A Trans-Species Missense SNP in Is Associated with Sex Determination in the Tiger Pufferfish, (Fugu)
Heterogametic sex chromosomes have evolved independently in various lineages of vertebrates. Such sex chromosome pairs often contain nonrecombining regions, with one of the chromosomes harboring a master sex-determining (SD) gene. It is hypothesized that these sex chromosomes evolved from a pair of autosomes that diverged after acquiring the SD gene. By linkage and association mapping of the SD locus in fugu (Takifugu rubripes), we show that a SNP (C/G) in the anti-Müllerian hormone receptor type II (Amhr2) gene is the only polymorphism associated with phenotypic sex. This SNP changes an amino acid (His/Asp384) in the kinase domain. While females are homozygous (His/His384), males are heterozygous. Sex in fugu is most likely determined by a combination of the two alleles of Amhr2. Consistent with this model, the medaka hotei mutant carrying a substitution in the kinase domain of Amhr2 causes a female phenotype. The association of the Amhr2 SNP with phenotypic sex is conserved in two other species of Takifugu but not in Tetraodon. The fugu SD locus shows no sign of recombination suppression between X and Y chromosomes. Thus, fugu sex chromosomes represent an unusual example of proto–sex chromosomes. Such undifferentiated X-Y chromosomes may be more common in vertebrates than previously thought.
Vyšlo v časopise:
A Trans-Species Missense SNP in Is Associated with Sex Determination in the Tiger Pufferfish, (Fugu). PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002798
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002798
Souhrn
Heterogametic sex chromosomes have evolved independently in various lineages of vertebrates. Such sex chromosome pairs often contain nonrecombining regions, with one of the chromosomes harboring a master sex-determining (SD) gene. It is hypothesized that these sex chromosomes evolved from a pair of autosomes that diverged after acquiring the SD gene. By linkage and association mapping of the SD locus in fugu (Takifugu rubripes), we show that a SNP (C/G) in the anti-Müllerian hormone receptor type II (Amhr2) gene is the only polymorphism associated with phenotypic sex. This SNP changes an amino acid (His/Asp384) in the kinase domain. While females are homozygous (His/His384), males are heterozygous. Sex in fugu is most likely determined by a combination of the two alleles of Amhr2. Consistent with this model, the medaka hotei mutant carrying a substitution in the kinase domain of Amhr2 causes a female phenotype. The association of the Amhr2 SNP with phenotypic sex is conserved in two other species of Takifugu but not in Tetraodon. The fugu SD locus shows no sign of recombination suppression between X and Y chromosomes. Thus, fugu sex chromosomes represent an unusual example of proto–sex chromosomes. Such undifferentiated X-Y chromosomes may be more common in vertebrates than previously thought.
Zdroje
1. CharlesworthDMankJE 2010 The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186 9 31
2. OhnoS 1967 Sex chromosomes and sex-linked genes Berlin, New York etc. Springer-Verlag 192
3. BergeroRCharlesworthD 2009 The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24 94 102
4. SinclairAHBertaPPalmerMSHawkinsJRGriffithsBL 1990 A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346 240 244
5. SmithCARoeszlerKNOhnesorgTCumminsDMFarliePG 2009 The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461 267 271
6. MatsudaMNagahamaYShinomiyaASatoTMatsudaC 2002 DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 559 563
7. YoshimotoSOkadaEUmemotoHTamuraKUnoY 2008 A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105 2469 2474
8. HattoriRSMuraiYOuraMMasudaSMajhiSK 2012 A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109 2955 2959
9. MyoshoTOtakeHMasuyamaHMatsudaMKurokiY 2012 Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics doi:10.1534/genetics.111.137497
10. KikuchiKKaiWHosokawaAMizunoNSuetakeH 2007 The sex-determining locus in the tiger pufferfish, Takifugu rubripes. Genetics 175 2039 2042
11. AparicioSChapmanJStupkaEPutnamNChiaJM 2002 Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297 1301 1310
12. KaiWKikuchiKTohariSChewAKTayA 2011 Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals. Genome Biol Evol 3 424 442
13. KaiWKikuchiKFujitaMSuetakeHFujiwaraA 2005 A genetic linkage map for the tiger pufferfish, Takifugu rubripes. Genetics 171 227 238
14. YanaiIBenjaminHShmoishMChalifa-CaspiVShklarM 2005 Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21 650 659
15. JaminSPArangoNAMishinaYHanksMCBehringerRR 2003 Genetic studies of the AMH/MIS signaling pathway for Müllerian duct regression. Mol Cell Endocrinol 211 15 19
