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Ustilaginoidea virens causes rice false smut, one of the most devastating rice diseases. The pathogen produces various types of mycotoxins, such as ustilaginoidins and ustiloxins, which are harmful to both human and animal health. Histone deacetylases in fungi play an important role in regulating chromatin structure and gene expression. However, there is limited knowledge about how histone deacetylases control pathogenicity and mycotoxin biosynthesis in U. virens. Here, we characterize a putative class I histone deacetylase UvHOS2 in U. virens. The UvHos2-deletion mutants exhibit retarded vegetative growth, reduced conidial production and germination, and attenuated virulence. UvHOS2 positively regulates tolerance to various environmental stresses, including cell wall, cell membrane integrity, osmotic and oxidative stresses. UvHOS2 reduces the acetylation levels of histones at multiple Lys sites, including H3K9, H3K14, H3K27, and H3K56. ChIP-PCR assays revealed that UvHOS2-mediated H3K9 deacetylation regulates the expression of ustilaginoidin biosynthesis genes. Consistently, transcriptome analysis indicates that UvHOS2 regulates the expression of the genes involved in secondary metabolism, mycelial growth, conidiogenesis, and pathogenicity, thereby controlling U. virens virulence and mycotoxin (ustilaginoidins and sorbicillinoids) biosynthesis. This study provides a theoretical reference for revealing the epigenetic regulation of pathogenicity and mycotoxin biosynthesis in plant pathogenic fungi. [ABSTRACT FROM AUTHOR]

Ustilaginoidea virens is the causal agent of rice false smut, which has recently become one of the most important rice diseases worldwide. Ustilaginoidins, a major type of mycotoxins produced in false smut balls, greatly deteriorates grain quality. Histone acetylation and deacetylation are involved in regulating secondary metabolism in fungi. However, little is yet known on the functions of histone deacetylases (HDACs) in virulence and mycotoxin biosynthesis in U. virens. Here, we characterized the functions of the HDAC UvHOS3 in U. virens. The ΔUvhos3 deletion mutant exhibited the phenotypes of retarded growth, increased mycelial branches and reduced conidiation and virulence. The ΔUvhos3 mutants were more sensitive to sorbitol, sodium dodecyl sulphate and oxidative stress/H2O2. ΔUvhos3 generated significantly more ustilaginoidins. RNA‐Seq and metabolomics analyses also revealed that UvHOS3 is a key negative player in regulating secondary metabolism, especially mycotoxin biosynthesis. Notably, UvHOS3 mediates deacetylation of H3 and H4 at H3K9, H3K18, H3K27 and H4K8 residues. Chromatin immunoprecipitation assays indicated that UvHOS3 regulates mycotoxin biosynthesis, particularly for ustilaginoidin and sorbicillinoid production, by modulating the acetylation level of H3K18. Collectively, this study deepens the understanding of molecular mechanisms of the HDAC UvHOS3 in regulating virulence and mycotoxin biosynthesis in phytopathogenic fungi. [ABSTRACT FROM AUTHOR]