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An Immune-Related Gene Evolved into the Master Sex-Determining Gene in Rainbow Trout, Oncorhynchus mykiss

2012; Elsevier BV; Volume: 22; Issue: 15 Linguagem: Inglês

10.1016/j.cub.2012.05.045

1879-0445

Ayaka Yano, René R. Guyomard, Barbara Nicol, Elodie Jouanno, Edwige Quillet, Christophe Klopp, Cédric Cabau, Olivier Bouchez, Alexis Fostier, Yann Guiguen,

Reproductive biology and impacts on aquatic species

Since the discovery of Sry in mammals [1Sinclair A.H. Berta P. Palmer M.S. Hawkins J.R. Griffiths B.L. Smith M.J. Foster J.W. Frischauf A.M. Lovell-Badge R. Goodfellow P.N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif.Nature. 1990; 346: 240-244Crossref PubMed Scopus (2575) Google Scholar, 2Koopman P. Gubbay J. Vivian N. Goodfellow P. Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry.Nature. 1991; 351: 117-121Crossref PubMed Scopus (1727) Google Scholar], few other master sex-determining genes have been identified in vertebrates [3Hattori R.S. Murai Y. Oura M. Masuda S. Majhi S.K. Sakamoto T. Fernandino J.I. Somoza G.M. Yokota M. Strüssmann C.A. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination.Proc. Natl. Acad. Sci. USA. 2012; 109: 2955-2959Crossref PubMed Scopus (351) Google Scholar, 4Yoshimoto S. Ito M. A ZZ/ZW-type sex determination in Xenopus laevis.FEBS J. 2011; 278: 1020-1026Crossref PubMed Scopus (58) Google Scholar, 5Matsuda M. Nagahama Y. Shinomiya A. Sato T. Matsuda C. Kobayashi T. Morrey C.E. Shibata N. Asakawa S. Shimizu N. et al.DMY is a Y-specific DM-domain gene required for male development in the medaka fish.Nature. 2002; 417: 559-563Crossref PubMed Scopus (1077) Google Scholar, 6Smith C.A. Roeszler K.N. Ohnesorg T. Cummins D.M. Farlie P.G. Doran T.J. Sinclair A.H. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.Nature. 2009; 461: 267-271Crossref PubMed Scopus (571) Google Scholar, 7Myosho T. Otake H. Masuyama H. Matsuda M. Kuroki Y. Fujiyama A. Naruse K. Hamaguchi S. Sakaizumi M. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis.Genetics. 2012; 191: 163-170Crossref PubMed Scopus (340) Google Scholar]. To date, all of these genes have been characterized as well-known factors in the sex differentiation pathway, suggesting that the same subset of genes have been repeatedly and independently selected throughout evolution as master sex determinants [8Schartl M. Sex chromosome evolution in non-mammalian vertebrates.Curr. Opin. Genet. Dev. 2004; 14: 634-641Crossref PubMed Scopus (169) Google Scholar, 9Marshall Graves J.A. Peichel C.L. Are homologies in vertebrate sex determination due to shared ancestry or to limited options?.Genome Biol. 2010; 11: 205Crossref PubMed Scopus (149) Google Scholar]. Here, we characterized in rainbow trout an unknown gene expressed only in the testis, with a predominant expression during testicular differentiation. This gene is a male-specific genomic sequence that is colocalized along with the sex-determining locus. This gene, named sdY for sexually dimorphic on the Y chromosome, encodes a protein that displays similarity to the C-terminal domain of interferon regulatory factor 9. The targeted inactivation of sdY in males using zinc-finger nuclease induces ovarian differentiation, and the overexpression of sdY in females using additive transgenesis induces testicular differentiation. Together, these results demonstrate that sdY is a novel vertebrate master sex-determining gene not related to any known sex-differentiating gene. These findings highlight an unexpected evolutionary plasticity in vertebrate sex determination through the demonstration that master sex determinants can arise from the de novo evolution of genes that have not been previously implicated in sex differentiation.