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Separation of DNA Replication from the Assembly of Break-Competent Meiotic Chromosomes


The meiotic cell division reduces the chromosome number from diploid to haploid to form gametes for sexual reproduction. Although much progress has been made in understanding meiotic recombination and the two meiotic divisions, the processes leading up to recombination, including the prolonged pre-meiotic S phase (meiS) and the assembly of meiotic chromosome axes, remain poorly defined. We have used genome-wide approaches in Saccharomyces cerevisiae to measure the kinetics of pre-meiotic DNA replication and to investigate the interdependencies between replication and axis formation. We found that replication initiation was delayed for a large number of origins in meiS compared to mitosis and that meiotic cells were far more sensitive to replication inhibition, most likely due to the starvation conditions required for meiotic induction. Moreover, replication initiation was delayed even in the absence of chromosome axes, indicating replication timing is independent of the process of axis assembly. Finally, we found that cells were able to install axis components and initiate recombination on unreplicated DNA. Thus, although pre-meiotic DNA replication and meiotic chromosome axis formation occur concurrently, they are not strictly coupled. The functional separation of these processes reveals a modular method of building meiotic chromosomes and predicts that any crosstalk between these modules must occur through superimposed regulatory mechanisms.


Vyšlo v časopise: Separation of DNA Replication from the Assembly of Break-Competent Meiotic Chromosomes. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002643
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002643

Souhrn

The meiotic cell division reduces the chromosome number from diploid to haploid to form gametes for sexual reproduction. Although much progress has been made in understanding meiotic recombination and the two meiotic divisions, the processes leading up to recombination, including the prolonged pre-meiotic S phase (meiS) and the assembly of meiotic chromosome axes, remain poorly defined. We have used genome-wide approaches in Saccharomyces cerevisiae to measure the kinetics of pre-meiotic DNA replication and to investigate the interdependencies between replication and axis formation. We found that replication initiation was delayed for a large number of origins in meiS compared to mitosis and that meiotic cells were far more sensitive to replication inhibition, most likely due to the starvation conditions required for meiotic induction. Moreover, replication initiation was delayed even in the absence of chromosome axes, indicating replication timing is independent of the process of axis assembly. Finally, we found that cells were able to install axis components and initiate recombination on unreplicated DNA. Thus, although pre-meiotic DNA replication and meiotic chromosome axis formation occur concurrently, they are not strictly coupled. The functional separation of these processes reveals a modular method of building meiotic chromosomes and predicts that any crosstalk between these modules must occur through superimposed regulatory mechanisms.


Zdroje

1. MoensPBPearlmanRE 1988 Chromatin organization at meiosis. Bioessays 9 151 153

2. ZicklerDKlecknerN 1999 Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33 603 754

3. WilliamsonDHJohnstonLHFennellDJSimchenG 1983 The timing of the S phase and other nuclear events in yeast meiosis. Exp Cell Res 145 209 217

4. PadmoreRCaoLKlecknerN 1991 Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66 1239 1256

5. HerrickJ 2010 The dynamic replicon: adapting to a changing cellular environment. Bioessays 32 153 164

6. StillmanB 2005 Origin recognition and the chromosome cycle. FEBS Lett 579 877 884

7. WyrickJJAparicioJGChenTBarnettJDJenningsEG 2001 Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294 2357 2360

8. RaghuramanMKWinzelerEACollingwoodDHuntSWodickaL 2001 Replication dynamics of the yeast genome. Science 294 115 121

9. YabukiNTerashimaHKitadaK 2002 Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 7 781 789

10. PatelPKArcangioliBBakerSPBensimonARhindN 2006 DNA replication origins fire stochastically in fission yeast. Mol Biol Cell 17 308 316

11. CzajkowskyDMLiuJHamlinJLShaoZ 2008 DNA combing reveals intrinsic temporal disorder in the replication of yeast chromosome VI. J Mol Biol 375 12 19

12. ChaRSWeinerBMKeeneySDekkerJKlecknerN 2000 Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev 14 493 503

13. CollinsINewlonCS 1994 Chromosomal DNA replication initiates at the same origins in meiosis and mitosis. Mol Cell Biol 14 3524 3534

