A multicopy Y-chromosomal SGNH hydrolase gene expressed in the testis of the platyfish has been captured and mobilized by a Helitron transposon

Marta Tomaszkiewicz,Manfred Schartl,Domitille Chalopin,Jean-Nicolas Volff,Delphine Galiana

doi:10.1186/1471-2156-15-44

Abstract

BackgroundTeleost fish present a high diversity of sex determination systems, with possible frequent evolutionary turnover of sex chromosomes and sex-determining genes. In order to identify genes involved in male sex determination and differentiation in the platyfish Xiphophorus maculatus, bacterial artificial chromosome contigs from the sex-determining region differentiating the Y from the X chromosome have been assembled and analyzed.ResultsA novel three-copy gene called teximY (for testis-expressed in Xiphophorus maculatus on the Y) was identified on the Y but not on the X chromosome. A highly related sequence called texim1, probably at the origin of the Y-linked genes, as well as three more divergent texim genes were detected in (pseudo)autosomal regions of the platyfish genome. Texim genes, for which no functional data are available so far in any organism, encode predicted esterases/lipases with a SGNH hydrolase domain. Texim proteins are related to proteins from very different origins, including proteins encoded by animal CR1 retrotransposons, animal platelet-activating factor acetylhydrolases (PAFah) and bacterial hydrolases. Texim gene distribution is patchy in animals. Texim sequences were detected in several fish species including killifish, medaka, pufferfish, sea bass, cod and gar, but not in zebrafish. Texim-like genes are also present in Oikopleura (urochordate), Amphioxus (cephalochordate) and sea urchin (echinoderm) but absent from mammals and other tetrapods. Interestingly, texim genes are associated with a Helitron transposon in different fish species but not in urochordates, cephalochordates and echinoderms, suggesting capture and mobilization of an ancestral texim gene in the bony fish lineage. RT-qPCR analyses showed that Y-linked teximY genes are preferentially expressed in testis, with expression at late stages of spermatogenesis (late spermatids and spermatozeugmata).ConclusionsThese observations suggest either that TeximY proteins play a role in Helitron transposition in the male germ line in fish, or that texim genes are spermatogenesis genes mobilized and spread by transposable elements in fish genomes.

Highlights

Teleost fish present a high diversity of sex determination systems, with possible frequent evolutionary turnover of sex chromosomes and sex-determining genes
In contrast to the situation observed in mammals and birds, where sex determination systems and master sexdetermining genes have been conserved over long periods of evolution, sex determination is hypervariable in teleost fish [1,2,3,4]
Three teximY genes are clustered in the sex-determining region of the platyfish Y chromosome but are absent from the X chromosome Four overlapping Y-linked bacterial artificial chromosome (BAC) clones (B14, B29, B17 and N20; Figure 1) from the Rio Jamapa platyfish BAC genome library [13] were sequenced to completion and assembled, resulting in a total sequence of 585,694 bp in length

Summary

Introduction

Teleost fish present a high diversity of sex determination systems, with possible frequent evolutionary turnover of sex chromosomes and sex-determining genes. Parallel studies on different fish models are necessary to better understand the evolutionary dynamics of sex determination in fish Such studies have demonstrated that different, even closely related fish species can have different master sexdetermining genes. The first master sex-determining gene in fish has been identified in the medaka Oryzias latipes This gene, dmrt1bY, is a Y-chromosomal duplicate of the autosomal gene dmrt, which encodes a transcription factor with DM domain involved in male development in vertebrates [5,6]. Dmrt1bY is not present in related species from the same genus, which must possess other master sex-determining genes This is the case in Oryzias luzonensis, where the putative master sex-determining gene is gsdf (gonadal soma-derived growth factor), another gene from the sex-determining cascade [7]

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