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

doi:10.1016/j.jia.2025.09.024

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Junhong Guo¹^,²^,^3*, Fasih Ullah Haider^2*, Bing Dai²^,³, Peng Mu², Xiangnan Li²^,^3#

¹National Key Laboratory for Tea Plant Germplasm Innovation and Resource Utilization, Anhui Agricultural University, Hefei, Anhui 230036, China

²Key Laboratory of Black Soil Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China

³College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China

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摘要

干旱锻炼能够增强植物对多种非生物胁迫（包括低温）的耐受性，然而，其在小麦中的跨代效应尚不清楚。本研究结合转录组测序和激素分析，系统解析连续六代干旱锻炼对小麦后代低温抗性的影响。结果表明，与对照组相比，干旱锻炼的后代在正常温度和低温胁迫下分别鉴定出424和1679个差异基因。低温胁迫后，干旱锻炼后代中N-(3-吲哚乙酰基)-L-缬氨酸含量显著下降，而色胺、二氢玉米素和赤霉素20含量显著上升；富集分析结果表明植物激素信号转导、油菜素内酯及玉米素生物合成途径受到显著影响，揭示激素调控在干旱锻炼诱导子代低温抗性中具有重要作用。碳水化合物代谢酶组学分析进一步揭示了不同的代际差异：祖代干旱锻炼主要增强葡萄糖代谢相关酶的活性，而亲代干旱锻炼直接影响蔗糖代谢，反映了阶段特异性的调控功能。这些代谢变化与生理水平的变化相一致，干旱锻炼后代在低温胁迫下具有更稳定的光系统及更高的抗氧化酶活性。综上，祖代干旱锻炼可通过跨代胁迫记忆诱导稳定的分子与代谢修饰，从而增强后代小麦的低温抗性，为培育耐寒和适应气候变化的小麦新品种提供了新的策略。

Abstract

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.

Keywords: drought priming low temperature phytohormones transcriptomics transgenerational effects

Online: 23 September 2025

Fund:

This research was funded by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28020400), the National Natural Science Fund (32372228), and the Danmarks Frie Forskningsfond (0217-00084B).

About author: #Correspondence Xiangnan Li, Tel: +86-431-82536087, E-mail: lixiangnan@iga.ac.cn *These two authors contributed equally to this work.

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Junhong Guo, Fasih Ullah Haider, Bing Dai, Peng Mu, Xiangnan Li. 2025. Integrated transcriptome and hormone reveals transgenerational effects of drought priming in enhancing low-temperature tolerance in wheat offspring. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.024

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