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

细胞器特异性硫化氢代谢调控氧化还原稳态,从而调节植物自噬和镉胁迫耐受性。

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Abstract

Hydrogen sulfide (H(2)S), 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 H(2)S in certain organelles help control stress responses remains unclear. In our study, how H(2)S is handled in various subcellular compartments of Arabidopsis thaliana was investigated in depth using null mutants defective in H(2)S production (des1, sir, cas-c1, str1 and str2) or consumption (oas-a1, oas-b and oas-c). Under normal physiological conditions, disruption of H(2)S homeostasis in any cellular compartment altered endogenous H(2)S levels and induced basal autophagy. These findings suggest that maintaining a specific subcellular H(2)S threshold is necessary to control ATG8-dependent autophagic flux. Under cadmium-induced stress, wild-type plants presented coordinated increases in cytosolic OAS-A1 levels, H(2)S accumulation, and protein persulfidation and decreases in sulfenylation and autophagy activation. This redox reprogramming establishes a protective redox control driven by H(2)S, where cadmium-induced H(2)O(2) 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 H(2)S or H(2)O(2) levels, demonstrating that the entire H(2)S 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.

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