Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish

Abstract

Background Carotenoids contribute significantly to animal body coloration, including the spectacular color pattern diversity among fishes. Fish, as other animals, derive carotenoids from their diet. Following uptake, transport and metabolic conversion, carotenoids allocated to body coloration are deposited in the chromatophore cells of the integument. The genes involved in these processes are largely unknown. Using RNA-Sequencing, we tested for differential gene expression between carotenoid-colored and white skin regions of a cichlid fish, Tropheus duboisi “Maswa”, to identify genes associated with carotenoid-based integumentary coloration. To control for positional gene expression differences that were independent of the presence/absence of carotenoid coloration, we conducted the same analyses in a closely related population, in which both body regions are white. Results A larger number of genes (n = 50) showed higher expression in the yellow compared to the white skin tissue than vice versa (n = 9). Of particular interest was the elevated expression level of bco2a in the white skin samples, as the enzyme encoded by this gene catalyzes the cleavage of carotenoids into colorless derivatives. The set of genes with higher expression levels in the yellow region included genes involved in xanthophore formation (e.g., pax7 and sox10), intracellular pigment mobilization (e.g., tubb, vim, kif5b), as well as uptake (e.g., scarb1) and storage (e.g., plin6) of carotenoids, and metabolic conversion of lipids and retinoids (e.g., dgat2, pnpla2, akr1b1, dhrs). Triglyceride concentrations were similar in the yellow and white skin regions. Extracts of integumentary carotenoids contained zeaxanthin, lutein and beta-cryptoxanthin as well as unidentified carotenoid structures. Conclusion Our results suggest a role of carotenoid cleavage by Bco2 in fish integumentary coloration, analogous to previous findings in birds. The elevated expression of genes in carotenoid-rich skin regions with functions in retinol and lipid metabolism supports hypotheses concerning analogies and shared mechanisms between these metabolic pathways. Overlaps in the sets of differentially expressed genes (including dgat2, bscl2, faxdc2 and retsatl) between the present study and previous, comparable studies in other fish species provide useful hints to potential carotenoid color candidate genes.

Red Coloration in an Anchialine Shrimp: Carotenoids, Genetic Variation, and Candidate Genes

“…In this case, Toews et al (2016) showed that the genomes of these bird species are highly differentiated at the locus that encodes the carotenoid degradation gene, BCO2. Similarly, a transcriptomic approach in an African cichlid fish, Tropheus duboisi, revealed greater expression of BCO2; and lower expression of carotenoid uptake gene SCARB1 was associated with white versus yellow skin (Ahi et al, 2020). Variation among H. rubra lineages in the functionality or expression of BCO2, carotenoid bioconversion enzymes, or any of the other carotenoid metabolism proteins could result in the observed differences in carotenoid content in this study.…”

Neural innervation as a potential trigger of morphological color change and sexual dimorphism in cichlid fish

“…The gene gch2 encoding a pivotal protein in the pteridine biosynthetic pathway and is required for xanthophore pigmentation in zebrafish 48 . Also hsd3b1 and ttc39b have been linked to lipid and carotenoid synthesis as well as carotenoid-based coloration differences in cichlids 47,[53][54][55] . Compared to the dark morph, xanthophores are numerous in the yellow morph and densely filled with xanthosomes as supported by light microscopy (Fig.…”

“…4; Table 2). Those six pigmentation genes were hydroxy-delta-5-steroid dehydrogenase, 3 beta-and steroid delta-isomerase 1 (hsd3b1) 47 , pteridine biosynthesis enzyme GTP cyclohydrolase 2 (gch2) 48 , carotenoid droplets disperser perilipin 6 (plin6) 49 , melanophore-linage cell marker microphthalmia-associated transcription factor a (mitfa) [50][51][52] , tetratricopeptide repeat protein 39B (ttc39b) [53][54][55] and oncogenic transcription factor forkhead box Q1 (foxq1a) 56 .…”

Full-length Transcriptome Sequences and Identification of Putative Genes for Carotenoids Accumulation in Polymorphic Noble Scallop Chlamys Nobilis

“…In recent years, carotenoids accumulation in bivalves was documented in Argopecten irradians [28], Hyriopsis cumingii [30] and Patinopecten yessoensis [30]. Previous studies have shown that the mechanisms of carotenoid accumulation in bivalves involved carotenoids absorption, transportation, deposition, and metabolic processing [3]. Several genes involved in carotenoid accumulation have been identi ed, for example, in our previous study, a scavenger receptor (SRB-like-3) gene shows a signi cantly correlation with the concentration of carotenoids in the tissues of noble scallops [18].…”

“…Carotenoids are ubiquitous in the natural environment, which synthesized by plants, some bacteria and fungi [1]. Animals must acquire carotenoids through their diet, and then modi ed carotenoids to self-speci c [2,3]. In recent years, the advance in sequencing methods has deepened our understanding of the genetics process of carotenoids in animals, for example, the genes and pathways involved in carotenoids absorption, transportation and metabolism [3].…”