Organelle-specific hydrogen sulfide metabolism governs redox homeostasis to regulate plant autophagy and cadmium stress resilience.

Hydrogen sulfide (H2S), traditionally regarded as a toxic threat to the environment and living organisms, is now considered an important gasotransmitter that helps regulate redox balance and autophagy in plants. However, how different sources of H2S in certain organelles help control stress responses remains unclear. In our study, how H2S is handled in various subcellular compartments of Arabidopsis thaliana was investigated in depth using null mutants defective in H2S production (des1, sir, cas-c1, str1 and str2) or consumption (oas-a1, oas-b and oas-c). Under normal physiological conditions, disruption of H2S homeostasis in any cellular compartment altered endogenous H2S levels and induced basal autophagy. These findings suggest that maintaining a specific subcellular H2S threshold is necessary to control ATG8-dependent autophagic flux. Under cadmium-induced stress, wild-type plants presented coordinated increases in cytosolic OAS-A1 levels, H2S accumulation, and protein persulfidation and decreases in sulfenylation and autophagy activation. This redox reprogramming establishes a protective redox control driven by H2S, where cadmium-induced H2O2 promotes cysteine sulfenylation followed by persulfidation, thus preventing irreversible overoxidation. Notably, this adaptive redox control was dysregulated in all the organelle-specific mutants, regardless of changes in H2S or H2O2 levels, demonstrating that the entire H2S network is required for redox protection. Cytosolic and mitochondrial mutants presented the greatest defects in Cd-induced autophagy, indicating that these compartments play a central role in stress-adaptive recycling.