Integrated BSA-seq and RNA-seq analysis uncovers a coordinated regulatory network for heat tolerance in Argopecten irradians concentricus

Global warming threatens the sustainability of bivalve aquaculture. Deciphering the molecular mechanisms of thermal adaptation is critical for breeding heat-resilient varieties. Argopecten irradians concentricus exhibits robust heat tolerance, making it an ideal model for investigating thermal adaptation mechanisms in marine invertebrates. This study elucidated the genetic regulatory mechanisms underlying heat tolerance in A. i. concentricus using an integrated approach of BSA-seq and multi-time-point RNA-seq. Extreme phenotype pools (heat-tolerant/heat-sensitive) were established through progressive heating and recovery experiments. BSA-seq identified heat tolerance-associated SNPs predominantly in non-coding regions, with their linked genes significantly enriched in immune recognition, sphingolipid metabolism, and cAMP/Rap1 signaling pathways. Transcriptomic analysis revealed the activation of protein folding and endoplasmic reticulum stress pathways during heat stress, and the restoration of ribosome biogenesis during the recovery phase. Weighted gene co-expression network analysis (WGCNA) identified a set of candidate hub genes associated with heat tolerance. Integrated analysis of WGCNA and BSA-seq pinpointed UGGT1 as a key candidate gene, which harbors two intronic SNPs (Chr13–27,408,961/27408967) in complete linkage disequilibrium. Genotyping validation confirmed that the TT-AA genotype was significantly associated with enhanced heat tolerance and conferred significantly higher UGGT1 expression under heat stress. These findings suggest that heat tolerance in A. i. concentricus is associated with a coordinated regulatory network centered on immune defense and apoptosis-related processes, which may contribute to stress resistance and improved thermotolerance. This study provides a theoretical foundation and valuable candidate genetic resources for molecular marker-assisted breeding of thermotolerant scallop varieties.