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Chromosome 4 Replicates in Two Phases That Correlate with Chromatin State


DNA replication programs have been studied extensively in yeast and animal systems, where they have been shown to correlate with gene expression and certain epigenetic modifications. Despite the conservation of core DNA replication proteins, little is known about replication programs in plants. We used flow cytometry and tiling microarrays to profile DNA replication of Arabidopsis thaliana chromosome 4 (chr4) during early, mid, and late S phase. Replication profiles for early and mid S phase were similar and encompassed the majority of the euchromatin. Late S phase exhibited a distinctly different profile that includes the remaining euchromatin and essentially all of the heterochromatin. Termination zones were consistent between experiments, allowing us to define 163 putative replicons on chr4 that clustered into larger domains of predominately early or late replication. Early-replicating sequences, especially the initiation zones of early replicons, displayed a pattern of epigenetic modifications specifying an open chromatin conformation. Late replicons, and the termination zones of early replicons, showed an opposite pattern. Histone H3 acetylated on lysine 56 (H3K56ac) was enriched in early replicons, as well as the initiation zones of both early and late replicons. H3K56ac was also associated with expressed genes, but this effect was local whereas replication time correlated with H3K56ac over broad regions. The similarity of the replication profiles for early and mid S phase cells indicates that replication origin activation in euchromatin is stochastic. Replicon organization in Arabidopsis is strongly influenced by epigenetic modifications to histones and DNA. The domain organization of Arabidopsis is more similar to that in Drosophila than that in mammals, which may reflect genome size and complexity. The distinct patterns of association of H3K56ac with gene expression and early replication provide evidence that H3K56ac may be associated with initiation zones and replication origins.


Vyšlo v časopise: Chromosome 4 Replicates in Two Phases That Correlate with Chromatin State. PLoS Genet 6(6): e32767. doi:10.1371/journal.pgen.1000982
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000982

Souhrn

DNA replication programs have been studied extensively in yeast and animal systems, where they have been shown to correlate with gene expression and certain epigenetic modifications. Despite the conservation of core DNA replication proteins, little is known about replication programs in plants. We used flow cytometry and tiling microarrays to profile DNA replication of Arabidopsis thaliana chromosome 4 (chr4) during early, mid, and late S phase. Replication profiles for early and mid S phase were similar and encompassed the majority of the euchromatin. Late S phase exhibited a distinctly different profile that includes the remaining euchromatin and essentially all of the heterochromatin. Termination zones were consistent between experiments, allowing us to define 163 putative replicons on chr4 that clustered into larger domains of predominately early or late replication. Early-replicating sequences, especially the initiation zones of early replicons, displayed a pattern of epigenetic modifications specifying an open chromatin conformation. Late replicons, and the termination zones of early replicons, showed an opposite pattern. Histone H3 acetylated on lysine 56 (H3K56ac) was enriched in early replicons, as well as the initiation zones of both early and late replicons. H3K56ac was also associated with expressed genes, but this effect was local whereas replication time correlated with H3K56ac over broad regions. The similarity of the replication profiles for early and mid S phase cells indicates that replication origin activation in euchromatin is stochastic. Replicon organization in Arabidopsis is strongly influenced by epigenetic modifications to histones and DNA. The domain organization of Arabidopsis is more similar to that in Drosophila than that in mammals, which may reflect genome size and complexity. The distinct patterns of association of H3K56ac with gene expression and early replication provide evidence that H3K56ac may be associated with initiation zones and replication origins.


Zdroje

1. BerezneyR

DubeyDD

HubermanJA

2000 Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108 471 484

2. GilbertDM

2004 In search of the holy replicator. Nat Rev Mol Cell Biol 5 848 855

3. AladjemMI

2007 Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8 588 600

4. HamlinJL

MesnerLD

LarO

TorresR

ChodaparambilSV

2008 A revisionist replicon model for higher eukaryotic genomes. J Cell Biochem 105 321 329

5. GondorA

OhlssonR

2009 Replication timing and epigenetic reprogramming of gene expression: a two-way relationship? Nat Rev Genet 10 269 276

6. RaghuramanMK

WinzelerEA

CollingwoodD

HuntS

WodickaL

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

7. MacAlpineDM

RodriguezHK

BellSP

2004 Coordination of replication and transcription along a Drosophila chromosome. Genes Dev 18 3094 3105

8. SchubelerD

ScalzoD

KooperbergC

van SteenselB

DelrowJ

2002 Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32 438 442

9. WhiteEJ

EmanuelssonO

ScalzoD

RoyceT

KosakS

2004 DNA replication-timing analysis of human chromosome 22 at high resolution and different developmental states. Proc Natl Acad Sci U S A 101 17771 17776

