Abstract
Forty-four species of Colletotrichum are confirmed as present in Australia based on DNA sequencing analyses. Many of these species were identified directly as a result of two workshops organised by the Subcommittee on Plant Health Diagnostics in Australia in 2015 that covered morphological and molecular approaches to identification of Colletotrichum. There are several other species of Colletotrichum reported from Australia that remain to be substantiated by DNA sequence-based methods. This body of work aims to provide a basis from which to critically examine a number of isolates of Colletotrichum deposited in Australian culture collections.
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Introduction
Colletotrichum (Ascomycota, Sordariomycetes) is one of the most important genera of plant pathogenic fungi worldwide, having been voted as one of the top 10 fungal pathogens by 495 scientists associated with the journal Molecular Plant Pathology (Dean et al. 2012). Species of Colletotrichum affect a range of plants, often causing diseases known as anthracnose, on many field and horticultural crops (Hyde et al. 2009a). On some tropical fruits, anthracnose can cause postharvest losses of up to 100 % in the absence of control measures. Colletotrichum species are also common endophytes, epiphytes and saprobes (Hyde et al. 2009b).
According to Taylor et al. (2000), the three most common ways to recognize species are the morphological, biological, and phylogenetic species concepts. The morphological species concept has been used for fungal species descriptions and diagnoses since 1753, when Linnaeus published Species Plantarum (McNeill et al. 2012, art. 13). However, between the 1880s and the 1950s, hundreds of new Colletotrichum species were described based on thepremise that Colletotrichum species were host-specific. The first monograph of Colletotrichum was published by von Arx (1957), who accepted 11 species, based on morphological characteristics alone, disregarding the plant hosts. Later Sutton (1980) reviewed this genus and accepted 23 species, and subsequently, 39 species of Colletotrichum (Sutton 1992). The identification and classification of species of Colletotrichum has undergone a taxonomic revolution in the last decade through the application of molecular phylogenetic methods (Cai et al. 2009, Crouch et al. 2009b, Hyde et al. 2009a, b). This approach has resulted in the recognition that several single species were actually complexes or aggregates of closely related cryptic species that were morphologically indistinguishable (Cannon et al. 2012), including C. acutatum (Damm et al. 2012b), C. boninense (Damm et al. 2012a), C. caudatum (Crouch 2014), C. destructivum (Damm et al. 2014), C. gloeosporioides (Weir et al. 2012), C. gigasporum (Liu et al. 2014), C. graminicola (Crouch and Beirn 2009, Du et al. 2005), C. orbiculare (Damm et al. 2013) and C. truncatum (Damm et al. 2009). Several major revisions of these species complexes have resulted in the formal description of many new species of Colletotrichum (Cai et al. 2009, Crouch et al. 2009a, b, Crouch 2014, Damm et al. 2009, 2012a, b, 2013, 2014, Hyde et al. 2009a, b, Shivas and Tan 2009, Weir et al. 2012). Cannon et al. (2012) summarised the history of the classification of Colletotrichum, which currently has over 100 ac cepted species. The importance of using a polyphasic approach to species delimitation in Colletotrichum, together with a large sample size, was emphasised in a recent study (Liu et al. 2016) that showed the apparent C. siamense species complex (Sharma et al. 2015) was a single species.
Very little is known about the biology, pathogenicity, host range and geographical distribution of many of the recently recognised species of Colletotrichum. This has created a dilemma for plant pathologists. Hyde et al. (2010) first noted that there was an urgent need to reassess inventories of many plant pathogenic genera, including Colletotrichum, in Australia where the effectiveness of biosecurity measures relies heavily on the accuracy of specimen-based databases of plant pathogens (Shivas et al. 2006). Hyde et al. (2010) recognised that the revision of checklists must be supported by examination of herbarium specimens, living cultures and DNA libraries.
Two complementary workshops were held in Australia in 2015 as part of annual training offered to the National Plant Biosecurity Diagnosticians Network in order to ensure Australian plant biosecurity diagnosticians were introduced to taxonomic changes and diagnostic challenges that surround recent changes in the taxonomy of Colletotrichum species. The workshops were funded by Plant Health Australia and arranged by the Subcommittee on Plant Health Diagnostics. The first workshop introduced the species complexes with a focus on morphology and biology. The second workshop introduced molecular and phylogenetic methods as applied to DNA sequence data obtained from isolates of Colletotrichum. Both workshops emphasised practical methods with more than 80 isolates examined from several Australian culture collections. Information gathered from these two workshops formed the basis for an up-to-date inventory of Colletotrichum species in Australia based on molecular phylogenetic evidence.
Materials and methods
Specimens and species identification
Living cultures of 86 specime ns were sourced fr om Austral ian plant pathogen culture collections, including BRIP (Queensland), DAR (New South Wales), VPRI (Victoria) and WAC (Western Australia). A literature and database search found a further 106 Australian specimens with publically accessible evidence of DNA sequence data from previous studies. This DNA sequence data was sourced from GenBank (http://www.ncbi.nlm.nih.gov) (Benson et al. 2013), and the Q-bank Fungi database (a reference database for mycological phytopathology, http://www.q-bank.eu/Fungi/). Confirmation that species of Colletotrichum occurred in Australia required that the specimen had an unambiguous DNA sequence that matched data from the ex-type specimen.
