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Annual Review of Plant Biology

Volume 66, 2015

RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants

Abstract

RNA-directed DNA methylation (RdDM) is an epigenetic process in plants that involves both short and long noncoding RNAs. The generation of these RNAs and the induction of RdDM rely on complex transcriptional machineries comprising two plant-specific, RNA polymerase II (Pol II)–related RNA polymerases known as Pol IV and Pol V, as well as a host of auxiliary factors that include both novel and refashioned proteins. We present current views on the mechanism of RdDM with a focus on evolutionary innovations that occurred during the transition from a Pol II transcriptional pathway, which produces mRNA precursors and numerous noncoding RNAs, to the Pol IV and Pol V pathways, which are specialized for RdDM and gene silencing. We describe recently recognized deviations from the canonical RdDM pathway, discuss unresolved issues, and speculate on the biological significance of RdDM for flowering plants, which have a highly developed Pol V pathway.

Keyword(s): epigenetics, RNA polymerase, RNA-directed DNA methylation, small RNAs
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/content/journals/10.1146/annurev-arplant-043014-114633
2015-04-29
2024-04-24
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Literature Cited

  1. Allard ST, Bingman CA, Johnson KA, Wesenberg GE, Bitto E. 1.  et al. 2005. Structure at 1.6 Å resolution of the protein from gene locus At3g22680 from Arabidopsis thaliana. Acta Crystallogr. F 61:647–50 [Google Scholar]
  2. 2. Amborella Genome Proj 2013. The Amborella genome and the evolution of flowering plants. Science 342:1241089 [Google Scholar]
  3. Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJM. 3.  2002. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21:6832–41 [Google Scholar]
  4. Ausin I, Mockler TC, Chory J, Jacobsen SE. 4.  2009. IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat. Struct. Mol. Biol 16:1325–27 [Google Scholar]
  5. Azevedo J, Cooke R, Lagrange T. 5.  2011. Taking RISCs with Ago hookers. Curr. Opin. Plant Biol. 14:594–600 [Google Scholar]
  6. Bargsten JW, Folta A, Mlynárová L, Nap JP. 6.  2013. Snf2 family gene distribution in higher plant genomes reveals DRD1 expansion and diversification in the tomato genome. PLOS ONE 8:e81147 [Google Scholar]
  7. Bellaoui M, Gruissem W. 7.  2004. Altered expression of the Arabidopsis ortholog of DCL affects normal plant development. Planta 219:819–26 [Google Scholar]
  8. Bies-Etheve N, Pontier D, Lahmy S, Picart C, Vega D. 8.  et al. 2009. RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 10:649–54 [Google Scholar]
  9. Blevins T, Pontvianne F, Cocklin R, Podicheti R, Chandrasekhara C. 9.  et al. 2014. A two-step process for epigenetic inheritance in Arabidopsis. Mol. Cell 54:30–42 [Google Scholar]
  10. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N. 10.  et al. 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40:663–69 [Google Scholar]
  11. Böhmdorfer G, Rowley MJ, Kuciński J, Zhu Y, Amies I, Wierzbicki AT. 11.  2014. RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J. 79:181–91 [Google Scholar]
  12. Böhmdorfer G, Schleiffer A, Brunmeir R, Ferscha S, Nizhynska V. 12.  et al. 2011. GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis. Plant J. 67:420–33 [Google Scholar]
  13. Bologna NG, Voinnet O. 13.  2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65:473–503 [Google Scholar]
  14. Brabbs TR, He Z, Hogg K, Kamenski A, Li Y. 14.  et al. 2013. The stochastic silencing phenotype of Arabidopsis morc6 mutants reveals a role in efficient RNA-directed DNA methylation. Plant J. 75:836–46 [Google Scholar]
  15. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS. 15.  et al. 2003. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13:2212–17 [Google Scholar]
  16. Cao X, Springer NM, Muszynski MG, Phillips RL, Kaeppler S, Jacobsen SE. 16.  2000. Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. PNAS 97:4979–84 [Google Scholar]
  17. Carter SD, Sjögren C. 17.  2012. The SMC complexes, DNA and chromosome topology: right or knot?. Crit. Rev. Biochem. Mol. Biol. 47:1–16 [Google Scholar]
  18. Castel SE, Martienssen RA. 18.  2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14:100–12 [Google Scholar]
  19. Cecere G, Grishok A. 19.  2014. A nuclear perspective on RNAi pathways in metazoans. Biochim. Biophys. Acta 1839:223–33 [Google Scholar]
