Functional allocation of Mitogen-activated protein kinases (MAPKs) unveils thermotolerance in scallop Argopecten irradians irradians

Abstract

Global warming has significantly impacted agriculture, particularly in animal husbandry and aquaculture industry. Rising ocean temperatures due to global warming are severely affecting shellfish production, necessitating an understanding of how shellfish cope with thermal stress. The mitogen-activated protein kinases (MAPK) signaling pathway plays a crucial role in cell growth, differentiation, adaptation to environmental stress, inflammatory response, and managing high temperature stress. To investigate the function of MAPKs in bay scallops, a comparative genomics and bioinformatics approach identified three MAPK genes: AiERK, Aip38, and AiJNK. Structural and phylogenetic analyses of these proteins were conducted to determine their evolutionary relationships. Spatiotemporal expression patterns were examined at different developmental stages and in various tissues of healthy adult scallops. Additionally, the expression regulation of these genes was studied in selected tissues (hemocyte, gill, heart, mantle) following exposure to high temperatures (32 °C) for different durations (0 h, 6 h, 12 h, 24 h, 3 d, 6 d, 10 d). The spatiotemporal expressions of AiMAPKs were ubiquitous, with significant increases in AiERK expression observed at the umbo larval stage (3.09-fold), while Aip38 and AiJNK were identified as potential maternal effect genes. In adult scallops, different gene expression patterns of AiMAPKs were observed across eight tissues, with high expressions in the foot and gill, and lower expressions in the striated muscle. Following high temperature stress, AiMAPKs expressions in the gill and mantle were mainly up-regulated, while in the hemocyte, they were primarily down-regulated. These findings indicate time- and tissue-dependent expression patterns with functional allocation in response to different thermal durations. This study enhances our understanding of the function and evolution of AiMAPKs genes in shellfish and provides a theoretical basis for elucidating the energy regulation mechanism of bay scallops in response to high temperature stress.