Molecular mechanisms underlying sex change in hermaphroditic groupers

Groupers are widely distributed throughout the tropical and subtropical waters of the world and are regarded as a favourite marine food fish. However, their large-scale aquaculture has been hindered by the rarity of natural males. Being protogynous hermaphrodites, groupers have been considered as study model for development and reproduction, especially for sex determination or sex differentiation, owing to the advantage that grouper gonad development undergoes transition from ovary to intersexual gonad and then to testis, and primordial germ cells and different stages of gametic cells during oogenesis and spermatogenesis are synchronously observed in the transitional gonads. Recently, a series of genes related to the reproduction regulation or sex differentiation have been identified in the groupers, mainly by researchers in China. One important finding was that the grouper gene, doublesex/male abnormal 3-related transcription factor 1 (DMRT1), is not only differentially expressed in gonads at different stages, but that it is also restricted to specific stages and specific cells of spermatogenesis. Grouper DMRT1 protein exists only in spermatogonia, primary spermatocytes and secondary spermatocytes, but not in the supporting Sertoli cells. Moreover, no introns were found in the grouper DMRT1, and no duplicated DMRT1 genes were detected. The finding implies that the intronless DMRT1 that is able to undergo rapid transcriptional turnover might be a significant gene for stimulating spermatogenesis in the protogynous hermaphroditic gonad. Additionally, we have found that grouper expression of sex-determining region Y-related high-mobility group-box gene 3 (SOX3) is a significant time point for enterable gametogenesis of primordial germ cells, because SOX3 is obviously expressed and localized in primordial germ cells. As SOX3 continues to express, the SOX3-positive primordial germ cells develop toward oogonia and then oocytes, whereas, when SOX3 expression is ceased, the SOX3-positive primordial germ cells develop toward spermatogonia. Therefore, we suggest that SOX3, as a transcription factor, might have more important roles in oogenesis than in spermatogenesis. Based on the findings, a hypothetic molecular mechanism underlying sex change is proposed in the hermaphroditic groupers, and some candidate genes related to the grouper sex change are also suggested for further research.