#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Contrasted Patterns of Crossover and Non-crossover at Meiotic Recombination Hotspots


The vast majority of meiotic recombination events (crossovers (COs) and non-crossovers (NCOs)) cluster in narrow hotspots surrounded by large regions devoid of recombinational activity. Here, using a new molecular approach in plants, called “pollen-typing”, we detected and characterized hundreds of CO and NCO molecules in two different hotspot regions in Arabidopsis thaliana. This analysis revealed that COs are concentrated in regions of a few kilobases where their rates reach up to 50 times the genome average. The hotspots themselves tend to cluster in regions less than 8 kilobases in size with overlapping CO distribution. Non-crossover (NCO) events also occurred in the two hotspots but at very different levels (local CO/NCO ratios of 1/1 and 30/1) and their track lengths were quite small (a few hundred base pairs). We also showed that the ZMM protein MSH4 plays a role in CO formation and somewhat unexpectedly we also found that it is involved in the generation of NCOs but with a different level of effect. Finally, factors acting in cis and in trans appear to shape the rate and distribution of COs at meiotic recombination hotspots.


Vyšlo v časopise: Contrasted Patterns of Crossover and Non-crossover at Meiotic Recombination Hotspots. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003922
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003922

Souhrn

The vast majority of meiotic recombination events (crossovers (COs) and non-crossovers (NCOs)) cluster in narrow hotspots surrounded by large regions devoid of recombinational activity. Here, using a new molecular approach in plants, called “pollen-typing”, we detected and characterized hundreds of CO and NCO molecules in two different hotspot regions in Arabidopsis thaliana. This analysis revealed that COs are concentrated in regions of a few kilobases where their rates reach up to 50 times the genome average. The hotspots themselves tend to cluster in regions less than 8 kilobases in size with overlapping CO distribution. Non-crossover (NCO) events also occurred in the two hotspots but at very different levels (local CO/NCO ratios of 1/1 and 30/1) and their track lengths were quite small (a few hundred base pairs). We also showed that the ZMM protein MSH4 plays a role in CO formation and somewhat unexpectedly we also found that it is involved in the generation of NCOs but with a different level of effect. Finally, factors acting in cis and in trans appear to shape the rate and distribution of COs at meiotic recombination hotspots.


Zdroje

1. Martinez-PerezE, ColaiacovoMP (2009) Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev 19 (2) 105–12.

2. de MassyB (2003) Distribution of meiotic recombination sites. Trends Genet 19: 514–522.

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

4. BergeratA, de MassyB, GadelleD, VaroutasPC, NicolasA, et al. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386: 414–417.

5. KeeneyS, GirouxCN, KlecknerN (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375–384.

6. BaudatF, de MassyB (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565–577.

7. KauppiL, JeffreysAJ, KeeneyS (2004) Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 5: 413–424.

8. WallJD (2004) Close look at gene conversion hot spots. Nat Genet 36: 114–115.

9. ManceraE, BourgonR, BrozziA, HuberW, SteinmetzLM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479–485.

10. ColeF, KeeneyS, JasinM (2010) Comprehensive, Fine-Scale Dissection of Homologous Recombination Outcomes at a Hot Spot in Mouse Meiosis. Mol Cell 39: 700–710.

11. DoonerHK (2002) Extensive interallelic polymorphisms drive meiotic recombination into a crossover pathway. Plant Cell 14: 1173–1183.

12. MercierR, JolivetS, VezonD, HuppeE, ChelyshevaL, et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15: 692–701.

13. ChelyshevaL, DialloS, VezonD, GendrotG, VrielynckN, et al. (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: 4621–4632.

14. Sanchez-MoranE, SantosJL, JonesGH, FranklinFC (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21: 2220–2233.

15. Sanchez-MoranE, ArmstrongSJ, SantosJL, FranklinFC, JonesGH (2002) Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162: 1415–1422.

16. LuP, HanX, QiJ, YangJ, WijeratneAJ, et al. (2012) Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis. Genome Res 22: 508–518.

