Histone H2B Monoubiquitination Facilitates the Rapid Modulation of Gene Expression during Arabidopsis Photomorphogenesis
Profiling of DNA and histone modifications has recently allowed the establishment of reference epigenomes from several model organisms. This identified a major chromatin state for active genes that contains monoubiquitinated H2B (H2Bub), a mark linked to transcription elongation. However, assessment of dynamic chromatin changes during the reprogramming of gene expression in response to extrinsic or developmental signals has been more difficult. Here we used the major developmental switch that Arabidopsis thaliana plants undergo upon their initial perception of light, known as photomorphogenesis, as a paradigm to assess spatial and temporal dynamics of monoubiquitinated H2B (H2Bub) and its impact on transcriptional responses. The process involves rapid and extensive transcriptional reprogramming and represents a developmental window well suited to studying cell division–independent chromatin changes. Genome-wide H2Bub distribution was determined together with transcriptome profiles at three time points during early photomorphogenesis. This revealed de novo marking of 177 genes upon the first hour of illumination, illustrating the dynamic nature of H2Bub enrichment in a genomic context. Gene upregulation was associated with H2Bub enrichment, while H2Bub levels generally remained stable during gene downregulation. We further report that H2Bub influences the modulation of gene expression, as both gene up- and downregulation were globally weaker in hub1 mutant plants that lack H2Bub. H2Bub-dependent regulation notably impacted genes with fast and transient light induction, and several circadian clock components whose mRNA levels are tightly regulated by sharp oscillations. Based on these findings, we propose that H2B monoubiquitination is part of a transcription-coupled, chromatin-based mechanism to rapidly modulate gene expression.
Vyšlo v časopise:
Histone H2B Monoubiquitination Facilitates the Rapid Modulation of Gene Expression during Arabidopsis Photomorphogenesis. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002825
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002825
Souhrn
Profiling of DNA and histone modifications has recently allowed the establishment of reference epigenomes from several model organisms. This identified a major chromatin state for active genes that contains monoubiquitinated H2B (H2Bub), a mark linked to transcription elongation. However, assessment of dynamic chromatin changes during the reprogramming of gene expression in response to extrinsic or developmental signals has been more difficult. Here we used the major developmental switch that Arabidopsis thaliana plants undergo upon their initial perception of light, known as photomorphogenesis, as a paradigm to assess spatial and temporal dynamics of monoubiquitinated H2B (H2Bub) and its impact on transcriptional responses. The process involves rapid and extensive transcriptional reprogramming and represents a developmental window well suited to studying cell division–independent chromatin changes. Genome-wide H2Bub distribution was determined together with transcriptome profiles at three time points during early photomorphogenesis. This revealed de novo marking of 177 genes upon the first hour of illumination, illustrating the dynamic nature of H2Bub enrichment in a genomic context. Gene upregulation was associated with H2Bub enrichment, while H2Bub levels generally remained stable during gene downregulation. We further report that H2Bub influences the modulation of gene expression, as both gene up- and downregulation were globally weaker in hub1 mutant plants that lack H2Bub. H2Bub-dependent regulation notably impacted genes with fast and transient light induction, and several circadian clock components whose mRNA levels are tightly regulated by sharp oscillations. Based on these findings, we propose that H2B monoubiquitination is part of a transcription-coupled, chromatin-based mechanism to rapidly modulate gene expression.
