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Stress-Induced Activation of Heterochromatic Transcription


Constitutive heterochromatin comprising the centromeric and telomeric parts of chromosomes includes DNA marked by high levels of methylation associated with histones modified by repressive marks. These epigenetic modifications silence transcription and ensure stable inheritance of this inert state. Although environmental cues can alter epigenetic marks and lead to modulation of the transcription of genes located in euchromatic parts of the chromosomes, there is no evidence that external stimuli can globally destabilize silencing of constitutive heterochromatin. We have found that heterochromatin-associated silencing in Arabidopsis plants subjected to a particular temperature regime is released in a genome-wide manner. This occurs without alteration of repressive epigenetic modifications and does not involve common epigenetic mechanisms. Such induced release of silencing is mostly transient, and rapid restoration of the silent state occurs without the involvement of factors known to be required for silencing initiation. Thus, our results reveal new regulatory aspects of transcriptional repression in constitutive heterochromatin and open up possibilities to identify the molecular mechanisms involved.


Vyšlo v časopise: Stress-Induced Activation of Heterochromatic Transcription. PLoS Genet 6(10): e32767. doi:10.1371/journal.pgen.1001175
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001175

Souhrn

Constitutive heterochromatin comprising the centromeric and telomeric parts of chromosomes includes DNA marked by high levels of methylation associated with histones modified by repressive marks. These epigenetic modifications silence transcription and ensure stable inheritance of this inert state. Although environmental cues can alter epigenetic marks and lead to modulation of the transcription of genes located in euchromatic parts of the chromosomes, there is no evidence that external stimuli can globally destabilize silencing of constitutive heterochromatin. We have found that heterochromatin-associated silencing in Arabidopsis plants subjected to a particular temperature regime is released in a genome-wide manner. This occurs without alteration of repressive epigenetic modifications and does not involve common epigenetic mechanisms. Such induced release of silencing is mostly transient, and rapid restoration of the silent state occurs without the involvement of factors known to be required for silencing initiation. Thus, our results reveal new regulatory aspects of transcriptional repression in constitutive heterochromatin and open up possibilities to identify the molecular mechanisms involved.


Zdroje

1. HeitzE

1928 Das Heterochromatin der Moose. Jahrb Wiss Botanik 69 762 818

2. LanderES

LintonLM

BirrenB

NusbaumC

ZodyMC

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

3. LiR

FanW

TianG

ZhuH

HeL

2010 The sequence and de novo assembly of the giant panda genome. Nature 463 311 317

4. The Chimpanzee Sequencing and Analysis Consortium 2005 Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437 69 87

5. BaucomRS

EstillJC

ChaparroC

UpshawN

JogiA

2009 Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5 e1000732 doi:10.1371/journal.pgen.1000732

