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Studies in Mycology 75 (June 2013) Phytopathogenic Dothideomycetes Pedro W. Crous, Gerard J.M. Verkley and Johannes Z. Groenewald, editors CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences Phytopathogenic Dothideomycetes StudieS in Mycology 75, 2013 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] Managing editor Prof. dr P.W. Crous, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] layout editorS Manon van den Hoeven-Verweij, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Marjan Vermaas, 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 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 2013 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: 30 June 2013 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 : 978-90-70351-96-0 Online ISSN : 1872-9797 Print ISSN : 0166-0616 Cover: Top from left to right: Conidia of Alternaria septospora, leaf symptoms induced by Pseudocercospora fijiensis, and conidia of Stagonospora paludosa. Bottom from left to right: Asci of Stagonospora perfecta, leaf symptoms induced by Cercospora coniogrammes, and conidiophores of a Cercospora sp. Phytopathogenic Dothideomycetes edited by Pedro W. Crous CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands Gerard J.M. Verkley CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands and Johannes Z. Groenewald 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 INTRODUCTION a quarantine organism at that time in Europe. The taxonomy of phoma-like species on potatoes was confusing, and he started his The present issue of Studies in Mycology focuses on plant fundamental study on Phoma. A second important problem, Phoma pathogenic Dothideomycetes. The Dothideomycetes represents lingam on seeds of Brassicaceae arose, and studies on many other the largest class of Ascomycota, with more than 100 families and Phoma species associated with plant material followed. 19 000 species. Of interest, however, is the fact that this class Gerhard described many synonyms of the Phoma species after also contains the most genera of plant pathogenic fungi, many of detailed studies of herbarium material. He recognised sections in which are frequently encountered by plant health officers at various Phoma and published his findings in numerous papers in the period ports of entry around the world. These officers are subsequently 1960–1988. He became the expert on Phoma worldwide. Isolates confronted by the fact that the fungus may be expressing its sexual and herbarium material were weekly received for identification and or asexual morph, or worse, maybe sterile mycelium. Traditionally the extensive correspondence in English, French and German these mycologists have had a range of books with which they could language is still preserved at the Dutch Plant Protection Service. try to identify these organisms based on the phenotype. In recent Gerhard established with his team a culture collection and years however, most of these taxa have been shown to represent herbarium at PD, and most of the strains were also deposited at species complexes, with some specific to certain regions or hosts. the culture collection of CBS. During his career, Phoma was his Integrating asexual and sexual names, dealing with species that are main topic, but he worked on the nomenclature of many important cryptic, and genera that are poly- and paraphyletic, and a general plant pathogens, published as "Check-list for scientific names of lack of DNA data authentic for these species, is a constant stress common parasitic fungi" in 12 supplement series in the Netherlands to which these mycologists are exposed. Identifications made by Journal of Plant Pathology. these mycologists could result in losses of millions of “dollars” to Gerhard collaborated in a new Phoma project started at the PD farmers and producers, while wrongful introductions could again to provide standardised in vitro descriptions of Phoma species. He destroy local industries and markets. established the morphological genus concept with a classification of Phoma in nine sections. In collaboration with his successor Chiel The present issue focuses on five main groups of fungi that Noordeloos, Hans de Gruyter and Marielle Hamers, “Contributions plant health officers deal with on a weekly, or daily basis, namely towards a monograph of Phoma” were published in Persoonia Alternaria, Cercospora, Phoma, Pseudocercospora, and Septoria. during the period 1992–2003. These papers formed the base for the “Phoma Identification Manual” published in 2004 (CABI Publishing, Wallingford, UK). The cultures deposited at the PD and DEDICATION: To the plant health officers of the the CBS, however, laid the foundation for the next phase, which