Zdroje
1. BakerM 2011 Making sense of chromatin states. Nat Methods 8 717 722
2. FilionGJvan BemmelJGBraunschweigUTalhoutWKindJ 2010 Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143 212 224
3. LiuTRechtsteinerAEgelhoferTAVielleALatorreI 2011 Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 21 227 236
4. RoudierFAhmedIBerardCSarazinAMary-HuardT 2011 Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. Embo J 30 1928 1938
5. GreerELMauresTJUcarDHauswirthAGManciniE 2011 Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479 365 371
6. MoazedD 2011 Mechanisms for the inheritance of chromatin states. Cell 146 510 518
7. HenryKWWyceALoWSDugganLJEmreNC 2003 Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 17 2648 2663
8. KaoCFHillyerCTsukudaTHenryKBergerS 2004 Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev 18 184 195
9. XiaoTKaoCFKroganNJSunZWGreenblattJF 2005 Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol Cell Biol 25 637 651
10. LangGBonnetJUmlaufDKarmodiyaKKofflerJ 2011 The Tightly Controlled Deubiquitination Activity of the Human SAGA Complex Differentially Modifies Distinct Gene Regulatory Elements. Mol Cell Biol 31 3734 3744
11. ShemaETiroshIAylonYHuangJYeC 2008 The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev 22 2664 2676
12. WeakeVMWorkmanJL 2011 SAGA function in tissue-specific gene expression. Trends Cell Biol
13. FierzBChatterjeeCMcGintyRKBar-DaganMRaleighDP 2011 Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 7 113 119
14. BelotserkovskayaROhSBondarenkoVAOrphanidesGStuditskyVM 2003 FACT facilitates transcription-dependent nucleosome alteration. Science 301 1090 1093
15. PavriRZhuBLiGTrojerPMandalS 2006 Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125 703 717
16. XinHTakahataSBlanksmaMMcCulloughLStillmanDJ 2009 yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35 365 376
17. FlemingABKaoCFHillyerCPikaartMOsleyMA 2008 H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31 57 66
18. SunZWAllisCD 2002 Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 104 108
19. BriggsSDXiaoTSunZWCaldwellJAShabanowitzJ 2002 Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418 498
20. SmithEShilatifardA 2010 The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell 40 689 701
21. WeakeVMWorkmanJL 2008 Histone ubiquitination: triggering gene activity. Mol Cell 29 653 663
22. LeeJSSmithEShilatifardA 2010 The language of histone crosstalk. Cell 142 682 685
23. GrasserKD 2005 Emerging role for transcript elongation in plant development. Trends Plant Sci 10 484 490
24. CrevillenPDeanC 2010 Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14 38 44
25. BerrAShafiqSShenWH 2011 Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809 567 576
26. FengSJacobsenSEReikW 2011 Epigenetic reprogramming in plant and animal development. Science 330 622 627
27. HeGEllingAADengXW 2011 The epigenome and plant development. Annu Rev Plant Biol 62 411 435
28. FisherAJFranklinKA 2011 Chromatin remodelling in plant light signalling. Physiol Plant 142 305 313
29. ChenMChoryJ 2011 Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol
30. JiaoYLauOSDengXW 2007 Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8 217 230
31. KamiCLorrainSHornitschekPFankhauserC 2010 Light-regulated plant growth and development. Curr Top Dev Biol 91 29 66
32. CharronJBHeHEllingAADengXW 2009 Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21 3732 3748
33. BenhamedMBertrandCServetCZhouDX 2006 Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18 2893 2903
34. JangICChungPJHemmesHJungCChuaNH 2011 Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus. Plant Cell 23 459 470
35. ChuaYLBrownAPGrayJC 2001 Targeted histone acetylation and altered nuclease accessibility over short regions of the pea plastocyanin gene. Plant Cell 13 599 612
36. BergmullerEGehrigPMGruissemW 2007 Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J Proteome Res 6 3655 3668
37. LiuYKoornneefMSoppeWJ 2007 The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19 433 444
38. FleuryDHimanenKCnopsGNelissenHBoccardiTM 2007 The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19 417 432
39. CaoYDaiYCuiSMaL 2008 Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20 2586 2602
40. GuXJiangDWangYBachmairAHeY 2009 Repression of the floral transition via histone H2B monoubiquitination. Plant J 57 522 533
