The Comparative Survey of Coordinated Regulation of Steroidogenic Pathway in Japanese Flounder (Paralichthys olivaceus) and Chinese Tongue Sole (Cynoglossus semilaevis)

Abstract

Steroidogenesis controls the conversion of cholesterol into steroid hormones through the complex cascade reaction of various enzymes, which play essential roles in sexual differentiation and gonadal development in vertebrates, including teleosts. Japanese flounder (Paralichthys olivaceus) and Chinese tongue sole (Cynoglossus semilaevis) are important marine cultured fishes in China and have remarkable sexual dimorphism with bigger females and sex reversal scenarios from female to neo-male. Several steroidogenic genes have been analyzed individually in the two species, but there is a lack of information on the coordinated interaction of steroidogenic gene regulation. Therefore, in this study, through genomic and transcriptomic analysis, 39 and 42 steroidogenic genes were systematically characterized in P. olivaceus and C. semilaevis genomes, respectively. Phylogenetic and synteny analysis suggested a teleost specific genome duplication origin for cyp19a1a/cyp19a1b, hsd17b12a/hsd17b12b, ara/arb and esr2a/esr2b but not for star/star2 and cyp17a1/cyp17a2. Comparative transcriptome analysis revealed conserved expression patterns for steroidogenic genes in P. olivaceus and C. smilaevis gonads; star/star2, cyp11a/cyp11c, cyp17a1/cyp17a2, cyp21a, hsd3b1, hsd11b and hsd20b were strongly expressed in testis, while cyp19a1a and hsd17b genes were highly expressed in ovaries. Only a few genes were differentially expressed between male and neo-male testis of both P. olivaceus and C. semilaevis, and even fewer genes were differentially regulated in the brains of both species. Network analysis indicated that cyp11c, cyp17a1 and hsd3b1 actively interacted with other steroidogenic genes in P. olivaceus and C. semilaevis, and may play a more sophisticated role in the steroid hormone biosynthesis cascade. The coordinated interaction of steroidogenic genes provided comprehensive insights into steroidogenic pathway regulation with a global biological impact, as well as sexual development in teleost species.