Abstract
DMY, the first sex-determining gene to be described in a nonmammal vertebrate was recently characterized in the medaka fish (Oryzias latipes). It is homologous to DMRT1, a conserved gene of the sex determination cascade in vertebrates. We have checked the near complete genomes of two other percomorph fishes, Tetraodon nigroviridis and Takifugu rubripes, for supplementary homologs of DMRT1 and DMY. We also compared the new gene, DMY, to its homolog DMRT1 from all available vertebrates. Finally, we found evidence for sex-specific expression and alternative splicing of the homolog from T. nigroviridis. Our results show that DMY is a recent duplicate of DMRT1 in the medaka. Its role in sex determination was not acquired through an acceleration of evolutionary rates, but by translocation to the Y chromosome and possibly changes at key positions.
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References
J Adachi M Hasegawa (1992) ArticleTitleMOLPHY: Programs for molecular phylogenetics, I. PROTML: Maximum likelihood inference of protein phylogeny. Computer Science Monographs 27 1–77
SF Altschul W Gish W Miller EW Myers DJ Lipman (1990) ArticleTitleBasic local alignment search tool. J Mol Biol 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712
S Aparicio J Chapman E Stupka N Putnam J-M Chia P Dehal et al. (2002) ArticleTitleWhole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297 1301–1310 Occurrence Handle10.1126/science.1072104 Occurrence Handle1:CAS:528:DC%2BD38Xms1ejtr8%3D Occurrence Handle12142439
A Baumstark M Akhverdyan A Schulze I Reisert W Vogel W Just (2001) ArticleTitleExclusion of SOX9 as the testis determining factor in Ellobius lutescens: Evidence for another testis determining gene besides SRY and SOX9. Mol Genet Metab 72 61–66 Occurrence Handle10.1006/mgme.2000.3105 Occurrence Handle1:CAS:528:DC%2BD3MXjt1yjtQ%3D%3D Occurrence Handle11161830
E Birney J Thompson TJ Gibson (1996) ArticleTitlePairWise and Search Wise: Finding the optimal alignment in a simultaneous comparison of a protein profile against all DNA translation frames. Nucleic Acids Res 24 2730–2739 Occurrence Handle10.1093/nar/24.14.2730 Occurrence Handle1:CAS:528:DyaK28XkslWls7g%3D Occurrence Handle8759004
B Brunner U Hornung Z Shan I Nanda M Kondo E Zend-Ajusch et al. (2001) ArticleTitleGenomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77 8–17 Occurrence Handle10.1006/geno.2001.6615 Occurrence Handle1:CAS:528:DC%2BD3MXmsVyrtbc%3D Occurrence Handle11543627
L Duret D Mouchiroud M Gouy (1994) ArticleTitleHOVERGEN: A database of homologous vertebrate genes. Nucleic Acids Res 22 2360–2365 Occurrence Handle1:CAS:528:DyaK2cXlt1Kltrg%3D Occurrence Handle8036164
J Felsenstein (1985) ArticleTitleConfidence limits on phylogenies: An approach using the bootstrap. Evolution 39 783–791
A Force M Lynch FB Pickett A Amores Y-L Yan J Postlethwait (1999) ArticleTitlePreservation of duplicate genes by complementary, degenerative mutations. Genetics 151 1531–473 Occurrence Handle1:CAS:528:DyaK1MXisV2rs7o%3D Occurrence Handle10101175
N Galtier M Gouy C Gautier (1996) ArticleTitleSEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12 543–548 Occurrence Handle1:CAS:528:DyaK2sXhtlWktLw%3D Occurrence Handle9021275
G Guan T Kobayashi Y Nagahama (2000) ArticleTitleSexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the Tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 272 662–666 Occurrence Handle10.1006/bbrc.2000.2840 Occurrence Handle1:CAS:528:DC%2BD3cXktVKktrw%3D Occurrence Handle10860811
X Huang H Cheng Y Guo L Liu J Gui R Zhou (2002) ArticleTitleA conserved family of doublesex-related genes from fishes. J Exp Zool 294 63–67 Occurrence Handle10.1002/jez.10044 Occurrence Handle1:CAS:528:DC%2BD38Xjt1Wqtbg%3D Occurrence Handle11932949
DT Jones WR Taylor JM Thornton (1992) ArticleTitleThe rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8 275–282 Occurrence Handle1:CAS:528:DyaK38Xlt1Okt7w%3D Occurrence Handle1633570
H Kishino M Hasegawa (1989) ArticleTitleEvaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29 170–179 Occurrence Handle1:CAS:528:DyaL1MXkvFCnsbc%3D Occurrence Handle2509717
M Kondo I Nanda U Hornung S Asakawa N Shimizu H Mitani et al. (2003) ArticleTitleAbsence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr Biol 13 41–42 Occurrence Handle10.1016/S0960-9822(03)00125-8 Occurrence Handle12526743
P Koopman KA Loffler (2003) ArticleTitleSex determination: The fishy tale of dmrt1. Curr Biol 13 R177–R179 Occurrence Handle10.1016/S0960-9822(03)00117-9 Occurrence Handle1:CAS:528:DC%2BD3sXhvFaitLg%3D Occurrence Handle12620206
WH Li (1993) ArticleTitleUnbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36 96–99 Occurrence Handle1:CAS:528:DyaK3sXnsVCmsA%3D%3D Occurrence Handle8433381