41. XuLMenardRBerrAFuchsJCognatV 2009 The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57 279 288
42. PeschkeFKretschT 2011 Genome-wide analysis of light-dependent transcript accumulation patterns during early stages of Arabidopsis seedling deetiolation. Plant Physiol 155 1353 1366
43. SchroederDFGahrtzMMaxwellBBCookRKKanJM 2002 De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr Biol 12 1462 1472
44. CroweMLSerizetCThareauVAubourgSRouzeP 2003 CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31 156 158
45. ZhangXBernatavichuteYVCokusSPellegriniMJacobsenSE 2009 Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 R62
46. HruzTLauleOSzaboGWessendorpFBleulerS 2008 Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008 420747
47. WeiNSerinoGDengXW 2008 The COP9 signalosome: more than a protease. Trends Biochem Sci 33 592 600
48. ChenHShenYTangXYuLWangJ 2006 Arabidopsis CULLIN4 Forms an E3 Ubiquitin Ligase with RBX1 and the CDD Complex in Mediating Light Control of Development. Plant Cell 18 1991 2004
49. DohmannEMLevesqueMPDe VeylderLReichardtIJurgensG 2008 The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability. Development 135 2013 2022
50. TamayoPSlonimDMesirovJZhuQKitareewanS 1999 Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci U S A 96 2907 2912
51. ChoryJPetoCFeinbaumRPrattLAusubelF 1989 Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58 991 999
52. LeivarPQuailPH 2010 PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16 19 28
53. ArmstrongGARungeSFrickGSperlingUApelK 1995 Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108 1505 1517
54. ShilatifardAConawayRCConawayJW 2003 The RNA polymerase II elongation complex. Annu Rev Biochem 72 693 715
55. SchmitzRJTamadaYDoyleMRZhangXAmasinoRM 2009 Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol 149 1196 1204
56. MinskyNShemaEFieldYSchusterMSegalE 2008 Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol 10 483 488
57. OhSParkSvan NockerS 2008 Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4 e1000077 doi:10.1371/journal.pgen.1000077
58. NgHHRobertFYoungRAStruhlK 2003 Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 709 719
59. ShilatifardA 2006 Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75 243 269
60. JiangDGuXHeY 2009 Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21 1733 1746
61. JiangDKongNCGuXLiZHeY 2011 Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7 e1001330 doi:10.1371/journal.pgen.1001330
62. DhawanRLuoHFoersterAMAbuqamarSDuHN 2009 HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell 21 1000 1019
63. BattaKZhangZYenKGoffmanDBPughBF 2011 Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev 25 2254 2265
64. ProudfootNJFurgerADyeMJ 2002 Integrating mRNA processing with transcription. Cell 108 501 512
65. PenheiterKLWashburnTMPorterSEHoffmanMGJaehningJA 2005 A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol Cell 20 213 223
66. PeralesMMasP 2007 A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19 2111 2123
67. LiYRossoMGViehoeverPWeisshaarB 2007 GABI-Kat SimpleSearch: an Arabidopsis thaliana T-DNA mutant database with detailed information for confirmed insertions. Nucleic Acids Res 35 D874 878
68. AlonsoJMStepanovaANLeisseTJKimCJChenH 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657
69. BernaGRoblesPMicolJL 1999 A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. Genetics 152 729 742
70. FankhauserCCasalJJ 2004 Phenotypic characterization of a photomorphogenic mutant. Plant J 39 747 760
71. CastellsEMolinierJBenvenutoGBourbousseCZabulonG 2011 The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. Embo J 30 1162 1172
72. LurinCAndrésCAubourgSBellaouiMBittonS 2004 Genome-wide analysis of Arabidopsis Pentratricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16 2089 2103
73. HilsonPSmallIKuiperMT 2003 European consortia building integrated resources for Arabidopsis functional genomics. Curr Opin Plant Biol 6 426 429
74. BarrettTTroupDBWilhiteSELedouxPRudnevD 2007 NCBI GEO: mining tens of millions of expression profiles–database and tools update. Nucleic Acids Res 35 D760 765
75. GagnotSTambyJPMartin-MagnietteMLBittonFTaconnatL 2008 CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res 36 D986 990
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 7
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