Transcriptomic analysis reveals PC4's participation in thermotolerance of scallop Argopecten irradians irradians by regulating myocardial bioelectric activity

Abstract

Rising ocean temperatures due to global warming pose a significant threat to the bay scallop aquaculture industry. Understanding the mechanisms of thermotolerance in bay scallops is crucial for developing thermotolerant breeds. Our prior research identified Arg0230340.1, part of the positive cofactor 4 (PC4) family, as a key gene associated with the thermotolerance index Arrhenius break temperature (ABT) in bay scallops. Further validation through RNA interference (RNAi) reinforced PC4's role in thermotolerance, offering a solid basis for investigating thermal response mechanisms in these scallops. In this study, we performed a comparative transcriptomic analysis on the temperature-sensitive hearts of bay scallops after siRNA-mediated RNAi targeting Arg0230340.1, to delve into the detailed molecular mechanism of PC4's participation in thermotolerance regulation. The analysis revealed that silencing Arg0230340.1 significantly reduced the expression of mitochondrial tRNA and rRNA, potentially affecting mitochondrial function and the heart's blood supply capacity. Conversely, the up-regulation of genes involved in energy metabolism, RNA polymerase II (RNAPII)-mediated basal transcription, and aminoacyl-tRNA synthesis pathways points to an intrinsic protective response, providing energy and substrates for damage repair and maintenance of essential functions under stress. GO and KEGG enrichment analyses indicated that the up-regulated genes were primarily associated with energy metabolism and spliceosome pathways, likely contributing to myocardial remodeling post-Arg0230340.1 knockdown. Down-regulated genes were enriched in ion channel pathways, particularly those for Na+, K+, and Ca2+ channels, whose dysfunction could disrupt normal myocardial bioelectric activity. The impaired cardiac performance resulting from RNAi targeting Arg0230340.1 reduced the cardiac workload in scallop hearts, thus affecting myocardial oxygen consumption and thermotolerance. We propose a hypothetical mechanism where PC4 down-regulation impairs cardiac bioelectric activity, leading to decreased thermotolerance in bay scallops, providing theoretical guidance for breeding thermotolerant scallop varieties and developing strategies for sustainable aquaculture in the face of long-term environmental changes.