available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 73: 37–113. The Colletotrichum acutatum species complex U. Damm1*, P.F. Cannon2, J.H.C. Woudenberg1, and P.W. Crous1,3,4 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2CABI Europe-UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK and Royal Botanic Gardens, Kew, Richmond TW9 3AB, UK; 3Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands; 4Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands *Correspondence: Ulrike Damm, [email protected] Abstract: Colletotrichum acutatum is known as an important anthracnose pathogen of a wide range of host plants worldwide. Numerous studies have reported subgroups within the C. acutatum species complex. Multilocus molecular phylogenetic analysis (ITS, ACT, TUB2, CHS-1, GAPDH, HIS3) of 331 strains previously identified as C. acutatum and other related taxa, including strains from numerous hosts with wide geographic distributions, confirmed the molecular groups previously recognised and identified a series of novel taxa. Thirty-one species are accepted, of which 21 have not previously been recognised. Colletotrichum orchidophilum clusters basal to the C. acutatum species complex. There is a high phenotypic diversity within this complex, and some of the species appear to have preferences to specific hosts or geographical regions. Others appear to be plurivorous and are present in multiple regions. In this study, only C. salicis and C. rhombiforme formed sexual morphs in culture, although sexual morphs have been described from other taxa (especially as laboratory crosses), and there is evidence of hybridisation between different species. One species with similar morphology to C. acutatum but not belonging to this species complex was also described here as new, namely C. pseudoacutatum. Key words: anthracnose, Ascomycota, Colletotrichum acutatum, Gloeosporium, Glomerella, phylogeny, systematics. Taxonomic novelties: New combinations - Colletotrichum limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. lupini (Bondar) Damm, P.F. Cannon & Crous, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. New species - C. acerbum Damm, P.F. Cannon & Crous, C. australe Damm, P.F. Cannon & Crous, C. brisbanense Damm, P.F. Cannon & Crous, C. cosmi Damm, P.F. Cannon & Crous, C. costaricense Damm, P.F. Cannon & Crous, C. cuscutae Damm, P.F. Cannon & Crous, C. guajavae Damm, P.F. Cannon & Crous, C. indonesiense Damm, P.F. Cannon & Crous, C. johnstonii Damm, P.F. Cannon & Crous, C. kinghornii Damm, P.F. Cannon & Crous, C. laticiphilum Damm, P.F. Cannon & Crous, C. melonis Damm, P.F. Cannon & Crous, C. orchidophilum Damm, P.F. Cannon & Crous, C. paxtonii Damm, P.F. Cannon & Crous, C. pseudoacutatum Damm, P.F. Cannon & Crous C. pyricola Damm, P.F. Cannon & Crous, C. rhombiforme Damm, P.F. Cannon & Crous, C. scovillei Damm, P.F. Cannon & Crous, C. sloanei Damm, P.F. Cannon & Crous, C. tamarilloi Damm, P.F. Cannon & Crous, C. walleri Damm, P.F. Cannon & Crous. Typifications: Epitypifications - C. acutatum J.H. Simmonds, C. limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. nymphaeae (Pass.) Aa, C. phormii (Henn.) D.F. Farr & Rossman, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. Lectotypifications - C. nymphaeae (Pass.) Aa, C. orchidearum Allesch. Published online: 16 August 2012; doi:10.3114/sim0010. Hard copy: September 2012. INTRODUCTION pathogen, C. acutatum was treated for many years as a regulated plant quarantine pest by the European and Mediterranean Plant Colletotrichum acutatum is one of the most frequently reported Protection Organization (EPPO), though it is absent from the species of the genus and causes diseases commonly known as current list (EPPO 2011) – presumably due to its now widespread anthracnose on numerous host plants worldwide (Farr & Rossman distribution in Europe. Inoculum sources are frequently transplant 2012). Originally described from diseased tissues of Carica material, mostly with quiescent infections (Rahman & Louws 2008), papaya, Capsicum frutescens and Delphinium ajacis in Australia infected plants, weeds and other hosts (McInnes et al. 1992, by Simmonds (1965), the C. acutatum species complex is today Parikka et al. 2006), while the survival rate of conidia in natural field known as especially destructive on fruits like strawberry (Garrido