A pronounced evolutionary shift of the pseudoautosomal region boundary in house mice

Mammalian Genome

Volumn 23, Issue 7-8, 2012, Pages 454-466

  White, Michael A ^a,b   Ikeda, Akihiro ^a   Payseur, Bret A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOSOME; GENE; GENE MAPPING; MALE FERTILITY; MID1 GENE; MOLECULAR EVOLUTION; MOUSE; MUS MUSCULUS CASTANEUS; MUS MUSCULUS DOMESTICUS; MUS SPRETUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOAUTOSOMAL REGION; SEQUENCE ANALYSIS; SUBSPECIES; X CHROMOSOME;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; CHROMOSOME MAPPING; CHROMOSOME SEGREGATION; EVOLUTION, MOLECULAR; FEMALE; GENETIC SPECIATION; GENETIC VARIATION; INFERTILITY, MALE; INTRONS; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, NUCLEIC ACID; X CHROMOSOME; Y CHROMOSOME;

MAMMALIA; MUS MUSCULUS; MUS MUSCULUS CASTANEUS; MUS MUSCULUS DOMESTICUS; MUS SPRETUS;

EID: 84865110688     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-012-9403-5     Document Type: Article

References (83)

1. Anunciado RV, Imamura T, Ohno T, Horio F, Namikawa T (2000) Developing a new model for non-insulin dependent diabetes mellitus (NIDDM) by using the Philippine wild mouse, Mus musculus castaneus. Exp Anim 49(1):1-8
2. Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24(2):94-102
3. Boursot P, Din W, Anand R, Darviche D, Dod B, VonDeimling F, Talwar G, Bonhomme F (1996) Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J Evol Biol 9(4):391-415
4. Burgoyne PS (1982) Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet 61(2):85-90 (Pubitemid 12029909)
5. Burgoyne PS, Mahadevaiah SK, Sutcliffe MJ, Palmer SJ (1992) Fertility in mice requires X-Y pairing and a Y-chromosomal "spermiogenesis" gene mapping to the long arm. Cell 71(3):391-398
6. Bussell JJ, Pearson NM, Kanda R, Filatov DA, Lahn BT (2006) Human polymorphism and human-chimpanzee divergence in pseudoautosomal region correlate with local recombination rate. Gene 368:94-100 (Pubitemid 43290147)
7. Charchar FJ, Svartman M, El-Mogharbel N, Ventura M, Kirby P, Matarazzo MR, Ciccodicola A, Rocchi M, D'Esposito M, Graves JAM (2003) Complex events in the evolution of the human pseudoautosomal region 2 (PAR2). Genome Res 13(2):281-286 (Pubitemid 36575776)
8. Chen JF, Lu F, Chen SS, Tao SH (2006) Significant positive correlation between the recombination rate and GC content in the human pseudoautosomal region. Genome 49(5):413-419 (Pubitemid 44284765)
9. Cooke HJ, Brown WR, Rappold GA (1985) Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature 317(6039):687-692 (Pubitemid 16223630)
10. Dal Zotto L, Quaderi NA, Elliott R, Lingerfelter PA, Carrel L, Valsecchi V, Montini E, Yen CH, Chapman V, Kalcheva I et al (1998) The mouse Mid1 gene: implications for the pathogenesis of Opitz syndrome and the evolution of the mammalian pseudoautosomal region. Hum Mol Genet 7(3):489-499 (Pubitemid 28120641)
11. Das PJ, Chowdhary BP, Raudsepp T (2009) Characterization of the bovine pseudoautosomal region and comparison with sheep, goat, and other mammalian pseudoautosomal regions. Cytogenet Genome Res 126(1-2):139-147
12. Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Ann Rev Genomics Hum Genet 10:285-311
13. Duret L, Mouchiroud D, Gautier C (1995) Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J Mol Evol 40(3):308-317
14. Ellis N, Goodfellow PN (1989) The mammalian pseudoautosomal region. Trends Genet 5(12):406-410 (Pubitemid 20011532)
15. Ellis N, Yen P, Neiswanger K, Shapiro LJ, Goodfellow PN (1990) Evolution of the pseudoautosomal boundary in old world monkeys and great apes. Cell 63(5):977-986 (Pubitemid 120034939)
16. Filatov DA, Gerrard DT (2003) High mutation rates in human and ape pseudoautosomal genes. Gene 317(1-2):67-77 (Pubitemid 37356919)
