Integrated Analysis of Phenotypic and Hepatic Transcriptomic Profiles Reveals Enhanced Cold Tolerance in Triploid Crucian Carp

Cold stress poses a critical threat to fish survival by triggering metabolic dysfunction, oxidative damage, immune suppression, and apoptosis. However, hybrid polyploid fish triploid crucian carp (3nRCR, 3n = 150) demonstrate superior stress tolerance. In this study, we investigated the cold adaptation mechanisms in different ploidy cyprinid fishes: triploid crucian carp compared to its diploid improved red crucian carp (Carassius auratus red var., RCC, 2n = 100, ♀) and improved allotetraploid (4nAT, 4n = 200, ♂) progenitors. Under controlled cooling, 3nRCR lost equilibrium at a significantly lower temperature (3.2 °C) than RCC (4.0 °C) and 4nAT (4.5 °C), confirming its superior enhanced cold resistance. Histological examination revealed minimal tissue damage in 3nRCR, characterized by reduced gill inflammation and cellular apoptosis. Transcriptomics revealed triploid-specific molecular strategies: 3nRCR uniquely activated retinol metabolism and metabolic rewiring (arginine/proline metabolism, oxidative phosphorylation). Notably, in the immune-related NLR signaling pathway, both nlrp1 and nlrp3 (key inflammasome components) were significantly downregulated in 3nRCR (p < 0.01). In contrast, genes involved in endoplasmic reticulum (ER) stress response, including chop and nrf2, were markedly upregulated, indicating a reinforced cellular stress resolution mechanism absent in both RCC and 4nAT. Our results demonstrate that triploid cold adaptation is orchestrated through a balanced interaction among mitochondrial apoptosis, ER stress, and inflammasome pathways. These findings provide novel insights into hybrid polyploid adaptation mechanisms and targets for cold-resilient aquaculture breeding.