Drought priming-induced low temperature stress tolerance in wheat: insight into stress memory dynamics

Drought priming is a promising strategy for enhancing plant tolerance to low temperature stress. However, the underlying stress memory mechanisms linking priming to subsequent stress responses remain understood. Here, we integrated physiological, transcriptomic, and metabolomic analyses to identify key stress memory genes or metabolites associated with priming-induced low temperature tolerance in wheat. Our results demonstrated that drought priming significantly improved cold tolerance by enhancing leaf photosynthesis, mitigating oxidative damage, and promoting osmolyte accumulation. These physiological advantages were tightly linked to transcriptional reprogramming of carbohydrate metabolism, antioxidant defense, and hormone signaling pathways, suggesting that drought priming establishes a long-term molecular and metabolic memory that enhances stress tolerance. During stress memory maintenance, primed plants sustained elevated expression of genes related to reactive oxygen species homeostasis, ethylene and brassinosteroid biosynthesis, and indole-3-acetic acid (IAA) catabolism, along with increased accumulation of abscisic acid glucosyl ester (ABA-GE). Additionally, primed plants exhibited higher expression of genes associated with carbon, nitrogen, and energy metabolism while downregulating secondary metabolite biosynthesis genes, optimizing their metabolic state for future stress adaptation. Upon stress retriggering, primed plants rapidly activated ABA, IAA, and Ca 2+ signaling pathways, upregulated antioxidant enzyme and sugar biosynthetic genes, and accumulated polyunsaturated fatty acids, lipids, and specific secondary metabolites, facilitating a swift and effective response to low temperature stress. These findings provide critical insights into the molecular and metabolic basis of stress memory in wheat, offering valuable genetic and biochemical targets for breeding climate-resilient crops and developing strategies to mitigate the impact of environmental stresses. • Drought priming enhances wheat tolerance to low-temperature stress. • It improves photosynthesis, reduces oxidative damage, and accumulates osmolytes. • Stress memory is mediated by specific genes involved in carbohydrate metabolism and hormonal regulation. • Maintenance mechanisms include ROS and hormone biosynthesis regulation. • Retriggering mechanisms involve ABA signaling and lipid accumulation.