Multiomics Integration Reveals Rearing System-Induced Variations in Volatile Organic Compounds, Metabolites, and Meat Quality of Lueyang Black-Bone Chickens

Indigenous chicken breeds are favored in China for superior meat quality. We compared the breast meat of Lueyang black-bone chickens reared under free-range and cage systems at four ages (120, 150, 180, and 360 days), integrating phenotypic, metabolomic, volatilomic, and transcriptomic analyses. Free-range chickens displayed a lighter meat color and reduced intramuscular fat content. At 120 days, caged chickens exhibited a richer volatile organic compound (VOC) profile correlating with fat deposition; as fat increased in the free-range group, this correlation lessened, with elevated 2-pentylfuran, tetradecanoic acid ethyl ester, and 2-nonanol. Multiomics integration revealed that the rearing system alters the muscle metabolic <i>O</i>-phosphorylethanolamine in adaptive regulation of muscle development and fat deposition via the Kennedy pathway and identified TGFB2, MAP3K, PPP3CA, and PPM1A as key regulators. These findings clarify the molecular mechanisms by which free-range rearing enhances meat quality, informing indigenous poultry production.