres-sion through secondary contact. Mol Biol Evol 28:459–471

Glienke C, Pereira OL, Stringari D, Fabris J, Kava-Cordeiro V, Galli-Terasawa L, Cunnington J, Shivas RG, Groenewald JZ, CrousPW (2011) Endophytic and pathogenic Phyllosticta species, withreference to those associated with Citrus Black Spot. Persoonia26:47–56

Goodwin SB, Dunkle LD, Dunkle LD, Zismann VL (2001)Phylogenetic analysis of Cercospora and Mycosphaerella basedon the internal transcribed spacer region of ribosomal DNA.Phytopathology 91(7):648–658

Groenewald M, Groenewald JZ, Crous PW (2005) Distinct speciesexist within the Cercospora apii morphotype. Phytopathology 95(8):951–959

Fungal Diversity

Author's personal copy

Groenewald M, Groenewald JZ, Braun U, Crous PW (2006a) Hostrange 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, CrousPW (2006b) Mating type gene analysis in apparently asexualCercospora species is suggestive of cryptic sex. Fungal GenetBiol 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 genusAnthracoidea (Basidiomycota, Ustilaginales): A molecularphylogenetic approach using LSU rDNA sequences. Mycol Res109:31–40

Hey J (2006) On the failure of modern species concepts. Trends EcolEvol 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, PowellMJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, VilgalysR, 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, HosakaK, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP,Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, MillerA, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F,Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, SampaioJP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA,Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, YaoY-J, Zhang N (2007) A higher-level phylogenetic classification ofthe Fungi. Mycol Res 111:509–547

Hsieh WH, Goh TK (1990) Cercospora species and similar fungi fromTaiwan. Maw Chang Book Company, Taiwan

Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H(2009a) Colletotrichum: a catalogue of confusion. Fungal Divers39:1–17

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, TanYP, 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, KoKoTW, Shivas RG, Summerell BA, Tan YP (2010) A case for re-inventory of Australia’s plant pathogens. Persoonia 25:50–60

James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence forlimited intercontinental gene flow in the cosmopolitan mushroomSchizophyllum commune. Evolution 53:1665–1677

Johnson EM, Valleau WD (1949) Synonomy in some common speciesof Cercospora. Phytopathology 39:763–770

Johnson JA, Harrington TC, Engelbrecht CJB (2005) Phylogeny andtaxonomy of the North American clade of the Ceratocystisfimbriata complex. Mycologia 97:1067–1092

Jülich W (1981) Higher taxa of basidiomycetes. BibliothecaMycologia 85:1–485

Kirk AM, Cannon PF, David JC, Stalpers JA (2001) Dictionary of theFungi, 9th edn. CABI Publishing, UK

Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary ofthe 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 ina group of widespread mycoparasitic fungi. Mol Ecol 20:1492–1507

Kohn LM (2005) Mechanisms of fungal speciation. Annu RevPhytopathol 43:279–308

Koufopanou V, Burt A, Szaro T, Taylor JW (2001) Gene genealogies,cryptic species, and molecular evolution in the human pathogenCoccidioides 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 isolationin wild yeast populations. Curr Biol 17:407–411

Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence ofendophytic fungi from Tripterygium wilfordii. Fungal Divers17:69–90

Kvas M, Marasas WFO, Wingfield BD, Wingfield MJ, Steenkamp ET(2009) Diversity and evolution of Fusarium species in theGibberella fujikuroi complex. Fungal Divers 34:1–21

Le Gac M, Hood ME, Fournier E, Giraud T (2007a) Phylogeneticevidence of host-specific cryptic species in the anther smutfungus. Evolution 61:15–26

Le Gac M, Hood ME, Giraud T (2007b) Evolution of reproductiveisolation within a parasitic fungal complex. Evolution 61:1781–1787

Le Gac M, Giraud T (2008) Existence of a pattern of reproductivecharacter 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 poly-merase chain reaction-restriction fragment length polymorphismdifferentiation of Tilletia walkeri and T. indica. Phytopathology91:935–940