17. YangS, YuanY, WangL, LiJ, WangW, et al. (2012) Great majority of recombination events in Arabidopsis are gene conversion events. Proc Natl Acad Sci U S A 109: 20992–20997.

18. SunY, AmbroseJH, HaugheyBS, WebsterTD, PierrieSN, et al. (2012) Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLoS Genet 8: e1002968.

19. LynnA, SoucekR, BornerGV (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605.

20. MullerHJ (1916) The mechanism of crossing-over. Am Nat 50: 193–434.

21. MezardC, VignardJ, DrouaudJ, MercierR (2007) The road to crossovers: plants have their say. Trends Genet 23: 91–99.

22. JeffreysAJ, MurrayJ, NeumannR (1998) High-resolution mapping of crossovers in human sperm defines a minisatellite-associated recombination hotspot. Mol Cell 2: 267–273.

23. DrouaudJ, CamilleriC, BourguignonPY, CanaguierA, BerardA, et al. (2006) Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination “hot spots”. Genome Res 16: 106–114.

24. DrouaudJ, MezardC (2011) Characterization of meiotic crossovers in pollen from Arabidopsis thaliana. Methods Mol Biol 745: 223–249.

25. BaudatF, de MassyB (2009) Parallel detection of crossovers and noncrossovers in mouse germ cells. Methods Mol Biol 305–322.

26. ColeF, JasinM (2011) Isolation of meiotic recombinants from mouse sperm. Methods Mol Biol 745: 251–282.

27. KauppiL, MayCA, JeffreysAJ (2009) Analysis of meiotic recombination products from human sperm. Methods Mol Biol 323–355.

28. ZhangX, ClarenzO, CokusS, BernatavichuteYV, PellegriniM, et al. (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5: e129.

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

30. KhademianH, GirautL, DrouaudJ, MezardC (2013) Characterization of meiotic non-crossover molecules from Arabidopsis thaliana pollen. Methods Mol Biol 990: 177–190.

31. 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.

32. HigginsJD, ArmstrongSJ, FranklinFC, JonesGH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18: 2557–2570.

33. BoisPR (2007) A highly polymorphic meiotic recombination mouse hot spot exhibits incomplete repair. Mol Cell Biol 27: 7053–7062.

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

35. WuZK, GetunIV, BoisPR (2010) Anatomy of mouse recombination hot spots. Nucleic Acids Res

36. AdamsDE, WestSC (1996) Bypass of DNA heterologies during RuvAB-mediated three- and four-strand branch migration. J Mol Biol 263: 582–596.

37. YaoH, SchnablePS (2005) Cis-effects on meiotic recombination across distinct a1-sh2 intervals in a common Zea genetic background. Genetics 170: 1929–1944.

38. YaoH, ZhouQ, LiJ, SmithH, YandeauM, et al. (2002) Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize. Proc Natl Acad Sci U S A 99: 6157–6162.

39. DoonerHK, HeL (2008) Maize genome structure variation: interplay between retrotransposon polymorphisms and genic recombination. Plant Cell 20: 249–258.

40. HeL, DoonerHK (2009) Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for Helitron and retrotransposon insertions. Proc Natl Acad Sci U S A 106: 8410–8416.

41. JeffreysAJ, KauppiL, NeumannR (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat Genet 29: 217–222.

42. 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.

43. 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.

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

45. SommermeyerV, BeneutC, ChaplaisE, SerrentinoME, BordeV (2013) Spp1, a member of the Set1 Complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol Cell 49: 43–54.

46. YamadaS, OhtaK, YamadaT (2013) Acetylated Histone H3K9 is associated with meiotic recombination hotspots, and plays a role in recombination redundantly with other factors including the H3K4 methylase Set1 in fission yeast. Nucleic Acids Res 41: 3504–3517.

