WGCNA-based integration of transcriptomics and metabolomics reveals key meat quality regulators during development in Jingyuan chickens

Jingyuan chickens are known for their unique meat flavor, but the molecular mechanisms underlying the dynamic changes in meat quality at different developmental stages remain unclear. In this study, we systematically measured the meat quality indicators of 42-, 126- and 180-day-old Jingyuan chickens, and integrated transcriptomic and metabolomic data using weighted gene co-expression network analysis (WGCNA) to identify key regulators of meat quality. The results showed that the growth and slaughter performance of 126- and 180-day-old chickens were significantly better than those of 42-day-old chickens (P < 0.05), but the slaughter rate and half-eviscerated rate of 42-day-old chickens were higher. With increasing age, the crude protein, drip loss, and crude ash content of the breast muscle increased significantly, while the water content decreased significantly (P < 0.05). WGCNA analysis revealed that in the 42- and 126-day-old groups, the greenyellow and blue modules were significantly positively correlated with meat quality indicators (P < 0.01), and their hub genes were significantly enriched in the PI3K - Akt signaling pathway, glycolysis/gluconeogenesis, fatty acid metabolism, and biosynthesis of amino acids. In the 42- and 180-day-old groups, the pink and brown modules were positively correlated with meat quality indicators(P < 0.01), and the hub genes were enriched in the MAPK signaling pathway, AMPK signaling pathway, and FoxO signaling pathway. In the 126- and 180-day-old groups, the magenta module was positively correlated with meat quality indicators (P < 0.01), and the hub genes were enriched in the MAPK signaling pathway, Wnt signaling pathway, glutathione metabolism, and GnRH signaling pathway. Metabolome data analysis showed that in the 42 - and 126 - day - old groups, the darkgrey, steelblue, sienna3, and blue modules were significantly positively correlated with meat quality indicators (P < 0.05), and their characteristic metabolites were significantly enriched in histidine metabolism, primary bile acid biosynthesis, and bile secretion. In the 42 - and 180 - day - old groups, the magenta and cyan modules were highly positively correlated with meat quality indicators (P < 0.05), and their metabolites were enriched in sphingolipid metabolism, vitamin B6 metabolism, thermogenesis, and purine metabolism. In the 126 - and 180 - day - old groups, the cyan module was highly significantly positively correlated with meat quality indicators (P < 0.05), with characteristic metabolites enriched in oxidative phosphorylation, nicotinate and nicotinamide metabolism, vitamin digestion and absorption, and the AMPK signaling pathway. Finally, eight key genes closely related to meat quality (SNORD14, IL7, HACD4, BFSP1, BCL6, FAM13A, ANKRD2, and AGXT2) and five key metabolites (p - Cresol sulfate, 2 - Piperidinone, 4 - Hydroxyquinoline, Succinic acid, and Dihydroxyacetone phosphate) were screened and identified. This study uncovers the age-dependent mechanisms regulating Jingyuan chicken meat quality. This study provides valuable insights into the genetic regulation of meat quality in Jingyuan chickens, which may inform breeding programs aiming to improve poultry meat quality.