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Sclerotinia Sclerotiorum and Botrytis Cinerea

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Sclerotinia Sclerotiorum and Botrytis Cinerea Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea Joelle Amselem1,2.*, Christina A. Cuomo3.*, Jan A. L. van Kan4.*, Muriel Viaud2.*, Ernesto P. Benito5, Arnaud Couloux6, Pedro M. Coutinho7, Ronald P. de Vries8,9, Paul S. Dyer10, Sabine Fillinger2, Elisabeth Fournier2,11, Lilian Gout2, Matthias Hahn12, Linda Kohn13, Nicolas Lapalu1, Kim M. Plummer14, Jean-Marc Pradier2, Emmanuel Que´villon1,15, Amir Sharon16, Adeline Simon2, Arjen ten Have17, Bettina Tudzynski18, Paul Tudzynski18, Patrick Wincker6, Marion Andrew13,Ve´ronique Anthouard6, Ross E. Beever19{, Rolland Beffa15, Isabelle Benoit8, Ourdia Bouzid8, Baptiste Brault1,2, Zehua Chen3, Mathias Choquer2,15,Je´rome Colle´mare4,15, Pascale Cotton15, Etienne G. Danchin20, Corinne Da Silva6, Ange´lique Gautier2, Corinne Giraud2, Tatiana Giraud21, Celedonio Gonzalez22, Sandrine Grossetete15, Ulrich Gu¨ ldener23, Bernard Henrissat7, Barbara J. Howlett24, Chinnappa Kodira3¤, Matthias Kretschmer12, Anne Lappartient15, Michaela Leroch12, Caroline Levis2, Evan Mauceli3,Ce´cile Neuve´glise25, Birgitt Oeser18, Matthew Pearson3, Julie Poulain6, Nathalie Poussereau15, Hadi Quesneville1, Christine Rascle15, Julia Schumacher18,Be´atrice Se´gurens6, Adrienne Sexton24, Evelyn Silva26, Catherine Sirven15, Darren M. Soanes27, Nicholas J. Talbot27, Matt Templeton28, Chandri Yandava3, Oded Yarden29, Qiandong Zeng3, Jeffrey A. Rollins30", Marc-Henri Lebrun1,2,15", Marty Dickman31" 1 Unite´ de Recherche Ge´nomique – Info, UR1164, INRA, Versailles, France, 2 Biologie et Gestion des Risques en Agriculture – Champignons Pathoge`nes des Plantes, UR1290, INRA, Grignon, France, 3 Broad Institute of MIT and Harvard, Cambridge, Massachusetts, United States of America, 4 Laboratory of Phytopathology, Wageningen University, Wageningen, The Netherlands, 5 Departamento de Microbiologı´a y Gene´tica, Centro Hispano-Luso de Investigaciones Agrarias, Universidad de Salamanca, Salamanca, Spain, 6 GENOSCOPE, Centre National de Se´quenc¸age, Evry, France, 7 Architecture et Fonction des Macromole´cules Biologiques, UMR6098, CNRS – Universite´ de la Me´diterrane´e et Universite´ de Provence, Marseille, France, 8 Microbiology and Kluyver Centre for Genomics of Industrial Fermentations, Utrecht, The Netherlands, 9 CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands, 10 School of Biology, University of Nottingham, Nottingham, United Kingdom, 11 Biologie et Ge´ne´tique des Interactions Plante-Parasite, CIRAD – INRA – SupAgro, Montpellier, France, 12 Faculty of Biology, Kaiserslautern University, Kaiserslautern, Germany, 13 Biology Department, University of Toronto, Mississauga, Canada, 14 Botany Department, La Trobe University, Melbourne, Australia, 15 Laboratoire de Ge´nomique Fonctionnelle des Champignons Pathoge`nes de Plantes, UMR5240, Universite´ de Lyon 1 – CNRS – BAYER S.A.S., Lyon, France, 16 Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, Israel, 17 Instituto de Investigaciones Biologicas – CONICET, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina, 18 Molekularbiologie und Biotechnologie der Pilze, Institut fu¨r Biologie und Biotechnologie der Pflanzen, Mu¨nster, Germany, 19 Landcare Research, Auckland, New Zealand, 20 Interactions Biotiques et Sante´ Plantes, UMR5240, INRA – Universite´ de Nice Sophia-Antipolis – CNRS, Sophia-Antipolis, France, 21 Laboratoire d’Ecologie, Syste´matique et Evolution, Universite´ Paris-Sud – CNRS – AgroParisTech, Orsay, France, 22 Departamento de Bioquı´mica y Biologı´a Molecular, Universidad de La Laguna, Tenerife, Spain, 23 Helmholtz Zentrum Mu¨nchen, German Research Center for Environmental Health, Institute of Bioinformatics and Systems Biology, Neuherberg, Germany, 24 School of Botany, University of Melbourne, Melbourne, Australia, 25 Biologie Inte´grative du Me´tabolisme Lipidique Microbien, UMR1319, INRA – Micalis – AgroParisTech, Thiverval-Grignon, France, 26 Fundacion Ciencia para la Vida and Facultad de Ciencias Biologicas, Universidad Andres Bello, Santiago, Chile, 27 School of Biosciences, University of Exeter, Exeter, United Kingdom, 28 Plant and Food Research, Mt. Albert Research Centre, Auckland, New Zealand, 29 Department of Plant Pathology and Microbiology, Hebrew University Jerusalem, Rehovot, Israel, 30 Department of Plant Pathology, University of Florida, Gainesville, Florida, United States of America, 31 Institute for Plant Genomics and Biotechnology, Borlaug Genomics and Bioinformatics