X Chromosome Control of Meiotic Chromosome Synapsis in Mouse Inter-Subspecific Hybrids

PLoS Genetics

Volumn 10, Issue 2, 2014, Pages

  Bhattacharyya, Tanmoy ^a   Reifova, Radka ^a,d   Gregorova, Sona ^a   Simecek, Petr ^a,e   Gergelits, Vaclav ^a   Mistrik, Martin ^b   Martincova, Iva ^c   Pialek, Jaroslav ^c   Forejt, Jiri ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b PALACKÝ UNIVERSITY   (Czech Republic)

^c INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^d CHARLES UNIVERSITY   (Czech Republic)

^e JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA POLYMORPHISM; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE CONTROL; GENE FLOW; GENE LOCUS; GENE MAPPING; GENOTYPE; HSTX1 GENE; HSTX2 GENE; HYBRID; HYBRID STERILITY; IMMUNOFLUORESCENCE; MALE; MEIOSIS; MOUSE; NONHUMAN; PACHYTENE; PHENOTYPE; PROTEIN LOCALIZATION; QUANTITATIVE TRAIT LOCUS; REPRODUCTIVE ISOLATION; SPERMATOGENESIS; SPERMATOZOON ABNORMALITY; SPERMATOZOON COUNT; TESTIS WEIGHT; X CHROMOSOME; ANIMAL; GENETICS; HUMAN; HYBRIDIZATION; MALE INFERTILITY; SYNAPTONEMAL COMPLEX;

HISTONE LYSINE METHYLTRANSFERASE; PRDM9 PROTEIN, MOUSE;

ANIMALS; CHROMOSOME PAIRING; FEMALE; GENETIC LOCI; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; HYBRIDIZATION, GENETIC; INFERTILITY, MALE; MALE; MEIOSIS; MICE; QUANTITATIVE TRAIT LOCI; REPRODUCTIVE ISOLATION; SYNAPTONEMAL COMPLEX; X CHROMOSOME;

EID: 84901727293     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004088     Document Type: Article

References (73)