DNA extraction, PCR amplification and DNA sequencing
Mycelia were collected from cultures grown on potato dextrose agar (DifcoTM, Becton, Dickinson and Company, New Jersey, USA) and macerated with 0.5 mm glass beads (Daintree Scientific) in a Tissue Lyser (QIAGEN). Genomic DNA was extracted with the Gentra Puregene DNA Extraction kit (QIAGEN) or with ISOLATE II Plant DNA kit (Bioline) according to the manufacturers’ instructions. Gene sequences were obtained from up to four nuclear gene regions for species identifications. These are glyceraldehyde-3-phosphate dehydrogenase (GAPDH), glutamine synthetase (GS), the internal transcribed spacer (ITS), and β-tubulin 2 (TUB). Primers used in this study are shown in Table 1. Where the standard GS primers (Stephenson et al. 1997) sequenced poorly, the primers from Weir et al. (2012) were used instead. All gene regions were amplified with the Phusion High-Fidelity PCR Master Mix (New England Biolabs). The PCR products were purified with the QIAquick PCR Purification Kit (QIAGEN), and sequenced on the 3730xl DNA Analyzer (Applied Biosystems) by a commercial company (Macrogen Incorporated, Korea) using the amplifying primers. All sequences generated were assembled using Geneious v. 9.1 (Biomatters Ltd), and deposited in GenBank (Table 2, in bold). These sequences were compared against those from type specimens using BLASTn (https://blast.ncbi.nlm.nih.gov/Blast.cgi).
Results
The names of Australian Colletotrichum species that were verified by DNA sequence analysis are given in the following numbered list. This list contains only species that were verified by comparison of their DNA sequence data against type specimens. The GenBank accession numbers of sequences generated in this study are provided in Table 2 (in bold font) together with reference sequences generated in other studies (Roman font).
Australian species of Colletotrichum verified by DNA sequence data
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1.
xColletotrichum acutatum J.H. Simmonds, Queensland Journal of Agricultural and Animal Science 25: 178A (1968).
Colletotrichum acutatum was first described from Redlands Horticultural Research Station, Cleveland, Queensland on papaya (Carica papaya) by Simmonds (1965, 1968). This species has since been recognised as an important pathogen that causes anthracnose on a range of plants worldwide. However, C. acutatum has long been recognised as a complex of closely related species that have conidia with acute ends (Simmonds 1965). The chequered taxonomic history of C. acutatum was summarized by Damm et al. (2012b), who designated an epitype that has ultimately provided taxonomic stability for this species. In Australia, C. acutatum is widespread and known to cause diseases or be associated with disease symptoms on a range of plants, including papaya, strawberry, olives and pistachio. The literature indicates that the C. acutatum species complex may have a much wider host range in Australia, where it has been reported to cause diseases on avocado, tomato (Simmonds 1965), grapes (Melksham et al. 2002, Whitelaw-Weckert et al. 2007), olive (Spooner-Hart et al. 2007) and almond (McKay et al. 2009). However, many of these records require verification. Colletotrichum acutatum can be distinguished from other species in the C. acutatum species complex by any of the six genes analysed in Damm et al. (2012b). The Australian specimens of C. acutatum were identified based on the 100 % identity of ITS, GS and/or TUB sequences to C. acutatum ex-type strain CBS 112996 (Table 2).
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2.
Colletotrichum alcornii J.A. Crouch, IMA Fungus 5: 27 (2014).
Colletotrichum alcornii belongs to the Colletotrichum caudatum species complex (Crouch 2014). Colletotrichum alcornii is only known from two native Australian grass species in south-east Queensland. Although morphologically similar to four other species in the C. caudatum species complex, C. alcornii is easily distinguished based on ITS sequences (Crouch 2014).
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3.
Colletotrichum alienum B.S. Weir & P.R. Johnst., Studies in Mycology 73: 139 (2012).
Colletotrichum alienum belongs to the C. gloeosporioides species complex (Weir et al. 2012). In Australia, C. alienum has been reported from avocado (Weir et al. 2012), Grevillea sp. (Liu et al. 2013b), Protea spp. (Crous et al. 2013) and Nerium oleander (oleander) (Schena et al. 2014). Colletotrichum alienum was identified as a serious anthracnose pathogen of Proteaceae in South Africa, Europe and Australia (Liu et al. 2013b, Crous et al. 2013). Colletotrichum alienum is best distinguished from other species in the C. gloesporioides species complex using GS sequences. The Australian specimens of C. alienum were identified based on the 99–100 % identity of GS sequences to C. alienum ex-type strain ICMP 12071 (Table 2).
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4.
Colletotrichum aotearoa B. Weir & P.R. Johnst. Studies in Mycology 73: 139 (2012).
Colletotrichum aotearoa belongs to the C. gloeosporioides species complex (Weir et al. 2012). Colletotrichum aotearoa was first reported from Australia on Banksia marginata (Liu et al. 2013b) in a study of Colletotrichum species on Proteaceae. Colletotrichum aotearoa can be distinguished from other species in the C. gloesporioides species complex with GAPDH, GS and/or TUB sequences (Weir et al. 2012). The Australian specimens of C. aotearoa were identified based on the 99–100 % identity of GS sequences to the C. aotearoa ex-type strain ICMP 18537 (Table 2).