Center, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas, United States of America Abstract Sclerotinia sclerotiorum and Botrytis cinerea are closely related necrotrophic plant pathogenic fungi notable for their wide host ranges and environmental persistence. These attributes have made these species models for understanding the complexity of necrotrophic, broad host-range pathogenicity. Despite their similarities, the two species differ in mating behaviour and the ability to produce asexual spores. We have sequenced the genomes of one strain of S. sclerotiorum and two strains of B. cinerea. The comparative analysis of these genomes relative to one another and to other sequenced fungal genomes is provided here. Their 38–39 Mb genomes include 11,860–14,270 predicted genes, which share 83% amino acid identity on average between the two species. We have mapped the S. sclerotiorum assembly to 16 chromosomes and found large-scale co-linearity with the B. cinerea genomes. Seven percent of the S. sclerotiorum genome comprises transposable elements compared to ,1% of B. cinerea. The arsenal of genes associated with necrotrophic processes is similar between the species, including genes involved in plant cell wall degradation and oxalic acid production. Analysis of secondary metabolism gene clusters revealed an expansion in number and diversity of B. cinerea–specific secondary metabolites relative to S. sclerotiorum. The potential diversity in secondary metabolism might be involved in adaptation to specific ecological niches. Comparative genome analysis revealed the basis of differing sexual mating compatibility systems between S. sclerotiorum and B. cinerea. The organization of the mating-type loci differs, and their structures provide evidence for the evolution of heterothallism from homothallism. These data shed light on the evolutionary and mechanistic bases of the genetically complex traits of necrotrophic pathogenicity and sexual mating. This resource should facilitate the functional studies designed to better understand what makes these fungi such successful and persistent pathogens of agronomic crops. PLoS Genetics | www.plosgenetics.org 1 August 2011 | Volume 7 | Issue 8 | e1002230 Genomes of Sclerotinia and Botrytis Citation: Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, et al. (2011) Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7(8): e1002230. doi:10.1371/journal.pgen.1002230 Editor: Paul M. Richardson, Progentech, United States of America Received March 14, 2011; Accepted June 22, 2011; Published August 18, 2011 Copyright: ß 2011 Amselem et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The Sclerotinia sclerotiorum genome project was supported by the USDA Cooperative State Research, Education and Extension Service (USDA-NRI 2004). Sclerotinia sclerotiorum ESTs were funded by a grant to JA Rollins from USDA specific cooperative agreement 58-5442-4-281. The genome sequence of Botrytis cinerea strain T4 was funded by Genoscope, CEA, France. M Viaud was funded by the ‘‘Projet INRA Jeune-Equipe’’. PM Coutinho and B Henrissat were funded by the ANR to project E-Tricel (grant ANR-07-BIOE-006). The CAZy database is funded in part by GIS-IBiSA. DM Soanes and NJ Talbot were partly funded by the UK Biotechnology and Biological Sciences Research Council. KM Plummer was partially funded by the New Zealand Bio-Protection Research Centre, http:// bioprotection.org.nz/. BJ Howlett and A Sexton were partially funded by the Australian Grains Research and Development Corporation, www.grdc.com.au. L Kohn was partially funded by NSERC Discovery Grant (Natural Sciences and Engineering Research Council of Canada) - Grant number 458078. M Dickman was supported by the NSF grant MCB-092391 and BARD grant US-4041-07C. O Yarden was supported by BARD grant US-4041-07C. EG Danchin obtained financial support from the European Commission (STREP FungWall grant, contract: LSHB - CT- 2004 - 511952). A Botrytis Genome Workshop (Kaiserslautern, Germany) was supported by a grant from the German Science Foundation (DFG; HA1486) to M Hahn. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: I have read the journal’s policy and have the following conflicts: author Chinnappa Kodira currently works at 454 Life Sciences, Roche. All of the work reported in this manuscript was completed when he was in residence at the Broad Institute. None of the other authors have declared any competing interests. * E-mail: [email protected] (J Amselem); [email protected] (CA Cuomo); [email protected] (JAL van Kan); [email protected] (M Viaud) ¤ Current address: 454 Life Sciences, Branford,
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