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Studies in Mycology 73 (September 2012) Colletotrichum: complex species or species complexes? Ulrike Damm, Paul F. Cannon and Pedro W. Crous, editors CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences Colletotrichum: complex species or species complexes? StudieS in Mycology 73, 2012 Studies in Mycology The Studies in Mycology is an international journal which publishes systematic monographs of filamentous fungi and yeasts, and in rare occasions the proceedings of special meetings related to all fields of mycology, biotechnology, ecology, molecular biology, pathology and systematics. For instructions for authors see www.cbs.knaw.nl. executive editor Prof. dr dr hc Robert A. Samson, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] layout editor Manon van den Hoeven-Verweij, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Scientific editorS Prof. dr Dominik Begerow, Lehrstuhl für Evolution und Biodiversität der Pflanzen, Ruhr-Universität Bochum, Universitätsstr. 150, Gebäude ND 44780, Bochum, Germany. E-mail: [email protected] Prof. dr Uwe Braun, Martin-Luther-Universität, Institut für Biologie, Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, D-06099 Halle, Germany. E-mail: [email protected] Dr Paul Cannon, CABI and Royal Botanic Gardens, Kew, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, U.K. E-mail: [email protected] Prof. dr Lori Carris, Associate Professor, Department of Plant Pathology, Washington State University, Pullman, WA 99164-6340, U.S.A. E-mail: [email protected] Prof. dr Pedro W. Crous, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr David M. Geiser, Department of Plant Pathology, 121 Buckhout Laboratory, Pennsylvania State University, University Park, PA, U.S.A. 16802. E-mail: [email protected] Dr Johannes Z. Groenewald, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr David S. Hibbett, Department of Biology, Clark University, 950 Main Street, Worcester, Massachusetts, 01610-1477, U.S.A. E-mail: [email protected] Dr Lorelei L. Norvell, Pacific Northwest Mycology Service, 6720 NW Skyline Blvd, Portland, OR, U.S.A. 97229-1309. E-mail: [email protected] Prof. dr Alan J.L. Phillips, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta de Torre, 2829-516 Caparica, Portugal. E-mail: [email protected] Dr Amy Y. Rossman, Rm 304, Bldg 011A, Systematic Botany & Mycology Laboratory, Beltsville, MD, U.S.A. 20705. E-mail: [email protected] Dr Keith A. Seifert, Research Scientist / Biodiversity (Mycology and Botany), Agriculture & Agri-Food Canada, KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, Canada K1A OC6. E-mail: [email protected] Prof. dr Hyeon-Dong Shin, Division of Environmental Science & Ecological Engineering, Korea University, Seoul 136-701, Korea. E-mail: [email protected] Dr Roger Shivas, Manager, Plant Biosecurity Science, Biosecurity Queensland, Department of Employment, Economic Development and Innovation, DEEDI, GPO Box 267, Brisbane, Qld 4001, Dutton Park 4102, Queensland, Australia. E-mail: [email protected] Dr Marc Stadler, InterMed Discovery GmbH, Otto-Hahn-Straße 15, D-44227 Dortmund, Germany. E-mail: [email protected] Prof. dr Jeffrey K. Stone, Department of Botany & Plant Pathology, Cordley 2082, Oregon State University, Corvallis, OR, U.S.A. 97331-2902. E-mail: [email protected] Dr Richard C. Summerbell, 27 Hillcrest Park, Toronto, Ont. M4X 1E8, Canada. E-mail: [email protected] Prof. dr Brett Summerell, Royal Botanic Gardens and Domain Trust, Mrs. Macquaries Road, Sydney, NSW 2000, Australia. E-mail: [email protected] Prof. dr Ulf Thrane, Department of Systems Biology, Center for Microbial Biotechnology, Technical University of Denmark, Søltofts Plads 221, DK-2800 Kgs. Lyngby, Denmark. E-mail: [email protected] Copyright 2012 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. 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. Publication date:15 Sep 2012 Published and distributed by CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. Internet: www.cbs.knaw.nl. E-mail: [email protected]. ISBN/EAN : 978-90-70351-92-2 Online ISSN : 1872-9797 Print ISSN : 0166-0616 Cover: Top from left to right: Conidia of Colletotrichum beeveri on SNA, anthracnose of strawberry fruit caused by C. nymphaeae, conidia of C. gloeosporioides on Anthriscus stem. Bottom from left to right: culture of C. alatae on PDA, conidia of C. fioriniae on Anthriscus stem, conidioma of C. novae-zelandiae on Anthriscus stem. Colletotrichum: complex species or species complexes? edited by Ulrike Damm CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands Paul F. Cannon CABI