17. Freije D, Helms C, Watson MS, Donis-Keller H (1992) Identification of a second pseudoautosomal region near the Xq and Yq telomeres. Science 258(5089):1784-1787 (Pubitemid 23087344)
18. Gabriel-Robez O, Rumpler Y, Ratomponirina C, Petit C, Levilliers J, Croquette MF, Couturier J (1990) Deletion of the pseudoautosomal region and lack of sex-chromosome pairing at pachytene in two infertile men carrying an X;Y translocation. Cytogenet Cell Genet 54(1-2):38-42
19. Galtier N (2004) Recombination, GC-content and the human pseudoautosomal boundary paradox. Trends Genet 20(8):347-349 (Pubitemid 38943024)
20. Gaudenz K, Roessler E, Quaderi N, Franco B, Feldman G, Gasser DL, Wittwer B, Horst J, Montini E, Opitz JM et al (1998) Opitz G/BBB syndrome in Xp22: mutations in the MID1 gene cluster in the carboxy-terminal domain. Am J Hum Genet 63(3):703-710 (Pubitemid 30422669)
21. Geraldes A, Basset P, Gibson B, Smith KL, Harr B, Yu H-T, Bulatova N, Ziv Y, Nachman MW (2008) Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol 17(24):5349-5363
22. Graves JA (1995) The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci 350(1333):305-311
23. Graves JA, Wakefield MJ, Toder R (1998) The origin and evolution of the pseudoautosomal regions of human sex chromosomes. Hum Mol Genet 7(13):1991-1996 (Pubitemid 28546406)
24. Guénet JL, Nagamine C, Simon-Chazottes D, Montagutelli X, Bonhomme F (1990) Hst-3: an X-linked hybrid sterility gene. Genet Res 56(2-3):163-165
25. Hale DW, Washburn LL, Eicher E (1993) Meiotic abnormalities in hybrid mice of the C57BL/6J × Mus spretus cross suggest a cytogenetic basis for Haldane's rule of hybrid sterility. Cytogenet Cell Genet 63(4):221-234 (Pubitemid 23212854)
26. Harbers K, Soriano P, Müller U, Jaenisch R (1986) High frequency of unequal recombination in pseudoautosomal region shown by proviral insertion in transgenic mouse. Nature 324(6098):682-685 (Pubitemid 17206361)
27. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160-174 (Pubitemid 16227864)
28. Hobolth A, Christensen OF, Mailund T, Schierup MH (2007) Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3(2):e7
29. Huang SW, Friedman R, Yu N, Yu A, Li WH (2005) How strong is the mutagenicity of recombination in mammals? Mol Biol Evol 22(3):426-431 (Pubitemid 40299491)
30. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754-755 (Pubitemid 32851390)
31. Ishikawa A, Matsuda Y, Namikawa T (2000) Detection of quantitative trait loci for body weight at 10 weeks from Philippine wild mice. Mamm Genome 11(10):824-830
32. Iwase M, Satta Y, Hirai Y, Hirai H, Imai H, Takahata N (2003) The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species. Proc Natl Acad Sci USA 100(9):5258-5263 (Pubitemid 36542692)
33. Iwase M, Kaneko S, Kim H, Satta Y, Takahata N (2007) Evolutionary history of sex-linked mammalian amelogenin genes. Cells Tissues Organs 186(1):49-59 (Pubitemid 47026716)
34. Janaswami PM, Birkenmeier EH, Cook SA, Rowe LB, Bronson RT, Davisson MT (1997) Identification and genetic mapping of a new polycystic kidney disease on mouse chromosome 8. Genomics 40(1):101-107 (Pubitemid 27108253)
35. Kasahara T, Abe K, Mekada K, Yoshiki A, Kato T (2010) Genetic variation of melatonin productivity in laboratory mice under domestication. Proc Natl Acad Sci USA 107(14):6412-6417
36. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M et al (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477(7364):289-294
37. Keitges E, Rivest M, Siniscalco M, Gartler SM (1985) X-linkage of steroid sulphatase in the mouse is evidence for a functional Y-linked allele. Nature 315(6016):226-227 (Pubitemid 15064447)
38. Kent WJ (2002) BLAT: the BLAST-like alignment tool. Genome Res 12(4):656-664
39. Kipling D, Salido EC, Shapiro LJ, Cooke HJ (1996a) High frequency de novo alterations in the long-range genomic structure of the mouse pseudoautosomal region. Nat Genet 13(1):78-80 (Pubitemid 26139297)
