Integrated molecular mechanisms of salinity response in Apostichopus japonicus: focus on miRNA-driven core pathways and target gene regulation.

Salinity fluctuations pose critical physiological challenges to the sea cucumber Apostichopus japonicus. This review elucidated its molecular salinity response mechanisms, focusing on miRNA-mediated regulation and core pathways. We highlight a hierarchical network in which 8 key miRNAs fine-tune responses. let-7 targeted Solute Carrier Family 34 Member 2 (SLC34A2) and Cystathionine Gamma-Lyase (CTH), coordinating ion transport and amino acid metabolism, respectively. miR-10 targeted genes Nicotinamide Phosphoribosyltransferase (NAMPT) in energy homeostasis and TGF-Beta Activated Kinase 1 (MAP3K7) Binding Protein 1 (Table 1) to regulate MAPK/ERK signaling. miR-278-3p targeted 5-Hydroxytryptamine Receptor 2B (Htr2b) and Chloride Channel Accessory 1 (CLCA1) to modulate GPCR signaling and chloride transport. miR-2008, miR-3, miR-16, miR-22, and miR-14 coordinate vesicular trafficking, transcription, apoptosis, and autophagy via targeting Pleckstrin Homology Domain Containing A3 (PLEKHA3), Upstream Binding Transcription Factor (UBTF), ATP Binding Cassette Subfamily C Member 2 (ABCC2), Polypeptide N-Acetylgalactosaminyltransferase 2 (GALNT2), Glutamic-Oxaloacetic Transaminase 2 (Got2), Aconitase 2 (Aco2), and RNA Polymerase II Associated Protein 2 (Rpap2). Salinity sensing initiates GPCR-mediated cAMP/PKA and MAPK/ERK cascades, activating transcription factors (UBTF) to drive stress gene expression. Ion transporters (SLC family), ABC transporters, and vesicular transport maintain cellular homeostasis. Cullin Associated and Neddylation Dissociated 1 (CAND1)/Listerin E3 ubiquitin protein ligase 1 (Ltn1) are involved in amino acid/protein metabolism and ubiquitinated proteins to participate in vesicular transport for protein sorting and secreting. These secreted molecules (Glyare/Taurine) act as ligands to bind membrane receptors and trigger GPCR pathways and energy metabolism and redox balance. Aco2/Got2/NAMPT supply ATP for adaptation and apoptosis/autophagy, repair damage and maintain homeostasis, alleviate oxidative damage, supported by innate immunity genes. These findings establish a framework for understanding sea cucumbers salinity adaption, further exploration of additional genes is needed to refine mechanistic details.