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RNA-directed DNA methylation in plants

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Abstract

In plants, many small interfering RNAs (siRNAs) direct de novo methylation by DNA methyltransferase. DNA methylation typically occurs by RNA-directed DNA methylation (RdDM), which directs transcriptional gene silencing of transposons and endogenous transgenes. RdDM is driven by non-coding RNAs (ncRNAs) produced by DNA-dependent RNA polymerases IV and V (PolIV and PolV). The production of siRNAs is initiated by PolIV and ncRNAs produced by PolIV are precursors of 24-nucleotide siRNAs. In contrast, ncRNAs produced by PolV are involved in scaffolding RNAs. In this review, we summarize recent studies of RdDM. In particular, we focus on the mechanisms involved in chromatin remodeling by PolIV and PolV.

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Abbreviations

lncRNAs:

Long non-coding RNAs

siRNAs:

Small interfering RNAs

PTGS:

Post-transcriptional gene silencing

TGS:

Transcriptional gene silencing

RdDM:

RNA-directed DNA methylation

AGO:

ARGONAUTE

PolII:

RNA polymerase II

RDR2:

RNA-dependent RNA polymerase 2

dsRNAs:

Double-stranded RNAs

DRM2:

Domain rearranged methyltransferase 2

RDM:

RNA-directed DNA methylation

RITS:

RNA-induced transcriptional silencing complex

References

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aufsatz W, Mette MF, Matzke AJ, Matzke M (2004) The role of MET1 in RNA-directed de novo and maintenance methylation of CG dinucleotides. Plant Mol Biol 54:793–804

    Article  CAS  PubMed  Google Scholar 

  • Ausin I, Mockler TC, Chory J, Jacobsen SE (2009) IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat Struct Mol Biol 16:1325–1327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ausin I, Greenberg MVC, Li CF, Jacobsen SE (2012) The splicing factor SR45 affects the RNA-directed DNA methylation pathway in Arabidopsis. Epigenetics 7:29–33

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that 294 selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 295(102):11928–11933

    Article  Google Scholar 

  • Billeter M (1996) Homeodomain-type DNA recognition. Prog Biophys Mol Biol 66:211–225

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144

    Article  CAS  PubMed  Google Scholar 

  • Castel SE, Martienssen RA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14:100–112

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dou K, Huang CF, Ma ZY, Zhang CJ, Zhou JX, Huang HW, Cai T, Tang K, Zhu JK, He XJ (2013) The PRP6-like splicing factor STA1 is involved in RNA-directed DNA methylation by facilitating the production of PolV-dependent scaffold RNAs. Nucl Acids Res 41:8489–8502

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:1166–1176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ebbs ML, Bartee L, Bender J (2005) H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol 25:10507–10515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haag JR, Ream TS, Marasco M, Nicora CD, Norbeck AD, Pasa-Tolic L, Pikaard CS (2012) In vitro transcription activities of PolIV, PolV, and RDR2 reveal coupling of PolIV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol Cell 48:811–818

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA, Dunn RM, Schwach F, Doonan JH, Baulcombe DC (2010) The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22:321–334

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He XJ, Hsu YF, Pontes O, Zhu J, Lu J, Bressan RA, Pikaard C, Wang CS, Zhu JK (2009a) 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He XJ, Hsu YF, Zhu S, Liu HL, Pontes O, Zhu J, Cui X, Wang CS, Zhu JK (2009b) A conserved transcriptional regulator is required for RNA directed DNA methylation and plant development. Genes Dev 23:2717–2722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424

    Article  CAS  PubMed  Google Scholar 

  • Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–120

    Article  CAS  PubMed  Google Scholar 

  • Huang CF, Zhu JK (2014) RNA splicing factors and RNA-directed DNA methylation. Biology 3:243–254

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang CF, Miki D, Tang K, Zhou HR, Zheng Z, Chen W, Ma ZY, Yang L, Zhang H, Liu R (2013) A Pre-mRNA-splicing factor is required for RNA-directed DNA methylation in Arabidopsis. PLoS Genet 9:e1003779

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, Jacobsen SE (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17:379–384

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14:801–805

    Article  CAS  PubMed  Google Scholar 

  • Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJ (2005) A typical RNA polymerase subunit required for RNA-directed DNA methylation. Nat Genet 37:761–765

