PRDM9 Drives Evolutionary Erosion of Hotspots in through Haplotype-Specific Initiation of Meiotic Recombination

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Sexually reproducing creatures need to produce germ cells, notably sperm and egg, and do so using a specialized cell division, termed meiosis. A hallmark of meiosis is the process of recombination, in which pieces of maternal and paternal genetic material are exchanged, creating new combinations that are inherited by their progeny. Recombination increases diversity in subsequent generations, facilitating evolution. However, if recombination goes awry, it can lead to genetic disorders and spontaneous abortions in humans. In most mammals the sites of recombination are directed by the enzyme PRDM9 to specific regions on DNA, termed hotspots. For several decades it has been speculated that the process of recombination should lead to the eventual inactivation of hotspots, resulting in the loss of ability to reproduce. The discovery of PRDM9 provided a potential solution to this dilemma when the appearance of new PRDM9 alleles with altered DNA binding specificity would immediately create a new set of hotspots. We have now used the power of mouse genetics and large scale measurements of PRDM9 location and activity to show that this cycle of hotspot loss and recovery does indeed occur over the course of hundreds of thousands of years, and is directed by PRDM9.

Vyšlo v časopise: PRDM9 Drives Evolutionary Erosion of Hotspots in through Haplotype-Specific Initiation of Meiotic Recombination. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004916
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004916

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Zdroje

1. BaudatF, ImaiY, de MassyB (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14 : 794–806.

2. PaigenK, PetkovP (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev Genet 11 : 221–233.

3. 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.

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

5. 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.

6. 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.

7. ParvanovED, PetkovPM, PaigenK (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327 : 835.

8. BakerCL, KajitaS, WalkerM, PetkovPM, PaigenK (2014) PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res 24 : 724–732.

9. BrickK, SmagulovaF, KhilP, Camerini-OteroRD, PetukhovaGV (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485 : 642–645.

10. KeeneyS (2008) Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis. Genome dynamics and stability 2 : 81–123.

11. ColeF, KeeneyS, JasinM (2010) Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol Cell 39 : 700–710.

12. NgSH, ParvanovE, PetkovPM, PaigenK (2008) A quantitative assay for crossover and noncrossover molecular events at individual recombination hotspots in both male and female gametes. Genomics 92 : 204–209.

13. BaudatF, de MassyB (2007) Cis -⁠ and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot. PLoS Genet 3: e100.

14. 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.

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

16. JeffreysAJ, NeumannR (2005) Factors influencing recombination frequency and distribution in a human meiotic crossover hotspot. Hum Mol Genet 14 : 2277–2287.

17. PaigenK, SzatkiewiczJP, SawyerK, LeahyN, ParvanovED, et al. (2008) The recombinational anatomy of a mouse chromosome. PLoS Genet 4: e1000119.

18. SzostakJW, Orr-WeaverTL, RothsteinRJ, StahlFW (1983) The double-strand-break repair model for recombination. Cell 33 : 25–35.

19. CoopG, MyersSR (2007) Live hot, die young: transmission distortion in recombination hotspots. PLoS Genet 3: e35.

20. JeffreysAJ, NeumannR (2009) The rise and fall of a human recombination hot spot. Nat Genet 41 : 625–629.

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

22. BuardJ, RivalsE, Dunoyer de SegonzacD, GarresC, CaminadeP, et al. (2014) Diversity of Prdm9 Zinc Finger Array in Wild Mice Unravels New Facets of the Evolutionary Turnover of this Coding Minisatellite. PLoS One 9: e85021.

23. KonoH, TamuraM, OsadaN, SuzukiH, AbeK, et al. (2014) Prdm9 polymorphism unveils mouse evolutionary tracks. DNA Res 21 : 315–326.

24. OliverPL, GoodstadtL, BayesJJ, BirtleZ, RoachKC, et al. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5: e1000753.

25. SchwartzJJ, RoachDJ, ThomasJH, ShendureJ (2014) Primate evolution of the recombination regulator PRDM9. Nat Commun 5 : 4370.

26. ThomasJH, EmersonRO, ShendureJ (2009) Extraordinary molecular evolution in the PRDM9 fertility gene. PLoS One 4: e8505.