  20. Chalker DL, Yao MC. 20.  2011. DNA elimination in ciliates: transposon domestication and genome surveillance. Annu. Rev. Genet. 45:227–46 [Google Scholar]
  21. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE. 21.  2004. RNA silencing genes control de novo methylation. Science 303:1336 [Google Scholar]
  22. Cho SH, Addo-Quaye C, Coruh C, Arif MA, Ma Z. 22.  et al. 2008. Physcomitrella patens DCL3 is required for 22–24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development. PLOS Genet. 4:e10000314 [Google Scholar]
  23. Coker H, Brockdorff N. 23.  2014. SMCHD1 accumulates at DNA damage sites and facilitates the repair of DNA double-strand breaks. J. Cell Sci. 127:1869–74 [Google Scholar]
  24. Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F. 24.  et al. 2008. Structure of eukaryotic RNA polymerases. Annu. Rev. Biophys. 37:337–52 [Google Scholar]
  25. Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B. 25.  et al. 2000. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288:640–49 [Google Scholar]
  26. Dalakouras A, Wassenegger M. 26.  2013. Revisiting RNA-directed DNA methylation. RNA Biol. 10:453–55 [Google Scholar]
  27. Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U. 27.  et al. 2009. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J. 28:48–57 [Google Scholar]
  28. Deleris A, Greenberg MV, Ausin I, Law RW, Moissiard G. 28.  et al. 2010. Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep. 11:950–55 [Google Scholar]
  29. DiPaolo C, Kieft R, Cross M, Sabatini R. 29.  2005. Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein. Mol. Cell 17:441–51 [Google Scholar]
  30. Du J, Johnson LM, Groth M, Feng S, Hale CJ. 30.  et al. 2014. Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol. Cell 55:495–504 [Google Scholar]
  31. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F. 31.  et al. 2010. An endogenous, systemic RNAi pathway in plants. EMBO J. 29:1699–712 [Google Scholar]
  32. Dürr J, Lolas IB, Sørensen BB, Schubert V, Houben A. 32.  et al. 2014. The transcript elongation factor SPT4/SPT5 is involved in auxin-related gene expression in Arabidopsis. Nucleic Acids Res. 42:4332–47 [Google Scholar]
  33. Earley K, Lawrence RJ, Pontes O, Reuther R, Enciso AJ. 33.  et al. 2006. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20:1283–93 [Google Scholar]
  34. Eick D, Geyer M. 34.  2013. The RNA polymerase II carboxy-terminal domain (CTD) code. Chem. Rev. 113:8456–90 [Google Scholar]
  35. El-Shami M, Pontier D, Lahmy S, Braun L, Picart C. 35.  et al. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21:2539–44 [Google Scholar]
  36. Enke RA, Dong Z, Bender J. 36.  2011. Small RNAs prevent transcription-coupled loss of histone H3 lysine 9 methylation in Arabidopsis thaliana. PLOS Genet. 7:e1002350 [Google Scholar]
  37. Eun C, Lorković ZJ, Sasaki T, Naumann U, Matzke AJM, Matzke M. 37.  2012. Use of forward genetic screens to identify genes required for RNA-directed DNA methylation in Arabidopsis thaliana. Cold Spring Harb. Symp. Quant. Biol. 77:195–204 [Google Scholar]
  38. Fels A, Hu K, Riesner D. 38.  2001. Transcription of potato spindle tuber viroid by RNA polymerase II starts predominantly at two specific sites. Nucleic Acids Res. 29:4589–97 [Google Scholar]
  39. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M. 39.  et al. 2010. Conservation and divergence of methylation patterning in plants and animals. PNAS 107:8689–94 [Google Scholar]
  40. Finke A, Kuhlmann M, Mette MF. 40.  2012. IDN2 has a role downstream of siRNA formation in RNA-directed DNA methylation. Epigenetics 7:950–60 [Google Scholar]
  41. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. 41.  2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucl. Acids Res. 34:2887–905 [Google Scholar]
  42. Gao Z, Liu HL, Daxinger L, Pontes O, He X. 42.  et al. 2010. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465:106–9 [Google Scholar]
  43. Greenberg MV, Ausin I, Chan SW, Cokus SJ, Cuperus JT. 43.  et al. 2011. Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6:344–54 [Google Scholar]
  44. Haag JR, Pikaard CS. 44.  2011. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12:483–92 [Google Scholar]
  45. Haag JR, Ream TS, Marasco M, Nicora CD, Norbeck AD. 45.  et al. 2012. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 48:811–18 [Google Scholar]
  46. Hale CJ, Stonaker JL, Gross SM, Hollick JB. 46.  2007. A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize. PLOS Biol. 5:e275 [Google Scholar]
