Journal of Biosciences

, Volume 39, Issue 3, pp 365–380

miRNAting control of DNA methylation

Article

Abstract

DNA methylation is a type of epigenetic modification where a methyl group is added to the cytosine or adenine residue of a given DNA sequence. It has been observed that DNA methylation is achieved by some collaborative agglomeration of certain proteins and non-coding RNAs. The assembly of IDN2 and its homologous proteins with siRNAs recruits the enzyme DRM2, which adds a methyl group at certain cytosine residues within the DNA sequence. In this study, it was found that de novo DNA methylation might be regulated by miRNAs through systematic targeting of the genes involved in DNA methylation. A comprehensive genome-wide and system-level study of miRNA targeting, transcription factors, DNA-methylation-causing genes and their target genes has provided a clear picture of an interconnected relationship of all these factors which regulate DNA methylation in Arabidopsis. The study has identified a DNA methylation system that is controlled by four different genes: IDN2, IDNl1, IDNl2 and DRM2. These four genes along with various critical transcription factors appear to be controlled by five different miRNAs. Altogether, DNA methylation appears to be a finely tuned process of opposite control systems of DNA-methylation-causing genes and certain miRNAs pitted against each other.

Keywords

Bioinformatics de novo DNA methylation expression genome genomic microarray miRNA NGS regulatory network transcription factors 

Abbreviations

AGO

argonaute

GFF

General Feature Format

GO

gene ontology

ncRNA

non-coding RNA

NGS

next-generation sequencing

RdDM

RNA-dependent DNA methylation

RDR2

RNA-dependent RNA polymerase 2

siRNA

small interfering RNA

SVR

support vector regression

TFBS

transcription factor binding site

Supplementary material

12038_2014_9437_MOESM1_ESM.pdf (33 kb)
ESM 1(PDF 32.8 kb)

