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Due to their economic relevance, the study of plant pathogen interactions is of importance. However, elucidating these interactions and their underlying molecular mechanisms remains challenging since both host and pathogen need to be fully genetically accessible organisms. Here we present milestones in the establishment of a new biotrophic model pathosystem: Ustilago bromivora and Brachypodium sp. We provide a complete toolset, including an annotated fungal genome and methods for genetic manipulation of the fungus and its host plant. This toolset will enable researchers to easily study biotrophic interactions at the molecular level on both the pathogen and the host side. Moreover, our research on the fungal life cycle revealed a mating type bias phenomenon. U. bromivora harbors a haplo-lethal allele that is linked to one mating type region. As a result, the identified mating type bias strongly promotes inbreeding, which we consider to be a potential speciation driver.

Summary Ustilago maydis is a biotrophic pathogen causing smut disease in maize. It secretes a cocktail of effector proteins, which target different host proteins during its biotrophic stages in the host plant. One such class of proteins we identified previously is TOPLESS (TPL) and TOPLESS‐RELATED (TPR) transcriptional corepressors. Here, we screened 297 U. maydis effector candidates for their ability to interact with maize TPL protein RAMOSA 1 ENHANCER LOCUS 2 LIKE 2 (RELK2) and their ability to induce auxin signaling and thereby identified three novel TPL‐interacting protein effectors (Tip6, Tip7, and Tip8). Structural modeling and mutational analysis allowed the identification of TPL‐interaction motifs of Tip6 and Tip7. In planta interaction between Tip6 and Tip7 with RELK2 occurs mainly in nuclear compartments, whereas Tip8 colocalizes with RELK2 in a compartment outside the nucleus. Overexpression of Tip8 in nonhost plants leads to cell death, indicating recognition of the effector or its activity. By performing infection assays with single and multideletion mutants of U. maydis, we demonstrate a positive role of Tip6 and Tip7 in U. maydis virulence. Transcriptional profiling of maize leaves infected with Tip effector mutants in comparison with SG200 strain suggests Tip effector activities are not merely redundant. [ABSTRACT FROM AUTHOR]