Genome-Wide Crossover Distribution in Meiosis Reveals Sex-Specific Patterns along Chromosomes
In most species, crossovers (COs) are essential for the accurate segregation of homologous chromosomes at the first meiotic division. Their number and location are tightly regulated. Here, we report a detailed, genome-wide characterization of the rate and localization of COs in Arabidopsis thaliana, in male and female meiosis. We observed dramatic differences between male and female meiosis which included: (i) genetic map length; 575 cM versus 332 cM respectively; (ii) CO distribution patterns: male CO rates were very high at both ends of each chromosome, whereas female CO rates were very low; (iii) correlations between CO rates and various chromosome features: female CO rates correlated strongly and negatively with GC content and gene density but positively with transposable elements (TEs) density, whereas male CO rates correlated positively with the CpG ratio. However, except for CpG, the correlations could be explained by the unequal repartition of these sequences along the Arabidopsis chromosome. For both male and female meiosis, the number of COs per chromosome correlates with chromosome size expressed either in base pairs or as synaptonemal complex length. Finally, we show that interference modulates the CO distribution both in male and female meiosis.
Vyšlo v časopise:
Genome-Wide Crossover Distribution in Meiosis Reveals Sex-Specific Patterns along Chromosomes. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002354
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002354
Souhrn
In most species, crossovers (COs) are essential for the accurate segregation of homologous chromosomes at the first meiotic division. Their number and location are tightly regulated. Here, we report a detailed, genome-wide characterization of the rate and localization of COs in Arabidopsis thaliana, in male and female meiosis. We observed dramatic differences between male and female meiosis which included: (i) genetic map length; 575 cM versus 332 cM respectively; (ii) CO distribution patterns: male CO rates were very high at both ends of each chromosome, whereas female CO rates were very low; (iii) correlations between CO rates and various chromosome features: female CO rates correlated strongly and negatively with GC content and gene density but positively with transposable elements (TEs) density, whereas male CO rates correlated positively with the CpG ratio. However, except for CpG, the correlations could be explained by the unequal repartition of these sequences along the Arabidopsis chromosome. For both male and female meiosis, the number of COs per chromosome correlates with chromosome size expressed either in base pairs or as synaptonemal complex length. Finally, we show that interference modulates the CO distribution both in male and female meiosis.
Zdroje
1. LynnAAshleyTHassoldT 2004 Variation in human meiotic recombination. Annu Rev Genomics Hum Genet 5 317 349
2. SturtevantAH 1915 The behavior of the chromosomes as studied through linkage. Molecular and General Genetics 13 234 287
3. CopenhaverGPHousworthEAStahlFW 2002 Crossover interference in Arabidopsis. Genetics 160 1631 1639
4. HousworthEAStahlFW 2003 Crossover interference in humans. Am J Hum Genet 73 188 197
5. FalqueMMercierRMezardCde VienneDMartinOC 2007 Patterns of recombination and MLH1 foci density along mouse chromosomes: modeling effects of interference and obligate chiasma. Genetics 176 1453 1467
6. FalqueMAndersonLKStackSMGauthierFMartinOC 2009 Two types of meiotic crossovers coexist in maize. Plant Cell 21 3915 3925
7. FossELandeRStahlFWSteinbergCM 1993 Chiasma interference as a function of genetic distance. Genetics 133 681 691
8. McPeekMSSpeedTP 1995 Modeling interference in genetic recombination. Genetics 139 1031 1044
9. TalbertPBHenikoffS 2010 Centromeres convert but don't cross. PLoS Biol 8 e1000326 doi:1000310.1001371/journal.pbio.1000326
10. WestphalTReuterG 2002 Recombinogenic effects of suppressors of position-effect variegation in Drosophila. Genetics 160 609 621
11. Jensen-SeamanMIFureyTSPayseurBALuYRoskinKM 2004 Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14 528 538
12. BackströmNForstmeierWSchielzethHMelleniusHNamK 2010 The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20 485 495
