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

Abstract

Since the discovery of Sry in mammals [1, 2], few other master sex-determining genes have been identified in vertebrates [3-7]. 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 [8, 9]. 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.

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.…”

A Comprehensive Transcriptome Provides Candidate Genes for Sex Determination/Differentiation and SSR/SNP Markers in Yellow Catfish

“…Interestingly, sex-determining genes were identified to be diverse in rainbow trout (Oncorhynchus mykiss), fugu (Takifugu rubripes), Patagonian pejerrey (Odontesthes hatcheri), and medaka (Oryzias latipes), and all of these genes are male-specific and located in the sex chromosome or sex-determining locus (Matsuda et al 2002;Hattori et al 2012;Kamiya et al 2012;Yano et al 2012). This variety of sex-determining genes among fish species suggests that plentiful of genetic resources and sexrelated genes should be collected and characterized to elucidate sex determination mechanism in fish, especially in yellow catfish that has no report for genes involved in sex determination and differentiation.…”

Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena

“…Sex chromosome turnover is widespread in non-mammalian vertebrates, especially in fish 9,10 , suggesting that many different genes can act as the sexdetermining signal. Several different sex-determining genes or candidates have been identified on the sex chromosomes of chicken 11 , frog 12 and fish [13][14][15][16][17][18] , but only rarely have they been formally demonstrated or their downstream pathways analysed. It is uncertain whether these genes are the major contributors to sex chromosome turnover, and it is unclear how these novel signals are integrated into the ancestral molecular pathway of sex determination.…”