Uvpks1, Involved in Ustilaginoidin Biosynthesis, Contributes to the Metabolic Profile, Development, Stress Responses, and Pathogenicity in Villosiclava virens

<i>Villosiclava virens</i> (anamorph: <i>Ustilaginoidea virens</i>) is a fungal pathogen that causes rice false smut, one of the most devastating diseases of rice. The <i>Uvpks1</i> gene encoding polyketide synthase is responsible for the biosynthesis of ustilaginoidins, a major group of mycotoxins in <i>V. virens</i>. In this study, three strains, including the <i>Uvpks1</i> deletion mutant Δ<i>Uvpks1</i>, the complementation strain Δ<i>Uvpks1</i>-C1, and the wild-type isogenic strain P1 of <i>V. virens</i>, were employed to investigate the role of <i>Uvpks1</i> in shaping the metabolic profile and in the development, stress responses, and pathogenicity of <i>V. virens</i>. The deletion of <i>Uvpks1</i> led to both the elimination of ustilaginoidin biosynthesis and the induction of many other secondary metabolite biosynthetic pathways. It decreased mycelial growth and sporulation, fungal tolerance to Congo red-induced cell wall damage stress, and susceptibility to the fungicides epoxiconazole and prochloraz. Meanwhile, it increased hyphal hydrophobicity, resistance to H₂O₂-induced oxidative stress and metal cation stress, and susceptibility to the fungicide azoxystrobin. Furthermore, the deletion of <i>Uvpks1</i> resulted in reduced fungal pathogenicity toward rice plants. The findings reveal the functions of <i>Uvpks1</i> in shaping the metabolic profile, development, stress responses, and pathogenicity of <i>V. virens</i>, which will be beneficial for developing new strategies to control rice false smut and ustilaginoidins.