Integrated transcriptomics and metabolomics analysis provide insights into the alleviation of waterlogging stress in maize by exogenous spermidine application

Waterlogging stress significantly impairs plant growth and reduces crop yields. Spermidine (Spd), functioning as a second messenger, demonstrates positive effects on plant growth under waterlogging stress conditions. However, the molecular mechanisms by which exogenous Spd application alleviates waterlogging stress remain unclear. This study employed physiological analysis and multi-omics approaches to investigate the effect of Spd application on waterlogging stress. The application of Spd enhanced the expression of genes related to light-harvesting complex (LHC), photosynthesis, and starch-related pathways, while inhibiting chlorophyll degradation and maintaining higher photosynthetic rates, thereby increasing biomass accumulation under waterlogging stress. The activation of genes associated with trehalose and Spd biosynthesis resulted in elevated accumulation of trehalose and endogenous Spd. The inhibition of 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACO) expression contributed to reduced ethylene emission, enhancing maize resistance to waterlogging. Following Spd application, auxin-related genes were up-regulated and indole acetic acid (IAA) content increased, promoting cell elongation in maize and maintaining normal growth under waterlogging stress. Additionally, the upregulation of lipid-related genes led to increased lipid content, protecting cell membranes under waterlogging conditions. These molecular and physiological modifications collectively enhanced resistance to waterlogging stress. These findings advance our understanding of Spd’s regulatory roles in mitigating waterlogging damage and provide valuable insights for breeding waterlogging-tolerant maize varieties.