27. ColeF, BaudatF, GreyC, KeeneyS, de MassyB, et al. (2014) Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet. 46 : 1072–1080.

28. SarbajnaS, DenniffM, JeffreysAJ, NeumannR, Soler ArtigasM, et al. (2012) A major recombination hotspot in the XqYq pseudoautosomal region gives new insight into processing of human gene conversion events. Hum Mol Genet 21 : 2029–2038.

29. GuenetJL, BonhommeF (2003) Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet 19 : 24–31.

30. SmagulovaF, GregorettiIV, BrickK, KhilP, Camerini-OteroRD, et al. (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472 : 375–378.

31. KeaneTM, GoodstadtL, DanecekP, WhiteMA, WongK, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477 : 289–294.

32. HuangS, HoltJ, KaoCY, McMillanL, WangW (2014) A novel multi-alignment pipeline for high-throughput sequencing data. Database (Oxford) 2014.

33. BillingsT, SargentEE, SzatkiewiczJP, LeahyN, KwakIY, et al. (2010) Patterns of recombination activity on mouse chromosome 11 revealed by high resolution mapping. PLoS One 5: e15340.

34. HeinzS, RomanoskiCE, BennerC, AllisonKA, KaikkonenMU, et al. (2013) Effect of natural genetic variation on enhancer selection and function. Nature 503 : 487–492.

35. KasowskiM, Kyriazopoulou-PanagiotopoulouS, GrubertF, ZauggJB, KundajeA, et al. (2013) Extensive variation in chromatin states across humans. Science 342 : 750–752.

36. KilpinenH, WaszakSM, GschwindAR, RaghavSK, WitwickiRM, et al. (2013) Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342 : 744–747.

37. McVickerG, van de GeijnB, DegnerJF, CainCE, BanovichNE, et al. (2013) Identification of genetic variants that affect histone modifications in human cells. Science 342 : 747–749.

38. PetersAD (2008) A combination of cis and trans control can solve the hotspot conversion paradox. Genetics 178 : 1579–1593.

39. WahlsWP, DavidsonMK (2011) DNA sequence-mediated, evolutionarily rapid redistribution of meiotic recombination hotspots. Genetics 189 : 685–694.

40. MiholaO, TrachtulecZ, VlcekC, SchimentiJC, ForejtJ (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323 : 373–375.

41. UbedaF, WilkinsJF (2011) The Red Queen theory of recombination hotspots. J Evol Biol 24 : 541–553.

42. GroeneveldLF, AtenciaR, GarrigaRM, VigilantL (2012) High diversity at PRDM9 in chimpanzees and bonobos. PLoS One 7: e39064.

43. SandorC, LiW, CoppietersW, DruetT, CharlierC, et al. (2012) Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle. PLoS Genet 8: e1002854.

44. SteinerCC, RyderOA (2013) Characterization of Prdm9 in equids and sterility in mules. PLoS One 8: e61746.

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

46. KhilPP, SmagulovaF, BrickKM, Camerini-OteroRD, PetukhovaGV (2012) Sensitive mapping of recombination hotspots using sequencing-based detection of ssDNA. Genome Res 22 : 957–965.

47. Ross-InnesCS, StarkR, TeschendorffAE, HolmesKA, AliHR, et al. (2012) Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 481 : 389–393.

48. DegnerJF, MarioniJC, PaiAA, PickrellJK, NkadoriE, et al. (2009) Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25 : 3207–3212.

49. MungerSC, RaghupathyN, ChoiK, SimonsAK, GattiDM, et al. (2014) RNA-Seq Alignment to Individualized Genomes Improves Transcript Abundance Estimates in Multiparent Populations. Genetics 198 : 59–73.

50. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

51. YeT, KrebsAR, ChoukrallahMA, KeimeC, PlewniakF, et al. (2011) seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 39: e35.

52. SaldanhaAJ (2004) Java Treeview–extensible visualization of microarray data. Bioinformatics 20 : 3246–3248.

53. QuinlanAR, HallIM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 : 841–842.

54. BaileyTL, BodenM, BuskeFA, FrithM, GrantCE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208.

55. JeeJ, RozowskyJ, YipKY, LochovskyL, BjornsonR, et al. (2011) ACT: aggregation and correlation toolbox for analyses of genome tracks. Bioinformatics 27 : 1152–1154.