O Marchand M Govoroun H D’Cotta O McMeel J Lareyre A Bernot et al. (2000) ArticleTitleDMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 1495 180–187
JA Marshall Graves S Shetty (2001) ArticleTitleSex from W to Z: Evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool 290 449–462 Occurrence Handle10.1002/jez.1088 Occurrence Handle1:STN:280:DC%2BD3MrgslSjsQ%3D%3D Occurrence Handle11555852
M Matsuda Y Nagahama A Shinomiya T Sato C Matsuda T Kobayashi et al. (2002) ArticleTitleDMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 559–563 Occurrence Handle10.1038/nature751 Occurrence Handle1:CAS:528:DC%2BD38XktVehtb8%3D Occurrence Handle12037570
B Moniot P Berta G Scherer P Sudbeck F Poulat (2000) ArticleTitleMale specific expression suggests role of DMRT1 in human sex determination. Mech Dev 91 323–325 Occurrence Handle10.1016/S0925-4773(99)00267-1 Occurrence Handle1:CAS:528:DC%2BD3cXhsVagtrg%3D Occurrence Handle10704857
I Nanda Z Shan M Schartl DW Burt M Koehler H Nothwang et al. (1999) ArticleTitle300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21 258–259 Occurrence Handle1:CAS:528:DyaK1MXitVCit7k%3D Occurrence Handle10080173
C Ottolenghi K McElreavey (2000) ArticleTitleDeletions of 9p and the quest for a conserved mechanism of sex determination. Mol Genet Metab 71 397–404 Occurrence Handle10.1006/mgme.2000.3060 Occurrence Handle1:CAS:528:DC%2BD3cXms1yjuro%3D Occurrence Handle11001833
P Pamilo NO Bianchi (1993) ArticleTitleEvolution of the Zfx and Zfy genes: Rates and interdependence between the genes. Mol Biol Evol 10 271–281 Occurrence Handle1:CAS:528:DyaK3sXitVKlurs%3D Occurrence Handle8487630
CS Raymond MW Murphy MG O’Sullivan VJ Bardwell D Zarkower (2000) ArticleTitleDmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14 2587–2595 Occurrence Handle10.1101/gad.834100 Occurrence Handle1:CAS:528:DC%2BD3cXnslGru70%3D Occurrence Handle11040213
M Robinson-Rechavi D Huchon (2000) ArticleTitleRRTree: Relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16 296–297 Occurrence Handle10.1093/bioinformatics/16.3.296 Occurrence Handle1:CAS:528:DC%2BD3cXksFaisr4%3D Occurrence Handle10869026
M Robinson-Rechavi V Laudet (2001) ArticleTitleEvolutionary rates of duplicate genes in fish and mammals. Mol Biol Evol 18 681–683 Occurrence Handle1:CAS:528:DC%2BD3MXis1eitrs%3D Occurrence Handle11264421
M Robinson-Rechavi O Marchand H Escriva P-L Bardet D Zelus S Hughes V Laudet (2001) ArticleTitleEuteleost fish genomes are characterized by expansion of gene families. Genome Res 11 781–788 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wmurg%3D Occurrence Handle11337474
H Roest Crollius O Jaillon C Dasilva C Ozouf-Costaz C Fizames C Fischer et al. (2000) ArticleTitleCharacterization and repeat analysis of the compact genome of the freshwater pufferfish Tetraodon nigroviridis. Genome Res 10 939–949 Occurrence Handle10899143
N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D
HA Schmidt K Strimmer M Vingron A von Haeseler (2002) ArticleTitleTREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 502–504
S Soullier C Hanni F Catzeflis P Berta V Laudet (1998) ArticleTitleMale sex determination in the spiny rat Tokudaia osimensis (Rodentia: Muridae) is not Sry dependent. Mamm Genome 9 590–592 Occurrence Handle10.1007/s003359900823 Occurrence Handle1:CAS:528:DyaK1cXks1Gjsr8%3D Occurrence Handle9657859
B Venkatesh Y Ning S Brenner (1999) ArticleTitleLate changes in spliceosomal introns define clades in vertebrate evolution. Proc Natl Acad Sci USA 96 10267–10271 Occurrence Handle10.1073/pnas.96.18.10267 Occurrence Handle1:CAS:528:DyaK1MXlvFensrY%3D Occurrence Handle10468597
PS Western AH Sinclair (2001) ArticleTitleSex, genes, and heat: Triggers of diversity. J Exp Zool 290 624–631 Occurrence Handle10.1002/jez.1113 Occurrence Handle1:CAS:528:DC%2BD3MXotlylsrc%3D Occurrence Handle11748611
CI Wu WH Li (1985) ArticleTitleEvidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82 1741–1745 Occurrence Handle1:CAS:528:DyaL2MXhvVSisro%3D Occurrence Handle3856856
Z Yang (1996) ArticleTitleAmong-site variation and its impact on phylogenetic analyses. Trends Ecol Evol 11 367–371
Z Yang (1997) ArticleTitlePAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555–556 Occurrence Handle9367129
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Lutfalla, G., Crollius, H., Brunet, F.G. et al. Inventing a Sex-Specific Gene: A Conserved Role of DMRT1 in Teleost Fishes Plus a Recent Duplication in the Medaka Oryzias latipes Resulted in DMY . J Mol Evol 57 (Suppl 1), S148–S153 (2003). https://doi.org/10.1007/s00239-003-0021-4
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DOI: https://doi.org/10.1007/s00239-003-0021-4