#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Homologs of Retinoblastoma-Associated Protein 46/48 Associate with a Histone Deacetylase to Act Redundantly in Chromatin Silencing


RNA molecules such as small-interfering RNAs (siRNAs) and antisense RNAs (asRNAs) trigger chromatin silencing of target loci. In the model plant Arabidopsis, RNA–triggered chromatin silencing involves repressive histone modifications such as histone deacetylation, histone H3 lysine-9 methylation, and H3 lysine-27 monomethylation. Here, we report that two Arabidopsis homologs of the human histone-binding proteins Retinoblastoma-Associated Protein 46/48 (RbAp46/48), known as MSI4 (or FVE) and MSI5, function in partial redundancy in chromatin silencing of various loci targeted by siRNAs or asRNAs. We show that MSI5 acts in partial redundancy with FVE to silence FLOWERING LOCUS C (FLC), which is a crucial floral repressor subject to asRNA–mediated silencing, FLC homologs, and other loci including transposable and repetitive elements which are targets of siRNA–directed DNA Methylation (RdDM). Both FVE and MSI5 associate with HISTONE DEACETYLASE 6 (HDA6) to form complexes and directly interact with the target loci, leading to histone deacetylation and transcriptional silencing. In addition, these two genes function in de novo CHH (H = A, T, or C) methylation and maintenance of symmetric cytosine methylation (mainly CHG methylation) at endogenous RdDM target loci, and they are also required for establishment of cytosine methylation in the previously unmethylated sequences directed by the RdDM pathway. This reveals an important functional divergence of the plant RbAp46/48 relatives from animal counterparts.


Vyšlo v časopise: Homologs of Retinoblastoma-Associated Protein 46/48 Associate with a Histone Deacetylase to Act Redundantly in Chromatin Silencing. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002366
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002366

Souhrn

RNA molecules such as small-interfering RNAs (siRNAs) and antisense RNAs (asRNAs) trigger chromatin silencing of target loci. In the model plant Arabidopsis, RNA–triggered chromatin silencing involves repressive histone modifications such as histone deacetylation, histone H3 lysine-9 methylation, and H3 lysine-27 monomethylation. Here, we report that two Arabidopsis homologs of the human histone-binding proteins Retinoblastoma-Associated Protein 46/48 (RbAp46/48), known as MSI4 (or FVE) and MSI5, function in partial redundancy in chromatin silencing of various loci targeted by siRNAs or asRNAs. We show that MSI5 acts in partial redundancy with FVE to silence FLOWERING LOCUS C (FLC), which is a crucial floral repressor subject to asRNA–mediated silencing, FLC homologs, and other loci including transposable and repetitive elements which are targets of siRNA–directed DNA Methylation (RdDM). Both FVE and MSI5 associate with HISTONE DEACETYLASE 6 (HDA6) to form complexes and directly interact with the target loci, leading to histone deacetylation and transcriptional silencing. In addition, these two genes function in de novo CHH (H = A, T, or C) methylation and maintenance of symmetric cytosine methylation (mainly CHG methylation) at endogenous RdDM target loci, and they are also required for establishment of cytosine methylation in the previously unmethylated sequences directed by the RdDM pathway. This reveals an important functional divergence of the plant RbAp46/48 relatives from animal counterparts.


Zdroje

1. LawJAJacobsenSE 2010 Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11 204 220

2. MatzkeMKannoTDaxingerLHuettelBMatzkeAJ 2009 RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21 367 376

3. SazeHKakutaniT 2010 Differentiation of epigenetic modifications between transposons and genes. Curr Opin Plant Biol 14 81 87

4. ChinnusamyVZhuJK 2009 RNA-directed DNA methylation and demethylation in plants. Sci China C Life Sci 52 331 343

5. WierzbickiATReamTSHaagJRPikaardCS 2009 RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41 630 634

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

7. JacobYStroudHLeblancCFengSZhuoL 2010 Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466 987 991

8. EbbsMLBenderJ 2006 Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18 1166 1176

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

10. DelerisAGreenbergMVAusinILawRWMoissiardG 2010 Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep 11 950 955

11. EarleyKWPontvianneFWierzbickiATBlevinsTTuckerS 2010 Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev 24 1119 1132

12. HeXJHsuYFPontesOZhuJLuJ 2009 NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev 23 318 330

13. AufsatzWMetteMFvan der WindenJMatzkeMMatzkeAJ 2002 HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. Embo J 21 6832 6841

14. ProbstAVFagardMProuxFMourrainPBoutetS 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

15. AufsatzWStoiberTRakicBNaumannK 2007 Arabidopsis HISTONE DEACETYLASE 6: a green link to RNA silencing. Oncogene 26 5477 5488

16. LoyolaAAlmouzniG 2004 Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 1677 3 11

17. MurzinaNVPeiXYZhangWSparkesMVicente-GarciaJ 2008 Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16 1077 1085

18. HennigLBouveretRGruissemW 2005 MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15 295 302

19. BouveretRSchonrockNGruissemWHennigL 2006 Regulation of flowering time by Arabidopsis MSI1. Development 133 1693 1702

20. KohlerCHennigLBouveretRGheyselinckJGrossniklausU 2003 Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. Embo J 22 4804 4814

21. De LuciaFCrevillenPJonesAMGrebTDeanC 2008 A PHD-Polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 105 16831 16836

