Integrated physiological, transcriptomic and metabolomic analyses reveal that ABA-linked carbohydrate metabolic imbalance causes low temperature-induced pollen sterility in peanut

doi:10.1016/j.jia.2026.03.035

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Zhao Li¹, Yu Liu¹, Zehua He¹, Xiaoguang Wang¹, Chunji Jiang¹, Shuli Kang¹, Xibo Liu¹, Shuli Zhao¹, Jing Wang¹, He Zhang¹, Xinhua Zhao¹, Chao Zhong¹^#, Haiqiu Yu^1,²^#

¹College of Agronomy, Shenyang Agricultural University, Shenyang 110866, China

²Liaoning Agricultural Vocational and Technical College, Yingkou 115009, China

Hightlights

Low temperature at the flowering stage reduces peanut yield primarily by impairing pollen viability and anther function.

ABA accumulation under low temperature suppresses sugar metabolism and energy production in anthers, leading to pollen sterility.

Inhibition of ABA biosynthesis restores carbon metabolism and pollen fertility, revealing ABA–sugar crosstalk as an important regulator of reproductive low temperature tolerance.

Abstract
References

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摘要

花生（Arachis hypogaea L.）是全球重要的经济作物，在世界农业生产与经济发展中具有重要地位。开花期低温是限制高海拔和高纬度地区花生产量的重因素。尽管目前对植物营养生长阶段低温响应机制的研究已取得较多进展，但生殖生长阶段对低温胁迫的分子响应机制仍有待深入解析。为阐明低温如何影响花药功能及花粉育性，本研究在人工控制低温条件下，对耐低温基因型NH5和低温敏感基因型NH9进行了比较研究。结果表明，低温显著抑制花生生殖发育，表现为果针和荚果形成减少、花器官形态异常以及花粉活力下降。耐低温基因型NH5的产量损失和花粉损伤程度明显低于敏感基因型NH9，表明低温主要通过降低花粉质量进而影响花生产量形成。进一步的多组学分析共鉴定到20,928个差异表达基因和1,613种差异代谢物，这些差异分子显著富集于碳水化合物代谢、糖酵解以及三羧酸循环（TCA cycle）等代谢通路，表明低温敏感基因型花药中发生了显著的代谢重编程。重要的是，低温胁迫在敏感基因型中诱导脱落酸（ABA）显著积累，进而抑制关键糖代谢酶（BAM、INV、HXK、PK和CS）的活性，限制了花粉的己糖利用率。进一步实验表明，外源ABA处理会加剧花粉败育，而通过化学方法抑制ABA生物合成则能够在低温条件下恢复花粉育性并恢复碳代谢过程。综上，本研究表明ABA通过限制花生花药中糖的利用，作为生殖阶段低温耐受性的关键负调控因子发挥作用。本研究为揭示花生花器官低温适应过程中ABA与糖代谢协同调控机制提供了新的理论认识，并为培育耐低温花生品种提供了重要理论依据。

Abstract

Peanut (Arachis hypogaea L.) is a globally recognized crop with a pivotal role in the agricultural and economic sectors worldwide. Low temperature during the flowering stage is a major constraint for peanut yield in high-altitude and high-latitude regions. Despite extensive progress in understanding vegetative low temperature responses, the molecular mechanisms governing reproductive-stage low temperature sensitivity remain largely unexplored. To clarify how low temperature disrupts anther function and pollen fertility, a comparative study was conducted between a low temperature-tolerant genotype (NH5) and a low temperature-sensitive genotype (NH9) under controlled low temperature conditions. Low temperature markedly impaired peanut reproductive development by reducing peg and pod formation, altering floral organ morphology, and decreasing pollen viability, while tolerant genotype NH5 exhibited milder yield and pollen damage than sensitive NH9, indicating that low temperature primarily affects peanut yield through pollen quality deterioration. Furthermore, multi-omics profiling identified 20,928 differentially expressed genes and 1,613 metabolites, showing significant enrichment in carbohydrate metabolism, glycolysis, and tricarboxylic acid (TCA) cycle pathways, thereby highlighting severe metabolic reprogramming in low temperature-sensitive anthers. Importantly, low temperature stress triggered a pronounced accumulation of abscisic acid (ABA) in sensitive genotypes, which in turn suppressed key sugar-metabolizing enzymes activities (BAM, INV, HXK, PK, and CS) and restricted hexose availability to developing pollen. Consistently, exogenous ABA application exacerbated pollen sterility, whereas chemical inhibition of ABA biosynthesis restored fertility and reactivated carbon metabolism under low temperature conditions. Together, these findings demonstrate that ABA acts as a pivotal negative regulator of reproductive low temperature tolerance by constraining sugar utilization in peanut anthers. This study thus provides new mechanistic insight into ABA–sugar metabolism coordination during floral low temperature adaptation and offer a theoretical basis for breeding peanut varieties with enhanced low temperature resilience.

Keywords: low temperature peanut pollen viability transcriptome metabolome abscisic acid

Online: 14 March 2026

Fund:

This work was supported by CARS-13 and Liaoning Major Science and Technology Special Project 2025 JH1/11700015.

About author: #Correspondence Chao Zhong, E-mail: zhongchao1123@syau.edu.cn; Haiqiu Yu, E-mail: yuhaiqiu@syau.edu.cn

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Zhao Li, Yu Liu, Zehua He, Xiaoguang Wang, Chunji Jiang, Shuli Kang, Xibo Liu, Shuli Zhao, Jing Wang, He Zhang, Xinhua Zhao, Chao Zhong, Haiqiu Yu. 2026. Integrated physiological, transcriptomic and metabolomic analyses reveal that ABA-linked carbohydrate metabolic imbalance causes low temperature-induced pollen sterility in peanut. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.03.035

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