H2S-mediated protein S-sulfhydration modulates infectivity and autophagy in the rice blast fungus
Hong Hu, Mengyuan Qin, Jiening Zhang, Jintao Jiang, Zhiqin Su, Lun Guan, Zhiguang Qu, Caiyun Liu, Xuan Cai, Zhiyong Jason Ren, Yuhan Duan, Deyao Zhang, Hao Liu, Lu Zheng, Junbin Huang, Xiaolin Chen
Abstract
Hydrogen sulfide (H2S) regulates cellular activities in plants and mammals through S-sulfhydration, a post-translational modification of proteins. The role of H2S and its molecular targets in fungi, however, remains unclear. Here we show that H2S, synthesized by cystathionine γ-lyase (CSE1) in the rice blast fungus Magnaporthe oryzae, is essential for optimal fungal infection. Excessive H2S, through S-sulfhydration, impairs fungal infectivity by inhibiting autophagy. Using quantitative proteomics, we identify numerous S-sulfhydrated proteins in M. oryzae, including the autophagy-related protein ATG18. S-sulfhydration of a cysteine residue (Cys78) in ATG18 is essential for its binding to phosphatidylinositol 3-phosphate, thereby maintaining the protein’s structural stability and regulating autophagy. Thus, our study reveals a mechanism by which H2S-mediated S-sulfhydration controls autophagy in the rice blast fungus and suggests the potential use of H2S donors as a strategy to control fungal diseases by targeting fungal development and infection structures. Hydrogen sulfide regulates cellular activities in some organisms through posttranslational S-sulfhydration of proteins. Here, Hu et al. reveal mechanisms by which S-sulfhydration controls infectivity and autophagy in a phytopathogenic fungus.