Letter

Nature 444, 97-101 (2 November 2006) | doi:10.1038/nature05248; Received 18 August 2006; Accepted 15 September 2006

Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis

Jörg Kämper1, Regine Kahmann1, Michael Bölker2, Li-Jun Ma3, Thomas Brefort1, Barry J. Saville4,27, Flora Banuett5, James W. Kronstad6, Scott E. Gold7, Olaf Müller1, Michael H. Perlin8, Han A. B. Wösten9, Ronald de Vries9, José Ruiz-Herrera10, Cristina G. Reynaga-Peña10, Karen Snetselaar11, Michael McCann11, José Pérez-Martín12, Michael Feldbrügge1, Christoph W. Basse1, Gero Steinberg1, Jose I. Ibeas13, William Holloman14, Plinio Guzman15, Mark Farman16, Jason E. Stajich17, Rafael Sentandreu18, Juan M. González-Prieto19, John C. Kennell20, Lazaro Molina1, Jan Schirawski1, Artemio Mendoza-Mendoza1, Doris Greilinger1, Karin Münch1, Nicole Rössel1, Mario Scherer1, Miroslav Vranes caron1, Oliver Ladendorf1, Volker Vincon1, Uta Fuchs1, Björn Sandrock2, Shaowu Meng4, Eric C. H. Ho4, Matt J. Cahill4, Kylie J. Boyce6, Jana Klose6, Steven J. Klosterman7, Heine J. Deelstra9, Lucila Ortiz-Castellanos10, Weixi Li21, Patricia Sanchez-Alonso15, Peter H. Schreier22, Isolde Häuser-Hahn22, Martin Vaupel22, Edda Koopmann22, Gabi Friedrich22, Hartmut Voss23, Thomas Schlüter23, Jonathan Margolis24, Darren Platt24, Candace Swimmer24, Andreas Gnirke24, Feng Chen24, Valentina Vysotskaia24, Gertrud Mannhaupt1,25, Ulrich Güldener25, Martin Münsterkötter25, Dirk Haase25, Matthias Oesterheld25, Hans-Werner Mewes25,26, Evan W. Mauceli3, David DeCaprio3, Claire M. Wade3, Jonathan Butler3, Sarah Young3, David B. Jaffe3, Sarah Calvo3, Chad Nusbaum3, James Galagan3 & Bruce W. Birren3

