The Red Queen Model of Recombination Hotspots Evolution in the Light of Archaic and Modern Human Genomes

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In eukaryotic genomes, recombination plays a central role by ensuring the proper segregation of chromosomes during meiosis and increasing genetic diversity at the population scale. Recombination events are not uniformly distributed along chromosomes, but cluster in narrow regions called hotspots. The absence of overlap between human and chimpanzee hotspots indicates that the location of these hotspots evolves rapidly. However, the reasons for this rapid dynamic are still unknown. To gain insight into the processes driving the evolution of recombination hotspots we analyzed the recent history of human hotspots, using the genome of a closely related archaic hominid, Denisovan. We searched for genomic signatures of past recombination activity and compared them to present-day patterns of recombination in humans. Our results show that human hotspots are younger than previously thought and that they are not conserved in Denisovans. Moreover, we confirm that hotspots are subject to a self-destruction process, due to biased gene conversion. We quantified this process, and showed that its intensity is strong enough to cause the fast turnover of human hotspots.

Vyšlo v časopise: The Red Queen Model of Recombination Hotspots Evolution in the Light of Archaic and Modern Human Genomes. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004790
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004790

Souhrn

Zdroje

1. CoopG, PrzeworskiM (2007) An evolutionary view of human recombination. Nat Rev Genet 8: 23–34 doi:10.1038/nrg1947

2. The International HapMap Consortium (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851–861 doi:10.1038/nature06258

3. MyersS, BottoloL, FreemanC, McVeanG, DonnellyP (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321–324 doi:10.1126/science.1117196

4. SmagulovaF, Gregoretti IV, BrickK, KhilP, Camerini-OteroRD, et al. (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472: 375–378 doi:10.1038/nature09869

5. 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 doi:10.1101/gr.124123.111

6. AutonA, Rui LiY, KiddJ, OliveiraK, NadelJ, et al. (2013) Genetic Recombination Is Targeted towards Gene Promoter Regions in Dogs. PLoS Genet 9: e1003984 doi:10.1371/journal.pgen.1003984

7. ChoiK, ZhaoX, KellyKA, VennO, HigginsJD, et al. (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45: 1327–1336 doi:10.1038/ng.2766

8. PanJ, SasakiM, KniewelR, MurakamiH, BlitzblauHG, et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719–731 doi:10.1016/j.cell.2011.02.009

9. 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 doi:10.1126/science.1183439

10. MyersS, BowdenR, TumianA, BontropRE, FreemanC, et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327: 876–879 doi:10.1126/science.1182363

11. BergIL, NeumannR, LamK-WG, SarbajnaS, Odenthal-HesseL, et al. (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 42: 859–863 doi:10.1038/ng.658

12. BrickK, SmagulovaF, KhilP, Camerini-OteroRD, Petukhova GV (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642–645 doi:10.1038/nature11089

13. HayashiK, YoshidaK, MatsuiY (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374–378 doi:10.1038/nature04112

14. GreyC, BarthèsP, 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

15. BergIL, NeumannR, SarbajnaS, Odenthal-HesseL, ButlerNJ, et al. (2011) Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc Natl Acad Sci U S A 108: 12378–12383 doi:10.1073/pnas.1109531108

16. HinchAG, TandonA, PattersonN, SongY, RohlandN, et al. (2011) The landscape of recombination in African Americans. Nature 476: 170–175 doi:10.1038/nature10336

17. MyersS, FreemanC, AutonA, DonnellyP, McVeanG (2008) A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet 40: 1124–1129 doi:10.1038/ng.213

18. PtakSE, HindsDA, KoehlerK, NickelB, PatilN, et al. (2005) Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37: 429–434 doi:10.1038/ng1529

19. AutonA, Fledel-AlonA, PfeiferS, VennO, SégurelL, et al. (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336: 193–198 doi:10.1126/science.1216872

20. WincklerW, MyersSR, RichterDJ, OnofrioRC, McDonaldGJ, et al. (2005) Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308: 107–111 doi:10.1126/science.1105322

21. 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

22. PontingCP (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends Genet 27: 165–171 doi:10.1016/j.tig.2011.02.001

23. BoultonA, MyersRS, RedfieldRJ (1997) The hotspot conversion paradox and the evolution of meiotic recombination. Proc Natl Acad Sci U S A 94: 8058–8063.