  47. Hartzog GA, Fu J. 47.  2013. The Spt4-Spt5 complex: a multi-faceted regulator of transcription elongation. Biochim. Biophys. Acta 1829:105–15 [Google Scholar]
  48. He XJ, Hsu YF, Zhu S, Liu HL, Pontes O. 48.  et al. 2009. A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev. 23:2717–22 [Google Scholar]
  49. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O. 49.  et al. 2009. An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137:498–508 [Google Scholar]
  50. Henderson IR, Deleris A, Wong W, Zhong X, Chin HG. 50.  et al. 2010. The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLOS Genet. 6:e100118 [Google Scholar]
  51. Henderson IR, Jacobsen SE. 51.  2008. Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev. 22:1597–606 [Google Scholar]
  52. Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC. 52.  et al. 2006. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38:721–25 [Google Scholar]
  53. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. 53.  2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–20 [Google Scholar]
  54. Huang CF, Zhu JK. 54.  2014. RNA splicing factors and RNA-directed DNA methylation. Biology 26:243–54 [Google Scholar]
  55. Huang L, Jones AM, Searle I, Patel K, Vogler H. 55.  et al. 2009. An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nat. Struct. Mol. Biol. 16:91–93 [Google Scholar]
  56. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJM, Matzke M. 56.  2006. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J. 25:2828–36 [Google Scholar]
  57. Inoue N, Hess KD, Moreadith RW, Richardson LL, Handel MA. 57.  et al. 1999. New gene family defined by MORC, a nuclear protein required for mouse spermatogenesis. Hum. Mol. Genet. 8:1201–7 [Google Scholar]
  58. Ito H, Kakutani T. 58.  2014. Control of transposable elements in Arabidopsis thaliana. Chromosome Res. 22:217–23 [Google Scholar]
  59. Iyer LM, Abhiman S, Aravind L. 59.  2008. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol. Direct 3:8 [Google Scholar]
  60. Johnson LM, Du J, Hale CJ, Bischof S, Feng S. 60.  et al. 2014. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507:124–28 [Google Scholar]
  61. Kang HG, Hyong WC, von Einem S, Manosalva P, Ehlers K. 61.  et al. 2012. CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity. Nat. Commun. 3:1297 [Google Scholar]
  62. Kang HG, Kuhl JC, Kachroo P, Klessig DF. 62.  2008. CRT1, an Arabidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to turnip crinkle virus. Cell Host Microbe 3:48–57 [Google Scholar]
  63. Kang HG, Oh CS, Sato M, Katagiri F, Glazebrook J. 63.  et al. 2010. Endosome-associated CRT1 functions early in resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell 22:918–36 [Google Scholar]
  64. Kanno T, Bucher E, Daxinger L, Huettel B, Böhmdorfer G. 64.  et al. 2008. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat. Genet. 40:670–75 [Google Scholar]
  65. Kanno T, Bucher E, Daxinger L, Huettel B, Kreil DP. 65.  et al. 2010. RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep. 11:65–71 [Google Scholar]
  66. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E. 66.  et al. 2005. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat. Genet. 37:761–65 [Google Scholar]
  67. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJM. 67.  2004. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14:801–5 [Google Scholar]
  68. Kanno T, Yoshikawa M, Habu Y. 68.  2013. Locus-specific requirements of DDR complexes for gene-body methylation of TAS genes in Arabidopsis thaliana. Plant Mol. Biol. Rep. 31:1048–52 [Google Scholar]
  69. Keller C, Bühler M. 69.  2013. Chromatin-associated ncRNA activities. Chromosome Res. 21:627–41 [Google Scholar]
  70. Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ. 70.  et al. 2007. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49:38–45 [Google Scholar]
  71. Kornienko AE, Guenzl PM, Barlow DP, Pauler FM. 71.  2013. Gene regulation by the act of long non-coding RNA transcription. BMC Biol. 11:59 [Google Scholar]
  72. Kuhlmann M, Finke A, Mascher M, Mette MF. 72.  2014. DNA methylation maintenance consolidates RNA-directed DNA methylation and transcriptional gene silencing over generations in Arabidopsis thaliana. Plant J. 80:269–81 [Google Scholar]
  73. Kuhlmann M, Mette MF. 73.  2012. Developmentally non-redundant SET domain proteins SUVH2 and SUVH9 are required for transcriptional gene silencing in Arabidopsis thaliana. Plant Mol. Biol. 79:623–33 [Google Scholar]
  74. Lahmy S, Guilleminot J, Cheng CM, Bechtold N, Albert S. 74.  et al. 2004. DOMINO1, a member of a small plant-specific gene family, encodes a protein essential for nuclear and nucleolar functions. Plant J. 39:809–20 [Google Scholar]