world was a phylogenetic study of the sections and species in the Phoma complex by two PhD students, Aveskamp and de Gruyter, of which This special issue is dedicated to three exceptional colleagues, one final paper is published in this issue. who dedicated their lives and careers to be plant health officers, striving to enhance trade, but also to protect borders from wrongful incursions. To these colleagues we owe a great deal of thanks for C.F. (Frank) Hill (1941–2009) their unselfish dedication and commitment. Without their published works, databases, specimens and cultures, we would not have Caleb Francis (Frank) Hill was a mycologist at the Ministry of been able to produce the papers reported in this special issue. Agriculture and Forestry (MAF) in Auckland, New Zealand. Frank always had a strong focus on diagnostics, and in the process isolated numerous interesting plant pathogenic fungi. Gerhard H. Boerema (1925–2008) For instance, Calonectria pseudonaviculata (= Cylindrocladium buxicola), which is now a major quarantine problem on Buxus Gerhard Boerema accepted a position as mycologist at the Dutch in Europe and the USA, was originally described from material Plant Protection Service (Plantenziektenkundige Dienst, PD) in Frank collected in New Zealand in 1998, and sent to CBS for 1956. Gerhard became head of the Mycology Department in 1959 a collaborative publication on Calonectria, a pathogen that he and fulfilled this position until his early retirement in 1988. The main frequently intercepted at ports of entry into New Zealand. During tasks of the Mycology Department at that time was the diagnosis his career Frank published descriptions of more than 70 novel on symptomatic plant material submitted by inspectors, advisory taxa, contributed to more than 3 000 pest records in the Ministry services, companies, research stations, etc. It covered all fields of Agriculture and Forestry Plant Pest database, and deposited such as agriculture, horticulture, greenhouse products as well as more than 1 500 specimens and cultures. To address the severe natural environment. Interesting findings were published annually shortage of cultures and lack of DNA data in the cercosporoid in the Dutch Tijdschrift over Plantenziekten, continued later as complex, the CBS started to purposefully cultivate all cercosporoid Mededelingen van de Plantenziektenkundige Dienst in Wageningen fungi encountered. One of the best collectors was Frank Hill, who (Yearbook PD). The diversity of topics is demonstrated in his first in his function as plant health diagnostician, encountered many reports that included bark canker of apple and pear, caused by pathogens both indigenous and exotic to New Zealand. Frank Pezicula corticola (1959), a new species of Sclerotinia as the cause collected a great many of the specimens treated in the papers of black leg in tulip (1960), and Chalaropsis thielavioides on carrots published in this issue (ranging from Alternaria to Phoma, and pre-packed in perforated polythene bags (1960). Another important cercosporoid). It is interesting to note that the collection dates task was to give internal advice concerning quarantine issues. largely correspond with weekends, which gave us the impression Shortly after he became head of the Mycology department, a that Frank was always roaming the countryside, botanical gardens new disease was found on potatoes, caused by Phoma foveata, and arboretums, looking for interesting diseases. Without Frank’s collections, these studies would not have been possible. It is only fitting then, that we also dedicate this work to him for his keen eye, and never ending enthusiasm for the subject. Frank may have passed on, but his collection of plant pathogenic fungal cultures will forever remain a living legacy for future generations to study. Flora G. Pollack (1919–1997) As the United States’ only plant quarantine mycologist for 12 years, Flora Pollack had the privilege of examining specimens of interesting and unusual fungi from around the world that had been intercepted at various ports of entry. Flora began working for the Bureau of Plant Quarantine in the early 1940’s when it was located in the U.S. Department of Agriculture building in downtown Washington. She resigned from her job to raise her children, and 15 years later went to work again as a mycologist at the American Type Culture Collection (ATCC), then in Rockville, MD. During her six and one-half years of employment there, she improved a technique for the preservation of cultures in their Gerhard H. Boerema original condition as received by ATCC that is still widely used for this purpose. When the opportunity arose, she returned to the U.S. Department of Agriculture in 1967. During her professional years