Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/14/2006
Publication Date: 11/2/2006
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.