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The Ustilago maydis Forkhead Transcription Factor Fox1 Is Involved in the Regulation of Genes Required for the Attenuation of Plant Defenses During Pathogenic Development

¹Karlsruhe Institute of Technology, Institute for Applied Biosciences, Department of Genetics, D-76187 Karlsruhe, Germany, and MPI for terrestrial Microbiology, Department for Organismic Interactions, Marburg, 35043, Germany; ²Philipps-University Marburg, Department for Systematic Botany and Mycology, Marburg, D-35032, Germany

Ustilago maydis is a plant-pathogenic fungus that establishes a biotrophic relationship with its host plant, Zea mays. The pathogenic stage of U. maydis is initiated by the fusion of two haploid cells, resulting in the formation of a dikaryotic hypha that invades the plant cell. The switch from saprophytic, yeast-like cells to the biotrophic hyphae requires the complex regulation of a multitude of biological processes to constitute the compatible host--fungus interaction. Transcriptional regulators involved in the establishment of the infectious dikaryon and penetration of the host tissue have been identified; however, regulators required during the post-penetration stages remained to be elucidated. In this study, we report the identification of a U. maydis forkhead transcription factor, Fox1, which is exclusively expressed during biotrophic development. Deletion of fox1 results in reduced virulence and impaired tumor development. The Δfox1 hyphae induce the accumulation of H₂O₂ in and around infected cells and a maize defense response phenotypically represented by the encasement of proliferating hyphae in a cellulose-containing matrix. The phenotype can be attributed to the fox1-dependent deregulation of several effector genes that are linked to pathogenic development and host defense suppression.