Transcriptome and metabolome analyses reveal the pivotal role of hydrogen sulfide in promoting submergence tolerance in Arabidopsis

Abstract As the global climate changes, the frequency and severity of flood disasters have increased significantly, seriously affecting agricultural production. Hydrogen sulfide (H2S), as a gaseous signal molecule, plays an important role in plant development and stress adaptation. Previous studies suggested that H2S acts as an oxygen sensor when animals experience hypoxia. However, the role of H2S in the response and adaptation to flooding-induced hypoxia stress in plants is poorly understood. Here, we report that pretreatment with exogenous H2S or Cys significantly improved tolerance to submergence in Arabidopsis. Total submergence of soil-grown Arabidopsis increased the levels of endogenous H2S and its main endogenously generated product, cysteine (Cys) over time, and altered the expression of H2S or Cys biosynthesis- or metabolism-related genes, implying that the H2S-Cys homeostasis may contribute to regulation of tolerance to flooding. Transcriptomic and metabolomic analyses demonstrated that exogenous H2S-pretreatment activated hypoxia-responsive transcription factors and hypoxia sensing-related genes in a timely manner and limited cellular activities associated with growth through regulation of hormonal signaling, but had less influence on transcripts associated with photosynthesis. H2S-pretreatment also altered the levels of metabolites, particularly of amino acids and plant hormones, during submergence. Taken together, this study provides new insight into how H2S regulates tolerance to submergence-induced hypoxia stress and lays the foundation to design new strategies for the improvement of submergence resistance in crops.