    Article  CAS  PubMed  Google Scholar 

  • Kanno T, Bucher E, Daxinger L, Huettel B, Kreil DP, Breinig F, Lind M, Schmitt MJ, Simon SA, Gurazada SG, Meyers BC, Lorkovic ZJ, Matzke AJ, Matzke M (2010) RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11:65–71

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK, Wohlschlegel JA, Jacobsen SE (2010) A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 20:951–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Law JA, Vashisht AA, Wohlschlegel JA, Jacobsen SE (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Law JA, Du J, Hale CJ, Feng S, Krajewski K, Palanca AM, Strahl BD, Patel DJ, Jacobsen SE (2013) Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:385–389

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SWL, Lagrange T, Pikaard CS, Jacobsen SE (2006) An ARGONAUTE4-containing nuclear processing center co-localized with Cajal bodies in Arabidopsis thaliana. Cell 126:93–106

    Article  CAS  PubMed  Google Scholar 

  • Li CF, Henderson IR, Song L, Fedoroff N, Lagrange T, Jacobsen SE (2008) Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. PLoS Genet 4:e27

    Article  PubMed Central  PubMed  Google Scholar 

  • Lorkovic ZJ, Naumann U, Matzke AJ, Matzke M (2012) Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr Biol 22:933–938

    Article  CAS  PubMed  Google Scholar 

  • Martinez de Alba AE, Elvira-Matelot E, Vaucheret H (2013) Gene silencing in plants: a diversity of pathways. Biochim Biophys Acta. doi:10.1016/j.bbagrm.2013.10.005

    PubMed  Google Scholar 

  • Morris GE (2008) The Cajal body. Biochim Biophys Acta 1783:2108–2115

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee K, Brocchieri L, Bürglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Onodera Y, Haag JR, Ream T, Costa Nunes P, Pontes O, Pikaard CS (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120:613–622

    Article  CAS  PubMed  Google Scholar 

  • Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J, Hakimi MA, Lerbs-Mache S, Colot V, Lagrange T (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19:2030–2040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanford JR, Ellis J, Caceres JF (2005) Multiple roles of arginine/serine-rich splicing factors in RNA processing. Biochem Soc Trans 33:443–446

    Article  CAS  PubMed  Google Scholar 

  • Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–1521

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa PM, Bressan RA, Zhu JK (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:735–738

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 2008(13):350–358

    Article  Google Scholar 

  • Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang Z, Ebright YW, Yu B, Chen X (2006) HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucl Acids Res 34:667–675

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yokthongwattana C, Bucher E, Caikovski M, Vaillant I, Nicolet J, Mittelsten Scheid O, Paszkowski J (2010) MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J 29:340–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128:763–776

    Article  CAS  PubMed  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, EshedWilliams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, Zhu JK (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14:142–147

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, He X, Zhu J (2013) RNA-directed DNA methylation in plants: where to start. RNA Biol 10 (In press)

  • Zhang H, Ma ZY, Zeng L, Tanaka K, Zhang CJ, Ma J, Bai G, Wang P, Zhang SW, Liu ZW (2013b) DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of PolIV. Proc Natl Acad Sci USA 110:8290–8295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang CJ, Zhou JX, Liu J, Ma ZY, Zhang SW, Dou K, Huang HW, Cai T, Liu R, Zhu JK, He XJ (2013c) The splicing machinery promotes RNA-directed DNA methylation and transcriptional silencing in Arabidopsis. EMBO J 32:1128–1140

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, Iida K, Kapoor A, Pikaard CS, Zhu JK (2008) ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455:1259–1262

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X (2009) Intergenic transcription by RNA polymerase II coordinates PolIV and PolV in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu JK (2008) Epigenome sequencing comes of age. Cell 133:395–397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu Y, Rowley MJ, Bohmdorfer G, Wierzbicki AT (2013) A SWI/SNF chromatin remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell 49:298–309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Science Foundation of China (No. 31170561), the International Science and Technology Cooperation Program of China (2014DFG32440), the Priority Academic Program Development of Jiangsu Higher Education Institutions, the Program for Innovative Research Team in University of Educational Department and Jiangsu Province, China.

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Correspondence to Qiang Zhuge.

Additional information

Communicated by N. Stewart.

W. Sun and J. Zhang contributed equally to this review.

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Movahedi, A., Sun, W., Zhang, J. et al. RNA-directed DNA methylation in plants. Plant Cell Rep 34, 1857–1862 (2015). https://doi.org/10.1007/s00299-015-1839-0

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