Molecular mechanisms underlying sex change in hermaphroditic groupers

Abstract

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 highmobility 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.

Molecular basis and genetic improvement of economically important traits in aquaculture animals

“…Actually, several important genes, such as Fushi Tarazu factor-1 (FTZ-F1), Sry-related HMG-box gene 9 (SOX9), Wilms tumor gene 1 (WT1), anti-mullerian hormone (AMH), DMRT1 and the zinc finger transcription factor GATA binding proteins 4 (GATA4), have been supposed as candidate sex determination genes, and a hypothetical regulation hierarchy for sex determination and differentiation has been suggested in the hermaphroditic groupers [86]. In mammals, primary sex determination genes have been divided into 4 classes, in which class I comprises Y genes that have a male-specific effect required for spermatogenesis, class II are X genes that are expressed at a higher level in females than in males by virtue of the 2:1 ratio, class III are X genes that receive a parental imprint, and class IV are sex-specific regions of heterochromatin that exert effects on the epigenetic status of the rest of the genome [87].…”

Characterization and virus susceptibility of a skin cell line from red-spotted grouper (Epinephelus akaara)

“…RT-PCR analysis of RGV-infected RGS cells showed that RGV could replicate in RGS cells. Further study of virus replications in RGS cells was conducted by electron microscopy and immunofluorescence microscopy has shown that virus particles Introduction Groupers, which are widely distributed throughout the tropical and subtropical waters of the world, are economically important marine fish and ideal study models for development and reproduction (Zhou et al 2007;Zhou and Gui 2010). Due to the development of intensive aquaculture industry in recent years, infectious diseases caused by viruses, bacteria, and parasites have become major constraints in grouper farming, of which viruses are the most devastating and most widely reported infectious agents for cultured groupers (Chi et al 1999;Lai et al 2003;Xu et al 2010).…”

Expression characterization of testicular DMRT1 in both Sertoli cells and spermatogenic cells of polyploid gibel carp

“…Increasing evidences have indicated that most of the known sex determination genes discovered so far in vertebrates are derived from the duplicated homologs of Dmrt1 gene (Chong et al, 2013;Gamble and Zarkower, 2012;Gempe and Beye, 2011;Graves, 2013;Herpin and Schartl, 2011;Kikuchi and Hamaguchi, 2013;Matson and Zarkower, 2012;Siegal and Baker, 2005;Zhou and Gui, 2010). For gibel carp, as a unisexual lineage that is able to utilize gynogenesis as a unisexual reproduction mode, how male individuals arise and how male determination genes evolve will be the merit for further investigation.…”