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5.
Colletotrichum asianum Prihastuti, L. Cai & K.D. Hyde, Fungal Diversity 39: 96 (2009).
Colletotrichum asianum belongs to the C. gloeosporioides species complex (Weir et al. 2012). In Australia, C. asianum has only been isolated from mango, on which it is associated with a range of disease symptoms (Weir et al. 2012; Anderson et al. 2013 as C. gloeosporioides, James et al. 2014). Colletotrichum asianum can be distinguished from other species in the C. gloeosporioides species complex by any of the eight genes analysed in Weir et al. (2012). The Australian specimens of C. asianum were identified based on the 99–100 % identity of ITS, and/or TUB sequences to C. asianum ex-type strain MFLU 090234 (Table 2).
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6.
Colletotrichum australe Damm, P.F. Cannon & Crous, Studies in Mycology 73: 57 (2012b).
Colletotrichum australe belongs to the C. acutatum species complex, and is distinguishable by either GAPDH, histone 3, ITS or TUB sequences (Damm et al. 2012b).
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7.
Colletotrichum axonopodi J.A. Crouch, B.B. Clarke, J.F. White & B.I. Hillman, Mycologia 101: 727 (2009).
Colletotrichum axonopodi belongs to the C. graminicola species complex, which comprises predominantly grass infecting species with falcate spores (Cannon et al. 2012). Colletotrichum axonopodi can be identified by its unique ITS sequence and association with leaf spots on some species of Axonopus (Crouch et al. 2009a).
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8.
Colletotrichum boninense Moriwaki, Toy. Sato & Tsukib., Mycoscience 44: 48 (2003).
Damm et al. (2012a) resolved the C. boninense species complex with multilocus phylogenetic analyses, describing several new species. Colletotrichum boninense is best identified by ITS and GAPDH sequences (Damm et al. 2012a). Damm et al. (2012a) reported C. boninense from Leucospermum sp. in Australia without specimen collection details (CBS 112115). Colletotrichum boninense has been reported as a pathogen and an endophyte on a range of plant species worldwide (Hyde et al. 2009a).
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9.
Colletotrichum brevisporum Noireung, Phouliv., L. Cai & K.D. Hyde, Cryptogamie Mycologie 33: 350 (2012).
This is the first record of C. brevisporum in Australia. Colletotrichum brevisporum has been recorded as an endophyte as well as a pathogen on a range of host plant species in several tropical countries. Colletotrichum brevisporum can be identified based on sequence identity of ITS, GAPDH and/or TUB (Noireung et al. 2012). The Australian specimens of C. brevisporum have been identified based on the 100 % identity of ITS sequences to C. brevisporum ex-type strain BCC 38876 (Table 2).
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10.
Colletotrichum brisbanense Damm. P.F. Cannon & Crous, Studies in Mycology 73: 59 (2012b).
Colletotrichum brisbanense belongs to the C. acutatum species complex (Damm et al. 2012b). This species is only known from the type specimen. Colletotrichum brisbanense was described from one of Simmonds’ (1968) paratype specimens of C. acutatum, which Shivas & Tan (2009) had assigned to C. simmondsii. GAPDH and TUB sequences clearly separate C. brisbanense and C. simmondsii (Damm et al. 2012b).
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11.
Colletotrichum chlorophyti S. Chandra & Tandon [as chlorophytumi], Current Science 34: 565 (1965).
In North America, C. chlorophyti has been reported as the cause of anthracnose in soybean (Glycine max) (Yang et al. 2012). The only Australian specimen was deposited in the CBS culture collection as C. dematium (Table 2). A multilocus phylogenetic analysis re-identified it as C. chlorophyti (Damm et al. 2009). The extent to which C. chlorophyti is responsible for anthracnose on Stylosanthes hamata in Australia is not known.
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12.
Colletotrichum circinans (Berk.) Voglino, Annali della Reale Academia d’Agricoltura di Torino 49: 175 (1907).
Colletotrichum circinans belongs to the C. dematium clade (Cannon et al. 2012). There are records of C. circinans in Australia from onion, shallot and leeks (Allium spp.) with smudge and bulb rot (Hall et al. 2009, Persley et al. 2010). The only Australian specimen has been identified based on the 100 % identity of ITS and GAPDH sequences to C. circinans ex-type strain CBS 221.81 (Table 2).
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13.
Colletotrichum coccodes (Wallr.) S. Hughes, Canadian Journal of Botany 36: 754 (1958).
Colletotrichum coccodes was recently neotypified (Liu et al. 2011), which stabilized the taxonomic concept of this species. Prior to this, C. coccodes was reported as the causal agent of brown root rot of tomato (Golzar 2009b) and black dot of potato (Ben-Daniel et al. 2010). Most isolates identified as C. coccodes in Australian culture collections require validation by molecular phylogenetic analyses. The Australian specimens have been identified based on the 100 % identity of ITS, GAPDH and/or TUB sequences to C. coccodes ex-type strain CBS 164.49 (Table 2).
