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United States Department of Agriculture

Agricultural Research Service

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

Authors
item Kamper, Jorg - MAX PLANCK INST.GERMANY
item Kahmann, Regine - MAX PLANCK INST.GERMANY
item Bolker, Michael - PHILIPPS UNIV.GERMANY
item Ma, Li-Jun - BROAD INST. CAMBRIDGE
item Brefort, Thomas - MAX PLANCK INST.GERMANY
item Saville, Barry - TRENT UNIV. CANADA
item Banuett, Flora - CA STATE UNIV.LONG BEACH
item Kronstad, James - UNIV.BRITISH COLUMBIA
item Gold, Scott - UNIV. GEORGIA
item Muller, Olaf - MAX PLANCK INST.GERMANY
item Perlin, Michael - UNIV. LOUISVILLE
item Wosten, Han - UTRECHT UNIV.NETHERLANDS
item Devries, Ronald - UTRECHT UNIV.NETHERLANDS
item Ruiz-Herrera, Jose - DEPT. GENETICA, MEXICO
item Reynaga-Pena, Cristina - DEPT. GENETICA, MEXICO
item Snetselaar, Karen - SAINT JOSEPHS'S UNIV.PA
item Mccann, Michael - SAINT JOSEPHS'S UNIV.PA
item Perez-Martin, Jose - DEPT.BIOTECHNOLOGY,SPAIN
item Feldrugge, Michael - MAX PLANCK INST.GERMANY
item Basse, Christoph - MAX PLANCK INST.GERMANY
item Steinberg, Gero - MAX PLANCK INST.GERMANY
item Ibeas, Jose - PABLO DE OLAVIDE,SPAIN
item Holloman, William - CORNELL UNIV. NY
item Guzman, Plinio - DEPT. PL. GENETIC, MEXICO
item Farman, Mark - UNIV. KENTUCKY, LEXINGTON
item Stajich, Jason - DUKE UNIV. NC
item Sentandreu, Rafael - UNIV. VALENCIA, SPAIN
item Gonzalez-Prietro, Juan - DEPT.BIOTECNOLOGIA,MEXICO
item Kennell, Jack - ST.LOUIS UNIV., MO.
item Molina, Lazaro - MAX PLANCK INST.GERMANY
item Schirawski, Jan - MAX PLANCK INST.GERMANY
item Mendoza-Mendoza, Artemio - MAX PLANCK INST.GERMANY
item Greilinger, Doris - MAX PLANCK INST.GERMANY
item Munch, Karin - MAX PLANCK INST.GERMANY
item Rossel, Nicole - MAX PLANCK INST.GERMANY
item Scherer, Mario - MAX PLANCK INST.GERMANY
item Vranes, Miroslav - MAX PLANCK INST.GERMANY
item Ladendorf, Oliver - MAX PLANCK INST.GERMANY
item Vincon, Volker - MAX PLANCK INST.GERMANY
item Fuchs, Uta - MAX PLANCK INST.GERMANY
item Sandrock, Bjorn - PHILIPPS UNIV., GERMANY
item Meng, Shaowu - TRENT UNIV., CANADA
item Ho, Eric - TRENT UNIV., CANADA
item Cahill, Matt - TRENT UNIV., CANADA
item Boyce, Kylie - UNIV.BRITISH COLUMBIA
item Klose, Jana - UNIV.BRITISH COLUMBIA
item Klosterman, Steven
item Deelstra, Heine - UTRECHT UNIV.,NETHERLANDS
item Ortiz-Castellanos, Lucilia - DEPT GENETICA, MEXICO
item Li, Weixi - UNIV. KENTUCKY,LEXINGTON
item Sanchez-Alonso, Patricia - DEPT. PL. GENETIC, MEXICO
item Schreier, Peter - BAYER CROP SCI., GERMANY
item Hauser-Hahn, Isolde - BAYER CROP SCI., GERMANY
item Vaupel, Martin - BAYER CROP SCI., GERMANY
item Koopmann, Edda - BAYER CROP SCI., GERMANY
item Griedrich, Gabi - BAYER CROP SCI., GERMANY
item Voss, Hartmut - LION BIOSCIENCE,GERMANY
item Schluter, Thomas - LION BIOSCIENCE,GERMANY
item Margolis, Jonathan - EXELIXIS, INC., SAN FRAN.
item Platt, Darren - EXELIXIS, INC., SAN FRAN.
item Swimmer, Candace - EXELIXIS, INC., SAN FRAN.
item Gnirke, Andreas - EXELIXIS, INC., SAN FRAN.
item Chen, Feng - EXELIXIS, INC., SAN FRAN.
item Vysotskaia, Valentina - EXELIXIS, INC., SAN FRAN.
item Mannhaupt, Gertrud - GSF RESEARCH CTR.,GERMANY
item Guldener, Ulrich - GSF RESEARCH CTR.,GERMANY
item Munsterkotter, Martin - GSF RESEARCH CTR.,GERMANY
item Haase, Dirk - GSF RESEARCH CTR.,GERMANY
item Oesterheld, Matthias - GSF RESEARCH CTR.,GERMANY
item Mewes, Hans-Werner - GSF RESEARCH CTR.,GERMANY
item Maucell, Evan - BROAD INST, CAMBRIDGE,MA
item Decaprio, David - BROAD INST.,CAMBRIDGE,MA
item Wade, Claire - BROAD INST.,CAMBRIDGE,MA
item Butler, Jonathan - BROAD INST.,CAMBRIDGE,MA
item Young, Sarah - BROAD INST.,CAMBRIDGE,MA
item Jaffe, David - BROAD INST.,CAMBRIDGE,MA
item Calvo, Sarah - BROAD INST.,CAMBRIDGE,MA
item Nusbaum, Chad - BROAD INST.,CAMBRIDGE,MA
item Galagan, James - BROAD INST.,CAMBRIDGE,MA
item Birren, Bruce - BROAD INST.,CAMBRIDGE,MA