24. JeffreysAJ, NeumannR (2002) Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nat Genet 31: 267–271 doi:10.1038/ng910

25. CoopG, MyersSR (2007) Live hot, die young: transmission distortion in recombination hotspots. PLoS Genet 3: e35 doi:10.1371/journal.pgen.0030035

26. KongA, BarnardJ, GudbjartssonDF, ThorleifssonG, JonsdottirG, et al. (2004) Recombination rate and reproductive success in humans. Nat Genet 36: 1203–1206 doi:10.1038/ng1445

27. UbedaF, WilkinsJF (2011) The Red Queen theory of recombination hotspots. J Evol Biol 24: 541–553 doi:10.1111/j.1420-9101.2010.02187.x

28. MeyerM, KircherM, GansaugeM-T, LiH, RacimoF, et al. (2012) A high-coverage genome sequence from an archaic Denisovan individual. Science 338: 222–226 doi:10.1126/science.1224344

29. LangergraberKE, PrüferK, RowneyC, BoeschC, CrockfordC, et al. (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci U S A 109: 15716–15721 doi:10.1073/pnas.1211740109

30. The 1000 Genomes Project Consortium (2010) A map of human genome variation from population-scale sequencing. Nature 467: 1061–1073 doi:10.1038/nature09534

31. The 1000 Genomes Project Consortium (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56–65 doi:10.1038/nature11632

32. NagylakiT (1983) Evolution of a finite population under gene conversion. Proc Natl Acad Sci U S A 80: 6278–6281.

33. Meyer M, Kircher M, Gansauge M-T, Li H, Racimo F, et al.. (2012) A High-Coverage Genome Sequence from an Archaic Denisovan Individual. Science (80-) in press: 1–10. doi:10.1126/science.1224344.

34. Eyre-WalkerA, WoolfitM, PhelpsT (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173: 891–900 doi:10.1534/genetics.106.057570

35. KongA, ThorleifssonG, GudbjartssonDF, MassonG, SigurdssonA, et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099–1103 doi:10.1038/nature09525

36. DuretL, GaltierN (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10: 285–311 doi:10.1146/annurev-genom-082908-150001

37. LesecqueY, MouchiroudD, DuretL (2013) GC-biased gene conversion in yeast is specifically associated with crossovers: molecular mechanisms and evolutionary significance. Mol Biol Evol 30: 1409–1419 doi:10.1093/molbev/mst056

38. DuretL, ArndtPF (2008) The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4: 1–19 doi:10.1371/journal.pgen.1000071

39. MeunierJ, DuretL (2004) Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 21: 984–990 doi:10.1093/molbev/msh070

40. MunchK, MailundT, DutheilJY, SchierupMH (2014) A fine-scale recombination map of the human-chimpanzee ancestor reveals faster change in humans than in chimpanzees and a strong impact of GC-biased gene conversion. Genome Res 24: 467–474 doi:10.1101/gr.158469.113

41. KongA, FriggeML, MassonG, BesenbacherS, SulemP, et al. (2012) Rate of de novo mutations and the importance of father's age to disease risk. Nature 488: 471–475 doi:10.1038/nature11396

42. Fledel-AlonA, LefflerEM, GuanY, StephensM, CoopG, et al. (2011) Variation in human recombination rates and its genetic determinants. PLoS One 6: e20321 doi:10.1371/journal.pone.0020321

43. BillingsT, ParvanovED, BakerCL, WalkerM, PaigenK, et al. (2013) DNA binding specificities of the long zinc-finger recombination protein PRDM9. Genome Biol 14: R35 doi:10.1186/gb-2013-14-4-r35

44. SchwartzJJ, RoachDJ, ThomasJH, ShendureJ (2014) Primate evolution of the recombination regulator PRDM9. Nature Communications 5: 4370 doi:10.1038/ncomms5370

45. KimuraM, OhtaT (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 14: 24–32.

46. PatenB, HerreroJ, FitzgeraldS (2008) Genome-wide nucleotide-level mammalian ancestor reconstruction. Genome Res 4: 1829–1843 doi:10.1101/gr.076521.108

47. FujitaPA, RheadB, ZweigAS, HinrichsAS, KarolchikD, et al. (2011) The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39: D876–82 doi:10.1093/nar/gkq963

48. ScallyA, DutheilJY, HillierLW, JordanGE, GoodheadI, et al. (2012) Insights into hominid evolution from the gorilla genome sequence. Nature 483: 169–175 doi:10.1038/nature10842

49. Smit A, Hubly R, Green P (2010) RepeatMasker Open-3.0. http://www.repeatmasker.org.

50. MuyleA, Serres-GiardiL, RessayreA, EscobarJ, GléminS (2011) GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Mol Biol Evol 28: 2695–2706 doi:10.1093/molbev/msr104

51. DuretL (2006) The GC content of primates and rodents genomes is not at equilibrium: a reply to Antezana. J Mol Evol 62: 803–806 doi:10.1007/s00239-005-0228-7

52. R Development Core Team (2012) R: A language and environment for statistical computing. Vienna: R foundation for statistical computing.