40. Kipling D, Wilson HE, Thomson EJ, Lee M, Perry J, Palmer S, Ashworth A, Cooke HJ (1996b) Structural variation of the pseudoautosomal region between and within inbred mouse strains. Proc Natl Acad Sci USA 93(1):171-175 (Pubitemid 26038122)
41. Kvaløy K, Galvagni F, Brown WR (1994) The sequence organization of the long arm pseudoautosomal region of the human sex chromosomes. Hum Mol Genet 3(5):771-778 (Pubitemid 24148622)
42. Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286(5441):964-967
43. Lancioni A, Pizzo M, Fontanella B, Ferrentino R, Napolitano LMR, De Leonibus E, Meroni G (2010) Lack of Mid1, the mouse ortholog of the Opitz syndrome gene, causes abnormal development of the anterior cerebellar vermis. J Neurosci 30(8):2880-2887
44. Lyons MA, Wittenburg H, Li R, Walsh KA, Leonard MR, Korstanje R, Churchill GA, Carey MC, Paigen B (2003) Lith6: a new QTL for cholesterol gallstones from an intercross of CAST/Ei and DBA/2J inbred mouse strains. J Lipid Res 44(9):1763-1771 (Pubitemid 37185888)
45. Lyons MA, Wittenburg H, Li R, Walsh KA, Korstanje R, Churchill GA, Carey MC, Paigen B (2004) Quantitative trait loci that determine lipoprotein cholesterol levels in an intercross of 129S1/SvImJ and CAST/Ei inbred mice. Physiol Genomics 17(1):60-68 (Pubitemid 38924151)
46. Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19(6):330-338 (Pubitemid 36694616)
47. Matsuda Y, Imai HT, Moriwaki K, Kondo K, Bonhomme F (1982) X-Y chromosome dissociation in wild derived Mus musculus subspecies, laboratory mice, and their F1 hybrids. Cytogenet Cell Genet 34(3):241-252 (Pubitemid 12019508)
48. Matsuda Y, Hirobe T, Chapman VM (1991) Genetic basis of X-Y chromosome dissociation and male sterility in interspecific hybrids. Proc Natl Acad Sci USA 88(11):4850-4854 (Pubitemid 21914640)
49. Matsuda Y, Moens PB, Chapman VM (1992) Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma 101(8):483-492
50. Mohandas TK, Speed RM, Passage MB, Yen PH, Chandley AC, Shapiro LJ (1992) Role of the pseudoautosomal region in sex-chromosome pairing during male meiosis: meiotic studies in a man with a deletion of distal Xp. Am J Hum Genet 51(3):526-533
51. Montoya-Burgos JI, Boursot P, Galtier N (2003) Recombination explains isochores in mammalian genomes. Trends Genet 19(3):128-130 (Pubitemid 36279177)
52. Palmer S, Perry J, Ashworth A (1995) A contravention of Ohno's law in mice. Nat Genet 10(4):472-476
53. Palmer S, Perry J, Kipling D, Ashworth A (1997) A gene spans the pseudoautosomal boundary in mice. Proc Natl Acad Sci USA 94(22):12030-12035 (Pubitemid 27467837)
54. Pamilo P, Bianchi NO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10(2):271-281 (Pubitemid 23103001)
55. Perry J, Ashworth A (1999) Evolutionary rate of a gene affected by chromosomal position. Curr Biol 9(17):987-989 (Pubitemid 29442487)
56. Perry J, Palmer S, Gabriel A, Ashworth A (2001) A short pseudoautosomal region in laboratory mice. Genome Res 11(11):1826-1832 (Pubitemid 33100422)
57. Posada D, Buckley T (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53(5):793-808 (Pubitemid 39568279)
58. Quaderi NA, Schweiger S, Gaudenz K, Franco B, Rugarli EI, Berger W, Feldman GJ, Volta M, Andolfi G, Gilgenkrantz S et al (1997) Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat Genet 17(3):285-291 (Pubitemid 27475990)
59. Rattray AJ, McGill CB, Shafer BK, Strathern JN (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158(1):109-122 (Pubitemid 32428634)
60. Raudsepp T, Chowdhary BP (2008) The horse pseudoautosomal region (PAR): characterization and comparison with the human, chimp and mouse PARs. Cytogenet Genome Res 121(2):102-109 (Pubitemid 351820616)
61. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572-1574 (Pubitemid 37038874)
62. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP et al (2005) The DNA sequence of the human X chromosome. Nature 434(7031):325-337 (Pubitemid 40469169)