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14.
Colletotrichum cymbidiicola Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, Studies in Mycology 73: 19 (2012a).
Colletotrichum cymbidiicola belongs to the C. boninense species complex (Damm et al. 2012a). Colletotrichum cymbidiicola causes anthracnose on Cymbidium spp. in Australia, India, Japan, New Zealand and USA (Damm et al. 2012a, Chowdappa et al. 2014, Bethke 2014), and is likely present in all countries where Cymbidium orchids are grown. The only Australian specimen (Table 2) is the holotype of C. cymbidiicola (Damm et al. 2012a).
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15.
Colletotrichum dematium (Pers.) Grove, Journal of Botany, British and Foreign Legion, London 56: 341 (1918).
Damm et al. (2009) designated an epitype for C. dematium derived from a culture isolated from a dead leaf of Eryngium campestre collected in France. Colletotrichum dematium has a wide host range with pathogenic, saprobic and endophytic strains (Damm et al. 2009). Although C. dematium has been claimed to cause several economically important diseases, this has rarely been demonstrated. The only Australian specimen (Table 2) was included in the study by Damm et al. (2009). Most isolates identified as C. dematium in Australian culture collections require validation by molecular phylogenetic analyses.
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16.
Colletotrichum destructivum O’Gara, Mycologia 7: 38 (1915).
Colletotrichum destructivum is a species complex that was recently revised by Damm et al. (2014) who designated an epitype for C. destructivum. Colletotrichum destructivum can be identified by its ITS and TUB2 sequences. In Australia, two isolates from pasture legumes (Ford et al. 2004) have ITS sequences identical to those of the epitype.
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17.
Colletotrichum dracaenophilum D.F. Farr & M.E. Palm, Mycological Research 110: 1401 (2006).
Colletotrichum dracaenophilum is a stem pathogen of Dracaena spp. (Farr et al. 2006). Colletotrichum dracaenophilum occupies a small clade that is basal to the entire genus, apart from the combined C. orbiculare and C. cliviae clade (Cannon et al. 2012). The Australian records have been identified based on the 100 % identity of ITS and GAPDH sequences to C. dracaenophilum ex-type strain CBS 118199 (Table 2).
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18.
Colletotrichum fioriniae (Marcelino & S. Gouli) R.G. Shivas & Y.P. Tan, Fungal Diversity 39: 117 (2009).
Colletotrichum fioriniae belongs to the C. acutatum species complex. Colletotrichum fioriniae was originally described as an entomopathogen from a scale insect in the USA, where it has also been reported as an endophyte in several plants (Marcelino et al. 2008). In Australia, C. fioriniae has been reported as the cause of leaf and stem blight on Acacia acuminata (Golzar 2009a as C. acutatum) and fruit rot of avocado (Shivas and Tan 2009). Colletotrichum fioriniae is readily identified by any of the six genes analysed by Damm et al. (2012b).
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19.
Colletotrichum fructicola Prihastuti, L.Cai & K.D. Hyde, Fungal Diversity 39: 158 (2009).
Colletotrichum fructicola belongs to the C. gloeosporioides species complex (Weir et al. 2012). Little is known about the host range and pathogenicity of this species in Australia. Colletotrichum fructicola can be distinguished from other species in the C. gloesporioides species complex with GS sequences (Weir et al. 2012).
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20.
Colletotrichum gloeosporioides (Penz.) Penz. & Sacc., Atti del Reale Istituto Veneto di Scienze, Lettere ed Arti, Serie 6, 2: 670 (1884).
Colletotrichum gloeosporioides is a name well known to plant pathologists. A major revision of Colletotrichum by von Arx (1957) based on morphology rather than host association, reduced the number of accepted species from 750 to 11, with the vast majority reduced to synonymy with C. gloeosporioides. This left C. gloeosporioides as a biologically and genetically diverse species associated with at least 470 different host genera (Sutton 1980). Cannon et al. (2008) epitypified C. gloeosporioides with a specimen and living culture from Citrus sinensis collected from Italy. In a major revision, Weir et al. (2012) used multilocus sequence analyses to resolve the C. gloeosporioides species complex into a number of segregate species. The species that gives its name to this complex, C. gloeosporioides, was found to be commonly associated with Citrus, although it also occurred on other host species (Weir et al. 2012).
Although C. gloeosporioides has been implicated as an important pathogen of a wide range of plants in Australia, there are relatively few published records that can be verified by DNA sequence data. The situation is similar for most applications of the name C. gloeosporioides in much of the plant pathology literature worldwide. The extent of the problem was highlighted by Cai et al. (2009), who estimated that more than 86 % of the records of C. gloeosporioides in GenBank had sequences that diverged considerably from the epitype and were likely to represent other species. Further, Phoulivong et al. (2010) considered that C. gloeosporioides was not a common pathogen on tropical fruits. In Australia, C. gloeosporioides has been recorded from cultivated Citrus spp. (Schena et al. 2014) and pecan (Weir et al. 2012). Colletotrichum gloeosporioides can be distinguished from other species in the C. gloeosporioides species complex by any of the eight genes analysed in Weir et al. (2012). The Australian records of C. gloeosporioides have been identified based on the 100 % identity of ITS, GAPDH and/or TUB sequences to the C. gloeosporioides ex-type strain IMI 356878 (Table 2).