10. WoodfineK

FieglerH

BeareDM

CollinsJE

McCannOT

2004 Replication timing of the human genome. Hum Mol Genet 13 191 202

11. JeonY

BekiranovS

KarnaniN

KapranovP

GhoshS

2005 Temporal profile of replication of human chromosomes. Proc Natl Acad Sci U S A 102 6419 6424

12. KarnaniN

TaylorC

MalhotraA

DuttaA

2007 Pan-S replication patterns and chromosomal domains defined by genome-tiling arrays of ENCODE genomic areas. Genome Res 17 865 876

13. HirataniI

RybaT

ItohM

YokochiT

SchwaigerM

2008 Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6 e245 doi:10.1371/journal.pbio.0060245

14. SchwaigerM

StadlerMB

BellO

KohlerH

OakeleyEJ

2009 Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev 23 589 601

15. CzajkowskyDM

LiuJ

HamlinJL

ShaoZ

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

16. PatelPK

ArcangioliB

BakerSP

BensimonA

RhindN

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

17. RhindN

2006 DNA replication timing: random thoughts about origin firing. Nat Cell Biol 8 1313 1316

18. LygerosJ

KoutroumpasK

DimopoulosS

LegourasI

KouretasP

2008 Stochastic hybrid modeling of DNA replication across a complete genome. Proc Natl Acad Sci U S A 105 12295 12300

19. GoldarA

LabitH

MarheinekeK

HyrienO

2008 A dynamic stochastic model for DNA replication initiation in early embryos. PLoS ONE 3 e2919 doi:10.1371/journal.pone.0002919

20. GoldarA

Marsolier-KergoatMC

HyrienO

2009 Universal temporal profile of replication origin activation in eukaryotes. PLoS ONE 4 e5899 doi:10.1371/journal.pone.0005899

21. HirataniI

TakebayashiS

LuJ

GilbertDM

2009 Replication timing and transcriptional control: beyond cause and effect—part II. Curr Opin Genet Dev 19 142 149

22. Farkash-AmarS

LipsonD

PoltenA

GorenA

HelmstetterC

2008 Global organization of replication time zones of the mouse genome. Genome Res 18 1562 1570

23. DespratR

Thierry-MiegD

LaillerN

LajugieJ

SchildkrautC

2009 Predictable dynamic program of timing of DNA replication in human cells. Genome Res 19 2288 2299

24. DonaldsonAD

2005 Shaping time: chromatin structure and the DNA replication programme. Trends Genet 21 444 449

25. Lima-de-FariaA

JaworskaH

1968 Late DNA synthesis in heterochromatin. Nature 217 138 142

26. KimSM

DubeyDD

HubermanJA

2003 Early-replicating heterochromatin. Genes Dev 17 330 335

27. CedarH

BergmanY

2009 Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10 295 304

28. FranszP

ten HoopenR

TessadoriF

2006 Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14 71 82

29. HendersonIR

JacobsenSE

2007 Epigenetic inheritance in plants. Nature 447 418 424

30. BarskiA

CuddapahS

CuiK

RohTY

SchonesDE

2007 High-resolution profiling of histone methylations in the human genome. Cell 129 823 837

31. LippmanZ

GendrelAV

BlackM

VaughnMW

DedhiaN

2004 Role of transposable elements in heterochromatin and epigenetic control. Nature 430 471 476

32. MikkelsenTS

KuM

JaffeDB

IssacB

LiebermanE

2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 553 560

33. VaughnMW

TanurdzicM

LippmanZ

JiangH

CarrasquilloR

2007 Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol 5 e174 doi:10.1371/journal.pbio.0050174

34. TanurdzicM

VaughnMW

JiangH

LeeTJ

SlotkinRK

2008 Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6 e302 doi:10.1371/journal.pbio.0060302