Europe-UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK and Royal Botanic Gardens, Kew, Richmond TW9 3AB, UK Pedro W. Crous CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences DEDICATION This volume is dedicated to Brian C. Sutton, fungal systematist non plus ultra and Chief Mycologist at the International Mycological Institute (IMI) until his retirement in 1995. After arrival at IMI straight from university in 1959, Brian was faced with the choice of specialising in rusts or coelomycetes (fungi forming conidia within fruit-bodies). His courageous decision to work with the then almost unknown coelomycete group paved the way for a long and diverse career. Many of the fungi he worked with are minute and require patient and meticulous analytical microscopy. Brian’s ability to see almost invisible details of conidiomatal anatomy, conidiogenesis and conidium morphology, and to translate these observations into detailed descriptions and beautiful line drawings, made him one of the most celebrated fungal systematists of the pre-molecular era. He has a voluminous publication record, and his 1980 monograph “The Coelomycetes – Fungi imperfecti with pycnidia, acervuli and stromata” is still the basic standard morphological reference work for this group of fungi. The diversity of his output can be judged by the list of 990 fungal names he authored or co-authored. Some of these were imaginatively named, including the genera Satchmopsis (in honour of his jazz hero Louis Armstrong) and Omega (the final taxon published in Transactions of the British Mycological Society, of which he was Senior Editor between 1977 and 1988). Brian was always generous with his time in support of fellow mycologists and students from all over the globe, who sent him numerous collections of “troublesome” coelomycetes. On many occasions, these initial requests for help led on to mentoring of the developing scientific careers of his correspondents, and to continuing collaborations in fungal systematics. Brian’s involvement with Colletotrichum began with a paper on C. dematium and C. trichellum in 1962, and developed as the subject for his PhD thesis which focused on the morphology and ontogeny of species associated with grasses. His were the first scientific contributions that established the importance of appressorium morphology in Colletotrichum systematics. After studies of conidial fungi in almost all the branches and bywaters of the Ascomycota, his second major contribution was to provide a user-friendly guide to Colletotrichum in the 1980 Coelomycetes monograph, which built on von Arx’s work to provide a framework for morphology-based identification that still has value today. This was followed by a further systematic account in 1992, which increased the number of accepted species to 39. Brian retired shortly before the fungal molecular phylogenetic revolution gained pace. Although the classification he developed in The Coelomycetes was unavoidably artificial, it continues to play a major role in ground-truthing of the results of new phylogenetic research, through integration with recent studies that add molecular data to Brian Sutton working in his office (1992), in the final days of the International Mycological Institute at Kew (photo by David Minter). Brian’s original morphological observations. Other than his love for fungi, Brian’s love for jazz music is well known among his mycological colleagues. Our decision to dedicate this volume to him comes with the expectation that he will be paging through it with something soothing playing in the background. Although the backbone of Colletotrichum systematics remains unaltered more than thirty years after The Coelomycetes was published, we hope that recognition of the cryptic lineages within the species complexes included in this volume goes some way towards explanation of their extraordinary variation. “And it feels like rain “ing species” – Buddy Guy The Editors September 2012 CONTENTS U. Damm, P.F. Cannon, J.H.C. Woudenberg, P.R. Johnston, B.S. Weir, Y.P. Tan, R.G. Shivas, and P.W. Crous. The Colletotrichum boninense species complex .............................................................................................................................................................................................. 1 U. Damm, P.F. Cannon, J.H.C. Woudenberg, and P.W. Crous. The Colletotrichum acutatum species complex .......................................... 37 B.S. Weir, P.R. Johnston, and U. Damm. The Colletotrichum gloeosporioides species complex ............................................................... 