References

  1. Ausin I, Greenberg MV, Simanshu DK, Hale CJ, Vashisht AA, Simon SA, Lee TF, Feng S, et al. 2012 INVOLVED IN DENOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis. Proc. Natl. Acad. Sci. USA 109 8374–8381 Google Scholar
  2. Ausin I, Mockler TC, Chory J and Jacobsen SE 2009 IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat. Struct. Mol. Biol. 16 1325–1327PubMedCentralPubMedCrossRefGoogle Scholar
  3. Beauclair L, Yu A and Bouché N 2010 microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J. 62 454–462Google Scholar
  4. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L and Voinnet O 2008 Widespread Translational Inhibition by Plant miRNAs and siRNAs. Science 320 1185–1190PubMedCrossRefGoogle Scholar
  5. Chae L, Lee I, Shin J and Rhee SY 2012 Towards understanding how molecular networks evolve in plants. Curr Opin Plant Biol 15 177–184PubMedCrossRefGoogle Scholar
  6. Chen K and Rajewsky N 2007 The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet 8 93–103Google Scholar
  7. Chen L, Song Y, Li S, Zhang L, Zou C and Yu D 2012 The role of WRKY transcription factors in plant abiotic stresses. Biochim. Biophys. Acta. 1819 120–128PubMedCrossRefGoogle Scholar
  8. Chen RZ, Pettersson U, Beard C, Jackson-Grusby L and Jaenisch R 1998 DNA hypomethylation leads to elevated mutation rates. Nature 395 89–93PubMedCrossRefGoogle Scholar
  9. Cheon J, Park SY, Schulz B and Choe S 2010 Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC Plant Biol. 10 270Google Scholar
  10. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, et al. 2008 Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning, Nature 452 215–219PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dalakouras A and Wassenegger M 2013 Revisiting RNA-directed DNA methylation. RNA Biol. 16 103Google Scholar
  12. Davin LB and Lewis NG 1992 Phenylpropanoid metabolism: biosynthesis of monolignols, lignans and neolignans, lignins and suberins (New York) pp 325–375Google Scholar
  13. Dixon RA 2001 Natural products and plant disease resistance. Nature 411 843–847PubMedCrossRefGoogle Scholar
  14. Dixon RA and Paiva NL 1995 Stress-induced phenylpropanoid metabolism. Plant Cell 77 1085–1097CrossRefGoogle Scholar
  15. Du Z, Zhou X, Ling Y, Zhang Z and Su Z 2010 agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38 W64–W70Google Scholar
  16. Edgar R, Domrachev M and Lash AE 2002 Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30 207–210Google Scholar
  17. Egger G, Liang G, Aparicio A and Jones PA 2004 Epigenetics in human disease and prospects for epigenetic therapy. Nature 429 457–463PubMedCrossRefGoogle Scholar
  18. Fabian MR, Sonenberg N and Filipowicz W 2010 Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79 351–379PubMedCrossRefGoogle Scholar
  19. Feng S, Cokus SJ, Zhang S, Chen PY, Bostick M, Goll MG, Hetzel J, Jane J, et al. 2010 Conservation and divergence of methylation patterning in plants and animals. Proc. Natl. Acad. Sci. USA 107 8689–8694Google Scholar
  20. Finnegan EJ, Peacock WJ and Dennis ES 2000 DNA methylation, a key regulator of plant development and other processes. Curr. Opin. Genet Dev. 10 217–223 Google Scholar
  21. Gehring M and Henikoff S 2007 DNA methylation dynamics in plant genomes. Biochim. Biophys. Acta. 1769 276–286 PubMedCrossRefGoogle Scholar
  22. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB and Fischer RL 2006 DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124 495–506PubMedCrossRefGoogle Scholar
  23. Gelato KA and Fischle W 2008 Role of histone modifications in defining chromatin structure and function. Biol. Chem. 389 353–363PubMedCrossRefGoogle Scholar
  24. German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA et al. 2008 Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26 941–946PubMedCrossRefGoogle Scholar
  25. Grandbastien MA, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa AP, Le QH, Melayah D, et al. 2005 Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet. Genome Res. 110 229–241Google Scholar
  26. Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA, Dunn RM, Schwach F, Doonan JH et al. 2010 The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22 321–234PubMedCentralPubMedCrossRefGoogle Scholar
  27. He XJ, Chen T and Zhu JK 2011 Regulation and function of DNA methylation in plants and animals. Cell Res. 21 442–465Google Scholar
  28. Herr AJ, Jensen MB, Dalmay T and Baulcombe DC 2005 RNA polymerase IV directs silencing of endogenous DNA. Science 308 118–120PubMedCrossRefGoogle Scholar
  29. Heusipp G, Fälker S and Schmidt MA 2007 DNA adenine methylation and bacterial pathogenesis. Int. J. Med. Microbiol. 297 1–7 PubMedCrossRefGoogle Scholar
  30. Jaillais Y and Vert G 2012 Brassinosteroids, gibberellins and light-mediated signalling are the three-way controls of plant sprouting. Nat. Cell Biol. 14 788–790Google Scholar
  31. Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T and Parcy F bZIP Research Group 2002 bZIP transcription factors in Arabidopsis. Trends Plant Sci. Mar. 7 106–111Google Scholar
  32. Jenuwein T 2006 The epigenetic magic of histone lysine methylation. FEBS J. 273 3121–3135 Google Scholar
  33. Jha A, Mehra M and Shankar R 2011 The regulatory epicenter of miRNAs. J. Biosci. 36 621–638Google Scholar
