Colletotrichum: complex species or species ... - CBS - KNAW

Cannon et al.Boninense cladeThe boninense clade contains 17 species as defined here (see Fig.3). It forms a sister taxon to the gloeosporioides clade, and ourmultilocus analysis reveals three subclades containing 12, threeand two species respectively. Colletotrichum boninense sensustricto falls within the largest subclade. The nodal structure iscomplex and we do not see good reason to name the subcladesformally. The ITS tree (Fig. 2) shows that the boninense clade canbe detected effectively using this single locus, but it is resolved as asister clade to the truncatum rather than the gloeosporioides clade.The clade has been revised in detail by Damm et al. (2012b).Dematium cladeThe dematium clade contains the type species of the genus,Colletotrichum lineola, and was investigated by Damm et al. (2009),as part of a study of Colletotrichum species with curved conidia.As defined by ourselves, the dematium clade contains six species(Fig. 3) and forms a sister clade to a superclade consisting of theacutatum, destructivum, graminicola and spaethianum clades,along with five further outlying taxa. In the ITS tree (Fig. 2) the cladeis fairly well resolved with a Bayesian posterior probability valueof 0.89, but the structure of the superclade referred to above isless well defined. An additional species, C. hemerocallidis, closelyrelated to C. dematium, was described just before finishing thisreview (Yang et al. 2012).Colletotrichum dematium and C. truncatum (often referredto under its synonym C. capsici) have been confused historically(Sutton 1981), but are found to occupy distinct clades, with thelatter species belonging to a small clade near the base of themultilocus phylogeny (Fig. 3). Strains of the six species includedin the dematium clade appear to be characteristic of temperateenvironments, though the sample size for several of the species isinadequate to allow definite conclusions as to their climatic range.In general, members of the dematium clade are not significantin economic terms, but C. spinaciae (a pathogen of Beta andSpinacia; Gourley 1966, Washington et al. 2006) and C. circinans(attacking Allium species; Hall et al. 2007, Kim et al. 2008) bothcause substantial crop losses under some circumstances. Thesetwo plant pathogenic species occupy a well-defined subcladedistinct from a separate subclade made up of the putatively saprobicspecies C. dematium, C. lineola, C. fructi and C. anthrisci (Dammet al. 2009; Fig. 3). The type species of Colletotrichum, C. lineola,belongs to the dematium clade; it was described by Corda (1831)but treated as a synonym of C. dematium by von Arx (1957) andSutton (1981). However, research based on newly collected strainsfrom the region of the original collection showed that C. lineola andC. dematium are separable based on DNA sequence data (Dammet al. 2009).Destructivum cladeThe destructivum clade contains several important plantpathogens, but to date has not been studied in depth usingmolecular methods. Economically significant constituent taxainclude Colletotrichum destructivum, C. fuscum, C. higginsianumand C. linicola. Colletotrichum destructivum is considered to bepathogenic on lucerne (alfalfa; Medicago sativa) and soybean(Glycine max) (Manandhar et al. 1986, Latunde-Dada et al. 1999),and has also been reported to parasitise a range of unrelated plantsincluding species in the Brassicaceae, Cuscutaceae, Lamiaceaeand Solanaceae (reviewed in Hyde et al. 2009a). Colletotrichumhigginsianum is known as a pathogen of Brassicaceae (Huser etal. 2009) that is responsible for crop losses in northern temperateclimates, and was found to be related to C. destructivum byO’Connell et al. (2004). The fungus is of particular significance asthe subject of a whole-genome analysis project, and is increasinglystudied as a model for host/pathogen interactions because of itspathogenicity to the model plant Arabidopsis thaliana (Birker et al.2009, Huser et al. 2009, Kleeman et al. 2012, O’Connell et al. 2012).Colletotrichum higginsianum was reported to be synonymous withC. destructivum by Sun & Zhang (2009) based on ITS sequencesimilarity, but multilocus phylogenies of strains provisionallyaccepted as representative of C. higginsianum and C. destructivumindicate that these two species are distinct entities (O’Connell etal. 2012 and Fig. 3 of this study). Thus, although formal taxonomicwork with authentic types is still pending, it appears that as withother Colletotrichum groups, the ITS sequence is not sufficientlydifferential within the destructivum clade to act as a species-levelmarker in isolation.Colletotrichum fuscum is a pathogen of Digitalis and Nemesia(Scrophulariaceae; Tomioka et al. 2001). ITS and multilocus dataplace this species within the destructivum clade (Moriwaki et al.2002, Cannon et al. 2008; Figs 2, 3), but more detailed informationon its taxonomy and phylogenetic relationships is needed. Similarly,C. linicola was shown to belong in this clade based on ITS2/D2rDNA sequences (Latunde-Dada & Lucas 2007), and preliminarymultilocus studies indicate that the species is clearly distinct fromothers belonging to the destructivum clade (O’Connell et al. 2012;Fig 2).Glomerella truncata was described as the teleomorph of C.truncatum (Armstrong-Cho & Banniza 2006, Menat et al. 2012), butthe strains studied (from lentil (Lens culinaris) in Canada) belong tothe destructivum rather than the truncatum clade (Damm et al. 2009;O’Connell et al. 2012; Figs 2, 3). The name G. truncata remainsvalid and legitimate to represent a taxon within the destructivumclade despite the misidentification of its anamorph, but assumingthat no earlier synonyms are discovered, it will require a newname now that separate binomials for teleomorph and anamorphare prohibited (Hawksworth 2011) to avoid homonymy with C.truncatum.An outline whole-genus multilocus phylogeny (O’Connell etal. 2012) shows that the destructivum clade is monophyletic anddistinct from other clades within Colletotrichum. This is confirmedby our present multilocus study (Fig. 3), with the destructivum cladebeing resolved as a sister taxon to the combined graminicola andspaethianum clades, and it is also clearly resolved using ITS dataalone (Fig. 2). However, none of the strains sequenced in thesestudies is derived from type or authentic material for the namesused, and further research is required to elucidate species conceptsand correct nomenclature.Gloeosporioides cladeThe C. gloeosporioides species complex has been studied byWeir et al. (2012, this issue). It is a well-supported clade (Bayesianposterior probability value 1) on a very long branch and shows fewdifferences in the gene loci studied between most of the 22 speciesincluded. However it is a diverse clade in terms of morphology andincludes a number of important plant pathogens. Weir et al. (2012)recognised two subclades within the species complex based on an204