Comparative Transcriptome Analysis Reveals Differential Cutaneous Gene Expression in the Color Variation of Two Ornamental Discus, Red Melon and Red Cover

Abstract

Red Melon (RM) and Red Cover (RC) discus (Symphysodon spp.) are ornamental fish varieties that were selectively bred from the wild parental lineages of the brown discus S. aquafaciatus over many generations, resulting in distinct cutaneous patterns from juveniles to adults. To better understand the underlying mechanisms, skin samples were collected from juveniles aged 60 days and adults aged 1 year from RM and RC for investigations. Microscopic observation detected xanthophores and erythrophores in all samples, except RC juveniles with no erythrophores. Melanophores were presented only in RC. The comparative analysis revealed that genes involved in pteridine synthesis (gch1 and zgc:153031), one-carbon metabolism (aldh1l2 and zgc153031), and lipid metabolism (apoda and klf1) were differentially expressed in RM juveniles, which may be associated with the development of erythrophores and xanthophores. The temporal inhibition of melanophore differentiation and development was observed in RM juveniles, coupled with elevated expression of notum2 and sost, two antagonist genes in Wnt-signaling, suggesting their roles in melanophore development. Distinct pigment pattern between RM and RC since the juvenile stage may be driven by the differential expression of multiple axial developmental genes, including GATA, ankyrin, and mitotic spindle orientation proteins. This is the first report to describe the differential growth of cutaneous pigments and the molecular processes involved in red discus. The results provided valuable insights into pigment pattern differences in an interesting ornamental fish model.