  75. Landick R. 75.  2009. Functional divergence in the growing family of RNA polymerases. Structure 17:323–25 [Google Scholar]
  76. Langen G, von Einem S, Koch A, Imani J, Pai SB. 76.  et al. 2014. The Compromised Recognition of Turnip Crinkle Virus1 subfamily of microrchidia ATPases regulates disease resistance in barley to biotrophic and necrotrophic pathogens. Plant Physiol. 164:866–78 [Google Scholar]
  77. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK. 77.  et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20:951–56 [Google Scholar]
  78. Law JA, Du J, Hale CJ, Feng S, Krajewski K. 78.  et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:385–89 [Google Scholar]
  79. Law JA, Jacobsen SE. 79.  2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204–20 [Google Scholar]
  80. Law JA, Vashisht AA, Wohlschlegel JA, Jacobsen SE. 80.  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 [Google Scholar]
  81. Lee TF, Gurazada SG, Zhai J, Li S, Simon SA. 81.  et al. 2012. RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics 7:781–95 [Google Scholar]
  82. Li DQ, Nair SS, Ohshiro K, Kumar A, Nair VS. 82.  et al. 2012. MORC2 signaling integrates phosphorylation-dependent, ATPase-coupled chromatin remodeling during the DNA damage response. Cell Rep. 2:1657–69 [Google Scholar]
  83. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG. 83.  1993. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5:1749–59 [Google Scholar]
  84. Liu ZW, Shao CR, Zhang CJ, Zhou JX, Zhang SW. 84.  et al. 2014. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLOS Genet. 10:e1003948 [Google Scholar]
  85. Lorković ZJ. 85.  2012. MORC proteins and epigenetic regulation. Plant Signal. Behav. 7:1561–65 [Google Scholar]
  86. Lorković ZJ, Naumann U, Matzke AJM, Matzke M. 86.  2012. Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr. Biol. 22:933–38 [Google Scholar]
  87. Luo J, Hall BD. 87.  2007. A multistep process gave rise to RNA polymerase IV of land plants. J. Mol. Evol. 64:101–12 [Google Scholar]
  88. Luteijn MJ, Ketting RF. 88.  2013. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat. Rev. Genet. 14:523–34 [Google Scholar]
  89. Ma XF, Gustafson JP. 89.  2005. Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenet. Genome Res. 109:236–49 [Google Scholar]
  90. Marí-Ordóñez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 90.  2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45:1029–39 [Google Scholar]
  91. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM. 91.  2009. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21:367–76 [Google Scholar]
  92. Matzke M, Matzke AJM. 92.  2004. Planting the seeds of a new paradigm. PLOS Biol. 2:e133 [Google Scholar]
  93. Matzke M, Mosher RA. 93.  2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:394–408 [Google Scholar]
  94. Matzke M, Primig M, Trnovsky J, Matzke AJM. 94.  1989. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 8:643–49 [Google Scholar]
  95. McClintock B. 95.  1984. The significance of responses of the genome to challenge. Science 226:792–801 [Google Scholar]
  96. McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. 96.  2012. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLOS Genet. 8:e1002474 [Google Scholar]
  97. Meister G. 97.  2013. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 14:447–59 [Google Scholar]
  98. Mette MF, Aufsatz W, van der Winden J, Matzke M, Matzke AJM. 98.  2000. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19:5194–5201 [Google Scholar]
  99. Meyer P. 99.  2013. Transgenes and their contributions to epigenetic research. Int. J. Dev. Biol. 57:509–15 [Google Scholar]
  100. Michael TP. 100.  2014. Plant genome size variation: bloating and purging DNA. Brief. Funct. Genomics 13:308–17 [Google Scholar]
  101. Moissiard G, Bischof S, Husmann D, Pastor WA, Hale CJ. 101.  et al. 2014. Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers. PNAS 111:7474–79 [Google Scholar]
  102. Moissiard G, Cokus SJ, Cary J, Feng S, Billi AC. 102.  et al. 2012. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336:1448–51 [Google Scholar]
  103. Napoli C, Lemieux C, Jorgensen R. 103.  1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–89 [Google Scholar]
  104. Naumann U, Daxinger L, Kanno T, Eun C, Long Q. 104.  et al. 2011. Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics 187:977–79 [Google Scholar]
