CfSnt2-CfRpd3-Mediated H3 Deacetylation Governs the ROS-Induced Autophagy and Pathogenicity of Colletotrichum fructicola.

Reactive oxygen species (ROS) serve as critical immune factors in plants, defending against pathogens infection, but whether pathogenic fungi respond to host-derived ROS through autophagy remains obscure. We previously found that CfSnt2-mediated H3 deacetylation regulates autophagy and responses to oxidative stress in Colletotrichum fructicola, a widespread pathogenic fungus that infects over 50 crops. However, the specific regulatory mechanism is unclear, particularly how oxidative stress is linked to autophagy. Here, we provided evidence that autophagy is highly induced during C. fructicola infection and oxidative stress. We further conducted mass spectrometry analysis of CfSnt2-interacting proteins and identified the histone deacetylase CfRpd3 for functional characterization. We found that CfRpd3 was primarily localized in the nucleus and cooperated with CfSnt2 to regulate the histone H3 deacetylation. Moreover, we demonstrated that both CfRpd3 and CfSnt2 are autophagy repressors that undergo down-regulated expression during ROS-induced autophagy. Targeted gene-deletion of CfRPD3 generated a ΔCfrpd3 mutant that showed defects in growth, conidiation, appressorial formation, and responses to oxidative stress, similar to those observed in the ΔCfsnt2 mutant. These combined effects resulted in their pathogenicity defects. Taken together, our study illustrates a new mechanism by which the CfSnt2-CfRpd3-mediated H3 deacetylation precisely coordinates with autophagy to regulate ROS response and pathogenicity in C. fructicola.