Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Gu, Xiaofeng ^a,b   Jiang, Danhua ^a,b   Yang, Wannian ^a,b,d   Jacob, Yannick ^c   Michaels, Scott D ^c   He, Yuehui ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b Temasek Life Sciences Laboratory   (Singapore)

^c INDIANA UNIVERSITY   (United States)

^d CENTRAL CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY RNA; CYTOSINE; HISTONE DEACETYLASE 6; MSI4 PROTEIN; MSI5 PROTEIN; RETINOBLASTOMA BINDING PROTEIN 46; RETINOBLASTOMA BINDING PROTEIN 48; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; FLF PROTEIN, ARABIDOPSIS; HDA6 PROTEIN, ARABIDOPSIS; HISTONE DEACETYLASE; MADS DOMAIN PROTEIN; MSI4 PROTEIN, ARABIDOPSIS; MSI5 PROTEIN, ARABIDOPSIS; RETINOBLASTOMA BINDING PROTEIN 4;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DEACETYLATION; DNA METHYLATION; FLC GENE; GENE LOCUS; GENE SILENCING; HISTONE DEACETYLATION; NONHUMAN; PLANT GENE; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; CHROMATIN; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE REPEAT; TRANSPOSON;

ANIMALIA; ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CHROMATIN; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; FLOWERS; GENE SILENCING; HISTONE DEACETYLASES; MADS DOMAIN PROTEINS; REPETITIVE SEQUENCES, NUCLEIC ACID; RETINOBLASTOMA-BINDING PROTEIN 4; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 81755187316     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002366     Document Type: Article

References (73)

