Abstract
Heat stress poses a critical threat to legume production, predominantly by inducing reproductive failure. To unravel the complex regulatory networks associated with thermotolerance, we conducted an integrated multi-omics analysis (mRNA, miRNA, lncRNA, circRNA) of the heat-tolerant common bean cultivar Perola and the heat-sensitive Karacaşehir-90 exposed to heat stress (32°C/27°C) from vegetative growth through pod formation. We demonstrate that heat tolerance in Perola is driven not by the magnitude of the stress response, but by a distinct ‘transcriptional resilience’ mechanism. This strategy prioritizes the precise maintenance of homeostatic gene expression, effectively buffering reproductive tissues against the systemic dysregulation observed in sensitive genotypes. In contrast, Karacaşehir-90 exhibits “dysregulated transcriptional reprogramming” characterized by the significant deregulation of more than 2,600 genes in flower buds. This extensive reprogramming in the sensitive genotype is inversely proportional to the suppression of the key flowering regulator SPL14 by a genotype-specific “miRNA burst” (e.g., novel_42) and the excessive induction of lncRNA TCONS_00080848, which is inversely correlated with the suppression of the antioxidant Chalcone Synthase (CHS) gene. Perola avoids these maladaptive regulatory cascades and instead deploys a “metabolic buffering” strategy, highlighted by the > 400-fold precocious induction of Albumin-2 and LTP1 to protect reproductive organs. Furthermore, integrated competing endogenous RNA (ceRNA) network analysis reveals that while the sensitive cultivar collapses into lipid catabolism, indicative of membrane damage, the tolerant cultivar actively maintains glycolytic flux and bioenergetic stability. These results redefine heat tolerance as the capacity to prevent complex regulatory changes and prioritize metabolic protection, identifying specific ncRNA-mRNA interactions, particularly novel_42/ SPL14 and Albumin-2 , as promising targets for breeding climate-resilient crops.