Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome

Cell

Volumn 152, Issue 1-2, 2013, Pages 352-364

  Stroud, Hume ^a   Greenberg, Maxim V C ^a   Feng, Suhua ^a   Bernatavichute, Yana V ^a   Jacobsen, Steven E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CHROMATIN ASSEMBLY FACTOR 1; METHYLOME; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENE MUTATION; GENE SILENCING; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENOME; PRIORITY JOURNAL; RNA INTERFERENCE;

ARABIDOPSIS;

EID: 84872614860     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.10.054     Document Type: Article

References (59)

1. W. Aufsatz, M.F. Mette, J. van der Winden, M. Matzke, and A.J. Matzke HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA EMBO J. 21 2002 6832 6841 (Pubitemid 36014555)
2. I. Ausin, T.C. Mockler, J. Chory, and S.E. Jacobsen IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana Nat. Struct. Mol. Biol. 16 2009 1325 1327
3. L.O. Baumbusch, T. Thorstensen, V. Krauss, A. Fischer, K. Naumann, R. Assalkhou, I. Schulz, G. Reuter, and R.B. Aalen The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes Nucleic Acids Res. 29 2001 4319 4333 (Pubitemid 33064772)
4. I. Bäurle, L. Smith, D.C. Baulcombe, and C. Dean Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing Science 318 2007 109 112 (Pubitemid 47538044)
5. Y.V. Bernatavichute, X. Zhang, S. Cokus, M. Pellegrini, and S.E. Jacobsen Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana PLoS ONE 3 2008 e3156
6. A. Berr, E.J. McCallum, R. Ménard, D. Meyer, J. Fuchs, A. Dong, and W.H. Shen Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development Plant Cell 22 2010 3232 3248
7. X. Cao, and S.E. Jacobsen Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes Proc. Natl. Acad. Sci. USA 99 Suppl 4 2002 16491 16498 (Pubitemid 35470998)
8. X. Cao, and S.E. Jacobsen Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing Curr. Biol. 12 2002 1138 1144 (Pubitemid 34766938)
9. H. Cedar, and Y. Bergman Linking DNA methylation and histone modification: patterns and paradigms Nat. Rev. Genet. 10 2009 295 304
10. S.W. Chan, D. Zilberman, Z. Xie, L.K. Johansen, J.C. Carrington, and S.E. Jacobsen RNA silencing genes control de novo DNA methylation Science 303 2004 1336 (Pubitemid 38269419)
11. P.Y. Chen, S.J. Cokus, and M. Pellegrini BS Seeker: precise mapping for bisulfite sequencing BMC Bioinformatics 11 2010 203
12. S.J. Cokus, S. Feng, X. Zhang, Z. Chen, B. Merriman, C.D. Haudenschild, S. Pradhan, S.F. Nelson, M. Pellegrini, and S.E. Jacobsen Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning Nature 452 2008 215 219 (Pubitemid 351380251)
13. K.W. Earley, F. Pontvianne, A.T. Wierzbicki, T. Blevins, S. Tucker, P. Costa-Nunes, O. Pontes, and C.S. Pikaard 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 2010 1119 1132
14. M.L. Ebbs, and J. Bender Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase Plant Cell 18 2006 1166 1176 (Pubitemid 43956123)
15. S. Feng, S.J. Cokus, X. Zhang, P.Y. Chen, M. Bostick, M.G. Goll, J. Hetzel, J. Jain, S.H. Strauss, and M.E. Halpern Conservation and divergence of methylation patterning in plants and animals Proc. Natl. Acad. Sci. USA 107 2010 8689 8694
16. S. Feng, L. Rubbi, S.E. Jacobsen, and M. Pellegrini Determining DNA methylation profiles using sequencing Methods Mol. Biol. 733 2011 223 238
17. M.V. Greenberg, I. Ausin, S.W. Chan, S.J. Cokus, J.T. Cuperus, S. Feng, J.A. Law, C. Chu, M. Pellegrini, J.C. Carrington, and S.E. Jacobsen Identification of genes required for de novo DNA methylation in Arabidopsis Epigenetics 6 2011 344 354
18. X. Gu, D. Jiang, W. Yang, Y. Jacob, S.D. Michaels, and Y. He Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing PLoS Genet. 7 2011 e1002366