47. LibeauP, DurandetM, GranierF, MarquisC, BerthomeR, et al. (2011) Gene expression profiling of Arabidopsis meiocytes. Plant Biol (Stuttg) 13: 784–793.

48. YelinaNE, ChoiK, ChelyshevaL, MacaulayM, de SnooB, et al. (2012) Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet 8: e1002844.

49. Yandeau-NelsonMD, NikolauBJ, SchnablePS (2006) Effects of trans-acting genetic modifiers on meiotic recombination across the a1-sh2 interval of maize. Genetics 174: 101–112.

50. BaudatF, NicolasA (1997) Clustering of meiotic double-strand breaks on yeast chromosome III. Proc Natl Acad Sci U S A 94: 5213–5218.

51. PetesTD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2: 360–369.

52. BuhlerC, BordeV, LichtenM (2007) Mapping Meiotic Single-Strand DNA Reveals a New Landscape of DNA Double-Strand Breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.

53. CromieGA, HyppaRW, CamHP, FarahJA, GrewalSI, et al. (2007) A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet 3: e141.

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

55. BordeV, RobineN, LinW, BonfilsS, GeliV, et al. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. Embo J 28: 99–111.

56. BuardJ, BarthesP, GreyC, de MassyB (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. Embo J 28: 2616–2624.

57. LiuS, YehCT, JiT, YingK, WuH, et al. (2009) Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet 5: e1000733.

58. ReddyKC, VilleneuveAM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118: 439–452.

59. WagnerCR, KuerversL, BaillieDL, YanowitzJL (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467: 839–843.

60. de CastroE, SorianoI, MarinL, SerranoR, QuintalesL, et al. (2012) Nucleosomal organization of replication origins and meiotic recombination hotspots in fission yeast. Embo J 31: 124–137.

61. GetunIV, WuZK, KhalilAM, BoisPR (2010) Nucleosome occupancy landscape and dynamics at mouse recombination hotspots. EMBO Rep 11: 555–560.

62. ZhangL, MaH, PughBF (2011) Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res 21: 875–884.

63. GoffeauA, BarrellBG, BusseyH, DavisRW, DujonB, et al. (1996) Life with 6000 genes. Science 274: 546, 563–547.

64. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

65. EvansE, SugawaraN, HaberJE, AlaniE (2000) The Saccharomyces cerevisiae Msh2 mismatch repair protein localizes to recombination intermediates in vivo. Mol Cell 5: 789–799.

66. BergIL, NeumannR, LamKW, SarbajnaS, Odenthal-HesseL, et al. (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 42: 859–863.

67. 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.

68. YeadonPJ, RasmussenJP, CatchesideDE (2001) Recombination events in Neurospora crassa may cross a translocation breakpoint by a template-switching mechanism. Genetics 159: 571–579.

69. GuillonH, BaudatF, GreyC, LiskayRM, de MassyB (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20: 563–573.

70. MartiniE, BordeV, LegendreM, AudicS, RegnaultB, et al. (2011) Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways. PLoS Genet 7: e1002305.

71. YoudsJL, BoultonSJ (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501–513.

72. StorlazziA, GarganoS, Ruprich-RobertG, FalqueM, DavidM, et al. (2010) Recombination Proteins Mediate Meiotic Spatial Chromosome Organization and Pairing. Cell 141: 94–106.

73. KneitzB, CohenPE, AvdievichE, ZhuL, KaneMF, et al. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14: 1085–1097.

74. AlonsoJM, StepanovaAN, LeisseTJ, KimCJ, ChenH, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

75. SundaresanV, SpringerP, VolpeT, HawardS, JonesJD, et al. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797–1810.

76. GrelonM, VezonD, GendrotG, PelletierG (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20: 589–600.

77. Weigel D, Glazebrook J (2002) Arabidopsis: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. 354 p.

78. JeffreysAJ, NeumannR, WilsonV (1990) Repeat unit sequence variation in minisatellites: a novel source of DNA polymorphism for studying variation and mutation by single molecule analysis. Cell 60: 473–485.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#