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21.
Colletotrichum godetiae Neerg., Friesia 4: 72 (1950).
Colletotrichum godetiae belongs to the C. acutatum species complex (Damm et al. 2012b). Colletotrichum godetiae is recorded as a pathogen of fruit, leaves and stems of Fragaria, Malus and Prunus, mainly in Europe and Western Asia (Damm et al. 2012b). These are new records for Australia. Colletotrichum godetiae can be distinguished from other species in the C. acutatum species complex by any of the six genes analysed in Damm et al. (2012b). The Australian records of C. godetiae have been identified based on the 100 % identity of ITS and/or TUB sequences to C. godetiae ex-type strain CBS 133.44 (Table 2).
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22.
Colletotrichum kahawae subsp. ciggaro B. Weir & P.R. Johnst., Studies in Mycology 73: 158 (2012).
Colletotrichum kahawae subsp. ciggaro belongs to the C. gloeosporioides species complex (Weir et al. 2012). Colletotrichum kahawae subsp. ciggaro has a broad host range and worldwide distribution. It differs only in one gene, glutamine synthetase, from the African coffee berry disease pathogen, C. kahawae subsp. kahawae, which is not present in Australia (Weir et al. 2012). The only Australian record listed in Table 2 is the ex-type culture of C. kahawae subsp. ciggaro (Weir et al. 2012).
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23.
Colletotrichum karsti You L. Yang, Zuo Y. Liu, K.D. Hyde & L. Cai [as ‘karstii’], Cryptogamie Mycologie 32: 241 (2011).
Colletotrichum karsti belongs to the C. boninense species complex (Damm et al. 2012a). Due to the high variation observed in morphology and sequences, a polyphasic approach is recommended to ensure accurate identification (Damm et al. 2012a). In Australia, C. karsti has a wide host range, although its role as a pathogen is not known.
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24.
Colletotrichum lupini (Bondar) Damm, P.F. Cannon & Crous, Studies in Mycology 73: 78 (2012).
Colletotrichum lupini belongs to the C. acutatum species complex (Damm et al. 2012b). Colletotrichum lupini is an economically important pathogen of lupin crops worldwide, including Australia, where it was first detected in Western Australia in 1994 (Sweetingham et al. 1995, Yang and Sweetingham 1998, as C. gloeosporioides). Colletotrichum lupini has established in Western Australia, where it has spread through wild populations of blue lupins (Lupinus cosentinii), as well as in parts of South Australia, where it is known to occur in Lupinus albus. Colletotrichum lupini is not known to occur in the lupin growing regions in New South Wales (Anon. 2015) or Victoria (Thomas 2010). Colletotrichum lupini can be distinguished from other species in the C. acutatum species complex by most of the six genes (excluding actin) analysed by Damm et al. (2012b), with TUB providiving the best resolution. The Australian records of C. lupini have been identified based on the 100 % identity of ITS, GAPDH and/or TUB sequences to C. lupini ex-type strain CBS 109225 (Table 2).
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25.
Colletotrichum musae (Berk. & M.A. Curtis) Arx, Verhandelingen Koninklijke Nederlandse Akademie van Wetenschappen, Sect. 51: 107 (1957).
Colletotrichum musae belongs to the C. gloeosporioides species complex (Weir et al. 2012). Su et al. (2011) designated an epitype for C. musae from banana (Musa sp.) fruit in the USA, collected from the geographic locality of the type. In Australia, C. musae has been associated with several banana diseases, including anthracnose, fruit speckle, black end and crown rot (Cooke et al. 2009). However, many of these records require verification by molecular methods. Colletotrichum musae can be distinguished from other species in the C. gloeosporioides species complex by any of eight genes analysed by Weir et al. (2012). The Australian records of C. musae have been identified based on the 100 % identity of ITS, GAPDH and/or TUB sequences to C. musae ex-type strain CBS 116870 (Table 2).
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26.
Colletotrichum nymphaeae (Pass.) Aa, Netherlands Journal of Plant Pathology, Supplement 1 84: 110 (1978).
Colletotrichum nymphaeae belongs to the C. acutatum species complex (Damm et al. 2012b). Colletotrichum nymphaeae was determined as the causal agent of celery stunt disease in Japan (Yamagishi et al. 2015). This raises the possibility that celery leaf curl disease in Queensland, which was attributed to C. acutatum sensu lato (Heaton and Dullahide 1993), may be caused by C. nymphaeae. Colletotrichum nymphaeae is easily distinguished from other species in the C. acutatum species complex with TUB (Damm et al. 2012b). The Australian records of C. nymphaeae have been identified based on the 100 % identity of TUB sequences to C. nymphaeae ex-type strain CBS 515.78 (Table 2).
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27.
Colletotrichum ocimi Damm, Studies in Mycology 79: 70 (2014).
