Integrated transcriptomic and metabolomic profiling deciphers breed-, age-, and rearing system-dependent regulation of muscle development and meat quality in chickens

Chicken is an important source of protein worldwide, and its quality is influenced by breed, age, and rearing methods. However, how these factors interact at the metabolic level is not fully understood. This study examined Yandang partridge chickens, a native Chinese breed, and commercial Arbor Acres (AA) broilers under caged and free-range systems, slaughtered at 49 days (during growth) or 65 days (during fat deposition). Using multi-omics approaches (metabolomics and transcriptomics), breast muscle (BM) and leg muscle (LM) were analyzed. BM showed higher levels of flavor-related compounds such as glutamine, serine, and malic acid, while LM contained more NAD⁺ and lipids. Free-range rearing increased precursors of flavor, including glutamine and malvidin-3-glucoside, by activating glycolysis and fatty acid metabolism pathways. In Yandang chickens, leg muscle exhibited greater concentrations of flavor metabolites like serine and proline, along with elevated expression of lipid-related genes such as APOA1, compared to AA broilers. With age, BM accumulated oleic acid, while LM showed increases in polyunsaturated fatty acids (PUFAs) like docosapentaenoic acid. PPAR signaling was identified as a key pathway integrating metabolic responses with rearing conditions. These results improve our understanding of meat quality development and can inform breeding and management practices.