  105. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C. 105.  et al. 2013. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 162:116–31 [Google Scholar]
  106. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC. 106.  et al. 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–84 [Google Scholar]
  107. Onodera Y, Haag JR, Ream T, Costa-Nunes P, Pontes O, Pikaard CS. 107.  2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120:613–22 [Google Scholar]
  108. Panda K, Slotkin RK. 108.  2013. Proposed mechanism for the initiation of transposable element silencing by the RDR6-directed DNA methylation pathway. Plant Signal. Behav. 8:e25206 [Google Scholar]
  109. Pélissier T, Thalmeir S, Kempe D, Sänger HL, Wassenegger M. 109.  1999. Heavy de novo methylation at symmetrical and non-symmetrical sites is a hallmark of RNA-directed DNA methylation. Nucleic Acids Res. 27:1625–34 [Google Scholar]
  110. Pélissier T, Wassenegger M. 110.  2000. A DNA target of 30 bp is sufficient for RNA-directed DNA methylation. RNA 6:55–65 [Google Scholar]
  111. Pikaard CS, Haag JR, Pontes OM, Blevins T, Cocklin R. 111.  2012. A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb. Symp. Quant. Biol. 77:205–12 [Google Scholar]
  112. Pikaard CS, Tucker S. 112.  2009. RNA-silencing enzymes Pol IV and Pol V in maize: more than one flavor?. PLOS Genet. 5:e1000736 [Google Scholar]
  113. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S. 113.  et al. 2012. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48:121–32 [Google Scholar]
  114. Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J. 114.  et al. 2005. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 19:2030–40 [Google Scholar]
  115. Ream TS, Haag JR, Wierzbicki AT, Nicora CD, Norbeck AD. 115.  et al. 2009. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 33:192–203 [Google Scholar]
  116. Rowley MJ, Avrutsky MI, Sifuentes CJ, Pereira L, Wierzbicki AT. 116.  2011. Independent chromatin binding of ARGONAUTE4 and SPT5L/KTF1 mediates transcriptional gene silencing. PLOS Genet. 7:e1002120 [Google Scholar]
  117. Sasaki T, Lee TF, Liao WW, Naumann U, Liao JL. 117.  et al. 2014. Distinct and concurrent pathways of Pol II- and Pol IV-dependent siRNA biogenesis at a repetitive trans-silencer locus in Arabidopsis thaliana. Plant J. 79:127–38 [Google Scholar]
  118. Sasaki T, Lorković ZJ, Liang SC, Matzke AJM, Matzke M. 118.  2014. The ability to form homodimers is essential for RDM1 to function in RNA-directed DNA methylation. PLOS ONE 9:e88190 [Google Scholar]
  119. Saze H, Tsugane K, Kanno T, Nishimura T. 119.  2012. DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol. 53:766–84 [Google Scholar]
  120. Schmitz KM, Mayer C, Postepska A, Grummt I. 120.  2010. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24:2264–69 [Google Scholar]
  121. Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC. 121.  2010. JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 24:986–91 [Google Scholar]
  122. Sijen T, Vijn I, Rebocho A, van Blokland R, Roelofs D. 122.  et al. 2001. Transcriptional and posttranscriptional gene silencing are mechanistically related. Curr. Biol. 11:436–40 [Google Scholar]
  123. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK. 123.  et al. 2007. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–21 [Google Scholar]
  124. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH. 124.  et al. 2009. Polyploidy and angiosperm diversification. Am. J. Bot. 96:336–48 [Google Scholar]
  125. Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T. 125.  et al. 2007. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:735–38 [Google Scholar]
  126. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. 126.  2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–64 [Google Scholar]
  127. Swarts DC, Jore MM, Westra ER, Zhu Y, Janssen JH. 127.  et al. 2014. DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507:258–61 [Google Scholar]
  128. Tan EH, Blevins T, Ream TS, Pikaard CS. 128.  2012. Functional consequences of subunit diversity in RNA polymerases II and V. Cell Rep. 1:208–14 [Google Scholar]
  129. Tayalé A, Parisod C. 129.  2013. Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenet. Genome Res. 140:79–96 [Google Scholar]
  130. Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG. 130.  et al. 2005. Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol. 6:R90 [Google Scholar]
  131. Tucker SL, Reece J, Ream TS, Pikaard CS. 131.  2010. Evolutionary history of plant multisubunit RNA polymerases IV and V: subunit origins via genome-wide and segmental gene duplications, retrotransposition, and lineage-specific subfunctionalization. Cold Spring Harb. Symp. Quant. Biol. 75:285–97 [Google Scholar]
