Integrated transcriptome and hormone reveals transgenerational effects of drought priming in enhancing low-temperature tolerance in wheat offspring

• Multigenerational drought priming enhances low-temperature tolerance in wheat. • Drought priming influences key hormonal pathways and metabolic processes in offspring. • Results support incorporating drought priming in breeding for resilient wheat varieties. Drought priming enhances plant tolerance to various abiotic stresses, including low temperature; however, its multigenerational effects in wheat remain incompletely characterized. To address this gap, we conducted a comprehensive multi-omics investigation combining transcriptomic profiling and hormone analysis to examine how drought priming across six consecutive generations influences offspring responses. Wheat plants primed during grain-filling produced offspring with substantial alterations in gene expression and metabolism when exposed to low-temperature stress. Analysis identified 424 and 1,679 differentially expressed genes (DEGs) between primed and non-primed offspring under normal and low-temperature conditions, respectively. Under low-temperature stress, primed progeny exhibited a significant reduction in N-(3-Indolylacetyl)-L-valine and marked increases in tryptamine, dihydrozeatin, and gibberellin A20 levels. Pathway enrichment analysis revealed predominant effects on plant hormone signal transduction, brassinosteroid biosynthesis, and zeatin biosynthesis pathways, highlighting the central role of hormonal regulation in enhancing stress tolerance. Analysis of carbohydrate metabolism revealed distinct generational patterns: grandparental drought priming primarily enhanced glucose-related enzyme activities, suggesting a sustained impact on glucose metabolism, while parental drought priming influenced sucrose metabolism more directly, indicating stage-specific regulatory roles. These metabolic alterations corresponded with improved physiological performance under low-temperature stress, evidenced by higher chlorophyll fluorescence and increased antioxidant enzyme activities in primed offspring. These findings demonstrate that ancestral drought priming induces heritable molecular and metabolic modifications that enhance low-temperature tolerance in wheat offspring. This transgenerational stress memory presents a promising approach for breeding wheat varieties with improved resilience to cold stress and variable climates. Integration of both parental and grandparental environmental histories into breeding programs may optimize crop stability under abiotic stress.