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Open Access Research article

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

Marta Tomaszkiewicz13, Domitille Chalopin1, Manfred Schartl2, Delphine Galiana1 and Jean-Nicolas Volff1*

Author Affiliations

1 Institut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, Centre National de la Recherche Scientifique UMR 5242, Université de Lyon I, 46 allée d'Italie, Lyon 69364, Lyon Cedex 07, France

2 Physiologische Chemie, Biozentrum, University of Würzburg, Am Hubland, and Comprehensive Cancer Center, University Clinic Würzburg, Josef Schneider Straße 6, Würzburg 97074, Germany

3 Present address: Center for Medical Genomics, Department of Biology, Penn State University, University Park, PA 16802, USA

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BMC Genetics 2014, 15:44  doi:10.1186/1471-2156-15-44

Published: 8 April 2014

Abstract

Background

Teleost 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.

Results

A 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).

Conclusions

These 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.

Keywords:
Platyfish; Xiphophorus maculatus; Sex determination; Sex chromosomes; Y chromosome; Testis; SGNH hydrolase; Helitron; Transposition