6. SchnablePS

WareD

FultonRS

SteinJC

WeiF

2009 The B73 maize genome: complexity, diversity, and dynamics. Science 326 1112 1115

7. DernburgAF

SedatJW

HawleyRS

1996 Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86 135 146

8. BernardP

MaureJF

PartridgeJF

GenierS

JaverzatJP

2001 Requirement of heterochromatin for cohesion at centromeres. Science 294 2539 2542

9. de LangeT

2005 Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19 2100 2110

10. SlotkinRK

MartienssenR

2007 Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8 272 285

11. RoudierF

TeixeiraFK

ColotV

2009 Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25 511 517

12. VaillantI

PaszkowskiJ

2007 Role of histone and DNA methylation in gene regulation. Curr Opin Plant Biol 10 528 533

13. CheongYH

ChangHS

GuptaR

WangX

ZhuT

2002 Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129 661 677

14. KrepsJA

WuY

ChangHS

ZhuT

WangX

2002 Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130 2129 2141

15. MahalingamR

Gomez-BuitragoA

EckardtN

ShahN

Guevara-GarciaA

2003 Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4 R20

16. MatsuiA

IshidaJ

MorosawaT

MochizukiY

KaminumaE

2008 Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49 1135 1149

17. ShinozakiK

Yamaguchi-ShinozakiK

SekiM

2003 Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6 410 417

18. ZellerG

HenzSR

WidmerCK

SachsenbergT

RatschG

2009 Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58 1068 1082

19. ChinnusamyV

ZhuJK

2009 Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12 133 139

20. SunkarR

ZhuJK

2004 Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16 2001 2019

21. BorsaniO

ZhuJ

VersluesPE

SunkarR

ZhuJK

2005 Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123 1279 1291

22. SunkarR

ChinnusamyV

ZhuJ

ZhuJK

2007 Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12 301 309

23. DingSW

VoinnetO

2007 Antiviral immunity directed by small RNAs. Cell 130 413 426

24. ShuklaLI

ChinnusamyV

SunkarR

2008 The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779 743 748

25. JinH

2008 Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 582 2679 2684

26. Lang-MladekC

PopovaO

KiokK

BerlingerM

RakicB

2010 Transgenerational Inheritance and Resetting of Stress-Induced Loss of Epigenetic Gene Silencing in Arabidopsis. Mol Plant

27. MayBP

LippmanZB

FangY

SpectorDL

MartienssenRA

2005 Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1 e79 doi:10.1371/journal.pgen.0010079

28. NumaH

KimJM

MatsuiA

KuriharaY

MorosawaT

2010 Transduction of RNA-directed DNA methylation signals to repressive histone marks in Arabidopsis thaliana. EMBO J 29 352 362

29. VaillantI

SchubertI

TourmenteS

MathieuO

2006 MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis. EMBO Rep 7 1273 1278

30. YokthongwattanaC

BucherE

CaikovskiM

VaillantI

NicoletJ

2010 MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J 29 340 351

31. ZhangX

YazakiJ

SundaresanA

CokusS

ChanSW

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

32. MathieuO

ReindersJ

CaikovskiM

SmathajittC

PaszkowskiJ

2007 Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130 851 862

33. Mittelsten ScheidO

ProbstAV

AfsarK

PaszkowskiJ

2002 Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc Natl Acad Sci U S A 99 13659 13662

34. ProbstAV

FranszPF

PaszkowskiJ

Mittelsten ScheidO

2003 Two means of transcriptional reactivation within heterochromatin. Plant J 33 743 749

35. MirouzeM

ReindersJ

BucherE

NishimuraT

SchneebergerK

2009 Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461 427 430

36. TsukaharaS

KobayashiA

KawabeA

MathieuO

MiuraA

2009 Bursts of retrotransposition reproduced in Arabidopsis. Nature 461 423 426

37. KatoM

MiuraA

BenderJ

JacobsenSE

KakutaniT

2003 Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13 421 426

38. ReindersJ

WulffBB

MirouzeM

Mari-OrdonezA

DappM

2009 Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23 939 950

39. HirochikaH

OkamotoH

KakutaniT

2000 Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12 357 369

40. MiuraA

YonebayashiS

WatanabeK

ToyamaT

ShimadaH

2001 Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411 212 214

41. KankelMW

RamseyDE

StokesTL

FlowersSK

HaagJR

2003 Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163 1109 1122

42. JeddelohJA

StokesTL

RichardsEJ

1999 Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22 94 97

43. SazeH

Mittelsten ScheidO

PaszkowskiJ

2003 Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34 65 69

44. MorelJB

MourrainP

BeclinC

VaucheretH

2000 DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10 1591 1594

45. ElmayanT

ProuxF

VaucheretH

2005 Arabidopsis RPA2: a genetic link among transcriptional gene silencing, DNA repair, and DNA replication. Curr Biol 15 1919 1925

