Autophagy Regulates Plant Tolerance to Submergence by Modulating Photosynthesis

ABSTRACT The increase in global climate variability has increased the frequency and severity of floods, profoundly affecting agricultural production and food security worldwide. Autophagy is an intracellular catabolic pathway that is dispensable for plant responses to submergence. However, the physiological role of autophagy in plant response to submergence remains unclear. In this study, a multi‐omics approach was applied by combining transcriptomics, proteomics, and lipidomics to characterize molecular changes in the Arabidopsis autophagy‐defective mutant ( atg5‐1 ) responding to submergence. Our results revealed that submergence resulted in remarkable changes in the transcriptome, proteome, and lipidome of Arabidopsis . Under submerged conditions, the levels of chloroplastidic lipids, including monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), and phosphatidylglycerol (PG), were lower in atg5‐1 than in wild‐type, suggesting that autophagy may affect photosynthesis by regulating lipid metabolism. Consistently, photosynthesis‐related proteins and photosynthetic efficiency decreased in atg5‐1 under submergence conditions. Phenotypic analysis revealed that inhibition of photosynthesis resulted in a decreased tolerance to submergence. Compared to wild‐type plants, atg5‐1 plants showed a significant decrease in starch content after submergence. Collectively, our findings reveal a novel role for autophagy in plant response to submergence via the regulation of underwater photosynthesis and starch content.