Low-salinity stress induces JNK-mediated apoptosis and inflammation in the gills of the pearl oyster, Pinctada fucata martensii

In the stress response, c-Jun N-terminal kinase (JNK) mediated inflammatory response plays a key role in maintaining homeostasis and removing damaged cells. In this study, Pinctada fucata martensii was used as the object, and the stress response mechanism of gill tissue under low-salinity stress ( 20ppt) was systematically discussed by using the techniques of fluorescence quantification, transcriptomics, histopathology and apoptosis analysis. The results showed that low-salinity stress significantly induced the up-regulation of Pm JNK gene expression, especially in gill and hepatopancreas. Transcriptome analysis of three groups of normal salinity ( 30 ppt), low salinity stress ( 20 ppt) and inhibitor ( 20 ppt + JNK inhibitor) showed that low salinity stress resulted in a large number of differentially expressed genes significantly enriched in important biological pathways such as immune inflammatory response, apoptosis and metabolic reprogramming. Among them, the NF-κB signaling pathway was significantly activated, and the cytochrome P450 metabolic pathway also changed significantly, suggesting that the body may adapt to the low-salt environment through metabolic reprogramming. The observation of tissue sections further showed that low-salinity stress damaged the gill structure, which was characterized by disordered arrangement of epithelial cells and destruction of basement membrane integrity. JNK inhibitor treatment can alleviate the above tissue damage, indicating that JNK pathway plays a central role in low salt-induced structural damage. TUNEL experiments confirmed that low-salinity stress significantly promoted apoptosis of gill cells, and inhibition of JNK pathway could reduce the level of apoptosis, which functionally verified the role of JNK in regulating low salt-induced apoptosis. This study revealed the core position of JNK signaling pathway in the response to low-salinity stress in Pinctada fucata martensii , and elucidated its process of mediating tissue damage by coordinating multiple mechanisms such as immune inflammation, apoptosis and metabolic reprogramming. It provides a new theoretical basis for further understanding the molecular mechanism of marine shellfish responding to environmental stress. • Inhibition of JNK can reduce the damage of low salt to gill structure and inflammatory cell infiltration. • Transcriptomics revealed that low salinity activated NF-κB and P450 pathways. • JNK pathway plays a key role in low salt induced apoptosis.