Comprehensive coding and non-coding RNA analysis unveils lncRNA- and circRNA-mediated ceRNA networks regulating ER stress response in Patinopecten yessoensis under thermal stress

The Yesso scallop ( Patinopecten yessoensis ), an ancient cold-water molluscan species, faces increasing threats from rising seawater temperatures caused by global warming. Large-scale mortality events of the species caused by extremely high summer temperatures have frequently occurred in recent years, resulting in large economic losses. Non-coding RNAs (ncRNAs) are vital regulators in various biological processes, but their regulatory mechanisms in thermal stress responses of marine organisms remain poorly understood. In the present study, whole-transcriptome sequencing was performed to characterize coding and non-coding RNA profiles in Yesso scallops under acute thermal stress. A total of 2017 mRNAs, 120 miRNAs, 1477 lncRNAs, and 1929 circRNAs were differentially expressed under thermal stress. Separate lncRNA- and circRNA-mediated competitive endogenous RNA (ceRNA) networks were constructed, revealing intricate regulatory relationships between ncRNAs and target genes. Notably, genes involved in endoplasmic reticulum (ER) stress-associated response processes—correct protein folding, ER-associated degradation, and unfolded protein response—were significantly upregulated in both networks. These results provide transcriptional evidence that ER-associated protein quality-control pathways are major components of the acute thermal stress response and may be modulated, at least in part, by predicted ceRNA interactions. Moreover, the study suggests a potential ceRNA crosstalk mechanism modulating the ER stress-associated response in marine invertebrates; that is, two types of ceRNAs are predicted to bind to the same miRNA regulating the same gene’s expression involved in the ER stress-associated response. The study provides novel insights into ncRNA-mediated regulatory mechanisms underlying thermal stress responses in mollusks, and offers a theoretical foundation for the genetic breeding of thermal-tolerant varieties of scallops.