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

Villosiclava virens (anamorph: Ustilaginoidea virens) is a fungal pathogen that causes rice false smut, one of the most devastating diseases of rice. The Uvpks1 gene encoding polyketide synthase is responsible for the biosynthesis of ustilaginoidins, a major group of mycotoxins in V. virens. In this study, three strains, including the Uvpks1 deletion mutant ΔUvpks1, the complementation strain ΔUvpks1-C1, and the wild-type isogenic strain P1 of V. virens, were employed to investigate the role of Uvpks1 in shaping the metabolic profile and in the development, stress responses, and pathogenicity of V. virens. The deletion of Uvpks1 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 Uvpks1 resulted in reduced fungal pathogenicity toward rice plants. The findings reveal the functions of Uvpks1 in shaping the metabolic profile, development, stress responses, and pathogenicity of V. virens, which will be beneficial for developing new strategies to control rice false smut and ustilaginoidins.