1. Dobzhansky T (1951). Genetics and the origin of Species: Columbia University, New York.
2. Coyne JA, Orr HA (2004) Speciation: Sinauer Associates, Inc., Sunderland, Massachusetts U.S.A.
3. Moehring AJ, Llopart A, Elwyn S, Coyne JA, Mackay TF, (2006) The genetic basis of postzygotic reproductive isolation between Drosophila santomea and D. yakuba due to hybrid male sterility. Genetics 173: 225-233.
4. Slotman M, Della Torre A, Powell JR, (2004) The genetics of inviability and male sterility in hybrids between Anopheles gambiae and An. arabiensis. Genetics 167: 275-287.
5. Maheshwari S, Barbash DA, (2011) The Genetics of Hybrid Incompatibilities. Annu Rev Genet 45: 331-55.
6. Haldane J, (1922) Sex ration and unisexual sterility in animal hybrids. J Genet 12: 101-109.
7. Muller H, Pontecorvo G, (1942) Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27: 157.
8. Coyne JA, (1989) Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci U S A 86: 5464-5468.
9. Turelli M, Orr HA, (1995) The dominance theory of Haldane's rule. Genetics 140: 389-402.
10. Turelli M, Orr HA, (2000) Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663-1679.
11. Forejt J, (1996) Hybrid sterility in the mouse. Trends Genet 12: 412-417.
12. Forejt J, (1985) Chromosomal and genic sterility of hybrid type in mice and men. Experimental and Clinical Immunogenetics 2: 106-119.
13. Forejt J, Pialek J, Trachtulec Z (2012) Hybrid male sterility genes in the mouse subspecific crosses. In: Macholan M, Baird SJE, Muclinger P, Pialek J, editors. Evolution of the House Mouse. Cambridge: Cambridge University Press. pp 482-503.
14. Din W, Anand R, Boursot P, Darviche D, Dod B, et al. (1996) Origin and radiation of the house mouse: Clues from nuclear genes. Journal of Evolutionary Biology 9: 519-539.
15. Baird SJE, Macholan M (2012) What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation? In: Macholan M, Baird SJ, Muclinger P, Pialek J, editors. Evolution of the house mouse. Cambridge: Cambridge University Press. pp. 334-372.
16. Payseur BA, Krenz JG, Nachman MW, (2004) Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58: 2064-2078.
17. Macholan M, Baird SJ, Dufkova P, Munclinger P, Bimova BV, et al. (2011) Assessing multilocus introgression patterns: a case study on the mouse X chromosome in central Europe. Evolution 65: 1428-1446.
18. Lewontin R (1974) The genetic basis of evolutionary change. New York: Columbia University Press.
19. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289-294.
20. Gregorova S, Divina P, Storchova R, Trachtulec Z, Fotopulosova V, et al. (2008) Mouse consomic strains: exploiting genetic divergence between Mus m. musculus and Mus m. domesticus subspecies. Genome Res 18: 509-515.
21. Anderson LK, Reeves A, Webb LM, Ashley T, (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569-1579.
22. Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, et al. (2013) Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci U S A 110: E468-477.
23. Forejt J, Ivanyi P, (1974) Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet Res 24: 189-206.
24. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J, (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323: 373-375.
25. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840.
26. Parvanov ED, Petkov PM, Paigen K, (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
27. Dzur-Gejdosova M, Simecek P, Gregorova S, Bhattacharyya T, Forejt J, (2012) Dissecting the genetic architecture of F1 hybrid sterility in house mice. Evolution 66: 3321-3335.
28. Flachs P, Mihola O, Simecek P, Gregorova S, Schimenti J, et al. (2012) Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility. Plos Genet 8: e1003044.
29. Turelli M, Moyle LC, (2007) Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.
30. Good JM, Handel MA, Nachman MW, (2008) Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution Int J Org Evolution 62: 50-65.
31. Brideau NJ, Barbash DA, (2011) Functional conservation of the Drosophila hybrid incompatibility gene Lhr. BMC Evol Biol 11: 57.
32. Gregorova S, Forejt J, (2000) PWD/Ph and PWK/Ph inbred mouse strains of Mus m. musculus subspecies-a valuable resource of phenotypic variations and genomic polymorphisms. Folia Biol (Praha) 46: 31-41.
33. Storchova R, Gregorova S, Buckiova D, Kyselova V, Divina P, et al. (2004) Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm Genome 15: 515-524.
34. Song R, Ro S, Michaels JD, Park C, McCarrey JR, et al. (2009) Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 41: 488-493.
35. Jansa P, Divina P, Forejt J, (2005) Construction and characterization of a genomic BAC library for the Mus m. musculus mouse subspecies (PWD/Ph inbred strain). BMC Genomics 6: 161.
36. Good JM, Vanderpool D, Smith KL, Nachman MW, (2011) Extraordinary sequence divergence at Tsga8, an X-linked gene involved in mouse spermiogenesis. Mol Biol Evol 28: 1675-1686.
37. Ting C, Tsaur S, Wu M, Wu C, (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene [see comments]. Science 282: 1501-1504.
