Integrated Transcriptomic and Proteomic Analysis Unveils the Multi-Organ Regulatory Mechanisms of Growth Divergence in Grass Carp (Ctenopharyngodon idella).

Grass carp (Ctenopharyngodon idella) is an important freshwater aquaculture species in China. However, high-density farming often leads to significant growth differentiation among individuals, seriously affecting yield and product quality. Here, we conducted an integrated transcriptomic and data-independent acquisition (DIA) proteomic analysis across the brain, liver, and muscle tissues of fast-growing (FG) and slow-growing (SG) grass carp after 9 months of high-density culture. Our analysis revealed that the core mechanism driving growth differentiation is a deep decoupling of transcription and translation, where enhanced muscle translational efficiency dictates the fast-growth phenotype, while slow growth is constrained by central stress and hepatic energy depletion. In the slow growth group, the brain exhibited translational arrest and neuroinflammation, and the liver entered a state of hypermetabolism mediated by AMPK, evidenced by the post-transcriptional up-regulation of key sensors such as CAB39 (PRM ratio = 1.634) and CAMKK2 (PRM ratio = 1.295). Conversely, in the fast-growing group, the mTOR-ribosome signaling axis was strongly activated at the post-transcriptional level in the muscle (GSEA NES = -1.852), triggering myofibrillar protein deposition despite transcriptional silence in classical growth pathways. These findings elucidate the systemic molecular mechanisms of growth divergence and provide high-confidence molecular targets for developing fast-growing, stress-resilient grass carp strains for precision aquaculture breeding.