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

Abstract

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 Ca²⁺ 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.

Keywords

Drought priming / Low temperature / Metabolomics / Stress memory / Transcriptome / Wheat

Abbreviations

Not applicable.

Availability of data and materials

Data will be made available upon request.

Authors’ contributions

Y.W.: Writing original draft, formal analysis, and data curation; L.Z. and J.S.: Data curation; J.C., Q.Z., Y.Z., and D.J.: Writing, review, and editing; and X.W.: Writing, review, editing, and funding acquisition.

Declaration of compe €ting interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Author Dong Jiang (Editorial Board member) was not involved in the journalś review nor decisions related to this manuscript.

Acknowledgements

This study was supported by the National Key Research and deve-lopment Program of China (2024YFD2301305), the Jiangsu Innovation Support Program for International Science and Technology Cooperation Project (BZ2023049), the National Natural Science Foundation of China (32272213, 31771693), the China Agriculture Research System (CARS-03), and the Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP).

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.crope.2025.03.003.

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