Evolutionarily Diverged Regulation of X-chromosomal Genes as a Primal Event in Mouse Reproductive Isolation

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Reproductive isolation characterized by male sterility and decreased viability is important for speciation, because it suppresses free genetic exchange between two diverged populations and accelerates the genetic divergence. One of the reproductive isolation phenomena, hybrid sterility (sterility in hybrid animals), is possibly caused by deleterious interactions between diverged genetic factors brought by two distinct populations. The polymorphism not only in protein-coding sequences but also in transcriptional regulatory sequences can cause the genetic incompatibility in hybrid animals. However, the precise genetic mechanisms of hybrid sterility are mostly unknown. Here, we report that the expression of X-linked genes derived from one mouse subspecies was largely misregulated in the genetic background of another subspecies. The misregulated expression of the X-linked genes subsequently affected the global expression of autosomal genes. The results collectively indicate that hybrid sterility between the two mouse subspecies is caused by misregulation of gene expression due to genetic incompatibility in the transcriptional regulatory circuitry. Such genetic incompatibility in transcriptional regulation likely underlies reproductive isolation in general.

Vyšlo v časopise: Evolutionarily Diverged Regulation of X-chromosomal Genes as a Primal Event in Mouse Reproductive Isolation. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004301
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004301

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Zdroje

1. DobzhanskyT (1936) Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics 21 : 113–135.

2. MullerH, PontecorvoG (1942) Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27 : 157.

3. Dobzhansky T (1951) Genetics and the Origin of Species. New York: Columbia Univ Press.

4. MaheshwariS, BarbashDA (2011) The Genetics of Hybrid Incompatibilities. Annu Rev Genet 45 : 331–355.

5. GoncalvesA, Leigh-BrownS, ThybertD, StefflovaK, TurroE, et al. (2012) Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res 22 : 2376–2384.

6. Coyne JA, Orr HA (1989) Two rules of speciation. In: Otte D, Endler J, editors. Speciation and its consequences. Sunderland: Sinauer. pp. 180–207.

7. CharlesworthB, CoyneJA, BartonNH (1987) The Relative Rates of Evolution of Sex Chromosomes and Autosomes. The American Naturalist 130 : 113–146.

8. VicosoB, CharlesworthB (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7 : 645–653.

9. KhilP, SmirnovaN, RomanienkoP, Camerini-OteroR (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36 : 642–646.

10. WangPJ, McCarreyJR, YangF, PageDC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27 : 422–426.

11. SaifiGM, ChandraHS (1999) An apparent excess of sex -⁠ and reproduction-related genes on the human X chromosome. Proc Biol Sci 266 : 203–209.

12. GoodJM, DeanMD, NachmanMW (2008) A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179 : 2213–2228.

13. OkaA, MitaA, TakadaY, KosekiH, ShiroishiT (2010) Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages. Genetics 186 : 339–351.

14. Oka A, Shiroishi T (2012) The role of the X chromosome in house mouse speciation. In: Macholán M, Baird SJE, Munclinger P, Piálek J, editors. Evolution of the House Mouse. Cambridge university press. pp. 431–454.

15. StorchováR, GregorováS, BuckiováD, KyselováV, DivinaP, et al. (2004) Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm Genome 15 : 515–524.

16. GeraldesA, BassetP, GibsonB, SmithK, HarrB, et al. (2008) Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol 17 : 5349–5363.

17. ForejtJ (1996) Hybrid sterility in the mouse. Trends Genet 12 : 412–417.

18. MiholaO, TrachtulecZ, VlcekC, SchimentiJC, ForejtJ (2009) A mouse speciation gene encodes a meiotic histone h3 methyltransferase. Science 323 : 373–375.

19. FlachsP, MiholaO, SimecekP, GregorovaS, SchimentiJC, et al. (2012) Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility. PLoS Genet 8: e1003044.

20. DodB, JermiinLS, BoursotP, ChapmanVH, NielsenJT, et al. (1993) Counterselection on sex chromosomes in the Mus musculus European hybrid zone. Journal of Evolutionary Biology 6 : 529–546.

21. MacholánM, MunclingerP, SugerkováM, DufkováP, BímováB, et al. (2007) Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61 : 746–771.

22. PayseurBA, KrenzJG, NachmanMW (2004) Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58 : 2064–2078.

23. TeeterK, PayseurB, HarrisL, BakewellM, ThibodeauL, et al. (2008) Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res 18 : 67–76.

24. TuckerPK, SageRD, WarnerJ, WilsonAC, EicherEM (1992) Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46 : 1146–1163.

25. WhiteMA, SteffyB, WiltshireT, PayseurBA (2011) Genetic dissection of a key reproductive barrier between nascent species of house mice. Genetics 189 : 289–304.

26. GoodJM, DeanMD, NachmanMW (2008) A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179 : 2213–2228.

27. OkaA, MitaA, Sakurai-YamataniN, YamamotoH, TakagiN, et al. (2004) Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies. Genetics 166 : 913–924.