35. BirneyE

StamatoyannopoulosJA

DuttaA

GuigoR

GingerasTR

2007 Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 799 816

36. SchubelerD

MacAlpineDM

ScalzoD

WirbelauerC

KooperbergC

2004 The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18 1263 1271

37. ZhangX

BernatavichuteYV

CokusS

PellegriniM

JacobsenSE

2009 Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 R62

38. ZhangX

YazakiJ

SundaresanA

CokusS

ChanSW

2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126 1189 1201

39. GorenA

TabibA

HechtM

CedarH

2008 DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. Genes Dev 22 1319 1324

40. KaplanT

LiuCL

ErkmannJA

HolikJ

GrunsteinM

2008 Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4 e1000270 doi:10.1371/journal.pgen.1000270

41. KnottSR

ViggianiCJ

TavareS

AparicioOM

2009 Genome-wide replication profiles indicate an expansive role for Rpd3L in regulating replication initiation timing or efficiency, and reveal genomic loci of Rpd3 function in Saccharomyces cerevisiae. Genes Dev 23 1077 1090

42. JorgensenHF

AzuaraV

AmoilsS

SpivakovM

TerryA

2007 The impact of chromatin modifiers on the timing of locus replication in mouse embryonic stem cells. Genome Biol 8 R169

43. Lande-DinerL

ZhangJ

CedarH

2009 Shifts in replication timing actively affect histone acetylation during nucleosome reassembly. Mol Cell 34 767 774

44. FalboKB

ShenX

2009 Histone modifications during DNA replication. Mol Cells 28 149 154

45. Vant' HofJ

1996 DNA replication in plants.

DePamphilisML

DNA replication in eukaryotic cells New York Cold Spring Harbor Laboratory Press 1005 1014

46. ShultzRW

LeeTJ

AllenGC

ThompsonWF

Hanley-BowdoinL

2009 Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants. Plant Physiol 150 658 669

47. ShultzRW

TatineniVM

Hanley-BowdoinL

ThompsonWF

2007 Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol 144 1697 1714

48. Vant' HofJ

KuniyukiA

BjerknesCA

1978 Size and number of replicon families of chromosomal DNA of Arabidopsis thaliana. Chromosoma 68 269 285

49. MartienssenRA

KlocA

SlotkinRK

TanurdzicM

2008 Epigenetic inheritance and reprogramming in plants and fission yeast. Cold Spring Harb Symp Quant Biol 73 265 271

50. FinneganEJ

DennisES

2007 Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17 1978 1983

51. FinneganEJ

KovacKA

2000 Plant DNA methyltransferases. Plant Mol Biol 43 189 201

52. PandeyR

MullerA

NapoliCA

SelingerDA

PikaardCS

2002 Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30 5036 5055

53. SpringerNM

NapoliCA

SelingerDA

PandeyR

ConeKC

2003 Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132 907 925

54. The Arabidopsis Genome Initiative 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796 815

55. LanderES

LintonLM

BirrenB

NusbaumC

ZodyMC

2001 Initial sequencing and analysis of the human genome. Nature 409 860 921

56. WaterstonRH

Lindblad-TohK

BirneyE

RogersJ

AbrilJF

2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420 520 562

57. AdamsMD

CelnikerSE

HoltRA

EvansCA

GocayneJD

2000 The genome sequence of Drosophila melanogaster. Science 287 2185 2195

58. MayerK

SchullerC

WambuttR

MurphyG

VolckaertG

1999 Sequence and analysis of chromosome 4 of the plant Arabidopsis thaliana. Nature 402 769 777

59. FranszP

De JongJH

LysakM

CastiglioneMR

SchubertI

2002 Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci U S A 99 14584 14589

