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

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Cannon et al.Table 1. (Continued).Publication Clade Host taxa Geographical limits Loci usedDamm et al. (2012a) acutatum ITS, ACT, GAPDH, CHS-1,TUB2, HIS3Damm et al. (2012b) boninense ITS, ACT, GAPDH, CHS-1,TUB2, HIS3, CALSilva et al. (2012a,b) gloeosporioides Coffee ITS, ApMAT, Apn15L,MAT1-2, MAT5L, Apn1Ex3,Apn13L, TUB2, GSWeir et al. (2012) gloeosporioides ITS, ACT, GAPDH, CHS-1,TUB2, CAL, GS, SOD2Yang et al. (2012) genus-wide Hemerocallis China ITS, ACT, GAPDH, CHS-1,TUB2cluster from strawberry and non-crop species. Crouch et al.(2006, 2009d) distinguished clades within the C. cereale clusterthat correlated with pathogenicity, with some causing diseaseof turfgrasses and others isolated from asymptomatic prairiegrasses. Gazis et al. (2011) compared Amazonian populationsof endophytic taxa belonging to the C. gloeosporioides clusterassociated with two species of Hevea, the cultivated H. brasiliensisand the non-cultivated H. guianensis. Higgins et al. (2011) studiedColletotrichum endophytes from grass and non-grass hosts intropical forest in Panama, recovering some genetically distincttaxa via direct sequence from surface-sterilised grass tissue thatwere not detected using cultural methods. They also observed thatmany taxa were detected from more than one grass host genus,corroborating observations by Lu et al. (2004) and Arnold & Lutzoni(2007) that the commonest tropical endophytes appear to be hostgeneralists. However, the ITS sequences used to define OTUs inall these studies are too conservative to reflect all speciation events(Crouch et al. 2009b, Gazis et al. 2011). Several endophyte taxaisolated from cacao in Panama by Rojas et al. (2010) were thoughtto comprise part of the background endophytic community in thePanamanian forest ecosystem, but most strains studied camefrom crop plants and their status as native species needs furtherinvestigation.All of the studies of Colletotrichum associated with non-cropplants detailed above demonstrate considerable diversity of taxa.Despite preliminary evidence that host specificity is less in nativetropical forest ecosystems compared with managed environments,the sheer number of habitats (in the form of leaves, fruits etc.) thatremain unsampled indicate the likelihood that overall species-leveldiversity of the genus is still significantly under-represented.PHYLOGENETIC POSITIONColletotrichum, as an asexual fungal genus, was included inmorphological classifications of the Ascomycota as its sexual genusGlomerella. Successive editions of the Dictionary of the Fungi untiledn 6 (Ainsworth, 1971) listed Glomerella as a member of thePhyllachoraceae in the order Sphaeriales. The Phyllachoraceaewas originally described by Theissen & Sydow (1915) as part of theDothideales. Petrak (1924) concluded that Phyllachora, Polystigmaand Physalosporina (= Stigmatula; see Cannon 1996) constituteda natural family that did not belong to the Dothideales. Chadefaud(1960) introduced (but did not validly publish) the ordinal nameGlomerellales, including Glomerella, Phyllachora and two othergenera in a non-ranked group “Eu-Glomérellales”. Barr (1976)introduced (but again did not validly publish) the ordinal namePhyllachorales, in which was included a disparate set of familieswith the Phyllachoraceae subsumed into the Melogrammataceae.Glomerella was accepted as part of that assemblage. Seven yearslater, Barr (1983) validated the ordinal name Phyllachorales butdid not explicitly alter its composition. The same year, Hawksworthet al. (1983) placed Glomerella in its traditional position in thePhyllachoraceae, but treated the family as the only representativeof the Polystigmatales, yet another name that appears not to havebeen validly published. Edition 8 of the Dictionary of the Fungi(Hawksworth et al. 1995) adopted a similar classification, thoughthe ordinal name Polystigmatales was replaced by Phyllachorales.Glomerella had long been considered to be an outlier within thePhyllachoraceae due to its non-stromatic nature (Cannon 1991).The family name Glomerellaceae was first published (invalidly)by Locquin (1984), in a general account of the fungi in which nofewer than 278 new families were introduced. Locquin’s work wasgenerally ignored, until preliminary sequence-based studies alongwith ontogenetic research (Uecker 1994) confirmed that Glomerellaand Phyllachora did not belong to the same order of fungi. TheGlomerellaceae was adopted in the 9 th edition of the Dictionary ofthe Fungi with an uncertain position within the Sordariomycetidae(Kirk et al. 2001), and in the 10 th edition as an unplaced taxon withinthe Hypocreomycetidae (Kirk et al. 2008).The first attempts to place Glomerella/Colletotrichum within amolecular phylogenetic system were published by Illingworth et al.