Interallelic and Intergenic Incompatibilities of the () Gene in Mouse Hybrid Sterility
The Dobzhansky-Muller model of incompatibilities explains reproductive isolation between species by incorrect epistatic interactions. Although the mechanisms of speciation are of great interest, no incompatibility has been characterized at the gene level in mammals. The Hybrid sterility 1 gene (Hst1) participates in the arrest of meiosis in F1 males of certain strains from two Mus musculus subspecies, e.g., PWD from M. m. musculus and C57BL/6J (henceforth B6) from M. m. domesticus. Hst1 has been identified as a meiotic PR-domain gene (Prdm9) encoding histone 3 methyltransferase in the male offspring of PWD females and B6 males, (PWD×B6)F1. To characterize the incompatibilities underlying hybrid sterility, we phenotyped reproductive and meiotic markers in males with altered copy numbers of Prdm9. A partial rescue of fertility was observed upon removal of the B6 allele of Prdm9 from the azoospermic (PWD×B6)F1 hybrids, whereas removing one of the two Prdm9 copies in PWD or B6 background had no effect on male reproduction. Incompatibility(ies) not involving Prdm9B6 also acts in the (PWD×B6)F1 hybrids, since the correction of hybrid sterility by Prdm9B6 deletion was not complete. Additions and subtractions of Prdm9 copies, as well as allelic replacements, improved meiotic progression and fecundity also in the progeny-producing reciprocal (B6×PWD)F1 males. Moreover, an increased dosage of Prdm9 and reciprocal cross enhanced fertility of other sperm-carrying male hybrids, (PWD×B6-C3H.Prdm9)F1, harboring another Prdm9 allele of M. m. domesticus origin. The levels of Prdm9 mRNA isoforms were similar in the prepubertal testes of all types of F1 hybrids of PWD with B6 and B6-C3H.Prdm9 despite their different prospective fertility, but decreased to 53% after removal of Prdm9B6. Therefore, the Prdm9B6 allele probably takes part in posttranscriptional dominant-negative hybrid interaction(s) absent in the parental strains.
Vyšlo v časopise:
Interallelic and Intergenic Incompatibilities of the () Gene in Mouse Hybrid Sterility. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003044
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003044
Souhrn
The Dobzhansky-Muller model of incompatibilities explains reproductive isolation between species by incorrect epistatic interactions. Although the mechanisms of speciation are of great interest, no incompatibility has been characterized at the gene level in mammals. The Hybrid sterility 1 gene (Hst1) participates in the arrest of meiosis in F1 males of certain strains from two Mus musculus subspecies, e.g., PWD from M. m. musculus and C57BL/6J (henceforth B6) from M. m. domesticus. Hst1 has been identified as a meiotic PR-domain gene (Prdm9) encoding histone 3 methyltransferase in the male offspring of PWD females and B6 males, (PWD×B6)F1. To characterize the incompatibilities underlying hybrid sterility, we phenotyped reproductive and meiotic markers in males with altered copy numbers of Prdm9. A partial rescue of fertility was observed upon removal of the B6 allele of Prdm9 from the azoospermic (PWD×B6)F1 hybrids, whereas removing one of the two Prdm9 copies in PWD or B6 background had no effect on male reproduction. Incompatibility(ies) not involving Prdm9B6 also acts in the (PWD×B6)F1 hybrids, since the correction of hybrid sterility by Prdm9B6 deletion was not complete. Additions and subtractions of Prdm9 copies, as well as allelic replacements, improved meiotic progression and fecundity also in the progeny-producing reciprocal (B6×PWD)F1 males. Moreover, an increased dosage of Prdm9 and reciprocal cross enhanced fertility of other sperm-carrying male hybrids, (PWD×B6-C3H.Prdm9)F1, harboring another Prdm9 allele of M. m. domesticus origin. The levels of Prdm9 mRNA isoforms were similar in the prepubertal testes of all types of F1 hybrids of PWD with B6 and B6-C3H.Prdm9 despite their different prospective fertility, but decreased to 53% after removal of Prdm9B6. Therefore, the Prdm9B6 allele probably takes part in posttranscriptional dominant-negative hybrid interaction(s) absent in the parental strains.
Zdroje
1. HaldaneJBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genetics 12: 101–109.
2. OrrHA, MaslyJP, PresgravesDC (2004) Speciation genes. Curr Opin Genet Dev 14: 675–679.
3. TingCT, TsaurSC, WuML, WuCI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501–1504.
4. SunS, TingCT, WuCI (2004) The normal function of a speciation gene, Odysseus, and its hybrid sterility effect. Science 305: 81–83.
5. MaslyJP, JonesCD, NoorMA, LockeJ, OrrHA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448–1450.
6. MiholaO, TrachtulecZ, VlcekC, SchimentiJC, ForejtJ (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323: 373–375.
7. PhadnisN, OrrHA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376–379.
8. BayesJJ, MalikHS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326: 1538–1541.
9. SawamuraK, MaeharaK, MashinoS, KagesawaT, KajiwaraM, et al. (2010) Introgression of Drosophila simulans nuclear pore protein 160 in Drosophila melanogaster alone does not cause inviability but does cause female sterility. Genetics 186: 669–676.
10. DobzhanskyT (1951) Experiments on sexual isolation in Drosophila: X. Reproductive isolation between Drosophila pseudoobscura and Drosophila persimilis under natural and under laboratory conditions. Proc Natl Acad Sci U S A 37: 792–796.