19. L. Guo, Y. Yu, J.A. Law, and X. Zhang SET DOMAIN GROUP2 is the major histone H3 lysine [corrected] 4 trimethyltransferase in Arabidopsis Proc. Natl. Acad. Sci. USA 107 2010 18557 18562
20. J.R. Haag, and C.S. Pikaard Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing Nat. Rev. Mol. Cell Biol. 12 2011 483 492
21. X.J. He, Y.F. Hsu, O. Pontes, J. Zhu, J. Lu, R.A. Bressan, C. Pikaard, C.S. Wang, and J.K. Zhu 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 2009 318 330
22. I.R. Henderson, X. Zhang, C. Lu, L. Johnson, B.C. Meyers, P.J. Green, and S.E. Jacobsen Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning Nat. Genet. 38 2006 721 725 (Pubitemid 43927318)
23. G.C. Hon, R.D. Hawkins, O.L. Caballero, C. Lo, R. Lister, M. Pelizzola, A. Valsesia, Z. Ye, S. Kuan, and L.E. Edsall Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer Genome Res. 22 2012 246 258
24. J.P. Jackson, A.M. Lindroth, X. Cao, and S.E. Jacobsen Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase Nature 416 2002 556 560 (Pubitemid 34288860)
25. Y. Jacob, S. Feng, C.A. LeBlanc, Y.V. Bernatavichute, H. Stroud, S. Cokus, L.M. Johnson, M. Pellegrini, S.E. Jacobsen, and S.D. Michaels ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing Nat. Struct. Mol. Biol. 16 2009 763 768
26. J.A. Jeddeloh, T.L. Stokes, and E.J. Richards Maintenance of genomic methylation requires a SWI2/SNF2-like protein Nat. Genet. 22 1999 94 97 (Pubitemid 29214813)
27. T. Kakutani, J.A. Jeddeloh, S.K. Flowers, K. Munakata, and E.J. Richards Developmental abnormalities and epimutations associated with DNA hypomethylation mutations Proc. Natl. Acad. Sci. USA 93 1996 12406 12411 (Pubitemid 26367156)
28. J.A. Law, and S.E. Jacobsen Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat. Rev. Genet. 11 2010 204 220
29. T.F. Lee, S.G. Gurazada, J. Zhai, S. Li, S.A. Simon, M.A. Matzke, X. Chen, and B.C. Meyers RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats Epigenetics 7 2012 781 795
30. A.M. Lindroth, X. Cao, J.P. Jackson, D. Zilberman, C.M. McCallum, S. Henikoff, and S.E. Jacobsen Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation Science 292 2001 2077 2080 (Pubitemid 32691574)
31. Z. Lippman, A.V. Gendrel, M. Black, M.W. Vaughn, N. Dedhia, W.R. McCombie, K. Lavine, V. Mittal, B. May, and K.D. Kasschau Role of transposable elements in heterochromatin and epigenetic control Nature 430 2004 471 476 (Pubitemid 38987911)
32. R. Lister, R.C. O'Malley, J. Tonti-Filippini, B.D. Gregory, C.C. Berry, A.H. Millar, and J.R. Ecker Highly integrated single-base resolution maps of the epigenome in Arabidopsis Cell 133 2008 523 536
33. X. Liu, C.W. Yu, J. Duan, M. Luo, K. Wang, G. Tian, Y. Cui, and K. Wu HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis Plant Physiol. 158 2012 119 129
34. F. Lu, X. Cui, S. Zhang, T. Jenuwein, and X. Cao Arabidopsis REF6 is a histone H3 lysine 27 demethylase Nat. Genet. 43 2011 715 719
35. O. Mathieu, J. Reinders, M. Caikovski, C. Smathajitt, and J. Paszkowski Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation Cell 130 2007 851 862 (Pubitemid 47334929)
36. A. Miura, M. Nakamura, S. Inagaki, A. Kobayashi, H. Saze, and T. Kakutani An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites EMBO J. 28 2009 1078 1086
37. Y. Onodera, K. Nakagawa, J.R. Haag, D. Pikaard, T. Mikami, T. Ream, Y. Ito, and C.S. Pikaard Sex-biased lethality or transmission of defective transcription machinery in Arabidopsis Genetics 180 2008 207 218
38. J. Penterman, D. Zilberman, J.H. Huh, T. Ballinger, S. Henikoff, and R.L. Fischer DNA demethylation in the Arabidopsis genome Proc. Natl. Acad. Sci. USA 104 2007 6752 6757 (Pubitemid 47175573)