13. BeyeMGattermeierIHasselmannMGempeTSchioettM 2006 Exceptionally high levels of recombination across the honey bee genome. Genome Res 16 1339 1344
14. GoreMAChiaJMElshireRJSunQErsozES 2009 A first-generation haplotype map of maize. Science 20 1115 1117
15. DuretLArndtPF 2008 The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4 e1000071 doi:1000010.1001371/journal.pgen1000071
16. Marsolier-KergoatMCYeramianE 2009 GC content and recombination: Reassessing the causal ffects for the Saccharomyces cerevisiae genome. Genetics 183 31 38
17. DrouaudJCamilleriCBourguignonPYCanaguierABerardA 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
18. MaraisGCharlesworthBWrightSI 2004 Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana. Genome Biol 5 R45
19. MyersSBottoloLFreemanCMcVeanGDonnellyP 2005 A fine-scale map of recombination rates and hotspots across the human genome. Science 310 321 324
20. NachmanMW 2002 Variation in recombination rate across the genome: evidence and implications. Curr Opin Genet Dev 12 657 663
21. PetesTD 2001 Meiotic recombination hot spots and cold spots. Nat Rev Genet 2 360 369
22. LenormandT 2003 The evolution of sex dimorphism in recombination. Genetics 163 811 822
23. HaldaneJBS 1922 Sex ratio and unisexual sterility in hybrid animals. J Genet 12 101 109
24. Ved BratS 1966 Genetic systems in Allium. Sex differences in meiosis. Chromosomes Today 1 31 40
25. KearseyMJRamsayLDJenningsDELydiateDJBohuonEJR 1996 Higher recombination frequencies in female compared to male meioses in Brassica oleracea. Theor Appl Genet 92 363 367
26. ArmstrongSJJonesGH 2001 Female meiosis in wild-type Arabidopsis thaliana and in two meiotic mutants. Sex Plant Reprod 13 177 183
27. DrouaudJMercierRChelyshevaLBerardAFalqueM 2007 Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3 e106 doi:110.1371/journal.pgen.0030106
28. MilesLGIsbergSRGlennTCLanceSLDalzellP 2009 A genetic linkage map for the saltwater crocodile (Crocodylus porosus). BMC Genomics 10 339
29. HedrickPW 2007 Sex: Differences in mutation, recombination, selection, gene flow and genetic drift. Evolution 61 2750 2771
30. HeytingCDietrichAJ 1992 Synaptosomal complexes and the organization of chromatin during meiotic prophase. Cell Biol Int Rep 16 749 760
31. KlecknerNStorlazziAZicklerD 2003 Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19 623 628
32. WallaceBMHultenMA 1985 Meiotic chromosome pairing in the normal human female. Ann Hum Genet 49 215 226
33. CroftJAJonesGH 1989 Chromosome pairing and chiasma formation in spermatocytes and oocytes of Dendrocoelum lacteum (Turbellaria, Tricladida): A cytogenetical and ultrastructural study. Heredity 63 97 106
34. WallaceBMWallaceH 2003 Synaptonemal complex karyotype of zebrafish. Heredity 90 136 140
35. FoxDP 1973 The control of chiasma distribution in the locust, Schistocerca gregaria (Forskål). Chromosoma 43 289 328
36. QuevedoCDel CerroALSantosJLJonesGH 1997 Correlated variation of chiasma frequency and synaptonemal complex length in Locusta migratoria. Heredity 78 515 519
37. TeaseCHultenMA 2004 Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenet Genome Res 107 208 215
38. AGI 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796 815
39. BennettMDLeitchIJPriceHJJohnstonJS 2003 Comparison with Caenorhabditis (∼100 Mb) and Drosophila (∼175 Mb) using flow cytometry show genome size in Arabidopsis to be ∼157 Mb and thus ∼25% larger than the Arabidopsis genome initiative estimate of ∼125 Mb. Annals of Botany 91 547 557
40. ToyotaMMatsudaKKakutaniTTerao MoritaMTasakaM 2010 Developmental changes in crossover frequency in Arabidopsis. Plant J 65 589 599
41. LopezEPradilloMRomeroCSantosJLCunadoN 2008 Pairing and synapsis in wild type Arabidopsis thaliana. Chromosome Res 16 701 708
42. AlbiniSM 1994 A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis. Plant Journal 5 665 672
43. KongAGudbjartssonDFSainzJJonsdottirGMGudjonssonSA 2002 A high-resolution recombination map of the human genome. Nat Genet 31 241 247
44. MetsDGMeyerBJ 2009 Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139 73 86
45. ManceraEBourgonRBrozziAHuberWSteinmetzLM 2008 High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454 479 485
