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

Jörg Kämper, Regine Kahmann, Michael Bölker, Li Jun Ma, Thomas Brefort, Barry J. Saville, Flora Banuett, James W. Kronstad, Scott E. Gold, Olaf Müller, Michael H. Perlin, Han A.B. Wösten, Ronald De Vries, José Ruiz-Herrera, Cristina G. Reynaga-Peña, Karen Snetselaar, Michael McCann, José Pérez-Martín, Michael Feldbrügge, Christoph W. BasseGero Steinberg, Jose I. Ibeas, William Holloman, Plinio Guzman, Mark Farman, Jason E. Stajich, Rafael Sentandreu, Juan M. González-Prieto, John C. Kennell, Lazaro Molina, Jan Schirawski, Artemio Mendoza-Mendoza, Doris Greilinger, Karin Münch, Nicole Rössel, Mario Scherer, Miroslav Vraněs, Oliver Ladendorf, Volker Vincon, Uta Fuchs, Björn Sandrock, Shaowu Meng, Eric C.H. Ho, Matt J. Cahill, Kylie J. Boyce, Jana Klose, Steven J. Klosterman, Heine J. Deelstra, Lucila Ortiz-Castellanos, Weixi Li, Patricia Sanchez-Alonso, Peter H. Schreier, Isolde Häuser-Hahn, Martin Vaupel, Edda Koopmann, Gabi Friedrich, Hartmut Voss, Thomas Schlüter, Jonathan Margolis, Darren Platt, Candace Swimmer, Andreas Gnirke, Feng Chen, Valentina Vysotskaia, Gertrud Mannhaupt, Ulrich Güldener, Martin Münsterkötter, Dirk Haase, Matthias Oesterheld, Hans Werner Mewes, Evan W. Mauceli, David DeCaprio, Claire M. Wade, Jonathan Butler, Sarah Young, David B. Jaffe, Sarah Calvo, Chad Nusbaum, James Galagan, Bruce W. Birren

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Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant-microbe interactions. 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 development. 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 factors 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.

Original languageEnglish
Pages (from-to)97-101
Number of pages5
Issue number7115
StatePublished - Nov 2 2006

Bibliographical note

Funding Information:
Acknowledgements J.K., M. B. and R.K. thank G. Sawers and U. Kämper for critical reading of the manuscript. The genome sequencing of Ustilago maydis strain 521 is part of the fungal genome initiative and was funded by National Human Genome Research Institute (USA) and BayerCropScience AG (Germany). F.B. was supported by a grant from the National Institutes of Health (USA). J.K. and R.K. thank the German Ministry of Education and Science (BMBF) for financing the DNA array setup and the Max Planck Society for their support of the manual genome annotation. F.B. was supported by a grant from the National Institutes of Health, B.J.S. was supported by the Natural Sciences and Engineering Research Council of Canada and the Canada Foundation for Innovation, J.W.K. received funding from the Natural Sciences and Engineering Research Council of Canada, J.R.-H. received funding from CONACYT, México, A.M.-M. was supported by a fellowship from the Humboldt Foundation, and L.M. was supported by an EU grant.

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