115 P.F. Cannon, U. Damm, P.R. Johnston, and B.S. Weir. Colletotrichum – current status and future directions ............................................ 181 y g o l o c y M n i s e i d u t S available online at www.studiesinmycology.org StudieS in Mycology 73: 1–36. The Colletotrichum boninense species complex U. Damm1*, P.F. Cannon2, J.H.C. Woudenberg1, P.R. Johnston3, B.S. Weir3, Y.P. Tan4, R.G. Shivas4, and P.W. Crous1,5,6 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; 3Landcare Research, Private Bag 92170 Auckland, New Zealand; 4Plant Biosecurity Science, Ecosciences Precinct, Dutton Park, Queensland 4102, Australia; 5Utrecht University, Department of Biology, Microbiology, Padualaan 8, 3584 CH Utrecht, The Netherlands; 6Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands *Correspondence: Ulrike Damm, [email protected] Abstract: Although only recently described, Colletotrichum boninense is well established in literature as an anthracnose pathogen or endophyte of a diverse range of host plants worldwide. It is especially prominent on members of Amaryllidaceae, Orchidaceae, Proteaceae and Solanaceae. Reports from literature and preliminary studies using ITS sequence data indicated that C. boninense represents a species complex. A multilocus molecular phylogenetic analysis (ITS, ACT, TUB2, CHS-1, GAPDH, HIS3, CAL) of 86 strains previously identified as C. boninense and other related strains revealed 18 clades. These clades are recognised here as separate species, including C. boninense s. str., C. hippeastri, C. karstii and 12 previously undescribed species, C. annellatum, C. beeveri, C. brassicicola, C. brasiliense, C. colombiense, C. constrictum, C. cymbidiicola, C. dacrycarpi, C. novae-zelandiae, C. oncidii, C. parsonsiae and C. torulosum. Seven of the new species are only known from New Zealand, perhaps reflecting a sampling bias. The new combination C. phyllanthi was made, and C. dracaenae Petch was epitypified and the name replaced with C. petchii. Typical for species of the C. boninense species complex are the conidiogenous cells with rather prominent periclinal thickening that also sometimes extend to form a new conidiogenous locus or annellations as well as conidia that have a prominent basal scar. Many species in the C. boninense complex form teleomorphs in culture. Key words: anthracnose, Ascomycota, Colletotrichum boninense, Glomerella, phylogeny, systematics. Taxonomic novelties: New combination - Colletotrichum phyllanthi (H. Surendranath Pai) Damm, P.F. Cannon & Crous. Name replacement - C. petchii Damm, P.F. Cannon & Crous. New species - C. annellatum Damm, P.F. Cannon & Crous, C. beeveri Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. brassicicola Damm, P.F. Cannon & Crous, C. brasiliense Damm, P.F. Cannon, Crous & Massola, C. colombiense Damm, P.F. Cannon, Crous, C. constrictum Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. cymbidiicola Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. dacrycarpi Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. novae-zelandiae Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. oncidii Damm, P.F. Cannon & Crous, C. parsonsiae Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir, C. torulosum Damm, P.F. Cannon, Crous, P.R. Johnst. & B. Weir. Typifications: Epitypifications - C. dracaenae Petch. Published online: 21 February 2012; doi:10.3114/sim0002. Hard copy: September 2012. INTRODUCTION Capsicum, Citrus, Cucurbita and Solanum species in New Zealand. Colletotrichum boninense was reported as the cause of anthracnose y Colletotrichum boninense was first described from Crinum asiaticum of pepper (Capsicum annuum) in Brazil (Tozze et al. 2009), of var. sinicum (Amaryllidaceae) collected in the Bonin Islands, Japan passion fruit (Passiflora) in Florida (Tarnowski & Ploetz 2010) g (Moriwaki et al. 2003). According to these authors, the species was and Brazil (Tozze et al. 2010) and of Crinum asiaticum in China o associated with a variety of host plants in Japan, including Clivia (Yang et al. 2009). Lee et al. (2005a, b) observed leaf anthracnose miniata (Amaryllidaceae), Cucumis melo (Cucurbitaceae), Cattleya on Japanese spindle tree (Euonymus japonica) in Korea and l sp., Cymbidium sp. and Dendrobium kingianum (Orchidaceae), demonstrated the pathogenicity of C. boninense. Nguyen et al. o Passiflora edulis (Passifloraceae) and Prunus mume (Rosaceae). (2009) reported C. boninense as a pathogen of berries and twigs of c Since 2003, C. boninense (in its wide sense prior to our research) Coffea in Vietnam. Recently, C. boninense was identified as one of has frequently been identified as a pathogen causing fruit and leaf the causal agents of anthracnose in avocado (Persea americana) y anthracnose, as well as an endophyte of a range of host plants in Mexico (Silva-Rojas & Ávila-Quezada 2011). M worldwide, especially belonging to Amaryllidaceae, Orchidaceae, Lu et al. (2004) detected probable C. boninense isolates as Proteaceae and Solanaceae. For example, C. boninense was endophytes in leaves of several tree species in the Iwokrama Forest found to be associated with diseases of Leucospermum and Reserve in Guyana. Other reports of C. boninense as endophytes n Protea cynaroides in Australia and Zimbabwe and with Eucalyptus include Pileggi et al. (2009), who isolated it from leaves of the in South Africa (Lubbe et al. 2004). In pathogenicity studies it was medicinal plant Maytenus ilicifolia in Brazil. Joshee et al. (2009) i shown to infect Protea leaves and stems (Lubbe et al. 2006). Farr studied foliar endophytes of Podocarpaceae and Myrtaceae trees s et al. (2006) reported C. boninense on Dracaena and Pachira in New Zealand and identified several of them as belonging to the in China, Passiflora in New Zealand and Hippeastrum in Brazil C. boninense group. Several other isolates causing anthracnose on e and the Netherlands. According to Johnston & Jones (1997) and tamarillo, Passiflora and mango from Colombia (Afanador-Kafuri i Johnston et al. (2005), C. boninense (= C. gloeosporioides groups et al. 2003) and endophytes in coffee plants from Colombia and d E–I in Johnston & Jones 1997) occurs on a range of hosts including Hawaii (Vega et al. 2010) belonging to the C. boninense species u Copyright CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. t You are free to share - to copy, distribute and transmit the work, under the following conditions: S 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. 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. 1 Damm et al. 3 2 0 5 4 6 3 1 2 7 8 9 6 5 3 4 5 9 8 9 7 8 7 3 3 1 2 3 0 7 5 8 4 9 8 7 7 7 8 8 8 7 7 7 5 5 9 9 9 5 5 8 8 8 5 7 5 5 5 2 4 2 0 2 7 6 6 6 6 6 6 6 6 6 6 6 7 7 6 6 6 7 7 6 6 6 7 6 7 7 7 7 7 7 7 7 L 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 C JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ 6 5 3 9 8 6 4 5 0 1 2 9 8 6 7 8 2 1 2 0 1 0 7 6 4 5 6 3 0 8 1 5 0 9 8 8 9 9 9 9 9 9 6 6 0 0 0 7 7 0 0 0 7 8 6 6 6 3 5 4 1 4 B2 056 056 055 055 055 055 055 055 055 055 055 056 056 056 056 056 056 056 056 056 056 056 055 056 056 056 056 056 056 056 056 TU JQ0 JQ0 JQ0 JQ0 JQ0 - JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 JQ0 0 9 7 2 1 3 0 8 9 4 5 6 3 2 0 1 2 6 5 6 4 5 4 0 0 8 9 0 7 4 2 5 7 1 0 0 0 0 1 0 0 0 0 0 8 8 2 2 2 8 8 1 1 1 8 0 8 7 7 5 6 5 3 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 T 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 05 C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 A JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ JQ o. 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Host/Substrate Hevea brasiliensis, leaf Brachyglottis repanda Camellia sp. Crinum asiaticum var. sinicum Crinum asiaticum var. sinicum Crinum asiaticum var. sinicum, leaf Dacrycarpus dacrydioides, leaf endophyte Leucospermum sp. Leucospermum sp. Solanum betaceum, flowers Solanum lycopersicum, fruit rot Tecomanthe speciosa Passiflora edulis, fruit anthracnose Passiflora edulis, fruit Brassica oleracea var. gemmifera, leaf spot Passiflora edulis, leaf Passiflora edulis, leaf Citrus limon, fruit rot Solanum betaceum, fruit rot Cymbidium sp. Cymbidium sp., leaf lesion Cymbidium sp., leaf spot Dacrycarpus dacrydioides, leaf endophyte Citrus sinensis Hippeastrum sp. Hippeastrum vittatum Hippeastrum vittatum, leaf Annona cherimola, fruit Annona cherimola, fruit anthracnose Anthurium sp. Bombax aquaticum Capsicum annuum o cti e coll S12* S10 otrichum spp. studied, with 1Accession No. CBS 129826, CH1* CBS 128527, ICMP 18594* CBS 128547, ICMP 10338 CBS 123756, MAFF 306094 CBS 123755, MAFF 305972* MAFF 306162, ICMP 18596 CBS 128526, ICMP 18591 CBS 112115, STE-U 2966 CBS 129831, STE-U 2965 CBS 128549, ICMP 15444 CBS 128506, ICMP 12950 CBS 128546, ICMP 18595 CBS 128501, ICMP 18607, PA CBS 128528, ICMP 18606, PA CBS 101059, LYN 16331* CBS 129817, G1 CBS 129818, G2* CBS 128504, ICMP 12941* CBS 128503, ICMP 12936 CBS 123757, MAFF 306100 IMI 347923* CBS 128543, ICMP 18584 CBS 130241, ICMP 19107* CBS 112999, STE-U 4295* CBS 241.78, IMI 304052 CBS 125377, CSSK4 CBS 125376, CSSG1* CBS 128500, ICMP 18585 CBS 128550, ICMP 17896 CBS 129927 CBS 861.72 CBS 128545, ICMP 18587 et oll C of Table 1. Strains Species C. annellatum C. beeveri C. boninense C. brasiliense C. brassicicola C. colombiense C. constrictum C. cymbidiicola C. dacrycarpi C. gloeosporioides C. hippeastri C. karstii 2