H <sub>2</sub> S-mediated protein persulfidation regulates redox metabolic flux underlying salt-stress resilience in rice
Abstract
Hydrogen sulfide (H 2 S) functions as a gaseous signaling molecule in plant stress responses through the persulfidation of protein cysteine (Cys) residues. A comprehensive, Cys site-specific map of the plant persulfidome has been lacking, despite its importance for achieving a systems-level understanding of the biological roles of Cys persulfidation. Using a state-of-the-art N -ethylmaleimide-biotin-based proteomics strategy, we generate a dynamic map of 1,691 persulfidated Cys sites in the rice ( Oryza sativa ) leaf proteome. Our results reveal a global dynamic changes in protein persulfidation during prolonged salt stress, with notable impacts on proteins involved in metal-dependent catalysis, redox metabolism, and the pentose phosphate pathway (PPP). Based on these patterns, we investigated the functional relevance of persulfidation within the nonoxidative PPP. H 2 S-mediated persulfidation decreased the activity of the representative nonoxidative PPP enzyme ribose-5-phosphate isomerase, leading to increased NADPH production and subsequent activation of NADPH-dependent redox enzymes, including monodehydroascorbate reductase (MDHAR) isoforms of the ascorbate-glutathione (AsA-GSH) cycle. Persulfidation protected MDHAR3/5 from oxidative inhibition and degradation, thereby sustaining AsA-GSH cycle capacity and supporting reactive oxygen species scavenging. This site-specific persulfidome provides a valuable resource for exploring plant redox regulation, and our functional analyses offer mechanistic insight into how H 2 S-dependent protein persulfidation modulates redox metabolic fluxes to bolster NADPH availability and maintain redox homeostasis during salt-stress adaptation.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (12)
Zhengyao Lin
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University
Mingjian Zhou
Laboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University
Xiaoyun Ma
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University
Miaomiao Li
Ling Fu
Hongfei Li
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University
Yinggao Liu
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University
Fu-Yuan Zhu
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University
Marc Van Montagu
Frank Van Breusegem
Department of Plant Biotechnology and Bioinformatics, Ghent University
Jingjing Huang
College of Life Sciences, South China Agricultural University
Yanjie Xie
State Key Laboratory for Development and Utilization of Forest Food Resources, Co-Innovation Center for Sustainable Forestry in Southern China, State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of State Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, College of Life Sciences, Nanjing Forestry University