  132. van der Krol AR, Mur LA, Beld M, Mol JNM, Stuitje AR. 132.  1990. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to suppression of gene expression. Plant Cell 2:291–99 [Google Scholar]
  133. Vaucheret H. 133.  2005. RNA polymerase IV and transcriptional silencing. Nat. Genet. 37:659–60 [Google Scholar]
  134. Wassenegger M. 134.  2000. RNA-directed DNA methylation. Plant Mol. Biol. 43:203–20 [Google Scholar]
  135. Wassenegger M, Heimes S, Riedel L, Sänger HL. 135.  1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–76 [Google Scholar]
  136. Wei L, Gu L, Song X, Cui X, Lu Z. 136.  et al. 2014. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. PNAS 111:3877–82 [Google Scholar]
  137. Wierzbicki AT. 137.  2012. The role of long non-coding RNAs in transcriptional gene silencing. Curr. Opin. Plant Biol. 15:517–22 [Google Scholar]
  138. Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ. 138.  et al. 2012. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 26:1825–36 [Google Scholar]
  139. Wierzbicki AT, Haag JR, Pikaard CS. 139.  2008. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–48 [Google Scholar]
  140. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. 140.  2009. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 4:630–34 [Google Scholar]
  141. Wild T, Cramer P. 141.  2012. Biogenesis of multisubunit RNA polymerases. Trends Biochem. Sci. 37:99–105 [Google Scholar]
  142. Wu L, Mao L, Qi Y. 142.  2012. Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160:990–99 [Google Scholar]
  143. Xie M, Ren G, Costa-Nunes P, Pontes O, Yu B. 143.  2012. A subgroup of SGS3-like proteins act redundantly in RNA-directed DNA methylation. Nucleic Acids Res. 40:4422–31 [Google Scholar]
  144. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD. 144.  et al. 2004. Genetic and functional diversification of small RNA pathways in plants. PLOS Biol. 2:e104 [Google Scholar]
  145. You W, Lorković ZJ, Matzke AJM, Matzke M. 145.  2013. Interplay among RNA polymerases II, IV and V in RNA-directed DNA methylation at a low copy transgene locus in Arabidopsis thaliana. Plant Mol. Biol. 82:85–96 [Google Scholar]
  146. You W, Tyczewska A, Spencer M, Daxinger L, Schmid MW. 146.  et al. 2012. Atypical DNA methylation of genes encoding cysteine-rich peptides in Arabidopsis thaliana. BMC Plant Biol. 12:51 [Google Scholar]
  147. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L. 147.  et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 28:193–205 [Google Scholar]
  148. Zemach A, Zilberman D. 148.  2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–19 [Google Scholar]
  149. Zhang CJ, Ning YQ, Zhang SW, Chen Q, Shao CR. 149.  et al. 2012. IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLOS Genet. 8:e1002693 [Google Scholar]
  150. Zhang H, Ma ZY, Zeng L, Tanaka K, Zhang CJ. 150.  et al. 2013. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. PNAS 110:8290–95 [Google Scholar]
  151. Zhang H, Zhu JK. 151.  2011. RNA-directed DNA methylation. Curr. Opin. Plant Biol. 14:142–47 [Google Scholar]
  152. Zhang H, Zhu JK. 152.  2012. Active DNA demethylation in plants and animals. Cold Spring Harb. Symp. Quant. Biol. 77:161–73 [Google Scholar]
  153. Zhao Y, Mo B, Chen X. 153.  2012. Mechanisms that impact microRNA stability in plants. RNA Biol. 9:1218–23 [Google Scholar]
  154. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X. 154.  2009. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23:2850–60 [Google Scholar]
  155. Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S. 155.  et al. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:1050–60 [Google Scholar]
  156. Zhong X, Hale CJ, Law JA, Johnson LM, Feng S. 156.  et al. 2012. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 19:870–75 [Google Scholar]
  157. Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki AT. 157.  2013. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol. Cell 49:298–309 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043014-114633
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RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants
Annual Review of Plant Biology 66, 243 (2015); https://doi.org/10.1146/annurev-arplant-043014-114633
/content/journals/10.1146/annurev-arplant-043014-114633
/content/journals/10.1146/annurev-arplant-043014-114633
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