1. Law JA, Jacobsen SE, (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220.
2. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ, (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21: 367-376.
3. Saze H, Kakutani T, (2010) Differentiation of epigenetic modifications between transposons and genes. Curr Opin Plant Biol 14: 81-87.
4. Chinnusamy V, Zhu JK, (2009) RNA-directed DNA methylation and demethylation in plants. Sci China C Life Sci 52: 331-343.
5. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS, (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630-634.
6. Zilberman D, Cao X, Jacobsen SE, (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719.
7. Jacob Y, Stroud H, Leblanc C, Feng S, Zhuo L, et al. (2010) Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466: 987-991.
8. Ebbs ML, Bender J, (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166-1176.
9. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE, (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62.
10. Deleris A, Greenberg MV, Ausin I, Law RW, Moissiard G, et al. (2010) Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep 11: 950-955.
11. Earley KW, Pontvianne F, Wierzbicki AT, Blevins T, Tucker S, et al. (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. He XJ, Hsu YF, Pontes O, Zhu J, Lu J, et al. (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. Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJ, (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. Embo J 21: 6832-6841.
14. Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, et al. (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. Aufsatz W, Stoiber T, Rakic B, Naumann K, (2007) Arabidopsis HISTONE DEACETYLASE 6: a green link to RNA silencing. Oncogene 26: 5477-5488.
16. Loyola A, Almouzni G, (2004) Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 1677: 3-11.
17. Murzina NV, Pei XY, Zhang W, Sparkes M, Vicente-Garcia J, et al. (2008) Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16: 1077-1085.
18. Hennig L, Bouveret R, Gruissem W, (2005) MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15: 295-302.
19. Bouveret R, Schonrock N, Gruissem W, Hennig L, (2006) Regulation of flowering time by Arabidopsis MSI1. Development 133: 1693-1702.
20. Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, et al. (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 Lucia F, Crevillen P, Jones AM, Greb T, Dean C, (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. Borghi L, Gutzat R, Futterer J, Laizet Y, Hennig L, et al. (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22: 1792-1811.
23. Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, et al. (2008) Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6: e194.
24. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM, (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36: 162-166.
25. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, et al. (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36: 167-171.
26. He Y, Michaels SD, Amasino RM, (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302: 1751-1754.
27. Doyle MR, Amasino RM, (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. Amasino R, (2010) Seasonal and developmental timing of flowering. Plant J 61: 1001-1013.
29. Crevillen P, Dean C, (2011) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14: 38-44.
30. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C, (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327: 94-97.
31. Hornyik C, Terzi LC, Simpson GG, (2010) The Spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18: 203-213.
32. Liu F, Quesada V, Crevillen P, Baurle I, Swiezewski S, et al. (2007) The Arabidopsis RNA-binding protein FCA requires a Lysine-Specific Demethylase 1 homolog to downregulate FLC. Mol Cell 28: 398-407.
33. Swiezewski S, Crevillen P, Liu F, Ecker JR, Jerzmanowski A, et al. (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. Finnegan EJ, Kovac KA, Jaligot E, Sheldon CC, James Peacock W, et al. (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. Scortecci KC, Michaels SD, Amasino RM, (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26: 229-236.
36. Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL, (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15: 1159-1169.
37. Kim DH, Sung S, (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. Baurle I, Dean C, (2008) Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3: e2733.
39. Veley KM, Michaels SD, (2008) Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiol 147: 682-695.
40. Chan SW, Zhang X, Bernatavichute YV, Jacobsen SE, (2006) Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4: e363.
41. Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, et al. (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49: 38-45.
42. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, et al. (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. Embo J 25: 2828-2836.
43. Jiang D, Yang W, He Y, Amasino RM, (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. Lippman Z, May B, Yordan C, Singer T, Martienssen R, (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1: e67.
45. Zheng B, Wang Z, Li S, Yu B, Liu JY, et al. (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. Chan SW, Henderson IR, Zhang X, Shah G, Chien JS, et al. (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet 2: e83.
47. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, et al. (2004) RNA silencing genes control de novo DNA methylation. Science 303: 1336.
48. Cao X, Jacobsen SE, (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1138-1144.
49. Wu K, Zhang L, Zhou C, Yu CW, Chaikam V, (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59: 225-234.
50. Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, et al. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40: 419-427.
51. To TK, Kim JM, Matsui A, Kurihara Y, Morosawa T, et al. (2011) Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7: e1002055.
52. Gao Z, Liu HL, Daxinger L, Pontes O, He X, et al. (2010) An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465: 106-109.
53. Pazhouhandeh M, Molinier J, Berr A, Genschik P, (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. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, et al. (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5: e129.
55. Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, et al. (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. Embo J 25: 4638-4649.
56. Jiang D, Wang Y, Wang Y, He Y, (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3: e3404.
57. Fleischer TC, Yun UJ, Ayer DE, (2003) Identification and characterization of three new components of the mSin3A corepressor complex. Mol Cell Biol 23: 3456-3467.
58. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, et al. (1999) Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13: 1924-1935.
59. Hakimi MA, Dong Y, Lane WS, Speicher DW, Shiekhattar R, (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. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, et al. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953.
61. Yu CW, Liu X, Luo M, Chen C, Lin X, et al. (2011) HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol 156: 173-184.
62. Jiang D, Gu X, He Y, (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. Tanaka M, Kikuchi A, Kamada H, (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146: 149-161.
64. Tian L, Wang J, Fong MP, Chen M, Cao H, et al. (2003) Genetic control of developmental changes induced by disruption of Arabidopsis HISTONE DEACETYLASE 1 (AtHD1) expression. Genetics 165: 399-409.
65. Michaels S, Amasino R, (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
66. Alonso JM, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
67. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629.
68. Curtis MD, Grossniklaus U, (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469.
69. Karimi M, De Meyer B, Hilson P, (2005) Modular cloning in plant cells. Trends Plant Sci 10: 103-105.
70. Gu X, Jiang D, Wang Y, Bachmair A, He Y, (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J 57: 522-533.
71. Jiang D, Kong NC, Gu X, Li Z, He Y, (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7: e1001330.
72. Johnson L, Cao X, Jacobsen S, (2002) Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360-1367.
73. Searle I, He Y, Turck F, Vincent C, Fornara F, et al. (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.