Prdm9 incompatibility controls oligospermia and delayed fertility but no selfish transmission in mouse intersubspecific hybrids

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Flachs, Petr ^a   Bhattacharyya, Tanmoy ^a   Mihola, Ondřej ^a   Piálek, Jaroslav ^b   Forejt, Jiří ^a   Trachtulec, Zdenek ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CHROMOSOME 10; CHROMOSOME 17; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA MODIFICATION; DROSOPHILA; GENE; GENE DOSAGE; GENE FUNCTION; GENETIC INCOMPATIBILITY; GENETIC REGULATION; HETEROZYGOTE; HSTX2 GENE; HYBRID; INTERSUBSPECIFIC HYBRID; MALE; MALE FERTILITY; MEIOSIS; MOUSE; MOUSE STRAIN; NONHUMAN; OLIGOSPERMIA; PHENOTYPE; PRDM9 GENE; AGE; ANIMAL; CHROMOSOME; CROSS BREEDING; FEMALE; GENETICS; GENOTYPE; MALE INFERTILITY; METABOLISM; PATHOLOGY; QUANTITATIVE TRAIT LOCUS; TESTIS;

HISTONE LYSINE METHYLTRANSFERASE; PRDM9 PROTEIN, MOUSE;

AGE FACTORS; ALLELES; ANIMALS; CHROMOSOMES, MAMMALIAN; CROSSES, GENETIC; FEMALE; GENE DOSAGE; GENOTYPE; HISTONE-LYSINE N-METHYLTRANSFERASE; INFERTILITY, MALE; MALE; MEIOSIS; MICE; OLIGOSPERMIA; PHENOTYPE; QUANTITATIVE TRAIT LOCI; TESTIS;

EID: 84899737231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095806     Document Type: Article

References (50)

1. Haldane JBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genet 12: 101-109.
2. Ting CT, Tsaur SC, Wu ML, Wu CI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501-1504.
3. Masly JP, Jones CD, Noor MA, Locke J, Orr HA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448-1450. (Pubitemid 44360275)
4. 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.
5. Phadnis N, Orr HA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376-379.
6. Baird SJE, Macholan M (2012) What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation? In: Baird SJE, Macholan M, Munclinger P, Pialek J, editors. Evolution of the House Mouse: Cambridge University Press. 334-372.
7. Forejt J, Pialek J, Trachtulec Z (2012) Hybrid male sterility genes in the mouse subspecific crosses. In: Baird SJE, Macholan M, Munclinger P, Pialek J, editors. Evolution of the House Mouse: Cambridge University Press. 482-503.
8. 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.
9. 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.
10. Bhattacharyya T, Reifova R, Gregorova S, Simecek P, Gergelits V, et al. (2014) X chromosome control of meiotic chromosome synapsis in mouse intersubspecific hybrids. PLoS Genet 10: e1004088.
11. 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.
12. Gregorova S, Mnukova-Fajdelova M, Trachtulec Z, Capkova J, Loudova M, et al. (1996) Sub-milliMorgan map of the proximal part of mouse Chromosome 17 including the hybrid sterility 1 gene. Mamm Genome 7: 107-113. (Pubitemid 126426570)
13. Trachtulec Z, Vincek V, Hamvas RM, Forejt J, Lehrach H, et al. (1994) Physical map of mouse chromosome 17 in the region relevant for positional cloning of the Hybrid sterility 1 gene. Genomics 23: 132-137. (Pubitemid 24296944)
14. Forejt J, Trachtulec Z, Hamvas R (1999) Mouse chromosome 17. Mamm Genome 10: 958. (Pubitemid 29470931)
15. Mihola O, Forejt J, Trachtulec Z (2007) Conserved alternative and antisense transcripts at the programmed cell death 2 locus. BMC Genomics 8: 20.
16. 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.
17. Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374-378. (Pubitemid 41643955)
18. 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.
19. Parvanov ED, Petkov PM, Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
20. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642-645.
21. Bateson W (1909) Heredity and variation in modern lights. In: Steward AC, editor. Darwin and modern science. Cambridge, U.K: Cambridge Univ. Press. 85-101.
22. Dobzhansky T (1937). Genetics and the origin of species. New York: Columbia Univ. Press.
23. Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biological Symposia. Lancaster: Jaques Cattell Press. 71-125.
24. Flachs P, Mihola O, Simecek P, Gregorova S, Schimenti JC, et al. (2012) Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility. PLoS Genet 8: e1003044.
25. 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. (Pubitemid 39348506)
26. 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.
27. Yoshiki A, Moriwaki K, Sakakura T, Kusakabe M (1993) Histological studies on male-sterility of hybrids between laboratory and wild mouse strains. Development Growth & Differentiation 35: 271-281. (Pubitemid 23285563)
28. Britton-Davidian J, Fel-Clair F, Lopez J, Alibert P, Boursot P (2005) Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biol J Lin Soc 84: 379-393. (Pubitemid 40441045)
29. Good JM, Handel MA, Nachman MW (2008) Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62: 50-65.
30. White MA, Steffy B, Wiltshire T, Payseur BA (2011) Genetic dissection of a key reproductive barrier between nascent species of house mice. Genetics 189: 289-304.
31. 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. (Pubitemid 38391750)
32. 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. (Pubitemid 38798842)
33. Oka A, Aoto T, Totsuka Y, Takahashi R, Ueda M, et al. (2007) Disruption of genetic interaction between two autosomal regions and the X chromosome causes reproductive isolation between mouse strains derived from different subspecies. Genetics 175: 185-197. (Pubitemid 46168564)
34. Oka A, Mita A, Takada Y, Koseki H, Shiroishi T (2010) Reproductive isolation in hybrid mice due to spermatogenesis defects at three meiotic stages. Genetics 186: 339-351.
35. Albrechtova J, Albrecht T, Baird SJ, Macholan M, Rudolfsen G, et al. (2012) Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse. Proc R Soc B 279: 4803-4810.
36. Turner LM, Schwahn DJ, Harr B (2012) Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution 66: 443-458.
37. 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. (Pubitemid 30079599)
38. 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.
39. 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. (Pubitemid 351261485)
40. Yang H, Wang JR, Didion JP, Buus RJ, Bell TA, et al. (2011) Subspecific origin and haplotype diversity in the laboratory mouse. Nat Genet 43: 648-655.
41. 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. (Pubitemid 351347094)
42. 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. (Pubitemid 40070938)
43. 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. (Pubitemid 29177564)
44. McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71-80. (Pubitemid 23040889)
45. Vyskocilova M, Trachtulec Z, Forejt J, Pialek J (2005) Does geography matter in hybrid sterility in house mice? Biol J Lin Soc 84: 663-674. (Pubitemid 40441067)
46. 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.
47. Dufkova P, Macholan M, Pialek J (2011) Inference of selection and stochastic effects in the house mouse hybrid zone. Evolution 65: 993-1010.
48. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, et al. (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet 36: 1133-1137.
49. Frank SA (1991) Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45: 262-267.
50. Hurst LD, Pomiankowski A (1991) Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics 128: 841-858.