(1991) and Berbee & Taylor (1992), using 18S rDNA sequences.Although the number of taxa sampled was insufficient to providereliable placement, the samples of C. gloeosporioides includedin these studies were shown to cluster with members of theHypocreales. Most subsequent phylogenetic studies includedGlomerella/Colletotrichum only as outgroups, or to provide an overallframework for the phylogeny of unrelated groups (e.g. Zhang &Blackwell 2002, Castlebury et al. 2004, Huhndorf et al. 2004).There is very little information available on sequences fromthe Phyllachoraceae sensu stricto. Winka & Eriksson (2000) foundthat two 18S rDNA sequences from Phyllachora species clusteredin the Sordariomycetidae clade, while Glomerella cingulata wasconsidered to be more closely related to the Hypocreomycetidae.Wanderlei-Silva et al. (2003) also published a study based on 18SrDNA, that claimed that the Phyllachoraceae was polyphyletic. Inthis work, core taxa clustered with the Sordariales, Ophiodothellavaccinii clustered within the Xylariales, and Glomerella/Colletotrichum was shown as a sister group to the Hypocreales.Zhang et al. (2006) confirmed the phylogenetic position ofGlomerella within the Hypocreomycetidae, and provided a Latin188
Colletotrichum – current status and future directionsdiagnosis for the Glomerellaceae. A sister taxon relationship withVerticillium was recovered (Zhang et al. 2006), but this clusteringappears to be an artefact of limited taxa sampling. Subsequentinvestigations assigned Verticillium to the Plectosphaerellaceae(Zare et al. 2007, Cannon et al. 2012), following the conclusions ofZare et al. (2000). The phylogenetic position of the Glomerellaceaewas further elucidated by Réblová et al. (2011) in a study usingITS, LSU, SSU and rpb2 genes. In this work, the Glomerellaceaeoccupied a common clade with two newly recognised families,the Australiascaceae and Reticulascaceae. They accordinglyvalidated the order Glomerellales (first introduced by Chadefaud1960 but without a Latin diagnosis) for the three families. Basedon SSU data, Réblová et al. (2011) showed that the Glomerellalesoccupied a well-supported clade that included the Hypocreales,Microascales and the Plectosphaerellaceae, equivalent to theHypocreomycetidae as delimited by Zhang et al. (2006). Similarresults were obtained with LSU sequence data, although theseparation of the Hypocreomycetidae was not supported bybootstrap analysis or posterior probability measures (Réblová etal. 2011). This is probably not the final word in elucidation of thephylogenetic position of Colletotrichum, but the Glomerellales cladeis well supported despite significant morphological differencesbetween the three families included.Sexual MORPHS and sexual-asexualconnectionsIn common with many other fungal pathogens, the Colletotrichumasexual morph is most commonly associated with diseasesymptoms, with the sexual morph tending to develop on moribundor dead host tissues (Sutton 1992). Colletotrichum sexual morphsare therefore under-studied in comparison with the asexual stages.This lack of attention to the sexual morphs is compounded by theneed to identify species from cultures, the preparation of which maykeep compatible strains separate. This makes it difficult to assessthe prominence of the Glomerella stages in nature compared withtheir asexual morphs.Colletotrichum sexual morphs were first described by Stoneman(1898) in the genus Gnomoniopsis Stoneman, in a comprehensiveand well-illustrated account of the development of anthracnosediseases in the USA. Four species were described in full, all ofwhich were linked to previously described asexual morphs; Gn.cingulata (anamorph Gloeosporium cingulatum, from Ligustrumvulgare), Gn. piperata (asexual Gl. piperatum, from Capsicumannuum), Gn. cincta (asexual Colletotrichum cinctum, from theorchids Maxillaria picta and Oncidium sp.) and Gn. rubicola(asexual C. rubicola, from Rubus strigosus). A fifth species, giventhe name Gnomoniopsis? vanillae (asexual Colletotrichum sp.,from Vanilla) was also described in a preliminary manner. All of thespecies accepted were linked to their asexual morphs by culturalmethods in the laboratory.Von Schrenk & Spaulding (1903) pointed out that Stoneman’sgenus was a later homonym of Gnomoniopsis Berl. (Berlese1893; type Gn. chamaemori), which is not closely related to theanthracnose pathogens. Gnomoniopsis Berl. has