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 A17:1–636

Liu XY, Duan JX, Xie XM (2007) Colletotrichum yunnanense sp.nov., a new endophytic species from Buxus sp. Mycotaxon100:137–144

Lutz M, Göker M, Piatek M, Kemler M, Begerow D, Oberwinkler F(2005) Anther smuts of Caryophyllaceae: molecular charactersindicate 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 revealfurther new species. Mycol Res 112:1280–1296

Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny ofthe rust fungi: an approach using nuclear large subunit ribosomalDNA sequences. Can J Bot 81:12–23

Marasas WFO, Nelson PE, Toussoun TA (1984) Toxigenic Fusariumspecies: identity and mycotoxicology. Pennsylvania StateUniversity Press, University Park

Matuo T, Snyder WC (1973) Use of morphology and matingpopulations in the identification of formae speciales in Fusariumsolani. Phytopathology 63:562–565

Mayr E (1963) Animal species and evolution. Harvard UniversityPress, Cambridge

McTaggart AR (2010) Systematics of the Ustilato-Sporisorium-Macalpinomyces complex of smut fungi. PhD thesis. QueenslandUniversity of Technology, Brisbane, Australia.

Micheli PA (1729) Nova plantarum genera. Firenze: Bernardo Paperini:1-234

Nelson PE, Tousson TA, Marasas WFO (1983) Fusarium species: anillustrated manual for identification. Pennylvania State UniversityPress, University Park

Fungal Diversity

Author's personal copy

O’Donnell K (2000) Molecular phylogeny of the Nectriahaematococca-Fusarium solani species complex. Mycologia92:919–938

O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematicsand phylogeography of the Gibberella fujikuroi species complex.Mycologia 90:465–493

O’Donnell K, Kisler HC, Tacke BK, Casper HH (2000) Genegenealogies reveal global phylogeographic structure and repro-ductive isolation among lineages of Fusarium graminearum, thefungus 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 andseven other nuclear genes supports formal recognition of ninephylogenetically distinct species within the Fusarium graminearumclade. Fungal Genet Biol 41:600–623

Park B, Park J, Cheong KC, Choi J, Jung K, Kim D, Lee YH, WardTJ, O’Donnell K, Geiser DM, Kang S (2011) Cyber infrastructurefor Fusarium: three integrated platforms supporting strain identifi-cation, phylogenetics, comparative genomics and knowledgesharing. Nucleic Acids Res 39:D640–D646

Pascoe IG, Priest MJ, Shivas RG, Cunnington JH (2005) Spores ofTilletia ehrhartae, a smut of Ehrharta calycina, are commoncontaminants of Australian wheat grain, and a potential source ofconfusion 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 Ascochytapathogens of cool season food legumes. Eur J Plant Pathol119:119–126

Perlin MH (1996) Pathovars of Formae speziales of Microbotryumviolaceum differ in electrophoretic karyotype. Int J Plant Sci157:447–452

Persoon CH (1801) Synopsis methodica fungorum. Apud HenricumDieterich, Gottingae, pp 1–708

Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophyticfungi of wild banana (Musaacuminata) at Doi Suthep PuiNational 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 Colletotrichumspecies from herbaceous plants in Thailand. Fungal Divers18:117–133

Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K,Chukeatirote E, Hyde KD (2010) Colletotrichum gloeosporioidesis not a common pathogen on tropical fruits. Fungal Divers44:33–43

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 ofColletotrichum species associated with coffee berries in ChiangMai, 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 humanpathogenic 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 plantpathogenic fungi: why it matters. Plant Dis 92:1376–1386

Rupe JC (1989) Frequency and pathogenicity of Fusarium solanirecovered from soybeans with Sudden-Death Syndrome. PlantDis 73:581–584

Seier MK, Morin L, van der Merwe M, Evans HC, Romero Á (2009)Are the microcyclic rust species Puccinia melampodii andPuccinia xanthii conspecific. Mycol Res 113:1271–1282