39. F. Pontvianne, T. Blevins, and C.S. Pikaard Arabidopsis Histone Lysine Methyltransferases Adv. Bot. Res. 53 2010 1 22
40. F. Roudier, I. Ahmed, C. Bérard, A. Sarazin, T. Mary-Huard, S. Cortijo, D. Bouyer, E. Caillieux, E. Duvernois-Berthet, and L. Al-Shikhley Integrative epigenomic mapping defines four main chromatin states in Arabidopsis EMBO J. 30 2011 1928 1938
41. N. Schönrock, V. Exner, A. Probst, W. Gruissem, and L. Hennig Functional genomic analysis of CAF-1 mutants in Arabidopsis thaliana J. Biol. Chem. 281 2006 9560 9568 (Pubitemid 43864674)
42. G. Schotta, A. Ebert, and G. Reuter SU(VAR)3-9 is a conserved key function in heterochromatic gene silencing Genetica 117 2003 149 158 (Pubitemid 36678725)
43. W.J. Soppe, Z. Jasencakova, A. Houben, T. Kakutani, A. Meister, M.S. Huang, S.E. Jacobsen, I. Schubert, and P.F. Fransz DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis EMBO J. 21 2002 6549 6559 (Pubitemid 35448432)
44. M. Tariq, H. Saze, A.V. Probst, J. Lichota, Y. Habu, and J. Paszkowski Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin Proc. Natl. Acad. Sci. USA 100 2003 8823 8827 (Pubitemid 36899182)
45. F.K. Teixeira, F. Heredia, A. Sarazin, F. Roudier, M. Boccara, C. Ciaudo, C. Cruaud, J. Poulain, M. Berdasco, and M.F. Fraga A role for RNAi in the selective correction of DNA methylation defects Science 323 2009 1600 1604
46. T.K. To, J.M. Kim, A. Matsui, Y. Kurihara, T. Morosawa, J. Ishida, M. Tanaka, T. Endo, T. Kakutani, and T. Toyoda Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1 PLoS Genet. 7 2011 e1002055
47. R.K. Tran, D. Zilberman, C. de Bustos, R.F. Ditt, J.G. Henikoff, A.M. Lindroth, J. Delrow, T. Boyle, S. Kwong, and T.D. Bryson Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis Genome Biol. 6 2005 R90
48. O. Voinnet Use, tolerance and avoidance of amplified RNA silencing by plants Trends Plant Sci. 13 2008 317 328
49. A. Vongs, T. Kakutani, R.A. Martienssen, and E.J. Richards Arabidopsis thaliana DNA methylation mutants Science 260 1993 1926 1928 (Pubitemid 23258270)
50. I. Weinhofer, E. Hehenberger, P. Roszak, L. Hennig, and C. Köhler H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation PLoS Genet. 6 2010 e1001152
51. H.R. Woo, T.A. Dittmer, and E.J. Richards Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis PLoS Genet. 4 2008 e1000156
52. L. Xu, Z. Zhao, A. Dong, L. Soubigou-Taconnat, J.P. Renou, A. Steinmetz, and W.H. Shen Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana Mol. Cell. Biol. 28 2008 1348 1360 (Pubitemid 351214136)
53. X. Zhang, Y.V. Bernatavichute, S. Cokus, M. Pellegrini, and S.E. Jacobsen Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana Genome Biol. 10 2009 R62
54. X. Zheng, J. Zhu, A. Kapoor, and J.K. Zhu Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing EMBO J. 26 2007 1691 1701 (Pubitemid 46480931)
55. B. Zheng, Z. Wang, S. Li, B. Yu, J.Y. Liu, and X. Chen Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis Genes Dev. 23 2009 2850 2860
56. X. Zhong, C.J. Hale, J.A. Law, L.M. Johnson, S. Feng, A. Tu, and S.E. Jacobsen DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons Nat. Struct. Mol. Biol. 19 2012 870 875
57. Langmead, B.; Trapnell, C.; Pop, M.; and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
58. Law, J.A.; Vashisht, A.A.; Wohlschlegel, J.A.; and Jacobsen, S.E. (2011). SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7, e1002195.
59. Stroud, H.; Hale, C.J.; Feng, S.; Caro, E.; Jacob, Y.; Michaels, S.D.; and Jacobsen, S.E. (2012). DNA methyltransferases are required to induce heterochromatic re-replication in Arabidopsis. PLoS Genet. 8, e1002808.