60. HansenRS

ThomasS

SandstromR

CanfieldTK

ThurmanRE

2009 Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc Natl Acad Sci U S A

61. SwarbreckD

WilksC

LameschP

BerardiniTZ

Garcia-HernandezM

2008 The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36 D1009 1014

62. CostantiniM

BernardiG

2008 Replication timing, chromosomal bands, and isochores. Proc Natl Acad Sci U S A 105 3433 3437

63. ZilbermanD

GehringM

TranRK

BallingerT

HenikoffS

2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39 61 69

64. GendrelAV

LippmanZ

YordanC

ColotV

MartienssenRA

2002 Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297 1871 1873

65. TrojerP

ReinbergD

2007 Facultative heterochromatin: is there a distinctive molecular signature? Mol Cell 28 1 13

66. XuF

ZhangK

GrunsteinM

2005 Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121 375 385

67. DasC

LuciaMS

HansenKC

TylerJK

2009 CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459 113 117

68. LiQ

ZhouH

WurteleH

DaviesB

HorazdovskyB

2008 Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134 244 255

69. MasumotoH

HawkeD

KobayashiR

VerreaultA

2005 A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 294 298

70. RufiangeA

JacquesPE

BhatW

RobertF

NouraniA

2007 Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27 393 405

71. WilliamsSK

TruongD

TylerJK

2008 Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A 105 9000 9005

72. HubbellE

LiuWM

MeiR

2002 Robust estimators for expression analysis. Bioinformatics 18 1585 1592

73. GautierL

CopeL

BolstadBM

IrizarryRA

2004 affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 307 315

74. XieW

SongC

YoungNL

SperlingAS

XuF

2009 Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell 33 417 427

75. WoodfineK

BeareDM

IchimuraK

DebernardiS

MungallAJ

2005 Replication timing of human chromosome 6. Cell Cycle 4 172 176

76. BernardiG

2000 Isochores and the evolutionary genomics of vertebrates. Gene 241 3 17

77. OliverJL

Bernaola-GalvanP

CarpenaP

Roman-RoldanR

2001 Isochore chromosome maps of eukaryotic genomes. Gene 276 47 56

78. ZhangR

ZhangCT

2004 Isochore structures in the genome of the plant Arabidopsis thaliana. J Mol Evol 59 227 238

79. FriedmanKL

BrewerBJ

FangmanWL

1997 Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2 667 678

80. CollinsN

PootRA

KukimotoI

Garcia-JimenezC

DellaireG

2002 An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet 32 627 632

81. FalboKB

ShenX

2006 Chromatin remodeling in DNA replication. J Cell Biochem 97 684 689

82. QuivyJP

GerardA

CookAJ

RocheD

AlmouzniG

2008 The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat Struct Mol Biol 15 972 979

83. VincentJA

KwongTJ

TsukiyamaT

2008 ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat Struct Mol Biol 15 477 484

84. TakebayashiS

SugimuraK

SaitoT

SatoC

FukushimaY

2005 Regulation of replication at the R/G chromosomal band boundary and pericentromeric heterochromatin of mammalian cells. Exp Cell Res 304 162 174

85. WuR

SinghPB

GilbertDM

2006 Uncoupling global and fine-tuning replication timing determinants for mouse pericentric heterochromatin. J Cell Biol 174 185 194

86. VasheeS

CveticC

LuW

SimancekP

KellyTJ

2003 Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev 17 1894 1908

87. StanojcicS

LemaitreJM

BrodolinK

DanisE

MechaliM

2008 In Xenopus egg extracts, DNA replication initiates preferentially at or near asymmetric AT sequences. Mol Cell Biol 28 5265 5274

88. SahaS

ShanY

MesnerLD

HamlinJL

2004 The promoter of the Chinese hamster ovary dihydrofolate reductase gene regulates the activity of the local origin and helps define its boundaries. Genes Dev 18 397 410

89. HarveyKJ

NewportJ

2003 CpG methylation of DNA restricts prereplication complex assembly in Xenopus egg extracts. Mol Cell Biol 23 6769 6779

90. LorinczMC

DickersonDR

SchmittM

GroudineM

2004 Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol 11 1068 1075

91. HanJ

ZhouH

HorazdovskyB

ZhangK

XuRM

2007 Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315 653 655

92. HanJ

ZhouH

LiZ

XuRM

ZhangZ

2007 The Rtt109-Vps75 histone acetyltransferase complex acetylates non-nucleosomal histone H3. J Biol Chem 282 14158 14164

93. DolbeareF

GratznerH

PallaviciniMG

GrayJW

1983 Flow Cytometric Measurement of Total DNA Content and Incorporated Bromodeoxyuridine. Proc Natl Acad Sci U S A 80 5573 5577

94. GendrelAV

LippmanZ

MartienssenR

ColotV

2005 Profiling histone modification patterns in plants using genomic tiling microarrays. Nature Methods 2 213 218

95. LippmanZ

GendrelAV

ColotV

MartienssenR

2005 Profiling DNA methylation patterns using genomic tiling microarrays. Nat Methods 2 219 224

96. Team RDC 2009 R: A language and environment for statistical computing. Vienna R Foundation for Statistical Computing

97. SmythGK

SpeedT

2003 Normalization of cDNA microarray data. Methods 31 265 273

98. SmythGK

2005 Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York Springer 397 420

99. GentlemanRC

CareyVJ

BatesDM

BolstadB

DettlingM

2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 R80

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