16. CharlesworthD 2006 Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2 e64 doi:10.1371/journal.pgen.0020064
17. WiufCZhaoKInnanHNordborgM 2004 The probability and chromosomal extent of trans-specific polymorphism. Genetics 168 2363 2372
18. YamanoueYMiyaMMatsuuraKMiyazawaSTsukamotoN 2009 Explosive speciation of Takifugu: another use of fugu as a model system for evolutionary biology. Mol Biol Evol 26 623 629
19. BentonMJDonoghuePC 2007 Paleontological evidence to date the tree of life. Mol Biol Evol 24 26 53
20. HoeggSBrinkmannHTaylorJSMeyerA 2004 Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59 190 203
21. ChristoffelsAKohEGLChiaJBrennerSAparicioS 2004 Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol Biol Evol 21 1146 1151
22. MorinagaCSaitoDNakamuraSSasakiTAsakawaS 2007 The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci USA 104 9691 9696
23. MatsuuraSNaitoTShinchoMYoshimuraKMatsuuraM 1994 Gonadal sex differentiation in tiger puffer, Takifugu rubripes. SUISANZOSHOKU 42 619 625
24. YamaguchiALeeKHFujimotoHKadomuraKYasumotoS 2006 Expression of the DMRT gene and its roles in early gonadal development of the Japanese pufferfish Takifugu rubripes. Comp Biochem Physiol D 1 59 68
25. ShiraishiEYoshinagaNMiuraTYokoiHWakamatsuY 2008 Müllerian inhibiting substance is required for germ cell proliferation during early gonadal differentiation in medaka (Oryzias latipes). Endocrinology 149 1813 1819
26. BelvilleCMaréchaJDPennetierSCarmilloPMasgrauL 2009 Natural mutations of the anti-Müllerian hormone type II receptor found in persistent Müllerian duct syndrome affect ligand binding, signal transduction and cellular transport. Hum Mol Genet 18 3002 3013
27. NeumannJCChandlerGLDamoulisVAFustinoNJLillardK 2011 Mutation in the type IB bone morphogenetic protein receptor Alk6b impairs germ-cell differentiation and causes germ-cell tumors in zebrafish. Proc Natl Acad Sci USA 108 13153 13158
28. KurokawaHSaitoDNakamuraSKatoh-FukuiYOhtaK 2007 Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci USA 104 16958 16963
29. LeeKYamaguchiARashidHKadomuraKYasumotoS 2009 Germ cell degeneration in high-temperature treated pufferfish, Takifugu rubripes. Sex Dev 3 225 232
30. di ClementeNGhaffariSPepinskyRPieauCJossoN 1992 A quantitative and interspecific test for biological activity of anti-Müllerian hormone: the fetal ovary aromatase assay. Development 114 721 727
31. DevlinRHNagahamaY 2002 Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208 191 364
32. VuilleumierSLandeRJJVANASeehausenO 2007 Invasion and fixation of sex-reversal genes. J Evol Biol 20 913 920
33. PomiankowskiANothigerRWilkinsA 2004 The evolution of the Drosophila sex-determination pathway. Genetics 166 1761 1773
34. van DoornGSKirkpatrickM 2007 Turnover of sex chromosomes induced by sexual conflict. Nature 449 909 912
35. SmithCASinclairAH 2004 Sex determination: insights from the chicken. Bioessays 26 120 132
36. FraserJAHeitmanJ 2005 Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev 15 645 651
37. KondoMHornungUNandaIImaiSSasakiT 2006 Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16 815 826
38. BewickAJAndersonDWEvansBJ 2011 Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus). Evolution 65 698 712
39. StockMHornAGrossenCLindtkeDSermierR 2011 Ever-young sex chromosomes in European tree frogs. PLoS Biol 9 e1001062 doi:10.1371/journal.pbio.1001062
40. LeeKHYamaguchiARashidHKadomuraKYasumotoS 2009 Estradiol-17ß treatment induces intersexual gonadal development in the pufferfish, Takifugu rubripes. Zool Sci 26 639 645
41. LaurieCCNickersonDAAndersonADWeirBSLivingstonRJ 2007 Linkage disequilibrium in wild mice. PLoS Genet 3 e144 doi:10.1371/journal.pgen.0030144
42. SlateJPembertonJ 2007 Admixture and patterns of linkage disequilibrium in a free-living vertebrate population. J Evo Biol 20 1415 1427
43. SaitohKChenWJ 2008 Reducing cloning artifacts for recovery of allelic sequences by T7 endonuclease I cleavage and single re-extension of PCR products - A benchmark. Gene 423 92 95
44. BarrettJCFryBMallerJDalyMJ 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 263 265
45. LarkinMBlackshieldsGBrownNChennaRMcGettiganP 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
46. OhtaniMMiyadaiT 2011 Functional analysis of fish BCL-6 and Blimp-1 in vitro: Transcriptional repressors for B-cell terminal differentiation in fugu (Takifugu rubripes). Mol Immunol 48 818 825
47. SchwedeTKoppJGuexNPeitschMC 2003 SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31 3381 3385
48. GuexNPeitschMC 1997 SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18 2714 2723
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 7
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