Colletotrichum ocimi belongs to the C. destructivum species complex (Damm et al. 2014). Persley et al. (2010) reported that black spot of basil, caused by C. ocimi (as C. gloeosporioides), is a minor disease in Australia. Colletotrichum ocimi is easily distinguished from other species in the C. acutatum species complex by its unique ITS and TUB sequences (Damm et al. 2014). The Australian record of C. ocimi was identified based on the 100 % identity of ITS sequence to C. ocimi ex-type strain CBS 298.94 (Table 2).
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28.
Colletotrichum orbiculare Damm, P.F. Cannon & Crous, Fungal Diversity 61: 39 (2013).
Colletotrichum orbiculare sensu Damm et al. (2013) was recently described and pragmatically given the same name as the earlier invalid name C. orbiculare sensu von Arx (1957), which is well known in the plant pathology literature worldwide as a pathogen of host plants in the Cucurbitaceae. In Australia, C. orbiculare sensu lato has been associated with diseases on several plant species in the Asteraceae, Cucurbitaceae and Fabaceae (Auld et al. 1994 as C. lagenarium, Simmonds 1965, Walker et al. 1991, Persley et al. 2010). However, most of these records require verification by molecular methods. The only verified Australian specimen (Table 2) was included in the study by Damm et al. (2013)
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29.
Colletotrichum petchii Damm, P.F. Cannon & Crous, Studies in Mycology 73: 29 (2012a).
Colletotrichum petchii belongs to the C. boninense species complex (Damm et al. 2012a). This fungus appears to be host specific to Dracaena spp., which are native to Africa (Damm et al. 2012a). The Australian record of C. petchii was identified based on the 100 % identity of ITS and GAPDH sequences to C. petchii ex-type strain CBS 378.94 (Table 2).
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30.
Colletotrichum phormii (Henn.) D.F. Farr & Rossman, Mycological Research 110: 1403 (2006).
Colletotrichum phormii belongs to the C. acutatum complex (Damm et al. 2012b). Colletotrichum phormii was first reported in Australia in 2010 from Perth, WA, based on the ITS sequence of isolate WAC 12416 (Golzar and Wang 2010). However, this record cannot be verified as there is no living culture available and the sequence data was not deposited in GenBank. Colletotrichum phormii is separated from other species in the C. acutatum species complex by sequences of secondary genes, namely TUB, GAPDH, histone and actin (Damm et al. 2012b). The Australian record of C. phormii was identified based on the 100 % identity of TUB sequences to C. phormii ex-type strain CBS 118194 (Table 2).
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31.
Colletotrichum pyricola Damm, P.F. Cannon & Crous, Studies in Mycology 73: 94 (2012b).
Colletotrichum pyricola belongs to the C. acutatum species complex (Damm et al. 2012b). This fungus was first described from fruit rot of pear (Pyrus communis) in New Zealand. Colletotrichum pyricola can be distinguished from other species in the C. acutatum species complex with GAPDH and TUB (Damm et al. 2012b). The Australian record of C. pyricola was identified based on the 100 % identity of GAPDH and TUB sequences to C. pyricola ex-type strain CBS 128531 (Table 2).
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32.
Colletotrichum queenslandicum B. Weir & P.R. Johnst., Studies in Mycology 73: 164 (2012).
Colletotrichum queenslandicum belongs to the C. gloeosporioides species complex (Weir et al. 2012). This fungus was first described from Queensland as C. gloeosporioides var. minor Simmonds (1968), who regarded this fungus as an important cause of fruit rot in avocado and papaya, as well as a wide range of other hosts (Simmonds 1965, 1966). A new name, C. queenslandicum, was given to this taxon as the orthographically correct species epithet minus was already occupied by C. minus Zimm. In Australia, C. queenslandicum has been reported from avocado (Weir et al. 2012), lychee (Anderson et al. 2013 as C. gloeosporioides), passionfruit (James et al. 2014) and pawpaw (Weir et al. 2012). Colletotrichum queenslandicum is best distinguished from other species in the C. gloeosporioides species complex by GAPDH, GS or TUB sequences (Weir et al. 2012). The Australian specimens of C. queenslandicum were identified based on the 100 % identity of GAPDH and/or TUB sequences to C. queenslandicum ex-type strain ICMP 1778 (Table 2).
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33.
Colletotrichum salicis (Fuckel) Damm, P.F. Cannon & Crous, Studies in Mycology 73: 97 (2012b).
Colletotrichum salicis belongs to the C. acutatum species complex (Damm et al. 2012b). This fungus was first reported on Salix spp. from mainland Australia as Glomerella miyabeana (Cunnington et al. 2007), which is considered a synonym of C. salicis by Damm et al. (2012b). Colletotrichum salicis is best distinguished from other species in the C. acutatum species complex with GAPDH or TUB sequences (Damm et al. 2012b). The Australian specimens of C. salicis were identified based on the 99–100 % identity of GAPDH and/or TUB sequences to C. salicis ex-type strain CBS 607.94 (Table 2).
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34.
Colletotrichum sansevieriae Miho Nakam. & Ohzono, Journal of General Plant Pathology 72: 253 (2006).
Colletotrichum sansevieriae causes leaf anthracnose on Sansevieria spp., which are native to Africa and Asia. The only Australian specimen (Table 2) was collected in 2008 (Aldaoud et al. 2011).
