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

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. 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.