Cucumber is an important vegetable crop with thermophilic but heat-sensitive growth characteristics. Heat stress threatens cucumber growth and development, leading to a decline in both quality and yield. However, the evaluation system and molecular mechanism of long-term heat tolerance remain unclear. Here, an evaluation system in response to long-term heat stress was established, and chlorophyll a content and catalase (CAT) activity were identified as key evaluation indices for determining the heat tolerance of cucumber seedlings. Transcriptomic and physiological analyses revealed that sugar metabolism played a pivotal role in the heat response. Notably, the expression of CsIAGLU (Indoleacetic Acid glucosyltransferase) was significantly upregulated in heat-tolerant genotype PS76, whereas it was not induced in the heat-sensitive genotype PWRG. Loss of function of CsIAGLU by gene editing resulted in increased sensitivity to heat stress along with higher sugar contents, accelerated stomatal closure, and chlorophyll degradation. Furthermore, CsDREB2C.L, a positive regulator of heat stress response, directly bound to the CsIAGLU promoter to enhance its expression. Overexpression of CsDREB2C.L and CsIAGLU maintained stable sugar contents, thereby keeping stomatal opening and sustaining leaf greening to resist heat stress. Taken together, our findings provide valuable insights into the mechanism of heat resistance in cucumber.

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