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35.
Colletotrichum siamense Prihastuti, L. Cai & K.D. Hyde, Fungal Diversity 39: 98 (2009).
Colletotrichum siamense belongs to the C. gloeosporioides species complex (Weir et al. 2012). In Australia, C. siamense has a diverse host range (Weir et al. 2012, James et al. 2014, Schena et al. 2014), although its role as a pathogen is unclear. Colletotrichum siamense is best distinguished from other species in the C. gloeosporioides species complex with TUB (Weir et al. 2012). The Australian specimens of C. siamense were identified based on the 100 % identity of TUB sequences to C. siamense ex-type strain ICMP 18578 (Table 2).
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36.
Colletotrichum simmondsii R.G. Shivas & Y.P. Tan, Fungal Diversity 39: 119 (2009).
Colletotrichum simmondsii belongs to the C. acutatum species complex (Damm et al. 2014). In Australia, C. simmondsii has been associated with fruit rots of papaya, strawberry, tomato and blueberry (Shivas and Tan, 2009). Colletotrichum simmondsii is easily distinguished from other species in the C. acutatum species complex with ITS or TUB sequences (Damm et al. 2012b). The Australian specimens of C. simmondsii were identified based on the 100 % identity of ITS and/or TUB to C. simmondsii ex-type strain BRIP 28519 (Table 2).
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37.
Colletotrichum sloanei Damm. P.F. Cannon & Crous., Studies in Mycology 73: 103 (2012b).
Colletotrichum sloanei belongs to the C. acutatum species complex (Damm et al. 2012b). Little is known about the host range and pathogenicity of this species. Colletotrichum sloanei is best distinguished from other species in the C. acutatum species complex with GAPDH or TUB sequences (Damm et al. 2012b). The Australian specimens of C. sloanei were identified based on the 100 % identity of GAPDH and TUB sequences to C. sloanei ex-type strain IMI 364297 (Table 2).
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38.
Colletotrichum spinaciae Ellis & Halst., Journal of Mycology 6: 34 (1890).
Colletotrichum spinaciae belongs to the C. dematium clade (Cannon et al. 2012). In Victoria, C. spinaciae (as C. dematium) was shown to cause anthracnose on spinach when it was first detected in 2004 (Washington et al. 2006). This detection invoked a biosecurity response of interstate surveys, which found that anthracnose on spinach was widespread in eastern Australia, resulting in no further quarantine action (Washington et al. 2006). The Australian specimens of C. spinaciae were identified based on the 100 % identity of ITS and GAPDH sequences to C. spinaciae ex-epitype strain CBS 128.57 (Table 2).
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39.
Colletotrichum spinosum Damm & P.F. Cannon, Fungal Diversity 61:46 (2013).
Colletotrichum spinosum belongs to the C. orbiculare species complex (Damm et al. 2013). Colletotrichum spinosum is a common pathogen of Xanthium spinosum in eastern Australia, where it caused seedling blight and stem anthracnose (Veitch 1942, Butler 1951, Anderson and Walker 1962, Simmonds 1965, 1966, Walker et al. 1991). In pathogenicity tests, the ex-holotype isolate was found to be highly virulent on Xanthium spp. as well as some other Asteraceae, and further infected some species of Cucurbitaceae, Fabaceae and Myrtaceae (Walker et al. 1991). It has been evaluated as a mycoherbicide for the biological control of Xanthium spinosum in Australia (Auld et al. 1988, 1990, Auld & Say 1999). Colletotrichum spinosum can be easily identified based on GAPDH, GS and/or TUB2 sequences (Damm et al. 2013).
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40.
Colletotrichum tanaceti M. Barimani et al., Plant Pathology 62: 1252 (2013).
Colletotrichum tanaceti belongs to the C. destructivum species complex (Damm et al. 2014). Colletotrichum tanaceti is a serious pathogen of pyrethrum in northern Tasmania (Barimani et al. 2013). The only Australian specimen (Table 2) is the holotype of C. tanaceti, which was distinguished from other Colletotrichum spp. by GAPDH, ITS and TUB sequences (Barimani et al. 2013)
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41.
Colletotrichum theobromicola Delacr., Bull. Soc. Mycol. France 31: 191 (1905).
Colletotrichum theobromicola belongs to the C. gloeosporioides species complex (Weir et al. 2012). Colletotrichum theobromicola has been reported on several diverse host species in Australia (James et al. 2014, Schena et al. 2014). The Type A and Type B isolates of C. gloeosporioides f. stylosanthis were shown to be pathogenic on Stylosanthes in northern Australia (Irwin & Cameron 1978). These isolates were subsequently named C. gloeosporioides f. stylosanthis “f. sp. guianensis” and C. gloeosporioides f. stylosanthis “f. sp. stylosanthis”, respectively, by Munaut et al. (2002). Weir et al. (2012) considered these names synonyms of C. theobromicola. Colletotrichum theobromicola can be distinguished from other species in the C. gloeosporioides species complex by any of the eight genes analysed in Weir et al. (2012). The Australian specimens of C. theobromicola have been identified based on the 100 % identity of ITS and/or TUB sequences to C. theobromicola ex-type strain CBS 124945 (Table 2).
