ClGAI-LIKE-ClPrx53 module regulates waterlogging-induced shoot elongation in watermelon

Waterlogging is a major abiotic stress that severely constrains plant growth and development. While studies on waterlogging tolerance have predominantly focused on wetland plants, the molecular adaptation mechanisms in xerophytes remain largely unexplored. Watermelon (Citrullus lanatus), a typical xerophyte, is highly susceptible to waterlogging and thus represents a valuable system for dissecting waterlogging adaptation in upland plants. We performed a genome-wide association study on waterlogging-induced shoot elongation using a diverse panel of 122 watermelon accessions and identified ClPrx53, which encodes a class III peroxidase, as a positive regulator of shoot elongation under waterlogging - a key component of the escape response. A causative G-to-T single-nucleotide polymorphism (SNP) in the promoter of ClPrx53 enhances its transcriptional activity and underlies natural variation in waterlogging tolerance. We further demonstrate that this SNP confers waterlogging-inducible expression of ClPrx53 and modulates the binding affinity of the DELLA protein ClGAI-LIKE to its promoter, thereby linking GA signaling to peroxidase-mediated reactive oxygen species homeostasis and shoot elongation under stress. Our work delineates a DELLA-ClPrx53 regulatory module that fine-tunes the waterlogging escape response in an upland crop, providing a precise molecular target for breeding climate-resilient crops.