Dynamic Deposition of Histone Variant H3.3 Accompanies Developmental Remodeling of the Transcriptome

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In animals, replication-coupled histone H3.1 can be distinguished from replication-independent histone H3.3. H3.3 variants are enriched at active genes and their promoters. Furthermore, H3.3 is specifically incorporated upon gene activation. Histone H3 variants evolved independently in plants and animals, and it is unclear whether different replication-independent H3.3 variants developed similar properties in both phyla. We studied Arabidopsis H3 variants in order to find core properties of this class of histones. Here we present genome-wide maps of H3.3 and H3.1 enrichment and the dynamic changes of their profiles upon cell division arrest. We find H3.3 enrichment to positively correlate with gene expression and to be biased towards the transcription termination site. In contrast with H3.1, heterochromatic regions are mostly depleted of H3.3. We report that, in planta, dynamic changes in H3.3 profiles are associated with the extensive remodeling of the transcriptome that occurs during cell differentiation. We propose that H3.3 dynamics are linked to transcription and are involved in resetting covalent histone marks at a genomic scale during plant development. Our study suggests that H3 variants properties likely result from functionally convergent evolution.

Vyšlo v časopise: Dynamic Deposition of Histone Variant H3.3 Accompanies Developmental Remodeling of the Transcriptome. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002658
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002658

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Zdroje

1. DalalYBuiM 2010 Down the rabbit hole of centromere assembly and dynamics. Curr Opin Cell Biol 22 392 402

2. TagamiHRay-galletDAlmouzniGNakataniY 2004 Histone H3.1 and H3.3 Complexes Mediate Nucleosome Assembly Pathways Dependent or Independent of DNA Synthesis. Cell 116 51 61

3. AhmadKHenikoffS 2002 The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9 1191 1200

4. AhmadKHenikoffS 2002 Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A 99 Suppl 4 16477 16484

5. BanaszynskiLAAllisCDLewisPW 2010 Histone variants in metazoan development. Dev Cell 19 662 674

6. HenikoffSMcKittrickEAhmadK 2004 Epigenetics, histone H3 variants, and the inheritance of chromatin states. Cold Spring Harb Symp Quant Biol 69 235 243

7. TalbertPBHenikoffS 2010 Histone variants–ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11 264 275

8. CorpetAAlmouzniG 2009 Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol 19 29 41

9. SchwartzBEAhmadK 2005 Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19 804 814

10. WirbelauerCBellOSchübelerD 2005 Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev 19 1761 1766

11. MitoYHenikoffJGHenikoffS 2005 Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37 1090 1097

12. DauryLChailleuxCBonvalletJTroucheD 2006 Histone H3.3 deposition at E2F-regulated genes is linked to transcription. EMBO reports 7 66 71

13. GoldbergADBanaszynskiLANohK-MLewisPWElsaesserSJ 2010 Distinct Factors Control Histone Variant H3.3 Localization at Specific Genomic Regions. Cell 140 678 691

14. Ray-GalletDWoolfeAVassiasIPellentzCLacosteN 2011 Dynamics of histone h3 deposition in vivo reveal a nucleosome gap-filling mechanism for h3.3 to maintain chromatin integrity. Mol Cell 44 928 941

15. TamuraTSmithMKannoTDasenbrockHNishiyamaA 2009 Inducible deposition of the histone variant H3.3 in interferon-stimulated genes. The Journal of biological chemistry 284 12217 12225

16. DranéPOuararhniKDepauxAShuaibMHamicheA 2010 The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24 1253 1265

17. WongLHMcGhieJDSimMAndersonMAAhnS 2010 ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20 351 360

18. LewisPWElsaesserSJNohKMStadlerSCAllisCD 2010 Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci U S A 107 14075 14080

19. MitoYHenikoffJGHenikoffS 2007 Histone replacement marks the boundaries of cis-regulatory domains. Science 315 1408 1411

20. ChowC-MGeorgiouASzutoriszHMaia e SilvaAPomboA 2005 Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO reports 6 354 360

21. WaterborgJH 2011 Evolution of histone H3: emergence of variants and conservation of post-translational modification sites. Biochem Cell Biol

22. WaterborgJHRobertsonAJ 1996 Common features of analogous replacement histone H3 genes in animals and plants. J Mol Evol 43 194 206

23. RobertsonAJKaprosTDuditsDWaterborgJH 1996 Identification of three highly expressed replacement histone H3 genes of alfalfa. DNA Seq 6 137 146