  34. Jha A and Shankar R 2011 Employing machine learning for reliable miRNA target identification in plants. BMC Genomics 12 636 PubMedCentralPubMedCrossRefGoogle Scholar
  35. Jones PA and Laird PW 1999 Cancer epigenetics comes of age. Nat. Genet. 21 163–167PubMedCrossRefGoogle Scholar
  36. Kersey PJ, Lawson D, Birney E, Derwent PS, Haimel M, Herrero J, Keenan S, Kerhornou A et al. 2010 Ensembl Genomes: extending Ensembl across the taxonomic space. Nucleic Acids Res. 38 D563–D569Google Scholar
  37. Kidner CA and Martienssen RA 2005 The developmental role of microRNA in plants. Curr. Opin. Plant Biol. 8 38–44Google Scholar
  38. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ and Marra MA 2009 Circos: an information aesthetic for comparative genomics. Genome Res. 19 1639–1645Google Scholar
  39. Lamesch P, Berardini TZ, Li D, et al. 2012 The Arabidopsis Information Resource TAIR: improved gene annotation and new tools. Nucleic Acids Res. 40 D1202–1210Google Scholar
  40. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crété P, Voinnet O and Robaglia C 2009 Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21 1762–1768PubMedCentralPubMedCrossRefGoogle Scholar
  41. Laubinger S, Zeller G, Henz SR, Buechel S, Sachsenberg T, Wang JW, Rätsch G and Weigel D 2010 Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome. Proc. Natl. Acad. Sci. USA 107 17466–17473Google Scholar
  42. Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA and Ferreira PC 2010 Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 54 e10326CrossRefGoogle Scholar
  43. Massari ME and Murre C 2000 Helix-loop-helix proteins: Regulators of transcription in eukaryotic organisms. Mol. Cell Biol. 20 429–440Google Scholar
  44. Ng HH and Bird A 1999 DNA methylation and chromatin modification. Curr. Opin. Genet. Dev. 9158–163Google Scholar
  45. Oliveros JC 2007 VENNY. An interactive tool for comparing lists with Venn Diagrams, http://bioinfogp.cnb.csic.es/tools/venny/index.html
  46. Pandey SP and Somssich IE 2009 The role of WRKY transcription factors in plant immunity. Plant Physiol. 150 1648–1655 Google Scholar
  47. Patalano S, Hore TA, Reik W and Sumner S 2012 Shifting behaviour: epigenetic reprogramming in eusocial insects. Curr. Opin. Cell Biol. 24 367–373Google Scholar
  48. Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B and Mueller-Roeber B 2010 PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res. 38 D822–D827Google Scholar
  49. Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J, Hakimi MA, Lerbs-Mache S, Colot V, 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 2030–2040Google Scholar
  50. Riechmann JL and Meyerowitz EM 2002 The AP2/EREBP family of plant transcription factors. Trends Plant Sci. 7 106–111Google Scholar
  51. Rodenhiser D and Mann M 2006 Epigenetics and human disease: translating basic biology into clinical applications. CMAJ. 174 341–348PubMedCentralPubMedCrossRefGoogle Scholar
  52. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, et al. 2012 A travel guide to Cytoscape plugins. Nat. Methods 9 1069–1076Google Scholar
  53. Shankar R, Grover D, Brahmachari SK and Mukerji M 2004 Evolution and distribution of RNA polymerase II regulatory sites from RNA polymerase III dependent mobile Alu elements. BMC Evol. Biol. 4 37Google Scholar
  54. Shen H, He H, Li J, Chen W, Wang X, Guo L, Peng Z, He G, et al. 2012 Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24 875–892 PubMedCentralPubMedCrossRefGoogle Scholar
  55. Sims RJ 3rd, Nishioka K and Reinberg D 2003 Histone lysine methylation: a signature for chromatin function. Trends Genet. 19 629–639Google Scholar
  56. Staiger D, Kaulen H and Schell J 1989 A CACGTG motif of the Antirrhinum majus chalcone synthase promoter is recognized by an evolutionarily conserved nuclear protein. Proc. Natl. Acad. Sci. USA 86 6930–6934Google Scholar
  57. Wassenegger M, Heimes S, Riedel L and Sänger HL 1994 RNA-directed de novo methylation of genomic sequences in plants, Cell 76 567–76PubMedCrossRefGoogle Scholar
  58. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M and Laird PW 2005 Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res. 33 6823–6836 Google Scholar
  59. Wierzbicki AT, Ream TS, Haag JR and Pikaard CS 2009 RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41 630–634PubMedCentralPubMedCrossRefGoogle Scholar
  60. Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L and Grotewold E 2011 AGRIS: Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res. 39 D1118–D1122Google Scholar
  61. Zhang B, Pan X, Cobb GP and Anderson TA 2006 Plant microRNA: a small regulatory molecule with big impact. Dev. Biol. 289 3–16PubMedCrossRefGoogle Scholar
  62. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, et al. 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126 1189–1201PubMedCrossRefGoogle Scholar
  63. Zheng Y, Li YF, Sunkar R and Zhang W 2012 SeqTar: an effective method for identifying microRNA guided cleavage sites from degradome of polyadenylated transcripts in plants. Nucleic Acids Res. 40 e28Google Scholar

Copyright information

© Indian Academy of Sciences 2014

Authors and Affiliations

  1. 1.Studio of Computational Biology & Bioinformatics, Biotechnology DivisionCSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT)PalampurIndia

Personalised recommendations