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PMID: 26497145 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Turnover of Sex Chromosomes in Celebensis Group Medaka Fishes.

G3 (Bethesda, Md.) ·Vol. 5 ·No. 12 ·2015-10-23 ·Pages 2685-91

Myosho T, Takehana Y, Hamaguchi S, Sakaizumi M

Abstract

Sex chromosomes and the sex-determining (SD) gene are variable in vertebrates. In particular, medaka fishes in the genus Oryzias show an extremely large diversity in sex chromosomes and the SD gene, providing a good model to study the evolutionary process by which they turnover. Here, we investigated the sex determination system and sex chromosomes in six celebensis group species. Our sex-linkage analysis demonstrated that all species had an XX-XY sex determination system, and that the Oryzias marmoratus and O. profundicola sex chromosomes were homologous to O. latipes linkage group (LG) 10, while those of the other four species, O. celebensis, O. matanensis, O. wolasi, and O. woworae, were homologous to O. latipes LG 24. The phylogenetic relationship suggested a turnover of the sex chromosomes from O. latipes LG 24 to LG 10 within this group. Six sex-linkage maps showed that the former two and the latter four species shared a common SD locus, respectively, suggesting that the LG 24 acquired the SD function in a common ancestor of the celebensis group, and that the LG 10 SD function appeared in a common ancestor of O. marmoratus and O. profundicola after the divergence of O. matanensis. Additionally, fine mapping and association analysis in the former two species revealed that Sox3 on the Y chromosome is a prime candidate for the SD gene, and that the Y-specific 430-bp insertion might be involved in its SD function.

Keywords
Sox convergent evolution genetics of sex medaka sex chromosome sex-determining gene
MeSH Terms
Animals Chromosome Mapping Crosses, Genetic Female Genetic Linkage Genetic Markers Inheritance Patterns Male Mutation Oryzias/classification,genetics Phylogeny Sex Chromosomes Sex Determination Processes/genetics
Chemicals
Genetic Markers
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Myosho Taijun
Institute of Science and Technology, Niigata University, Niigata 950-2181, Japan [email protected].
Takehana Yusuke
Laboratory of Bioresources, National Institute for Basic Biology, Okazaki 444-8585, Japan.
Hamaguchi Satoshi
Institute of Science and Technology, Niigata University, Niigata 950-2181, Japan.
Sakaizumi Mitsuru
Institute of Science and Technology, Niigata University, Niigata 950-2181, Japan.
References (35)
35 references, click to expand
  1. Identification of the sex-determining locus in the Thai medaka, Oryzias minutillus.
    Cytogenet Genome Res. 2008;121(2):137-42 PMID: 18544937
  2. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination.
    Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):2955-9 PMID: 22323585
  3. Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish.
    Genetics. 2008 Aug;179(4):2173-82 PMID: 18689886
  4. Evolution of different Y chromosomes in two medaka species, Oryzias dancena and O. latipes.
    Genetics. 2007 Mar;175(3):1335-40 PMID: 17194774
  5. A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution.
    Genetics. 2000 Apr;154(4):1773-84 PMID: 10747068
  6. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes.
    Nature. 1990 Jul 19;346(6281):245-50 PMID: 2374589
  7. Turnover of sex chromosomes in the stickleback fishes (gasterosteidae).
    PLoS Genet. 2009 Feb;5(2):e1000391 PMID: 19229325
  8. Identification of SOX3 as an XX male sex reversal gene in mice and humans.
    J Clin Invest. 2011 Jan;121(1):328-41 PMID: 21183788
  9. Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis.
    J Cell Biol. 1996 May;133(3):667-81 PMID: 8636240
  10. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome.
    Curr Biol. 2004 Aug 24;14(16):1416-24 PMID: 15324658
  11. Functional analysis of Sox8 and Sox9 during sex determination in the mouse.
    Development. 2004 May;131(9):1891-901 PMID: 15056615
  12. Different origins of ZZ/ZW sex chromosomes in closely related medaka fishes, Oryzias javanicus and O. hubbsi.
    Chromosome Res. 2008;16(5):801-11 PMID: 18607761
  13. DMY is a Y-specific DM-domain gene required for male development in the medaka fish.
    Nature. 2002 May 30;417(6888):559-63 PMID: 12037570
  14. Molecular phylogeny of the medaka fishes genus Oryzias (Beloniformes: Adrianichthyidae) based on nuclear and mitochondrial DNA sequences.
    Mol Phylogenet Evol. 2005 Aug;36(2):417-28 PMID: 15955519
  15. The XX-XY sex-determination system in Oryzias luzonensis and O. mekongensis revealed by the sex ratio of the progeny of sex-reversed fish.
    Zoolog Sci. 2004 Oct;21(10):1015-8 PMID: 15514470
  16. Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene.
    Genetics. 2007 Dec;177(4):2075-81 PMID: 17947439
  17. Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development.
    Hum Mol Genet. 2010 Feb 1;19(3):506-16 PMID: 19933217
  18. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids.
    Evol Appl. 2013 Apr;6(3):486-96 PMID: 23745140
  19. Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes.
    Zoolog Sci. 2003 Feb;20(2):159-61 PMID: 12655179
  20. Evolution of ZZ/ZW and XX/XY sex-determination systems in the closely related medaka species, Oryzias hubbsi and O. dancena.
    Chromosoma. 2007 Oct;116(5):463-70 PMID: 17882464
  21. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators.
    Dev Biol. 2000 Nov 15;227(2):239-55 PMID: 11071752
  22. An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1927-31 PMID: 8127908
  23. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8.
    Dev Biol. 2009 Mar 15;327(2):301-12 PMID: 19124014
  24. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu).
    PLoS Genet. 2012;8(7):e1002798 PMID: 22807687
  25. Sox15 is up regulated in the embryonic mouse testis.
    Gene Expr Patterns. 2003 Aug;3(4):413-7 PMID: 12915303
  26. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif.
    Nature. 1990 Jul 19;346(6281):240-4 PMID: 1695712
  27. Origin and intra-island diversification of Sulawesi endemic Adrianichthyidae.
    Mol Phylogenet Evol. 2015 Dec;93:150-60 PMID: 26256644
  28. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss.
    Curr Biol. 2012 Aug 7;22(15):1423-8 PMID: 22727696
  29. A medaka gene map: the trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping.
    Genome Res. 2004 May;14(5):820-8 PMID: 15078856
  30. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis.
    Proc Natl Acad Sci U S A. 2008 Feb 19;105(7):2469-74 PMID: 18268317
  31. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.
    Nature. 2009 Sep 10;461(7261):267-71 PMID: 19710650
  32. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis.
    Genetics. 2012 May;191(1):163-70 PMID: 22367037
  33. Comparative genome analysis of the primary sex-determining locus in salmonid fishes.
    Genome Res. 2003 Feb;13(2):272-80 PMID: 12566405
  34. Male development of chromosomally female mice transgenic for Sry.
    Nature. 1991 May 9;351(6322):117-21 PMID: 2030730
  35. Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena.
    Nat Commun. 2014;5:4157 PMID: 24948391
Article Info
Journal
G3 (Bethesda, Md.)
Abbr.
G3 (Bethesda)
ISSN
2160-1836
Published
2015-10-23
Epub
2015-00-23
Pages
2685-91
Language
English
Region
England
NLM ID
101566598
PMCID
PMC4683641
Subset
IM
Databases
GENBANK
LC037173, LC037174, LC037175, LC037176
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