Multi-Omics Integration Reveals Synergistic Metabolic Rewiring Underpinning Growth Acceleration in a Hybrid Pompano “Chenhai No. 1”

The hybrid golden pompano “Chenhai No. 1” (CH), generated through distant hybridization [(♀ Trachinotus ovatus × ♂ T. blochii) × ♂ T. ovatus], exhibits significantly enhanced growth performance compared to its parental T. ovatus (TO). To elucidate the molecular mechanisms underlying this rapid growth, we performed integrated transcriptomic and untargeted metabolomic profiling of muscle tissue. Transcriptomic analysis identified 3172 differentially expressed genes (DEGs), with weighted gene co-expression network analysis (WGCNA) highlighting the ‘darkorange2’ module as strongly associated with rapid growth. Key DEGs, including mapk8a, acacb, and pkmb, were upregulated and implicated in energy metabolism, glycolysis, and signal transduction. Metabolomic profiling detected 576 significantly altered metabolites, predominantly enriched in glycolysis, the tricarboxylic acid (TCA) cycle, amino acid metabolism, lipid biosynthesis, and mTOR signaling. Integrated analysis revealed coordinated alterations between core module genes and differential metabolites in interrelated pathways, including correlations between pfkpa/pfkma and glyceraldehyde-3-phosphate, acacb and phosphatidylcholine/phosphatidylethanolamine, and sesn2 and leucine. These findings suggest that the growth advantage of CH arises from the coordinated enhancement of energy metabolism, amino acid sensing, and lipid metabolic remodeling, establishing a synergistic transcription–metabolism regulatory network. This study provides multi-omics insights into the molecular basis of rapid growth in an economically important teleost fish.