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Sex Determination in the Teleost Medaka, Oryzias

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Sex Determination in the Teleost Medaka, Oryzias A N RV260- G E39-14 ARI 15 O ctober 2005 12:55 Sex D etermination in the Teleost Medaka, Oryzias latipes Masaru Matsuda PR ES T O , Japan Science and Technology Corporation (JS T ), Laboratory of Reproductive Biology, N ational Institute for Basic Biology, O kazaki 444-8585, Japan; email: [email protected] Annu. Rev. G enet. K ey Words 2005. 39:293–307 sexual differentiation of gonads, sex-determining gene, medaka, T he Annual Review of Genetics is online at D MY D MRT1, Oryzias species http://genet.annualreviews.org Abstract doi: 10.1146/ annurev.genet.39.110304.095800 Although the sex of most animals is determined by genetic informa- Copyright c 2005 by tion, sex-determining genes had been identified only in mammals, by AUSTRALIAN NATIONAL UNIVERSITY on 03/22/09. For personal use only. Annu. Rev. Genet. 2005.39:293-307. Downloaded from arjournals.annualreviews.org Annual Reviews. All rights several flies, and the worm Caenorhabditis elegans until the recent reserved discovery of D MY (D M-domain gene on the Y chromosome) in 0066-4197/05/1215- the sex-determining region on the Y chromosome of the teleost 0293$20.00 fish medaka, Oryzias latipes. Functional and expression analyses of D MY have shown it to be the master gene for male sex determi- nation in the medaka. T he only sex-determining genes found so far in vertebrates are Sry and D MY. T herefore, the medaka is ex- pected to become a good experimental animal for investigating the precise mechanisms involved in primary sex determination in non- mammalian vertebrates. T his article reviews the origin of D MY and the sexual development of gonads in the medaka. T he putative func- tions of D MY are also discussed. 293 A N RV260- G E39-14 ARI 15 O ctober 2005 12:55 genic mice (28). N onmammalian vertebrates C ontents also have a male heterogametic (X X-X Y) sex- determination system, but no homolog of Sry I N T R O D U C T I O N . 294 could be found. Recently, we have identified M E D A K A AS A M O D E L the gene at the top of the sex-determination O R G A N ISM . 294 cascade in the teleost medaka, Oryzias latipes. SE X- D E T E R M I N AT I O N A N D T his gene, named D MY, is the first sex- SE X- D E T E R M I N I N G G E N E determining gene to be found among non- O F M E D A K A . 296 mammalian vertebrates. Sex- D etermining System of In nonmammalian vertebrates, sex- Medaka . 296 determining systems are quite diverse. Sex Identification of the is determined by heredity, environment, or Sex- D etermining G ene of both, and the pathway of sex determina- Medaka . 296 tion can be manipulated by administering E V O L U T I O N O F exogenous sex steroids during gonadal sex SE X- D E T E R M I N I N G G E N ES differentiation. T his suggests that sex steroids I N ORYZIAS SPE C I ES . 297 play a critical role in recruiting the undiffer- O rigin of D MY . 297 entiated gonad to develop either as a testis or Sex- D etermining Systems of an ovary in nonmammalian vertebrates. In Oryzias Species . 298 fish species, all the various sex-determining F U N C T I O NS O F D MY . 299 systems that exist in other vertebrate classes Morphological D evelopment of have been observed, including male het- Medaka Gonads . 299 erogametic, female heterogametic, and G ene Expression During temperature-dependent systems. Further- N ormal Sexual D evelopment of more, fish constitute the only vertebrate class Medaka Gonads . 299 that shows natural hermaphroditism, either Sexual D evelopment in simultaneous or sequential, in a significant Sex-Reversed Medaka Gonads . 300 number of species. Although much is known P U TAT I V E F U N C T I O NS about the process of sex differentiation in O F D MY . 301 fish, the precise mechanisms involved in C O N C L USI O NS . 301 primary sex determination remain undefined (7). Sex-determining systems in fish appear to be at a primitive stage of evolution (65). T herefore, knowledge of the relationships I N T R O D U C T I O N between sex-determining genes and sex by AUSTRALIAN NATIONAL UNIVERSITY on 03/22/09. For personal use only. Annu. Rev. Genet. 