A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis

Abstract

In the XX/XY sex-determining system, the Y-linked SRY genes of most mammals and the DMY/Dmrt1bY genes of the teleost fish medaka have been characterized as sex-determining genes that trigger formation of the testis. However, the molecular mechanism of the ZZ/ZW-type system in vertebrates, including the clawed frog Xenopus laevis, is unknown. Here, we isolated an X. laevis female genome-specific DM-domain gene, DM-W, and obtained molecular evidence of a W-chromosome in this species. The DNA-binding domain of DM-W showed a strikingly high identity (89%) with that of DMRT1, but it had no significant sequence similarity with the transactivation domain of DMRT1. In nonmammalian vertebrates, DMRT1 expression is connected to testis formation. We found DMRT1 or DM-W to be expressed exclusively in the primordial gonads of both ZZ and ZW or ZW tadpoles, respectively. Although DMRT1 showed continued expression after sex determination, DM-W was expressed transiently during sex determination. Interestingly, DM-W mRNA was more abundant than DMRT1 mRNA in the primordial gonads of ZW tadpoles early in sex determination. To assess the role of DM-W, we produced transgenic tadpoles carrying a DM-W expression vector driven by Ϸ3 kb of the 5-flanking sequence of DM-W or by the cytomegalovirus promoter. Importantly, some developing gonads of ZZ transgenic tadpoles showed ovarian cavities and primary oocytes with both drivers, suggesting that DM-W is crucial for primary ovary formation. Taken together, these results suggest that DM-W is a likely sex (ovary)-determining gene in X. laevis.T he sexual fate of metazoans is determined genetically or by environmental factors, such as temperature. In the former case, heterogametic sex chromosomes determine the male (XY() or female (ZW&) fate in many species of vertebrates. In the XX/XY sex-determining system, the Y-linked SRY genes of most mammals and the DMY/Dmrt1bY gene of the teleost fish medaka have been characterized as sex-determining genes that initiate testis formation, leading to male sexual development (1-5). In contrast, the molecular mechanism for the ZZ/ZW sex-determining system remains unclear, because no sexdetermining genes have been isolated.The Drosophila melanogaster doublesex (dsx) and Caenorhabditis elegans male abnormal (mab)-3 genes are known to control sexual development in these animals (6, 7). The two genes encode proteins containing a zinc finger-like DNA-binding motif called the DM domain. In vertebrates, the DM-domain gene DMRT1 is implicated in sexual development. In the mouse, DMRT1 is essential for postnatal testis differentiation (8, 9). In some other vertebrates, such as the chicken and turtle, DMRT1 expression is connected to testis formation in undifferentiated gonads (10-12). As mentioned above, the medaka fish gene DMY/Dmrt1bY, which is a coorthologue of DMRT1, causes testis formation as a sex-determining gene (3-5). In the chicken, which has the ZZ/ZW system, DMRT1 is located on the Z chromosome, suggesting that gene dosage may induce male development (...

Did sex chromosome turnover promote divergence of the major mammal groups?

“…However, this need not represent identity by descent, for a flatfish also has a ZW sex pair with homology to the bird ZW, and uses DMRT1 dosage to determine sex 32. DMRT1 has also been pressed into service independently by spawning copies that became a dominant male‐determiner in medaka 16, 65 or female determiner in Xenopus 66; clearly this gene is simply good at sex determination and has been independently recruited in several lineages 67.…”

Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus

“…In addition, dmy/dmrt1Yb is only found in two subspecies among more than 20 related species of medaka (Matsuda et al, 2003). Over the past several years, sex-determining genes 25 have been identified in numerous lower vertebrates, including dm-W in the amphibian Xenopus laevis (Yoshimoto et al, 2008) and gsdfY, amhY, sdY, amhr2 and sox3 in a suite of species of teleost fish, i.e., a medaka-related fish, (Oryzias luzonensis) (Myosho et al, 2012), Patagonian pejerrey (Odontesthes bonariensis) (Hattori et al, 2012), rainbow trout (Onchorhynchus mykiss) (Yano et al, 2012), tiger pufferfish (Takifugu rubripes) (Kamiya et al, 2012), and another 30 medaka-related fish (Oryzias dancena) (Takehara et al, 2014), respectively. Thus, in contrast to many other developmental processes, evolutionary diversity exists in the initial switches of sex determination.…”

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

“…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.…”