11. ForejtJ, IvanyiP (1974) Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet Res 24: 189–206.
12. Dzur-GejdosovaM, SimecekP, GregorovaS, BhattacharyyaT, ForejtJ (2012) Dissecting the genetic architecture of F1 hybrid sterility in house mice. Evolution in press. doi: 10.1111/j.1558-5646.2012.01684.x.
13. ForejtJ (1996) Hybrid sterility in the mouse. Trends Genet 12: 412–417.
14. ForejtJ, VincekV, KleinJ, LehrachH, Loudova-MickovaM (1991) Genetic mapping of the t-complex region on mouse chromosome 17 including the Hybrid sterility-1 gene. Mamm Genome 1: 84–91.
15. TrachtulecZ, VincekV, HamvasRM, ForejtJ, LehrachH, 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.
16. GregorovaS, Mnukova-FajdelovaM, TrachtulecZ, CapkovaJ, LoudovaM, 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.
17. TrachtulecZ, MiholaO, VlcekC, HimmelbauerH, PacesV, et al. (2005) Positional cloning of the Hybrid sterility 1 gene: fine genetic mapping and evaluation of two candidate genes. Biol J Linn Soc 84: 637–641.
18. MiholaO, ForejtJ, TrachtulecZ (2007) Conserved alternative and antisense transcripts at the programmed cell death 2 locus. BMC Genomics 8: 20.
19. TrachtulecZ, VlcekC, MiholaO, GregorovaS, FotopulosovaV, et al. (2008) Fine haplotype structure of a chromosome 17 region in the laboratory and wild mouse. Genetics 178: 1777–1784.
20. HayashiK, YoshidaK, MatsuiY (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374–378.
21. BuardJ, BarthesP, GreyC, de MassyB (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28: 2616–2624.
22. BaudatF, BuardJ, GreyC, Fledel-AlonA, OberC, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836–840.
23. ParvanovED, PetkovPM, PaigenK (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
24. GreyC, BarthesP, Chauveau-Le FriecG, LangaF, BaudatF, et al. (2011) Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol 9: e1001176 doi:10.1371/journal.pbio.1001176.
25. Forejt J, Pialek J, Trachtulec Z (2012) Hybrid male sterility genes in the mouse subspecific crosses. In: Macholan M, Baird SJE, Muclinger P and Pialek J, editors. Evolution of the House Mouse. Cambridge: Cambridge University Press, pp. 482–503.
26. OliverPL, GoodstadtL, BayesJJ, BirtleZ, RoachKC, et al. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5: e1000753 doi:10.1371/journal.pgen.1000753.
27. GregorovaS, DivinaP, StorchovaR, TrachtulecZ, FotopulosovaV, et al. (2008) Mouse consomic strains: exploiting genetic divergence between Mus m. musculus and Mus m. domesticus subspecies. Genome Res 18: 509–515.
28. BergstromDE, BergstromRA, MunroeRJ, LeeBK, BrowningVL, et al. (2003) Overlapping deletions spanning the proximal two-thirds of the mouse t complex. Mamm Genome 14: 817–829.
29. BrowningVL, BergstromRA, DaigleS, SchimentiJC (2002) A haplolethal locus uncovered by deletions in the mouse T complex. Genetics 160: 675–682.
30. PialekJ, VyskocilovaM, BimovaB, HavelkovaD, PialkovaJ, et al. (2008) Development of unique house mouse resources suitable for evolutionary studies of speciation. J Hered 99: 34–44.
31. VyskocilovaM, PrazanovaG, PialekJ (2009) Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17. Mamm Genome 20: 83–91.
32. MaheshwariS, BarbashDA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45: 331–355.
33. BarbashDA, RooteJ, AshburnerM (2000) The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747–1771.
34. MaheshwariS, BarbashDA (2012) Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8: e1002597 doi:10.1371/journal.pgen.1002597.
35. Munoz-FuentesV, Di RienzoA, VilaC (2011) Prdm9, a major determinant of meiotic recombination hotspots, is not functional in dogs and their wild relatives, wolves and coyotes. PLoS ONE 6: e25498 doi:10.1371/journal.pone.0025498.
36. AxelssonE, WebsterMT, RatnakumarA, PontingCP, Lindblad-TohK (2012) Death of PRDM9 coincides with stabilization of the recombination landscape in the dog genome. Genome Res 22: 51–63.
37. TurnerLM, SchwahnDJ, HarrB (2011) Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution 66: 443–458.
38. MacholanM, MunclingerP, SugerkovaM, DufkovaP, BimovaB, et al. (2007) Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61: 746–771.
39. DeanMD, ArdlieKG, NachmanMW (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15: 4141–4151.
40. WhiteMA, SteffyB, WiltshireT, PayseurBA Genetic dissection of a key reproductive barrier between nascent species of house mice. Genetics 189: 289–304.
41. KeaneTM, GoodstadtL, DanecekP, WhiteMA, WongK, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289–294.
42. GregorovaS, ForejtJ (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.
43. VyskocilovaM, TrachtulecZ, ForejtJ, PialekJ (2005) Does geography matter in hybrid sterility in house mice? Biol J Linn Soc 84: 663–674.
44. TurnerJM, MahadevaiahSK, Fernandez-CapetilloO, NussenzweigA, XuX, et al. (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37: 41–47.
45. AndersonLK, ReevesA, WebbLM, AshleyT (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569–1579.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 11
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