Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish

Abstract

A plethora of corroborative genetic studies led to the view that, across the animal kingdom, the gene‐regulatory cascades triggering sexual development bear little resemblance to each other. As a result, the common emerging picture is that the genes at the top of the cascade are not conserved, whereas the downstream genes have homologues in a much broader spectrum of species. Among these downstream effectors, a gene family involved in sex differentiation in organisms as phylogenetically divergent as corals, Caenorhabditis elegans, Drosophila, frogs, fish, birds and mammals is the dmrt gene family. Despite the attention that Dmrt1 factors have received, to date it has not been elucidated how Dmrt1s mediate their activities and putative downstream targets have yet to be characterized. However, a remarkable amount of descriptive expression data has been gathered in a large variety of fish, particularly with respect to early gonadal differentiation and sex change. This minireview aims at distilling the current knowledge of fish dmrt1s, in terms of expression and regulation. It is shown how gonadal identities correlate with dimorphic dmrt1 expression in gonochoristic and hermaphroditic fish species. It is also described how sex steroid hormones affect gonadal identity and dmrt1 expression. Emphasis is also given to recent findings dealing with transcriptional, post‐transcriptional, post‐translational and functional regulations of the dmrt1a/dmrt1bY gene pair in medaka.

Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp

“…Dmrt1 (dsx and mab-3 related transcription factor 1) is a member of a gene family of putative transcription factors that share a highly conserved DNA binding domain (DM domain) believed to play critical roles in testis development and differentiation of vertebrates (Herpin and Schartl, 2011;Masuyama et al, 2012;Xia et al, 2007;Zarkower, 2013). Several sex determination and sex chromosome-linked genes in vertebrates such as Dmy in medaka (Matsuda et al, 2002;Nanda et al, 2002), DM-W in the W chromosome of African clawed frog (Yoshimoto et al, 2008), and Dmrt1 in the Z chromosome of birds (Smith et al, 2009), have been shown to be recently duplicated homologs of Dmrt1.…”

“…Several sex determination and sex chromosome-linked genes in vertebrates such as Dmy in medaka (Matsuda et al, 2002;Nanda et al, 2002), DM-W in the W chromosome of African clawed frog (Yoshimoto et al, 2008), and Dmrt1 in the Z chromosome of birds (Smith et al, 2009), have been shown to be recently duplicated homologs of Dmrt1. Because of the high evolutionary conservation and the newly recruited role in vertebrates (Herpin and Schartl, 2011;Xia et al, 2007), Dmrt1 also allows us to analyze the evolutionary history of genome duplication through examination of divergence and phylogeny of the duplicated genes. In this study, we analyzed Dmrt1 genes of polyploid gibel carp and closely related species to reveal genetic evidence for supporting hypotheses of the polyploidy origins.…”

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

“…4 and 5). Previously, the expressed DMRT1 was reported to be present in all of about 20 examined teleost fish species and to correlate with testis development, but the Dmrt1 expressed cells were found to be various (Herpin and Schartl, 2011;Zarkower, 2013), such as only in Sertoli cells , both in Sertoli and germ cells (Lei et al, 2007), or only in germ cells (Xia et al, 2007). In this study, we have clearly captured the cell types of Dmrt1 expression in testes, the Sertoli cells and spermatogenic cells.…”

“…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.…”

“…Although upstream sex-determination signals are diverse and changeable among species, the genes involved in the pathway are relatively conserved, which commonly contain the DNA binding motif (DM) domain (Gempe and Beye, 2011;Matson and Zarkower, 2012;Siegal and Baker, 2005;Zarkower, 2013). Especially, the Dmrt1 (dsx and mab-3 related transcription factor 1) gene had been revealed to play important roles in sex differentiation and testis development of vertebrates (Herpin and Schartl, 2011;Matson and Zarkower, 2012;Xia et al, 2007;Zarkower, 2013), and many sexdetermination or sex chromosome-linked genes had been demonstrated to be the duplicated homologs of Dmrt1 gene. For examples, DMY in medaka (Oryzias latipes), the first sex-determination gene found in nonmammalian vertebrates, was confirmed as a duplicated copy of Dmrt1 (Matsuda, 2005;Matsuda et al, 2002Matsuda et al, , 2007.…”