soil is low (Freeman et al. 2002). et al. 2009), citrus (Peres et al. 2008), apple (Lee et al. 2007), The most well-known morphological feature of C. acutatum (s. olive (Talhinhas et al. 2011), cranberry (Polashock et al. 2009) and lat.) is the shape of its conidia, which have acute ends (Simmonds blueberry (Wharton & Schilder 2008). It is also implicated in the 1965). However, other conidial shapes, especially ± cylindrical “terminal crook” disease of pine (Dingley & Gilmour 1972) and in with only one acute end, are frequently encountered, especially in the anthracnose of leather leaf fern (Schiller et al. 2006). There are strains that have been repeatedly subcultured, but these conidial also reports of a disseminated infection of a sea turtle (Manire et shapes can also occur in species outside the C. acutatum species al. 2002) and the infection of a scale insect (Marcelino et al. 2008). complex. Even the differentiation between C. acutatum (s. lat.) and Reviews of the species in its broad sense and its pathology were C. gloeosporioides (s. lat.) is difficult, because many intermediate published by Wharton & Diéguez-Uribeondo (2004) and Peres et strains exist with a restricted number of typical fusiform conidia and al. (2005). many cylindrical ones (Van der Aa et al. 1990). On the host, conidia On strawberry, C. acutatum mainly causes black spot of fruit are formed in acervuli; in culture, conidia are often also produced but can also attack crowns, roots and leaves (Freeman & Katan in the aerial mycelium (Johnston & Jones 1997). Colletotrichum 1997), and is one of the most serious diseases in commercial fruit acutatum has also been observed to form secondary conidia on the production. Largely due to its economic importance as a strawberry surface of living strawberry leaves (Leandro et al. 2001) that were Copyright CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. Studies in Mycology For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 37 DAMM ET AL. stimulated by strawberry plant extracts, especially flower extracts Our research aims to present a comprehensive revision of (Leandro et al. 2003). According to Buddie et al. (1999) secondary the C. acutatum species complex. We thoroughly survey the conidia may be produced directly from germinating primary conidia, constituent taxa and delineate additional species where needed. and are smaller and more variable in shape, thus obscuring We have examined a large number of C. acutatum s. lat. strains, differences between taxa. Additionally, C. acutatum forms simple isolated from various hosts and in various geographic areas. Multi- pigmented appressoria, but few or no setae (Simmonds 1965). locus molecular analysis is the basis of species recognition, but Guerber & Correll (1997, 2001) described Glomerella acutata, morphological and cultural characters allowing alternative means the sexual morph of C. acutatum, as the product of mating of species recognition are given where possible. experiments, while some related species are homothallic, including Ga. acutata var. fioriniae (Marcelino et al. 2008), later regarded as a separate species (C. fioriniae, Shivas & Tan 2009) and an isolate MATERIALS AND METHODS of a Glomerella species related to C. acutata from Acer platanoides in the USA (LoBuglio & Pfister 2008). Talgø et al. (2007) observed Isolates the sexual morph Ga. acutata on naturally infected fruits of highbush blueberry in Norway. Numerous studies have shown A total of 331 strains have been studied, mostly previously that C. acutatum is morphologically and phylogenetically diverse identified as C. acutatum, as well as other related strains from the (Sreenivasaprasad et al. 1994, Johnston & Jones 1997, Lardner CBS, IMI and other culture collections. Type material (holotypes et al. 1999, Freeman et al. 2001a, Nirenberg et al. 2002, Talhinhas and epitypes) of the species studied are located in the Herbarium et al. 2002, Guerber et al. 2003, Lubbe et al. 2004, Du et al. 2005, of the Centraalbureau voor Schimmelcultures (CBS), Utrecht, Peres et al. 2005, Sreenivasaprasad & Talhinhas 2005, Talhinhas The Netherlands, in the IMI Fungarium, which is based in the et al. 2005, Johnston et al. 2008). Sreenivasaprasad et al. (1996) Royal Botanic Gardens, Kew (IMI and K(M)), UK, US National were the first to recognise thatC. acutatum was unusually