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42.
Colletotrichum tofieldiae (Pat.) Damm, P.F. Cannon & Crous, Fungal Diversity 39: 77 (2009).
Colletotrichum tofieldiae was previously treated as a variant of C. dematium var. minus, but was confirmed as a distinct species after an epitype was designated (Damm et al. 2009). Colletotrichum tofieldiae has been reported as an endophyte (Tao et al. 2013, Hiruma et al. 2016). Its role as a pathogen is unknown. The Australian specimens of C. tofieldiae were identified based on the 100 % identity of ITS and TUB sequences to C. tofieldiae ex-type strain CBS 495.85 (Table 2).
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43.
Colletotrichum truncatum (Schwein.) Andrus & W.D. Moore, Phytopathology 25: 122 (1935).
In Australia, most records of this fungus (e.g. Ford et al. 2004) still require verification by molecular methods. Worldwide, C. truncatum causes anthracnose diseases of many hosts in the Solanaceae and Fabaceae (Damm et al. 2009). An epitype from Phaseolus lunatus in the USA was designated by Damm et al. (2009), who used multilocus phylogenetic analyses to show that C. capsici and C. curvatum were synonyms of C. truncatum. The Australian specimens of C. truncatum were identified based on the 100 % identity of ITS sequences to C. truncatum ex-type strain CBS 151.35 (Table 2).
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44.
Colletotrichum xanthorrhoeae R.G. Shivas, Bathgate & Podger, Mycological Research 102: 280 (1998).
Colletotrichum xanthorrhoeae belongs to the C. gloeosporioides species complex (Weir et al. 2012). Colletotrichum xanthorrhoeae was widespread in Western Australia, where it caused a leaf spot disease on Xanthorrhoea spp. (Shivas et al. 1998). Colletotrichum xanthorrhoeae can be easily identified by its distinctive morphology, very slow growth rate in culture, and its unique ITS sequence (Weir et al. 2012).
Discussion
The species listed above have been verified by molecular phylogenetic analyses. There are several other names of Colletotrichum species that have been either (i) reported in the scientific literature as occurring in Australia, or (ii) listed (often unpublished) in culture collections of Australian isolates, which have yet to be verified by DNA sequence analyses. Some omissions from the Australian list of verified names are worthy of comment, in particular, C. lindemuthianum (Sacc. & Magnnus) Briosi & Cavara, C. graminicola (Ces.) G.W. Wilson and C. sublineola Henn. ex Sacc. & Trotter. Colletotrichum lindemuthianum, belongs to the C. orbiculare species complex (Damm et al. 2013) and is the causal agent of anthracnose of common bean (Phaseolus vulgaris) (Cruickshank 1966), although it has been practically eradicated from commercial production in Australia (Persley et al. 2010). The name C. lindemuthianum was only recently stabilised with the designation of an epitype (Liu et al. 2013a). Liu et al. (2013a) also noted that very few studies of C. lindemuthianum incorporated DNA sequence analysis, which is the case in Australia and explains its absence from our list. Colletotrichum graminicola and C. sublineola belong to a monophyletic clade of species with falcate conidia that are mostly host specific on grasses (Crouch et al. 2009a, b, Cannon et al. 2012). Worldwide, C. graminicola and C. sublineola are important pathogens of maize (Zea mays) and corn (Sorghum spp.), respectively (Crouch and Beirn 2009), yet rarely important in Australia (Simmonds 1966, Plant Health Australia (2001) Australian Plant Pest Database, online database http://appd.ala.org.au/ accessed 2 Sep. 2016). The graminicolous Colletotrichum isolates in Australian collections have yet, for the most part, to be identified and classified by molecular phylogenetic methods.
Other Australian species that remain to be verified by DNA sequence analyses include C. acaciae Gutner, C. caudatum (Peck ex Sacc.) Peck, C. crassipes (Speg.) Arx, C. falcatum Went, C. fuscum Laubert, C. higginsianum Sacc., C. malvarum (A. Braun & Casp.) Southw., C. orchidearum Allesch., C. schizanthi C.N. Jensen & V.B. Stewart, C. trichellum (Fr.) Duke, C. trifolii Bain, and C. xanthii Halst. These species require verification by DNA sequencing to confirm their presence in Australia.
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Acknowledgments
We thank Plant Health Australia (PHA) who provided funds for two workshops on the identification and classification of Colletotrichum species. The workshops were organised by the Subcommittee on Plant Health Diagnostics in collaboration with PHA as part of a professional development program for plant health diagnosticians. PHA sourced funding from the Department of Agriculture and Water Resources through a grant from the Plant Biosecurity and Response Reform program. The authors especially wish to thank Julie McClements (Culture Collection WAC, WA), and Robyn Brett (Herbarium VPRI, Vic) for providing cultures.
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Shivas, R.G., Tan, Y.P., Edwards, J. et al. Colletotrichum species in Australia. Australasian Plant Pathol. 45, 447–464 (2016). https://doi.org/10.1007/s13313-016-0443-2
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DOI: https://doi.org/10.1007/s13313-016-0443-2