2005.39:293-307. Downloaded from arjournals.annualreviews.org T he sex of an individual is established by the steroids should help us to understand animal D M Y: D M-domain sex of the gonad, and in most cases, whether sex determination and sex differentiation in gene on the Y a gonad becomes a testis or an ovary is de- general, and in particular to elucidate the chromosome termined by the genome of that individual. conserved mechanisms that operate behind In most mammals, several flies, and the worm sex determination in vertebrates. Caenorhabditis elegans, the gene at the top of the sex-determination cascade is known. In mammals, the sex-determining gene SRY is M E D A K A AS A M O D E L located on the Y chromosome: SRY was first O R G A N ISM identified from a deletion analysis of the hu- T he characteristics of medaka as a model or- man Y chromosome (63). Furthermore, Sry, ganism have been reviewed by Ishikawa (15) the mouse homologue of SRY, was shown to and Wittbrodt et al. (78). Briefly, this species, be sufficient for male development in trans- a small, egg-laying freshwater fish native 294 Matsuda A N RV260- G E39-14 ARI 15 O ctober 2005 12:55 to Asia, has been established as a model diploids and triploids, Sato et al. (52) per- experimental animal in Japan. In addition to formed gene-centromere mapping of medaka its small size and short generation time like ze- sex chromosomes. ES T: expressed brafish, medaka has three advantages: a large In addition to these characteristics, sequence tag interstrain diversity among inbred strains; genome sequence and ES T (expressed se- many related species, which can be mated with quence tag) information have been expanded medaka to provide F 1 progeny; and a small rapidly to take advantage of the compact genome size (800 Mb), half that of zebrafish genome size of medaka. Sequencing of the and one third those of human and mouse. approximately 800-Mb medaka genome was Furthermore, the sex of medaka is genetically an important target of the group grant project determined, whereas the sex-determining sys- “ G enome Science” (G rant-in-Aid for Scien- tems in zebrafish and fugu, the other model tific Research on Priority Areas supported by fish, are unclear. H ence the medaka is a useful the Ministry of Education, Culture, Sports, experimental fish for analyses of the mecha- Science and Technology of Japan) that was nisms underlying sex determination and sex started at the Academia Sequencing Center differentiation. of the N ational Institute of G enetics ( N I G) Wild populations of medaka have been in mid-2002. T he H d-rR strain chosen for divided into four genetically distinct groups this purpose is an inbred strain that belongs (the N orthern, Southern, East Korean, and to the Southern population, and sequencing China- West Korean populations), which have is being conducted by the whole-genome a large genomic diversity (32, 49, 71, 72). shotgun strategy. T he initial plan was to T he nucleotide sequences of exons and in- assemble six- to eightfold coverage of 2-Kb trons of these populations differ by about 1% and 3%, respectively (43, 46). Furthermore, many inbred strains have been established from these populations; examples include the H d-rR strain (Figure 1a) from the Southern population and the H N I strain (Figure 1b) from the N orthern population (13, 14). Many Oryzias species have been used to clone many genes. D N A sequences derived from 13 species of Oryzias have been sub- mitted to public D N A databases and may be confirmed by the Taxonomy Browser of the N C BI ( N ational Center for Biotech- by AUSTRALIAN NATIONAL UNIVERSITY on 03/22/09. For personal use only. Annu. Rev. Genet. 2005.39:293-307. Downloaded from arjournals.annualreviews.org nology Information). Some species can be mated with each other to produce F 1 progeny. T his feature has wide-ranging applications in genetic and evolutionary studies of Oryzias species (78). For example, sterile males can be obtained by interbreeding different Oryzias species (9). W hen Oryzias latipes males are mated with O. curvinotus (Figure 1c) females, the male offspring are sterile but still do well Figure 1 in the mating dance. T hey can therefore in- Photographs of medaka and related species. (a) T he H d-rR strain of duce the spawning of unfertilized eggs in Oryzias latipes, male (left) and female (right); (b) the H N I strain of O. latipes, O. latipes females. Using hybrid mortality male (left) and female (right); (c) O. curvinotus, male (left) and female (right); differences between O. latipes–O. luzonensis and (d ) O. hubbsi, male (left) and female (right). www.annualreviews.org • Sex-Determination in Medaka 295 A N RV260- G E39-14 ARI 15 O ctober 2005 12:55 shotgun libraries together with longer insert Identification of the libraries (10 Kb, 40 Kb, etc.); this undertaking Sex- D etermining G ene of M edaka is currently in progress to produce a set of Identification of the sex-determining gene high-quality scaffolds.
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