14. MoriSShirahigeK 2007 Perturbation of the activity of replication origin by meiosis-specific transcription. J Biol Chem 282 4447 4452

15. HeichingerCPenkettCJBahlerJNurseP 2006 Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25 5171 5179

16. KleinFMahrPGalovaMBuonomoSBCMichaelisC 1999 A Central Role for Cohesins in Sister Chromatid Cohesion, Formation of Axial Elements and Recombination during Yeast Meiosis. Cell 98 91 103

17. PanizzaSMendozaMABerlingerMHuangLNicolasA 2011 Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146 372 383

18. Mao-DraayerYGalbraithAMPittmanDLCoolMMaloneRE 1996 Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics 144 71 86

19. KugouKFukudaTYamadaSItoMSasanumaH 2009 Rec8 guides canonical Spo11 distribution along yeast meiotic chromosomes. Mol Biol Cell 20 3064 3076

20. BordeVGoldmanASHLichtenM 2000 Direct Coupling Between Meiotic DNA Replication and Recombination Initiation. Science 290 806 809

21. SnyderMSapolskyRJDavisRW 1988 Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae. Mol Cell Biol 8 2184 2194

22. BenjaminKRZhangCShokatKMHerskowitzI 2003 Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17 1524 1539

23. DirickLGoetschLAmmererGByersB 1998 Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae. Science 281 1854 1857

24. BrewerBJChlebowicz-SledziewskaEFangmanWL 1984 Cell cycle phases in the unequal mother/daughter cell cycles of Saccharomyces cerevisiae. Mol Cell Biol 4 2529 2531

25. KorenASoiferIBarkaiN 2010 MRC1-dependent scaling of the budding yeast DNA replication timing program. Genome Res 20 781 790

26. HyrienOMarheinekeKGoldarA 2003 Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. Bioessays 25 116 125

27. AlvinoGMCollingwoodDMurphyJMDelrowJBrewerBJ 2007 Replication in Hydroxyurea: It's a matter of time. Mol Cell Biol

28. LambTMMitchellAP 2001 Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3. Genetics 157 545 556

29. ZhaoXMullerEGRothsteinR 1998 A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 2 329 340

30. GranovskaiaMVJensenLJRitchieMEToedlingJNingY 2010 High-resolution transcription atlas of the mitotic cell cycle in budding yeast. Genome Biol 11 R24

31. BordeVRobineNLinWBonfilsSGeliV 2009 Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28 99 111

32. LardenoisALiuYWaltherTChalmelFEvrardB 2011 Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proc Natl Acad Sci U S A 108 1058 1063

33. MacAlpineDMBellSP 2005 A genomic view of eukaryotic DNA replication. Chromosome Res 13 309 326

34. KorenATsaiHJTiroshIBurrackLSBarkaiN 2010 Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6 e1001068 doi:10.1371/journal.pgen.1001068

35. PanJSasakiMKniewelRMurakamiHBlitzblauHG 2011 A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144 719 731

36. BlitzblauHGBellGWRodriguezJBellSPHochwagenA 2007 Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Curr Biol 17 2003 2012

37. StuartDWittenbergC 1998 CLB5 and CLB6 Are Required for Premeiotic DNA Replication and Activation of the Meiotic S/M Checkpoint. Genes Dev 12 2698 2710

38. LinWWangMJinHYuHG 2011 Cohesin plays a dual role in gene regulation and sister-chromatid cohesion during meiosis in Saccharomyces cerevisiae. Genetics 187 1041 1051

39. BrarGAHochwagenAEeLSAmonA 2009 The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 20 1030 1047

40. BlatYProtacioRUHunterNKlecknerN 2002 Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111 791 802

41. GlynnEFMegeePCYuHGMistrotCUnalE 2004 Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2 e259 doi:10.1371/journal.pbio.0020259