63. Rouyer F, Simmler MC, Johnsson C, Vergnaud G, Cooke HJ, Weissenbach J (1986) A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319(6051):291-295 (Pubitemid 16212947)
64. Rugarli EI, Adler DA, Borsani G, Tsuchiya K, Franco B, Hauge X, Disteche C, Chapman V, Ballabio A (1995) Different chromosomal localization of the Clcn4 gene in Mus spretus and C57BL/6J mice. Nat Genet 10(4):466-471
65. Salcedo T, Geraldes A, Nachman MW (2007) Nucleotide variation in wild and inbred mice. Genetics 177(4):2277-2291
66. Salido EC, Li XM, Yen PH, Martin N, Mohandas TK, Shapiro LJ (1996) Cloning and expression of the mouse pseudoautosomal steroid sulphatase gene (Sts). Nat Genet 13(1):83-86 (Pubitemid 126528232)
67. Schiebel K, Meder J, Rump A, Rosenthal A, Winkelmann M, Fischer C, Bonk T, Humeny A, Rappold G (2000) Elevated DNA sequence diversity in the genomic region of the phosphatase PPP2R3L gene in the human pseudoautosomal region. Cytogenet Cell Genet 91(1-4):224-230 (Pubitemid 32110370)
68. She JX, Bonhomme F, Boursot P, Thaler L, Catzeflis F (1990) Molecular phylogenies in the genus Mus: comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP data. Biol J Linn Soc 41(1-3):83-103
69. Shi Q, Spriggs E, Field LL, Ko E, Barclay L, Martin RH (2001) Single sperm typing demonstrates that reduced recombination is associated with the production of aneuploid 24, XY human sperm. Am J Med Genet 99(1):34-38 (Pubitemid 32121582)
70. Simmler MC, Rouyer F, Vergnaud G, Nyström-Lahti M, Ngo KY, de la Chapelle A, Weissenbach J (1985) Pseudoautosomal DNA sequences in the pairing region of the human sex chromosomes. Nature 317(6039):692-697 (Pubitemid 16223631)
71. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423(6942):825-837 (Pubitemid 36781267)
72. Soriano P, Keitges EA, Schorderet DF, Harbers K, Gartler SM, Jaenisch R (1987) High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci USA 84(20):7218-7220 (Pubitemid 18017329)
73. Strathern JN, Shafer BK, McGill CB (1995) DNA synthesis errors associated with double-strand-break repair. Genetics 140(3):965-972
74. Suzuki H, Shimada T, Terashima M, Tsuchiya K, Aplin K (2004) Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 33(3):626-646 (Pubitemid 39444505)
75. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland
76. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596-1599 (Pubitemid 47236692)
77. Van Laere AS, Coppieters W, Georges M (2008) Characterization of the bovine pseudoautosomal boundary: Documenting the evolutionary history of mammalian sex chromosomes. Genome Res 18(12):1884-1895
78. White MA, Ané C, Dewey CN, Larget BR, Payseur BA (2009) Fine-scale phylogenetic discordance across the house mouse genome. PLoS Genet 5(11):e1000729
79. White MA, Stubbings M, Dumont BL, Payseur BA (2012) Genetics and evolution of hybrid male sterility in house mice. Genetics 191(3)
80. Winter J, Lehmann T, Krauss S, Trockenbacher A, Kijas Z, Foerster J, Suckow V, Yaspo M-L, Kulozik A, Kalscheuer V et al (2004) Regulation of the MID1 protein function is fine-tuned by a complex pattern of alternative splicing. Hum Genet 114(6):541-552 (Pubitemid 39010851)
81. Yi S, Summers TJ, Pearson NM, Li WH (2004) Recombination has little effect on the rate of sequence divergence in pseudoautosomal boundary 1 among humans and great apes. Genome Res 14(1):37-43 (Pubitemid 38088523)
82. Yi N, Zinniel DK, Kim K, Eisen EJ, Bartolucci A, Allison DB, Pomp D (2006) Bayesian analyses of multiple epistatic QTL models for body weight and body composition in mice. Genet Res 87(1):45-60
83. Young AC, Kirkness EF, Breen M (2008) Tackling the characterization of canine chromosomal breakpoints with an integrated in-situ/in-silico approach: the canine PAR and PAB. Chromosome Res 16(8):1193-1202