Coordinated Transcriptional and Metabolic Reprogramming Confers Heat Tolerance in Cucumber

Global warming has intensified frequency and severity of extreme heat events, critically threatening cucumber (Cucumis sativus L.) production worldwide. To elucidate the mechanisms underlying heat tolerance, a comparative study was conducted between a heat-tolerant cultivar (N24) and a heat-sensitive cultivar (G30) under 43 °C stress. Using a combination of RNA sequencing and widely targeted metabolomics, we found that genotype N24 exhibited superior phenotypic at ability, characterized by reduced leaf wilting, lower membrane lipid peroxidation, and more stable reactive oxygen species (ROS) homeostasis. Genotype N24 exhibited superior phenotypic stability, characterized by reduced leaf wilting, lower membrane lipid peroxidation, and more stable reactive oxygen species (ROS) homeostasis. Transcriptomic profiling showed genes associated with photosynthesis and thylakoid membrane function were upregulated in N24, while hormone signaling pathways was enriched in G30. 93 N24-specific and 83 G30-specific differentially expressed genes were identified, including transcription factors such as HSF, bHLH, and bZIP. Widely targeted metabolomics further demonstrated that specific protective metabolite, such as 3-methyluric acid was accumulated and showed the ABC transporter pathway was also significant enriched in N24 plants. Integrated transcriptomic and metabolomic analysis suggested that ABC transporters may enhanced thermotolerance by facilitating the transport and subcellular compartmentalization of antioxidant metabolites. Collectively, these findings indicated heat tolerance in cucumber involved a synergistic regulatory network encompassing photosynthesis maintenance, transcription factor activation, and ABC transporter-mediated metabolic reprogramming. This study provides novel insights and valuable genetic resources for breeding heat-resilient cucumber varieties in a warming climate.