Shivas RG, Hyde KD (1997) Biodiversity of plant pathogenic fungi inthe 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 ofColletotrichum acutatum, introducing C. fioriniae comb. etstat. nov. and C. simmondsii sp. nov. Fungal Divers 39:111–122

Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, HillCF, Zalar P, de Hong GS, Crous PW (2007) Biodiversity in theCladosporium herbarum complex (Davidiellaceae, Capnodiales),with standardisation of methods for Cladosporium taxonomy anddiagnostics. Stud Mycol 58:105–156

Snyder WC, Hansen HN (1941) The species concept in Fusarium withreference to section Martiella. Am J Bot 28:738–742

Snyder WC, Hansen HN (1945) The species concept in Fusariumwith reference to Discolor and other sections. Am J Bot32:657–666

Starkey DE, Ward TJ, Aoki T, Gale LR, Kisler HC (2007) Globalmolecular surveillance reveals novel Fusarium head blightspecies and trichothecene toxin diversity. Fungal Genet Biol44:1191–1204

Stewart EL, Liu ZW, Crous PW, Szabo LJ (1999) Phylogeneticrelationships among some cercosporoid anamorphs of Mycos-phaerella based on rDNA sequence analysis. Mycol Res103:1491–1499

Stoll M, Piepenbring M, Begerow D, Oberwinkler F (2003) Molecularphylogeny 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 ofUstilago, Sporisorium, and related taxa based on combinedanalyses of rDNA sequences. Mycol Res 109:342–356

Su YY, Noireung P, Liu F, Hyde KD, Moslem MA, Bahkalii AH, Abe-Elsalam KA, Cai L (2011) Epitypification of Colletotrichummusae, the causative agent of banana anthracnose. Mycosciense.doi:10.1007/s10267-011-0120-9

Summerell BA, Laurence MH, Liew ECY, Leslie JF (2010) Biogeog-raphy and phylogeography of Fusarium: a review. Fungal Divers44:3–13

Sutton BC (1980) The coelomycetes. Commonwealth MycologicalInstitute, Kew, pp 1–696

Sutton BC (1992) The genus Glomerella and its anamorphColletotrichum. 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 asexualfungi: Reproduction, speciation and classification. Annu RevPhytopathol 37:197–246

Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS,Fisher MC (2000) Phylogenetic species recognition and speciesconcepts 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 geographiclimits of species: examples from the kingdom Fungi. Phil TransR Soc B Biol Sci 361:1947–1963

Tessmann DJ, Charudattan R, Kistler HC, Rosskopf EN (2001) Amolecular characterization of Cercospora species pathogenic towater hyacinth and emendation of C-piaropi. Mycologia 93(2):323–334

Tharp BC (1917) Texas parasitic fungi. Mycologia 9:105–124

Fungal Diversity

Author's personal copy

Tillet M (1755) Dissertation sur la cause qui corrompt et noircit le bleddans les épis; et sur les moyens de prévenir ces accidens.Bordeaux

To-Anun C, Hidayat I, Meeboon J (2011) Genus Cercospora inThailand: taxonomy and phylogeny (with a dichotomous key tospecies). Plant Pathology & Quarantine 1:11–87

Tode HJ (1790) Fungi Mecklenbergensis Selecti 1: 1-64Toussoun TA, Nelson PE (1975) Variation and speciation in the

fusaria. Annu Rev Phytopathol 13:71–82Tulasne 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 thepollinator guilds of Silene dioica and Silene latifolia: possibleconsequences for sympatric host race differentiation of a vectoredplant 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 Restionaceaes. 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 Cercosporaleaf 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 ofthe coffee berry disease pathogen. Colletotrichum kahawae sp.nov. Mycol Res 97:989–994

Weir BS, Johnston PR (2010) Characterisation and neotypification ofGloeosporium 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) Phyllostictacitriasiana sp. nov., the cause of Citrus tan spot of Citrusmaxima in Asia. Fungal Divers 34:23–39

Yamaoka Y (2002) Artificial culture of rust fungi. Yet-to-be-culturedmicroorganisms 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 solanispecies complex that cause infections in both humans and plantsare 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

Fungal Diversity

Author's personal copy