  1. Department of Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse, D-35043 Marburg, Germany
  2. Department of Biology, Philipps-University Marburg, Karl-von-Frisch-Strasse 8, D-35032 Marburg, Germany
  3. The Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, Massachusetts 02142, USA
  4. Department of Biology, University of Toronto at Mississauga, 3359 Mississauga Rd, Mississauga, Ontario, L5L 1C6, Canada
  5. Department of Biological Sciences, California State University, 1250 Bellflower Boulevard, Long Beach, California 90840, USA
  6. The Michael Smith Laboratories, University of British Columbia, 2185 East Mall, Vancouver, British Columbia, V6T 1Z4, Canada
  7. Department of Plant Pathology, The University of Georgia, Athens, Georgia 30602-7274, USA
  8. Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, Kentucky 40292, USA
  9. Department of Microbiology, Institute of Biomembranes, Utrecht University, Padualaan 8, 3705 SN Utrecht, The Netherlands
  10. Departamento de Ingenieria Genetica, Unidad de Biotecnologia e Ingenieria Genetica de Plantas, Centro de Investigacion y de Estudios Avanzados del IPN, 36500 Irapuato, Gto. Mexico
  11. Department of Biology, Saint Joseph's University, 5600 City Ave, Philadelphia, Pennsylvania 19131, USA
  12. Department of Microbial Biotechnology, Centro Nacional de Biotecnologia–CSIC, Campus de Cantoblanco–UAM, 28049 Madrid, Spain
  13. Centro Andaluz de Biologia del Desarrollo, CSIC/Universidad Pablo de Olavide, Carretera de Utrera Km1, 41013 Sevilla, Spain
  14. Department of Microbiology and Immunology, Weill Medical College of Cornell University, 1300 York Avenue, New York, New York 10021, USA
  15. Department of Plant Genetic Engineering, Cinvestav, Campus-Guanajuato, Km 9.6 Libramiento Norte, 36821 Irapuato, Guanajuato, Mexico
  16. Department of Plant Pathology, University of Kentucky, 1405 Veteran's Drive, Lexington, Kentucky 40546, USA
  17. Department of Molecular Genetics and Microbiology, Duke University, Durham, North Carolina 27710, USA
  18. Departamento de Microbiología i Ecología, Facultat de Farmacia, Universitat de València, Vicent Andrés Estelles s/n, 46100 Burjassot, València, Spain
  19. Departamento de Biotecnología Vegetal II, Centro de Biotecnología Genómica-IPN, Blvd del Maestro s/n, Cd. Reynosa, Tamaulipas, 88710, México
  20. Department of Biology, St Louis University, 3507 Laclede Avenue, St Louis, Missouri 63103-2010, USA
  21. Department of Biology, University of Kentucky, 101 T. H. Morgan Building, Lexington, Kentucky 40546, USA
  22. Bayer CropScience AG, Alfred-Nobel-Strasse 50, D-40789 Monheim, Germany
  23. LION bioscience AG, Waldhofer Strasse 98, D-69123 Heidelberg, Germany
  24. Exelixis, Inc., 210 East Grand Avenue, South San Francisco, California 94080, USA
  25. Institute for Bioinformatics (MIPS), GSF National Research Center for Environment and Health, Ingolstädter Landstrasse 1, D-85764 Neuherberg, Germany
  26. Genome-oriented Bioinformatics, Technische Universität München, Am Forum 1, D-85354 Freising-Weihenstephan, Germany
  27. Present address: Forensic Science Program, Trent University, Peterborough, Ontario, K9J 7B8, Canada.

Correspondence to: Jörg Kämper1Regine Kahmann1Michael Bölker2 Correspondence and requests for materials should be addressed to R.K. (Email: kahmann@mpi-marburg.mpg.de), M.B. (Email: boelker@staff.uni-marburg.de) or J.K. (Email: kaemper@mpi-marburg.mpg.de). Author Information The whole-genome shotgun data have been deposited at GenBank under the project accession number AACP00000000. Individual, automatically generated gene models have been deposited under accession numbers XM_751055 to XM_757567.

Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant–microbe interactions1. This basidiomycete fungus does not use aggressive virulence strategies to kill its host. U. maydis belongs to the group of biotrophic parasites (the smuts) that depend on living tissue for proliferation and development2. Here we report the genome sequence for a member of this economically important group of biotrophic fungi. The 20.5-million-base U. maydis genome assembly contains 6,902 predicted protein-encoding genes and lacks pathogenicity signatures found in the genomes of aggressive pathogenic fungi, for example a battery of cell-wall-degrading enzymes. However, we detected unexpected genomic features responsible for the pathogenicity of this organism. Specifically, we found 12 clusters of genes encoding small secreted proteins with unknown function. A significant fraction of these genes exists in small gene families. Expression analysis showed that most of the genes contained in these clusters are regulated together and induced in infected tissue. Deletion of individual clusters altered the virulence of U. maydis in five cases, ranging from a complete lack of symptoms to hypervirulence. Despite years of research into the mechanism of pathogenicity in U. maydis, no 'true' virulence factors3 had been previously identified. Thus, the discovery of the secreted protein gene clusters and the functional demonstration of their decisive role in the infection process illuminate previously unknown mechanisms of pathogenicity operating in biotrophic fungi. Genomic analysis is, similarly, likely to open up new avenues for the discovery of virulence determinants in other pathogens.

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