The Methyltransferase Protein Encoded by Ustilaginoidea virens Polymycovirus 1 Suppresses Autophagy in Ustilaginoidea virens to Promote Viral Infection and Confer Host Hypovirulence.

Rice false smut (RFS), caused by the ascomycete fungus Ustilaginoidea virens (Cooke) Takahashi (teleomorph: Villosiclava virens), is a major panicle disease affecting rice production. Hypovirulence-associated mycoviruses represent promising biocontrol agents against plant fungal diseases. Here, we isolated a novel mycovirus, Ustilaginoidea virens polymycovirus 1 (UvPMV1), which alters the biological characteristics of the host fungus. Our findings demonstrate that UvPMV1 suppresses the autophagy pathway in U. virens and that autophagy is an essential defense mechanism during UvPMV1 infection. The methyltransferase (MT) protein encoded by UvPMV1 acted as an autophagy inhibitor and hypovirulence inducer by specifically interacting with the autophagy-related protein UvAtg6. Furthermore, transcriptomic and proteomic analyses revealed intricate virus-host interaction mechanisms. Collectively, we propose a model in which viral disruption of UvAtg6-mediated autophagy suppresses host defenses to enhance mycoviral proliferation. These findings present a promising biocontrol strategy against RFS and provide new insights into the agricultural application of mycoviruses.