46. BashevaEABidauCJBorodinPM 2008 General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization. Chromosome Res 16 709 719
47. FroenickeLAndersonLKWienbergJAshleyT 2002 Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71 1353 1368
48. PigozziMISolariAJ 1999 Equal frequencies of recombination nodules in both sexes of the pigeon suggest a basic difference with eutherian mammals. Genome 42 315 321
49. JonesGH 1984 The control of chiasma distribution. Symp Soc Exp Biol 38 293 320
50. JonesGHFranklinFC 2006 Meiotic crossing-over: Obligation and Interference. Cell 126 246 248
51. Pardo-Manuel de VillenaFSapienzaC 2001 Recombination is proportional to the number of chromosome arms in mammals Mammalian Genome 12 318 322
52. CoopGPrzeworskiM 2007 An evolutionary view of human recombination. Nat Rev Genet 8 23 34
53. Fledel-AlonAWilsonDJBromanKWenXOberC 2009 Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet 5 e1000658 doi:1000610.1001371/journal.pgen.1000658
54. LiWFreudenbergJ 2011 A mathematical framework for examining whether a minimum number of chiasmata is required per metacentric chromosome or chromosome arm in human. Genomics 97 186 192
55. LiWFreudenbergJ 2009 Two-parameters characterization of chromosome-scale recombination rate. Genome Res 19 2300 2307
56. MezardCVignardJDrouaudJMercierR 2007 The road to crossovers: plants have their say. Trends Genet 23 91 99
57. OsmanKHigginsJDSanchez-MoranEArmstrongSJFranklinFCH 2011 Pathways to meiotic recombination in Arabidopsis thaliana. New Phytologist 190 523 544
58. LhuissierFGOffenbergHHWittichPEVischerNOHeytingC 2007 The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19 862 876
59. de BoerELhuissierFGHeytingC 2009 Cytological analysis of interference in mouse meiosis. Methods Mol Biol 355 382
60. BorodinPMKaramyshevaTVRubtsovNB 2008 Immunofluorescent analysis of meiotic recombination and interference in the domestic cat. Tsitologiia 50 62 66
61. MatiseTCChenFChenWDe La VegaFMHansenM 2007 A second-generation combined linkage physical map of the human genome. Genome Res 17 1783 1786
62. RasmussenSHolmP 1978 Human meiosis II. Chromosome pairing and recombination nodules in human spermatocytes. Carlsberg Research Communications 43 275 327
63. BojkoM 1983 Human meiosis VIII. Chromosome pairing and formation of the synaptonemal complex in oocytes. Carlsberg Research Communications 48 457 483
64. ChelyshevaLGendrotGVezonDDoutriauxMPMercierR 2007 Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3 e83 doi:10.1371/journal.pgen.0030083
65. DaweRK 1998 Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol 49 371 395
66. GertonJLDeRisiJShroffRLichtenMBrownPO 2000 Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97 11383 11390
67. BirdsellJA 2002 Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19 1181 1197
68. MyersSSpencerCCAutonABottoloLFreemanC 2006 The distribution and causes of meiotic recombination in the human genome. Biochem Soc Trans 34 526 530
69. Eyre-WalkerA 1993 Recombination and mammalian genome evolution. Proc Biol Sci 252 237 243
70. MaraisG 2003 Biased gene conversion: implications for genome and sex evolution. Trends Genet 19 330 338
71. Marsolier-KergoatM-C 2011 A simple model for the influence of meiotic conversion tracts on GC content. PLoS One 6 e16109 doi:16110.11371/journal.pone.0016109
72. BombliesKYantLLaitinenRAKimSTHollisterJD 2010 Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet 6 e1000890 doi:1000810.1001371/journal.pgen.1000890
73. JanderGNorrisSRRounsleySDBushDFLevinIM 2002 Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129 440 450
74. BromanKWWeberJL 2000 Characterization of human crossover interference. Am J Hum Genet 66 1911 1926
75. BenjaminiYHochbergY 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc, Ser B, Methodol 57 289 300
76. RoudierFAhmedIBerardCSarazinAMary-HuardT 2011 Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30 1928 1938
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 11
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Evidence-Based Annotation of Gene Function in MR-1 Using Genome-Wide Fitness Profiling across 121 Conditions
- De Novo Origins of Human Genes
- TRY-5 Is a Sperm-Activating Protease in Seminal Fluid
- Cyclin D/CDK4 and Cyclin E/CDK2 Induce Distinct Cell Cycle Re-Entry Programs in Differentiated Muscle Cells