Gene co-expression network analysis reveals key regulatory and responsive genes regulating the intensity of carotenoid coloration in scallop muscle

Abstract

Carotenoids are biologically active pigments widely distributed in nature, playing crucial roles in the growth, development, immunity, and coloration of animals. As important nutrients, carotenoids are also considered important parameters for evaluating the economic value of farmed animals, including aquatic organisms. However, for marine animals that accumulate a large amount of specific carotenoids, the molecular mechanism underlying the bioavailability of carotenoids remains insufficiently explored, particularly with regard to the regulation of carotenoid pigmentation intensity. This study investigated the carotenoid coloration mechanism in the adductor muscle of “Haida golden scallop”, a variety of Yesso scallop (Patinopecten yessoensis), with high carotenoid content and varying coloration intensity in adductor muscle. Through transcriptomic analysis and weighted gene co-expression network analysis (WGCNA), three carotenoid accumulation-associated modules (MEgreenyellow module, MEgreen, and MEsalmon) were identified. Two PARP9/14/15 genes, previously identified as crucial regulators of carotenoid accumulation at the genomic level, were identified as the hub genes of MEgreenyellow module, which exhibited a significant positive correlation with the concentrations of both pectenolone and pectenoxanthin. Specifically, PARP9/14/15–1 showed strong connectivity with genes involved in carotenoid absorption and transport, such as LRP1, SRB-like 1, ABCA3, and StARD; while PARP9/14/15–2 was associated with NPC1L1, a gene critical for carotenoid absorption. It is proposed that PARP9/14/15s may modulate the accumulation of pectenolone and pectenoxanthin in the adductor muscle of “Haida golden scallop” by regulating the expression of these carotenoid-related genes. Furthermore, genes within the other two carotenoid accumulation-associated modules were significantly enriched in pathways related to immune response (MEgreen) and DNA damage repair (MEsalmon), suggesting that these pathways may be in response to carotenoid accumulation levels. This study provides valuable insights into the molecular mechanisms underlying carotenoid accumulation and pigmentation intensity in bivalves, offering theoretical guidance for the breeding of carotenoid-rich aquaculture strains.