recently beenconfirmed as a genus of the Gnomoniaceae (Diaporthales) ratherthan the Glomerellaceae (Sogonov et al. 2008). Von Schrenk andSpaulding (1903) accordingly proposed the name Glomerella forthe anthracnose-causing species, making new combinations forthe four species definitely accepted by Stoneman in her genusand adding a fifth, Glomerella rufomaculans, considered to be thecausal agent of bitter rot of apple (see also Du et al. 2005). Thetype of Gnomoniopsis Stonem. was not originally specified, and norwas that of Glomerella. The earliest lectotypification of Glomerellaappears to be by Clements & Shear (1931), who designated Ga.cingulata as type. This choice has been accepted by subsequentauthors, most notably by von Arx & Müller (1954) and von Arx(1987).A comprehensive monograph for Glomerella has never beenpublished. The broadest treatment to date is by von Arx & Müller(1954), at a similar level of detail to the revision of Colletotrichumthree years later by von Arx (1957b). Von Arx & Müller recognisedonly five species, two of which are poorly known and cannot beconfirmed as belonging to Glomerella.Those excluded by us from von Arx & Müller’s concept ofGlomerella include Ga. guevinae (syn. Chiloëlla guevinae),which has ascospores that are covered in a gelatinous sheathand are much smaller than those of typical Glomerella species.No asexual morph has been seen. Sydow (1928) suggested thatChiloëlla has affinities with Physalospora (Hyponectriaceae) orPlagiostoma (Gnomoniaceae). Type material has not been traced,and so Chiloëlla remains of uncertain affinity. Ga. montana (syn.Physalospora montana, Phyllachora montana) was considered byParbery (1964) to have affinities with a small group of Phyllachoraspecies on montane grasses with sexual morphs that mature ondead plant tissues. Authentic material of the species in K conformswith this interpretation. Von Arx & Müller (1954) did find the typematerial to be in association with old Colletotrichum fruit-bodies,but there is no demonstrated connection between the morphs.The three species treated by von Arx & Müller (1954) thatdefinitely belong to Glomerella are the type Ga. cingulata, Ga.tucumanensis and Ga. amenti. Glomerella tucumanensis is widelyaccepted as the sexual morph of Colletotrichum falcatum, thecause of red rot of sugarcane. Work by Sutton (1968) and Crouchet al. (2009c) confirm this species as a distinct and apparentlyhost-specific pathogen using both morphological and molecularcriteria. Glomerella amenti (syn. Phyllachora amenti, Haplotheciumamenti) was described from flower stalks and bracts of the arcticalpinespecies Salix reticulata, an unexpected habitat for a speciesof Glomerella, but its phylogenetic position has been reassessed(Damm et al. 2012a), and confirmed as a synonym of C. salicis, amember of the C. acutatum clade.Glomerella cingulata is now widely recognised as a speciesaggregate and the sexual counterpart to the C. gloeosporioidesaggregate, although the connection has not been explicitly proved,and the link at species level may well be incorrect. As far as we areaware, type material of Ga. cingulata has not been examined inmodern times (though a possible authentic specimen is preservedin BPI). Similarly, the identity of Gloeosporium cingulatum Atk.,with which Ga. cingulata was linked by Stoneman (1898), has notbeen critically reassessed, and the conidia of Gloeo. cingulatum asillustrated by Stoneman could also belong to the C. acutatum clade.Shear & Wood (1907) and Edgerton (1908) considered thatat least several of the putatively host-specific taxa described byStoneman (1898) as species of Gnomoniopsis were conspecific,although they did not include material ascribed to Ga. cingulata intheir studies. The equation of the name Ga. cingulata with the speciesaggregate rather than the fungus causing disease of Ligustrum wasfurther established in works by Dastur (1920) and Small (1921,1926), which focused on cross-inoculation experiments.Since the name Glomerella cingulata was originally published,unnecessary or poorly justified taxa proliferated for the same reasonwww.studiesinmycology.org189
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Damm et al.Table 1. Strains of Coll
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Damm et al.to olivaceous grey, filt
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Damm et al.Arx JA von (1957). Die A
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Weir et al.11ICMP 17789 Malus USA1I
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Weir et al.Fig. 10. Colletotrichum
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