22. BorghiLGutzatRFuttererJLaizetYHennigL 2010 Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22 1792 1811

23. JullienPEMosqunaAIngouffMSakataTOhadN 2008 Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6 e194

24. AusinIAlonso-BlancoCJarilloJARuiz-GarciaLMartinez-ZapaterJM 2004 Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36 162 166

25. KimHJHyunYParkJYParkMJParkMK 2004 A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36 167 171

26. HeYMichaelsSDAmasinoRM 2003 Regulation of flowering time by histone acetylation in Arabidopsis. Science 302 1751 1754

27. DoyleMRAmasinoRM 2009 A single amino acid change in the Enhancer of Zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiol 151 1688 1697

28. AmasinoR 2010 Seasonal and developmental timing of flowering. Plant J 61 1001 1013

29. CrevillenPDeanC 2011 Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14 38 44

30. LiuFMarquardtSListerCSwiezewskiSDeanC 2010 Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327 94 97

31. HornyikCTerziLCSimpsonGG 2010 The Spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18 203 213

32. LiuFQuesadaVCrevillenPBaurleISwiezewskiS 2007 The Arabidopsis RNA-binding protein FCA requires a Lysine-Specific Demethylase 1 homolog to downregulate FLC. Mol Cell 28 398 407

33. SwiezewskiSCrevillenPLiuFEckerJRJerzmanowskiA 2007 Small RNA-mediated chromatin silencing directed to the 3′ region of the Arabidopsis gene encoding the developmental regulator, FLC. Proc Natl Acad Sci U S A 104 3633 3638

34. FinneganEJKovacKAJaligotESheldonCCJames PeacockW 2005 The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J 44 420 432

35. ScortecciKCMichaelsSDAmasinoRM 2001 Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26 229 236

36. RatcliffeOJKumimotoRWWongBJRiechmannJL 2003 Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15 1159 1169

37. KimDHSungS 2010 The Plant Homeo Domain finger protein, VIN3-LIKE 2, is necessary for photoperiod-mediated epigenetic regulation of the floral repressor, MAF5. Proc Natl Acad Sci U S A 107 17029 17034

38. BaurleIDeanC 2008 Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3 e2733

39. VeleyKMMichaelsSD 2008 Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiol 147 682 695

40. ChanSWZhangXBernatavichuteYVJacobsenSE 2006 Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4 e363

41. KinoshitaYSazeHKinoshitaTMiuraASoppeWJ 2007 Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49 38 45

42. HuettelBKannoTDaxingerLAufsatzWMatzkeAJ 2006 Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. Embo J 25 2828 2836

43. JiangDYangWHeYAmasinoRM 2007 Arabidopsis relatives of the human Lysine-Specific Demethylase 1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19 2975 2987

44. LippmanZMayBYordanCSingerTMartienssenR 2003 Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1 e67

45. ZhengBWangZLiSYuBLiuJY 2009 Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23 2850 2860

46. ChanSWHendersonIRZhangXShahGChienJS 2006 RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet 2 e83

47. ChanSWZilbermanDXieZJohansenLKCarringtonJC 2004 RNA silencing genes control de novo DNA methylation. Science 303 1336

48. CaoXJacobsenSE 2002 Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12 1138 1144

49. WuKZhangLZhouCYuCWChaikamV 2008 HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59 225 234

50. Bracha-DroriKShichrurKKatzAOlivaMAngeloviciR 2004 Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40 419 427

51. ToTKKimJMMatsuiAKuriharaYMorosawaT 2011 Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7 e1002055

52. GaoZLiuHLDaxingerLPontesOHeX 2010 An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465 106 109

53. PazhouhandehMMolinierJBerrAGenschikP 2011 MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc Natl Acad Sci U S A 108 3430 3435

54. ZhangXClarenzOCokusSBernatavichuteYVPellegriniM 2007 Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5 e129

55. SchubertDPrimavesiLBishoppARobertsGDoonanJ 2006 Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. Embo J 25 4638 4649

56. JiangDWangYWangYHeY 2008 Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3 e3404

57. FleischerTCYunUJAyerDE 2003 Identification and characterization of three new components of the mSin3A corepressor complex. Mol Cell Biol 23 3456 3467

58. ZhangYNgHHErdjument-BromageHTempstPBirdA 1999 Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13 1924 1935

59. HakimiMADongYLaneWSSpeicherDWShiekhattarR 2003 A candidate X-linked mental retardation gene is a component of a new family of histone deacetylase-containing complexes. J Biol Chem 278 7234 7239

60. ShiYLanFMatsonCMulliganPWhetstineJR 2004 Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119 941 953

61. YuCWLiuXLuoMChenCLinX 2011 HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol 156 173 184

62. 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

63. TanakaMKikuchiAKamadaH 2008 The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146 149 161

64. TianLWangJFongMPChenMCaoH 2003 Genetic control of developmental changes induced by disruption of Arabidopsis HISTONE DEACETYLASE 1 (AtHD1) expression. Genetics 165 399 409

65. MichaelsSAmasinoR 1999 FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11 949 956

66. AlonsoJM 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657

67. EarleyKWHaagJRPontesOOpperKJuehneT 2006 Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45 616 629

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

69. KarimiMDe MeyerBHilsonP 2005 Modular cloning in plant cells. Trends Plant Sci 10 103 105

70. GuXJiangDWangYBachmairAHeY 2009 Repression of the floral transition via histone H2B monoubiquitination. Plant J 57 522 533

71. JiangDKongNCGuXLiZHeY 2011 Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7 e1001330

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

73. SearleIHeYTurckFVincentCFornaraF 2006 The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20 898 912

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#