Histone Deacetylase UvHST2 Is a Global Regulator of Secondary Metabolism in Ustilaginoidea virens

Ustilaginoidea virens,
the causal
agent of rice false smut, produces a large amount of mycotoxins, including
ustilaginoidins and sorbicillinoids. However, little is known about
the regulatory mechanism of mycotoxin biosynthesis inU. virens. Here, we demonstrate that the NAD+-dependent histone deacetylase UvHST2 negatively regulates
ustilaginoidin biosynthesis. UvHst2 knockout caused
retarded hypha growth and reduced conidiation and pathogenicity inU. virens. Transcriptome analysis revealed that the
transcription factor genes, transporter genes, and other tailoring
genes in eight biosynthetic gene clusters (BGCs) including ustilaginoidin
and sorbicillinoid BGCs were upregulated in ΔUvhst2. Interestingly, the UvHst2 deletion affects alternative
splicing. Metabolomics revealed that UvHST2 negatively regulates the
biosynthesis of various mycotoxins including ustilaginoidins, sorbicillin,
ochratoxin B, zearalenone, and O-M-sterigmatocystin. Combined transcriptome and metabolome analyses
uncover that UvHST2 positively regulates pathogenicity but negatively
modulates the expression of BGCs involved in secondary metabolism.
Collectively, UvHST2 functions as a global regulator of secondary
metabolism inU. virens.