she published many scientific articles in Mycologia and other journals often authored in collaboration with others. She described numerous new species in a wide range of fungal groups but had a particular fondness for coelomycetous fungi, a group that still evades accurate classification. At least one unusual species, aptly named Monosporascus cannonballus was described by Pollack with F.A. Uecker. Originally encountered as a harmless oddity associated with the roots of cantaloupes, many years later this fungus gained prominence as a virulent pathogen limiting the production of melons in dry areas of the world. While working for APHIS, Flora was associated with the Mycology Laboratory, now Systematic Mycology & Microbiology Laboratory. As the plant quarantine mycologist she encountered on a daily basis fungi from around the world, many of which she deposited in the U.S. National Fungus Collections. A search of herbarium database yields over 5 000 specimens identified by Flora that remain an important resource for the identification of C.F. (Frank) Hill plant quarantine fungi as well as fodder for taxonomists tackling these difficult species. Following the tradition established by her predecessor, Alice Watson, she maintained a card file of important literature for the identification of plant-associated fungi. This file became the basis for a publication (Rossman AY, Palm ME, Spielman LJ. 1987. A Literature Guide for the Identification of Plant Pathogenic Fungi. St. Paul, Minnesota: American Phytopathological Society), and later the database of literature available on the Internet <http://nt.ars-grin.gov/fungaldatabases/literature/litframe. cfm>. After retiring in 1979, Flora was asked to publish a project she had started in her spare time while working in Beltsville. She spent many hours pulling together her “Annotated Compilation of Cercospora Names”. Published in 1987, it served as the most comprehensive reference on this genus, and provided the basis for a later update by Crous & Braun (2003) on “Mycosphaerella and its anamorphs: 1. Names published in Cercospora and Passalora” (CBS Biodiversity Series 1, CBS-KNAW Fungal Biodiversity Centre, Utrecht, Netherlands), which in turn set the stage for the molecular phylogenetic papers published on this complex in this Flora G. Pollack issue of Studies in Mycology. Johannes (Hans) de Gruyter National Reference Centre, National Plant Protection Organization, P.O. Box 9102, 6700 HC Wageningen, the Netherlands Brett J.R. Alexander Mycology and Bacteriology, Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand Amy Y. Rossman Mary E. Palm Systematic Mycology & Microbiology Laboratory, Agricultural Research Service, & Animal and Plant Health Inspection Service, USDA, Beltsville, Maryland 20705, USA Pedro W. Crous CBS-KNAW Fungal Biodiversity Centre, Upssalalaan 8, 3584 CT, Utrecht, the Netherlands CONTENTS J. de Gruyter, J.H.C. Woudenberg, M.M. Aveskamp, G.J.M. Verkley, J.Z. Groenewald and P.W. Crous. Redisposition of phoma-like anamorphs in Pleosporales ................................................................................................................................................................................................ 1 P.W. Crous, U. Braun, G.C. Hunter, M.J. Wingfield, G.J.M. Verkley, H.-D. Shin, C. Nakashima and J.Z. Groenewald. Phylogenetic lineages in Pseudocercospora ......................................................................................................................................................................................... 37 J.Z. Groenewald, C. Nakashima, J. Nishikawa, H.-D. Shin, J.-H. Park, A.N. Jama, M. Groenewald, U. Braun and P.W. Crous. Species concepts in Cercospora: spotting the weeds among the roses ................................................................................................................... 115 J.H.C. Woudenberg, J.Z. Groenewald, M. Binder and P.W. Crous. Alternaria redefined ............................................................................ 171 G.J.M. Verkley, W. Quaedvlieg, H.-D. Shin and P.W. Crous. A new approach to species delimitation in Septoria ...................................... 213 W. Quaedvlieg, G.J.M. Verkley, H.-D. Shin, R.W. Barreto, A.C. Alfenas, W.J. Swart, J.Z. Groenewald and P.W. Crous. Sizing up Septoria ....................................................................................................................................................................................................... 307 Index of Fungal Names ............................................................................................................................................................................... 391 y g o l o c y M n i s e i d u t S