24. WaterborgJH 1991 Multiplicity of histone h3 variants in wheat, barley, rice, and maize. Plant Physiol 96 453 458

25. MalikHSHenikoffS 2003 Phylogenomics of the nucleosome. Nat Struct Biol 10 882 891

26. IngouffMBergerF 2009 Histone3 variants in plants. Chromosoma 119 27 33

27. WuSCGyorgyeyJDuditsD 1989 Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucleic Acids Res 17 3057 3063

28. ChaubetNClementBGigotC 1992 Genes encoding a histone H3.3-like variant in Arabidopsis contain intervening sequences. J Mol Biol 225 569 574

29. LepetitMEhlingMChaubetNGigotC 1992 A plant histone gene promoter can direct both replication-dependent and -independent gene expression in transgenic plants. Mol Gen Genet 231 276 285

30. OkadaTEndoMSinghMBBhallaPL 2005 Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44 557 568

31. IngouffMRademacherSHolecSSoljicLXinN 2010 Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20 2137 2143

32. ShiLWangJHongFSpectorDLFangY 2011 Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. Proc Natl Acad Sci USA 108 10574 10578

33. ChodavarapuRKFengSBernatavichuteYVChenPYStroudH 2010 Relationship between nucleosome positioning and DNA methylation. Nature 466 388 392

34. JohnsonLCaoXJacobsenS 2002 Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12 1360 1367

35. SoppeWJJasencakovaZHoubenAKakutaniTMeisterA 2002 DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21 6549 6559

36. TurckFRoudierFFarronaSMartin-MagnietteMLGuillaumeE 2007 Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3 e86 doi:10.1371/journal.pgen.0030086

37. RoudierFAhmedIBerardCSarazinAMary-HuardT 2011 Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30 1928 1938

38. ChoiESShinJAKimHSJangYK 2005 Dynamic regulation of replication independent deposition of histone H3 in fission yeast. Nucleic acids research 33 7102 7110

39. JohnsonLMollahSGarciaBAMuratoreTLShabanowitzJ 2004 Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32 6511 6518

40. WaterborgJH 1990 Sequence Analysis of Acetylation and Methylation in Two Histone H3 Variants of Alfalfa *. The Journal of biological chemistry 265 17157 17161

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

42. JinCZangCWeiGCuiKPengW 2009 H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nature genetics 41 941 945

43. OoiSLHenikoffJGHenikoffS 2010 A native chromatin purification system for epigenomic profiling in Caenorhabditis elegans. Nucleic Acids Res 38 e26

44. DonnellyPMBonettaDTsukayaHDenglerREDenglerNG 1999 Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215 407 419

45. GauthierNPJensenLJWernerssonRBrunakSJensenTS 2010 Cyclebase.org: version 2.0, an updated comprehensive, multi-species repository of cell cycle experiments and derived analysis results. Nucleic Acids Res 38 D699 702

46. ElsaesserSJGoldbergADAllisCD 2010 New functions for an old variant: no substitute for histone H3.3. Current opinion in genetics & development 20 110 117

47. OkadaTSinghMBBhallaPL 2006 Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol Biol 62 503 512

48. CurtisMDGrossniklausU 2003 A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133 462 469

49. ItoTTakahashiNShimuraYOkadaK 1997 A serine/threonine protein kinase gene isolated by an in vivo binding procedure using the Arabidopsis floral homeotic gene product, AGAMOUS. Plant Cell Physiol 38 248 258

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

51. ZhangYLiuTMeyerCAEeckhouteJJohnsonDS 2008 Model-based analysis of ChIP-Seq (MACS). Genome Biol 9 R137

52. FujitaPARheadBZweigASHinrichsASKarolchikD 2011 The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39 D876 882

53. TrapnellCPachterLSalzbergSL 2009 TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 1105 1111

54. LangmeadBTrapnellCPopMSalzbergSL 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10 R25

55. LiHHandsakerBWysokerAFennellTRuanJ 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 2078 2079

56. TrapnellCWilliamsBAPerteaGMortazaviAKwanG 2010 Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28 511 515

57. BernatavichuteYVZhangXCokusSPellegriniMJacobsenSE 2008 Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3 e3156 doi:10.1371/journal.pone.0003156

58. BulowLBrillYHehlR 2010 AthaMap-assisted transcription factor target gene identification in Arabidopsis thaliana. Database (Oxford) 2010 baq034