42. TanakaSHalterDLivingstone-ZatchejMReszelBThomaF 1994 Transcription through the yeast origin of replication ARS1 ends at the ABFI binding site and affects extrachromosomal maintenance of minichromosomes. Nucleic Acids Res 22 3904 3910

43. MantieroDMackenzieADonaldsonAZegermanP 2011 Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30 4805 4814

44. TanakaSArakiH Multiple regulatory mechanisms to inhibit untimely initiation of DNA replication are important for stable genome maintenance. PLoS Genet 7 e1002136 doi:10.1371/journal.pgen.1002136

45. DonaldsonADRaghuramanMKFriedmanKLCrossFRBrewerBJ 1998 CLB5-dependent activation of late replication origins in S. cerevisiae. Mol Cell 2 173 182

46. McCuneHJDanielsonLSAlvinoGMCollingwoodDDelrowJJ 2008 The temporal program of chromosome replication: genomewide replication in clb5{Delta} Saccharomyces cerevisiae. Genetics 180 1833 1847

47. WanLZhangCShokatKMHollingsworthNM 2006 Chemical inactivation of cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination. Genetics 174 1767 1774

48. BoussetKDiffleyJF 1998 The Cdc7 protein kinase is required for origin firing during S phase. Genes Dev 12 480 490

49. DonaldsonADFangmanWLBrewerBJ 1998 Cdc7 is required throughout the yeast S phase to activate replication origins. Genes Dev 12 491 501

50. SandoNMiyakeS 1971 Biochemical changes in yeast during sporulation. I. Fate of nucleic acids and related compounds. Dev Growth Differ 12 273 283

51. PohlTJBrewerBJRaghuramanMK 2012 Functional centromeres determine the activation time of pericentric origins of DNA replication in Saccharomyces cerevisiae. PLoS Genet 8 e1002677 doi:10.1371/journal.pgen.1002677

52. FengWBachantJCollingwoodDRaghuramanMKBrewerBJ 2009 Centromere replication timing determines different forms of genomic instability in Saccharomyces cerevisiae checkpoint mutants during replication stress. Genetics 183 1249 1260

53. UhlmannFNasmythK 1998 Cohesion between Sister Chromatids Must Be Established during DNA Replication. Curr Biol 8 1095 1101

54. HochwagenAThamWHBrarGAAmonA 2005 The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122 861 873

55. MurakamiHBordeVShibataTLichtenMOhtaK 2003 Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites. Nucleic Acids Res 31 4085 4090

56. Lopez-MosquedaJMaasNLJonssonZODefazio-EliLGWohlschlegelJ 2010 Damage-induced phosphorylation of Sld3 is important to block late origin firing. Nature 467 479 483

57. ZegermanPDiffleyJF 2010 Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature 467 474 478

58. MurakamiHNurseP 2001 Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast. Nat Genet 28 290 293

59. TonamiYMurakamiHShirahigeKNakanishiM 2005 A checkpoint control linking meiotic S phase and recombination initiation in fission yeast. Proc Natl Acad Sci U S A 102 5797 5801

60. LongtineMSMcKenzieA3rdDemariniDJShahNGWachA 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 953 961

61. AparicioOMWeinsteinDMBellSP 1997 Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 91 59 69

62. YangYHDudoitSLuuPSpeedTP Normalization of cDNA microarray data.; 2001; San Jose, CA

63. EatonMLGalaniKKangSBellSPMacAlpineDM 2010 Conserved nucleosome positioning defines replication origins. Genes Dev 24 748 753

64. PrimigMWilliamsRMWinzelerEATevzadzeGGConwayAR 2000 The Core Meiotic Transcriptome in Budding Yeasts. Nat Genet 26 415 423

65. FriedlanderGJoseph-StraussDCarmiMZenvirthDSimchenG 2006 Modulation of the transcription regulatory program in yeast cells committed to sporulation. Genome Biol 7 R20

66. FalkJEChanACHoffmannEHochwagenA 2010 A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19 599 611

67. VaderGBlitzblauHGTameMAFalkJECurtinL 2011 Protection of repetitive DNA borders from self-induced meiotic instability. Nature 477 115 119

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