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 14, 2006
Publication Date: November 2, 2006
Citation: Kamper, J., Kahmann, R., Bolker, M., Ma, L., Brefort, T., Saville, B.J., Banuett, F., Kronstad, J.W., Gold, S.E., Muller, O., Perlin, M.H., Wosten, H.A., Devries, R., Ruiz-Herrera, J., Reynaga-Pena, C.G., Snetselaar, K., Mccann, M., Perez-Martin, J., Feldrugge, M., Basse, C.W., Steinberg, G., Ibeas, J., Holloman, W., Guzman, P., Farman, M., Stajich, J.E., Sentandreu, R., Gonzalez-Prietro, J.M., Kennell, J.C., Molina, L., Schirawski, J., Mendoza-Mendoza, A., Greilinger, D., Munch, K., Rossel, N., Scherer, M., Vranes, M., Ladendorf, O., Vincon, V., Fuchs, U., Sandrock, B., Meng, S., Ho, E.C., Cahill, M.J., Boyce, K.J., Klose, J., Klosterman, S.J., Deelstra, H.J., Ortiz-Castellanos, L., Li, W., Sanchez-Alonso, P., Schreier, P.H., Hauser-Hahn, I., Vaupel, M., Koopmann, E., Griedrich, G., Voss, H., Schluter, T., Margolis, J., Platt, D., Swimmer, C., Gnirke, A., Chen, F., Vysotskaia, V., Mannhaupt, G., Guldener, U., Munsterkotter, M., Haase, D., Oesterheld, M., Mewes, H., Maucell, E.W., Decaprio, D., Wade, C.M., Butler, J., Young, S., Jaffe, D.D., Calvo, S., Nusbaum, C., Galagan, J., Birren, B.W. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 2006. 444:97-101. DOI:10.1038/nature05248

Interpretive Summary: The fungus Ustilago maydis is a pathogen of maize world-wide. This fungus is a model system for the study of plant-pathogen interactions and related to other economically important fungi such as the rusts. The fungus has a saprophytic phase and biotrophic phase in which it depends on living tissue for its development. It survives and grows within the plant by the acquisition of nutrients from host tissues. One of the key findings from the analysis of the genome or the entire DNA content of Ustilago maydis are clusters of genes that encode secreted proteins. Deletion of some of these clusters encoding these secreted proteins results in a decreased or increased ability of the fungus to behave as a pathogen in maize. The secreted proteins represent unique factors that directly influence the pathogenicity of Ustilago maydis. This finding provides insights on the mechanisms of pathogenicity in Ustilago maydis and likely other biotrophic fungi.

Technical Abstract: 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 first genome sequence for amember of this economically important group of biotrophic fungi. The 20.5 Mb U. maydis genome assembly contains 6902 protein-encoding genes and lacks pathogenicity signatures found in other aggressive pathogenic fungal genomes, e.g. a battery of cell wall degrading enzymes. However, we detected unexpected genomic features responsible for the pathogenicity of this organism. Specifically, we have found 12 clusters of genes encoding small, secreted proteins with unknown function. A significant fraction of these genes exist in small gene families. Expression analysis demonstrated that most of the genes contained in these clusters are co-regulated and induced in infected tissue. Deletion of individual clusters altered the virulence of U. maydis in five cases, ranging from 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 represent the first recognition of such factors, and illuminates novel mechanisms of pathogenicity operating in biotrophic fungi. Genomic analysis is likely to similarly open up new avenues for the discovery of virulence determinants in other pathogens.

Last Modified: 7/24/2014
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