38. Barbash DA, Siino DF, Tarone AM, Roote J, (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A 100: 5302-5307.
39. Presgraves DC, Balagopalan L, Abmayr SM, Orr HA, (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715-719.
40. Bono H, Yagi K, Kasukawa T, Nikaido I, Tominaga N, et al. (2003) Systematic expression profiling of the mouse transcriptome using RIKEN cDNA microarrays. Genome Res 13: 1318-1323.
41. Good JM, Dean MD, Nachman MW, (2008) A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179: 2213-2228.
42. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, et al. (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747.
43. Homolka D, Ivanek R, Capkova J, Jansa P, Forejt J, (2007) Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res 17: 1431-1437.
44. Vyskocilova M, Prazanova G, Pialek J, (2009) Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17. Mamm Genome 20: 83-91.
45. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873-886.
46. Coyne JA, Orr HA (1989) Two rules of speciation. In: Otte D, Endler J, editors. Speciation and Its Consequences. Sunderland, Massachusetts: Sinauer. pp. 180-207.
47. Coyne JA, Orr HA (2004) Speciation. SunderlandMassachusetts: Sinauer Associates. 545 p.
48. Good JM, Giger T, Dean MD, Nachman MW, (2010) Widespread over-expression of the X chromosome in sterile F hybrid mice. PLoS Genet 6: e1001148.
49. Oka A, Mita A, Sakurai-Yamatani N, Yamamoto H, Takagi N, et al. (2004) Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies. Genetics 166: 913-924.
50. Mueller JL, Skaletsky H, Brown LG, Zaghlul S, Rock S, et al. (2013) Independent specialization of the human and mouse X chromosomes for the male germ line. Nat Genet 45: 1083-1087.
51. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, et al. (2008) The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40: 794-799.
52. Trachtulec Z, Vlcek C, Mihola O, Gregorova S, Fotopulosova V, et al. (2008) Fine haplotype structure of a chromosome 17 region in the laboratory and wild mouse. Genetics 178: 1777-1784.
53. Pialek J, Vyskocilova M, Bimova B, Havelkova D, Pialkova J, et al. (2008) Development of unique house mouse resources suitable for evolutionary studies of speciation. J Hered 99: 34-44.
54. Elliott R, Miller D, Pearsall R, Hohman C, Zhang Y, et al. (2001) Genetic analysis of testis weight and fertility in an interspecies hybrid congenic strain for Chromosome X. Mamm Genome 12: 45-51.
55. Elliott RW, Poslinski D, Tabaczynski D, Hohman C, Pazik J, (2004) Loci affecting male fertility in hybrids between Mus macedonicus and C57BL/6. Mamm Genome 15: 704-710.
56. Teeter KC, Payseur BA, Harris LW, Bakewell MA, Thibodeau LM, et al. (2008) Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res 18: 67-76.
57. Janousek V, Wang L, Luzynski K, Dufkova P, Vyskocilova MM, et al. (2012) Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol Ecol 21: 3032-3047.
58. Campbell P, Good JM, Nachman MW, (2013) Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193: 819-828.
59. Bolcun-Filas E, Schimenti JC, (2012) Genetics of meiosis and recombination in mice. Int Rev Cell Mol Biol 298: 179-227.
60. Hayashi K, Yoshida K, Matsui Y, (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374-378.
61. Burgoyne PS, Mahadevaiah SK, Turner JM, (2009) The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10: 207-216.
62. Burgoyne PS, Mahadevaiah S, Mittwoch U, (1985) A reciprocal autosomal translocation which causes male sterility in the mouse also impairs oogenesis. J Reprod Fertil 75: 647-652.
63. Setterfield LA, Mahadevaiah S, Mittwoch U, (1988) Chromosome pairing and germ cell loss in male and female mice carrying a reciprocal translocation. J Reprod Fertil 82: 369-379.
64. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, et al. (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52-54.
65. Homolka D, Ivanek R, Forejt J, Jansa P, (2011) Differential expression of non-coding RNAs and continuous evolution of the X chromosome in testicular transcriptome of two mouse species. PLoS One 6: e17198.
66. Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. \New York: Springer.
67. Bult CJ, Eppig JT, Kadin JA, Richardson JE, Blake JA, (2008) The Mouse Genome Database (MGD): mouse biology and model systems. Nucleic Acids Res 36: D724-728.
68. Bastos H, Lassalle B, Chicheportiche A, Riou L, Testart J, et al. (2005) Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 65: 40-49.
69. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
70. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 3.
71. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, et al. (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37: 41-47.
72. Inselman A, Eaker S, Handel MA, (2003) Temporal expression of cell cycle-related proteins during spermatogenesis: establishing a timeline for onset of the meiotic divisions. Cytogenet Genome Res 103: 277-284.
73. Kauppi L, Barchi M, Baudat F, Romanienko PJ, Keeney S, et al. (2011) Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331: 916-920.