Abstract
BACKGROUND: Golden pompano (Trachinotus ovatus) is a commercially important aquaculture species in southern China. However, its delayed sexual maturation hampers breeding efficiency. Nell2 interacting cell ontogeny regulator 1 (Nicol1) is a novel peptide implicated in reproductive regulation in mammals and growth-related processes in fish, but its molecular mechanisms in teleosts remain poorly understood. RESULTS: This study investigated the effects of Nicol1-17, the biologically active form of Nicol1, on hepatic gene expression and metabolism in golden pompano. RNA-Seq analysis identified 59 differentially expressed (DE) long non-coding RNAs (lncRNAs) and 305 DE mRNAs following Nicol1-17 treatment. Functional enrichment analysis revealed significant involvement of these transcripts in steroid biosynthesis, MAPK signaling, and energy metabolism pathways. Protein-protein interaction and lncRNA-mRNA co-expression analyses revealed interconnected networks linking hepatic metabolism with downstream growth and reproductive regulation, suggesting a coordinated regulatory role of Nicol1. Co-expression network analysis highlighted three candidate lncRNAs (MSTRG.29233.1, MSTRG.29362.4, and MSTRG.29409.9), which were highly expressed in the brain, pituitary, liver, and gonads, and potentially regulate key genes associated with reproduction and growth. In addition, biochemical assays showed that Nicol1-17 significantly increased hepatic levels of high-density lipoprotein cholesterol and free fatty acids, as well as the activities of lipid synthesis enzymes (fatty acid synthase, malic enzyme), β-oxidation enzyme (acyl-CoA oxidase), and glucose metabolism enzyme (glucose-6-phosphate dehydrogenase). CONCLUSIONS: These findings suggest that Nicol1 participates in regulating hepatic metabolic remodeling and gene expression to coordinate growth- and reproduction-related pathways in golden pompano. This work provides a molecular framework for understanding how endocrine peptides integrate hepatic metabolism with growth and reproductive processes in teleosts and lays the groundwork for future functional and applied research in aquaculture. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-025-12264-8.