28. OkaA, AotoT, TotsukaY, TakahashiR, UedaM, 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.

29. YonekawaH, MoriwakiK, GotohO, WatanabeJ, HayashiJI, et al. (1980) Relationship between laboratory mice and the subspecies Mus musculus domesticus based on restriction endonuclease cleavage sites. Jpn J Genet 55 : 289–296.

30. YonekawaH, MoriwakiK, GotohO, MiyashitaN, MatsushimaY, et al. (1988) Hybrid origin of Japanese mice “Mus musculus molossinus”: evidence from restriction analysis of mitochondrial DNA. Mol Biol Evol 5 : 63–78.

31. Moriwaki K (1994) Wild mice from the geneticist's viewpoint. In: Moriwaki K, Shiroishi T, Yonekawa H, editors. Genetics in Wild Mice: Its Application to Biomedical Research. Tokyo: Japan Scientific Press and Karger. pp. 13–25.

32. SakaiT, KikkawaY, MiuraI, InoueT, MoriwakiK, et al. (2005) Origins of mouse inbred strains deduced from whole-genome scanning by polymorphic microsatellite loci. Mamm Genome 16 : 11–19.

33. EllisPJ, FurlongRA, WilsonA, MorrisS, CarterD, et al. (2004) Modulation of the mouse testis transcriptome during postnatal development and in selected models of male infertility. Mol Hum Reprod 10 : 271–281.

34. OhboK, YoshidaS, OhmuraM, OhnedaO, OgawaT, et al. (2003) Identification and characterization of stem cells in prepubertal spermatogenesis in mice. Dev Biol 258 : 209–225.

35. YangL, WuW, QiH (2013) Gene expression profiling revealed specific spermatogonial stem cell genes in mouse. Genesis 51 : 83–96.

36. TakadaT, EbataT, NoguchiH, KeaneT, AdamsD, et al. (2013) The ancestor of extant Japanese fancy mice contributed to the mosaic genomes of classical inbred strains. Genome Res 23 : 1329–1338.

37. IrizarryR, HobbB, CollinF, Beazer-BarclayY, AntonellisK, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 : 249–264.

38. Lehmann EL (2006) Nonparametrics: Statistical Methods Based on Ranks. Berlin, Germany: Springer.

39. UechiT, MaedaN, TanakaT, KenmochiN (2002) Functional second genes generated by retrotransposition of the X-linked ribosomal protein genes. Nucleic Acids Res 30 : 5369–5375.

40. UechiT, TanakaT, KenmochiN (2001) A complete map of the human ribosomal protein genes: assignment of 80 genes to the cytogenetic map and implications for human disorders. Genomics 72 : 223–230.

41. CampbellP, GoodJM, NachmanMW (2013) Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193 : 819–828.

42. GoodJ, GigerT, DeanM, NachmanM (2010) Widespread over-expression of the X chromosome in sterile F1 hybrid mice. PLoS Genet

43. TakadaT, MitaA, MaenoA, SakaiT, ShitaraH, et al. (2008) Mouse inter-subspecific consomic strains for genetic dissection of quantitative complex traits. Genome Res 18 : 500–508.

44. RiceW (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38 : 735–742.

45. GurbichT, BachtrogD (2008) Gene content evolution on the X chromosome. Current Opinion in Genetics & Development 18 : 493–498.

46. ChengY, BuffoneMG, KouadioM, GoodheartM, PageDC, et al. (2007) Abnormal sperm in mice lacking the Taf7l gene. Mol Cell Biol 27 : 2582–2589.

47. PointudJC, MengusG, BrancorsiniS, MonacoL, ParvinenM, et al. (2003) The intracellular localisation of TAF7L, a paralogue of transcription factor TFIID subunit TAF7, is developmentally regulated during male germ-cell differentiation. J Cell Sci 116 : 1847–1858.

48. PanJ, EckardtS, LeuNA, BuffoneMG, ZhouJ, et al. (2009) Inactivation of Nxf2 causes defects in male meiosis and age-dependent depletion of spermatogonia. Dev Biol 330 : 167–174.

49. ZhouJ, PanJ, EckardtS, LeuNA, McLaughlinKJ, et al. (2011) Nxf3 is expressed in Sertoli cells, but is dispensable for spermatogenesis. Mol Reprod Dev 78 : 241–249.

50. TakanoK, MikiT, KatahiraJ, YonedaY (2007) NXF2 is involved in cytoplasmic mRNA dynamics through interactions with motor proteins. Nucleic Acids Res 35 : 2513–2521.

51. GordonKL, RuvinskyI (2012) Tempo and mode in evolution of transcriptional regulation. PLoS Genet 8: e1002432.

52. AndersonEL, BaltusAE, Roepers-GajadienHL, HassoldTJ, de RooijDG, et al. (2008) Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A 105 : 14976–14980.

53. KoubovaJ, MenkeDB, ZhouQ, CapelB, GriswoldMD, et al. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 103 : 2474–2479.

54. VernetN, DennefeldC, Rochette-EglyC, Oulad-AbdelghaniM, ChambonP, et al. (2006) Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147 : 96–110.