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An Ustilago maydis Gene Involved in H₂O₂ Detoxification Is Required for Virulence^[W]

Max Planck Institute for Terrestrial Microbiology, D-35043 Marburg, Germany

¹ Address correspondence to kahmann{at}mpi-marburg.mpg.de.

The fungus Ustilago maydis is a biotrophic pathogen of maize (Zea mays). In its genome we have identified an ortholog of YAP1 (for Yeast AP-1-like) from Saccharomyces cerevisae that regulates the oxidative stress response in this organism. yap1 mutants of U. maydis displayed higher sensitivity to H₂O₂ than wild-type cells, and their virulence was significantly reduced. U. maydis yap1 could partially complement the H₂O₂ sensitivity of a yap1 deletion mutant of S. cerevisiae, and a Yap1-green fluorescent protein fusion protein showed nuclear localization after H₂O₂ treatment, suggesting that Yap1 in U. maydis functions as a redox sensor. Mutations in two Cys residues prevented accumulation in the nucleus, and the respective mutant strains showed the same virulence phenotype as yap1 mutants. Diamino benzidine staining revealed an accumulation of H₂O₂ around yap1 mutant hyphae, which was absent in the wild type. Inhibition of the plant NADPH oxidase prevented this accumulation and restored virulence. During the infection, Yap1 showed nuclear localization after penetration up to 2 to 3 d after infection. Through array analysis, a large set of Yap1-regulated genes were identified and these included two peroxidase genes. Deletion mutants of these genes were attenuated in virulence. These results suggest that U. maydis is using its Yap1-controlled H₂O₂ detoxification system for coping with early plant defense responses.

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