Revealing the key molecular mechanisms of grass carp muscle quality formation under three aquaculture modes based on multi-omics analysis

Grass carp reared under low-intervention conditions are widely recognized by consumers for their superior texture and distinct flavor. However, the mechanisms underlying the formation of their quality and flavor remain scientifically unexplored. Through multi-omics analysis, this study reveals for the first time the critical role of the "PI3K/AKT" signaling pathway in shaping grass carp muscle quality. Comparative analyses show that grass carp from spring water ecological farming and natural reservoir systems exhibit significant advantages in muscle texture, microstructure, fatty acid composition, and reduced off-flavor compounds, relative to their conventionally farmed counterparts. Transcriptomic and metabolomic evidence indicates that these quality improvements are primarily mediated through inhibition of the "PI3K/AKT" pathway. Such inhibition attenuates glycolysis and the canonical TCA cycle, while promoting an atypical TCA cycle that enhances amino acid metabolism and boosts the accumulation of glutamate (Glu) and glycine (Gly) in muscle tissue. Furthermore, PI3K downregulation suppresses peroxisome proliferator-activated receptor alpha (PPAR-α) expression, thereby reducing the synthesis of long-chain fatty acids and decreasing the abundance of fatty acids and volatile organic compounds (VOCs). In parallel, grass carp activate the leptin receptor (LEPR)-mediated glycerolipid metabolic pathway, which promotes glycerophospholipids synthesis and elevates the levels of polyunsaturated fatty acids (PUFAs) and docosahexaenoic acid (DHA). These findings provide novel insights into the molecular mechanisms underlying muscle quality formation in grass carp and establish a theoretical foundation for quality optimization and precision management in aquaculture.