UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in Ustilaginoidea virens

Epigenetic modification is important for cellular functions. Trimethylation of histone H3 lysine 4 (H3K4me3), which associates with transcriptional activation, is one of the important epigenetic modifications. In this study, the biological functions of UvKmt2-mediated H3K4me3 modification were characterized in Ustilaginoidea virens, which is the causal agent of the false smut disease, one of the most destructive diseases in rice. Phenotypic analyses of the Delta Uvkmt2 mutant revealed that UvKMT2 is necessary for growth, conidiation, secondary spore formation, and virulence in U. virens. Immunoblotting and chromatin immunoprecipitation assay followed by sequencing (ChIP-seq) showed that UvKMT2 is required for the establishment of H3K4me3, which covers 1729 genes of the genome in U. virens. Further RNA-seq analysis demonstrated that UvKmt2-mediated H3K4me3 acts as an important role in transcriptional activation. In particular, H3K4me3 modification involves in the transcriptional regulation of conidiation-related and pathogenic genes, including two important mitogen-activated protein kinases UvHOG1 and UvPMK1. The down-regulation of UvHOG1 and UvPMK1 genes may be one of the main reasons for the reduced pathogenicity and stresses adaptability of the increment Uvkmt2 mutant. Overall, H3K4me3, established by histone methyltransferase UvKMT2, contributes to fungal development, secondary spore formation, virulence, and various stress responses through transcriptional regulation in U. virens.