46. AmedeoP

HabuY

AfsarK

Mittelsten ScheidO

PaszkowskiJ

2000 Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405 203 206

47. ProbstAV

FagardM

ProuxF

MourrainP

BoutetS

2004 Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16 1021 1034

48. TakedaS

TadeleZ

HofmannI

ProbstAV

AngelisKJ

2004 BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev 18 782 793

49. BurnJE

BagnallDJ

MetzgerJD

DennisES

PeacockWJ

1993 DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci U S A 90 287 291

50. DennisES

PeacockWJ

2007 Epigenetic regulation of flowering. Curr Opin Plant Biol 10 520 527

51. BastowR

MylneJS

ListerC

LippmanZ

MartienssenRA

2004 Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427 164 167

52. SungS

AmasinoRM

2004 Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427 159 164

53. JeffersonRA

KavanaghTA

BevanMW

1987 GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6 3901 3907

54. HabuY

MathieuO

TariqM

ProbstAV

SmathajittC

2006 Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep 7 1279 1284

55. JacksonJP

LindrothAM

CaoX

JacobsenSE

2002 Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416 556 560

56. LindrothAM

CaoX

JacksonJP

ZilbermanD

McCallumCM

2001 Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292 2077 2080

57. MathieuO

ProbstAV

PaszkowskiJ

2005 Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24 2783 2791

58. SteimerA

AmedeoP

AfsarK

FranszP

Mittelsten ScheidO

2000 Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12 1165 1178

59. KimJM

ToTK

IshidaJ

MorosawaT

KawashimaM

2008 Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49 1580 1588

60. GendrelAV

LippmanZ

YordanC

ColotV

MartienssenRA

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

61. VongsA

KakutaniT

MartienssenRA

RichardsEJ

1993 Arabidopsis thaliana DNA methylation mutants. Science 260 1926 1928

62. AufsatzW

MetteMF

van der WindenJ

MatzkeM

MatzkeAJ

2002 HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21 6832 6841

63. LippmanZ

MayB

YordanC

SingerT

MartienssenR

2003 Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1 e67 doi:10.1371/journal.pbio.0000067

64. MurfettJ

WangXJ

HagenG

GuilfoyleTJ

2001 Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13 1047 1061

65. EarleyK

LawrenceRJ

PontesO

ReutherR

EncisoAJ

2006 Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20 1283 1293

66. LinX

KaulS

RounsleyS

SheaTP

BenitoMI

1999 Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402 761 768

67. MeyerP

LinnF

HeidmannI

MeyerH

NiedenhofI

1992 Endogenous and environmental factors influence 35S promoter methylation of a maize A1 gene construct in transgenic petunia and its colour phenotype. Mol Gen Genet 231 345 352

68. TanurdzicM

VaughnMW

JiangH

LeeTJ

SlotkinRK

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

69. GowenJW

GayEH

1933 Effect of Temperature on Eversporting Eye Color in Drosophila Melanogaster. Science 77 312

70. AllshireRC

JaverzatJP

RedheadNJ

CranstonG

1994 Position effect variegation at fission yeast centromeres. Cell 76 157 169

71. KlocA

ZaratieguiM

NoraE

MartienssenR

2008 RNA interference guides histone modification during the S phase of chromosomal replication. Curr Biol 18 490 495

72. VolpeTA

KidnerC

HallIM

TengG

GrewalSI

2002 Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297 1833 1837

73. FagegaltierD

BougeAL

BerryB

PoisotE

SismeiroO

2009 The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. Proc Natl Acad Sci U S A 106 21258 21263

74. TariqM

SazeH

ProbstAV

LichotaJ

HabuY

2003 Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci U S A 100 8823 8827

75. XieZ

JohansenLK

GustafsonAM

KasschauKD

LellisAD

2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2 e104 doi:10.1371/journal.pbio.0020104

76. KumarSV

WiggePA

2010 H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140 136 147

77. ZilbermanD

Coleman-DerrD

BallingerT

HenikoffS

2008 Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456 125 129

78. KilianJ

WhiteheadD

HorakJ

WankeD

WeinlS

2007 The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50 347 363

79. BrowseJ

XinZ

2001 Temperature sensing and cold acclimation. Curr Opin Plant Biol 4 241 246

80. ChinnusamyV

ZhuJ

ZhuJK

2007 Cold stress regulation of gene expression in plants. Trends Plant Sci 12 444 451

81. BurkeJJ

O'MahonyPJ

OliverMJ

2000 Isolation of Arabidopsis mutants lacking components of acquired thermotolerance. Plant Physiol 123 575 588

82. LimCJ

YangKA

HongJK

ChoiJS

YunDJ

2006 Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. J Plant Res 119 373 383

83. HashidaSN

KitamuraK

MikamiT

KishimaY

2003 Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol 132 1207 1216

84. HashidaSN

UchiyamaT

MartinC

KishimaY

SanoY

2006 The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell 18 104 118

85. Mittelsten ScheidO

AfsarK

PaszkowskiJ

1998 Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc Natl Acad Sci U S A 95 632 637

86. ZilbermanD

CaoX

JacobsenSE

2003 ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299 716 719

87. ChanSW

HendersonIR

ZhangX

ShahG

ChienJS

2006 RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in arabidopsis. PLoS Genet 2 e83 doi:10.1371/journal.pgen.0020083

88. OnoderaY

HaagJR

ReamT

NunesPC

PontesO

2005 Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120 613 622

89. KannoT

BucherE

DaxingerL

HuettelB

BohmdorferG

2008 A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40 670 675

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