Frontiers in Biology

, Volume 6, Issue 2, pp 133–139 | Cite as

MicroRNA-mediated DNA methylation in plants

  • Xiaoyun Jia
  • Jun Yan
  • Guiliang TangEmail author


DNA methylation, a major event in epigenetics, plays an essential role in the control of gene expression. Increasing evidence suggests that long and short non-coding RNAs are involved extensively in plants to direct the establishment, spread, and removal of DNA cytosine methylation throughout their genomes. Yet, little has been known about the role of microRNAs (miRNAs) in DNA methylation although the role of small interfering RNAs (siRNAs) in DNA methylation has been well established. Several recent studies, however, provided the evidence for miRNA-directed DNA methylation in plants, and the working mechanisms still need to be fully explored. In this review, we highlight the key features of miRNA-directed DNA methylation in plants and provide insight into the complexities of such an event in plants. The interaction between miRNAs and the epigenetic machinery and the future potential research questions are briefly discussed.


miRNA Gene miRNA Binding Site Transcriptional Gene Silence Target Gene Locus Canonical miRNAs 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ahmad A, Zhang Y, Cao X F (2010). Decoding the epigenetic language of plant development. Mol Plant, 3(4): 719–728PubMedCrossRefGoogle Scholar
  2. Axtell M J, Snyder J A, Bartel D P (2007). Common functions for diverse small RNAs of land plants. Plant Cell, 19(6): 1750–1769PubMedCrossRefGoogle Scholar
  3. Bao N, Lye K W, Barton M K (2004). MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell, 7(5): 653–662PubMedCrossRefGoogle Scholar
  4. Bartel D P (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2): 281–297PubMedCrossRefGoogle Scholar
  5. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto Y Y, Sieburth L, Voinnet O (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320(5880): 1185–1190PubMedCrossRefGoogle Scholar
  6. Cao X, Jacobsen S E (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol, 12(13): 1138–1144PubMedCrossRefGoogle Scholar
  7. Carthew R W, Sontheimer E J (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136(4): 642–655PubMedCrossRefGoogle Scholar
  8. Chan SW, Henderson I R, Jacobsen S E (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet, 6(5): 351–360PubMedCrossRefGoogle Scholar
  9. Chapman E J, Carrington J C (2007). Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet, 8(11): 884–896PubMedCrossRefGoogle Scholar
  10. Chellappan P, Xia J, Zhou X, Gao S, Zhang X, Coutino G, Vazquez F, Zhang W, Jin H (2010). siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Res, 38(20): 6883–6894PubMedCrossRefGoogle Scholar
  11. Chen X (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303(5666): 2022–2025PubMedCrossRefGoogle Scholar
  12. Chinnusamy V, Zhu J K (2009). Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol, 12(2): 133–139PubMedCrossRefGoogle Scholar
  13. Cokus S J, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild C D, Pradhan S, Nelson S F, Pellegrini M, Jacobsen S E (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452(7184): 215–219PubMedCrossRefGoogle Scholar
  14. Das S, Foley N, Bryan K, Watters K M, Bray I, Murphy D M, Buckley P G, Stallings R L (2010). MicroRNA mediates DNA demethylation events triggered by retinoic acid during neuroblastoma cell differentiation. Cancer Res, 70(20): 7874–7881PubMedCrossRefGoogle Scholar
  15. Fattash I, Voss B, Reski R, Hess W R, Frank W (2007). Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biol, 7(1): 13PubMedCrossRefGoogle Scholar
  16. Ghildiyal M, Zamore P D (2009). Small silencing RNAs: an expanding universe. Nat Rev Genet, 10(2): 94–108PubMedCrossRefGoogle Scholar
  17. Gonzalez S, Pisano D G, Serrano M (2008). Mechanistic principles of chromatin remodeling guided by siRNAs and miRNAs. Cell Cycle, 7(16): 2601–2608PubMedCrossRefGoogle Scholar
  18. Henderson I R, Jacobsen S E (2007). Epigenetic inheritance in plants. Nature, 447(7143): 418–424PubMedCrossRefGoogle Scholar
  19. Herr A J, Jensen M B, Dalmay T, Baulcombe D C (2005). RNA polymerase IV directs silencing of endogenous DNA. Science, 308(5718): 118–120PubMedCrossRefGoogle Scholar
  20. Kanno T, Huettel B, Mette M F, Aufsatz W, Jaligot E, Daxinger L, Kreil D P, Matzke M, Matzke A J (2005). Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet, 37(7): 761–765PubMedCrossRefGoogle Scholar
  21. Khraiwesh B, Arif M A, Seumel G I, Ossowski S, Weigel D, Reski R, Frank W (2010). Transcriptional control of gene expression by microRNAs. Cell, 140(1): 111–122PubMedCrossRefGoogle Scholar
  22. Kim D H, Saetrom P, Snøve O Jr, Rossi J J (2008). MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA, 105(42): 16230–16235PubMedCrossRefGoogle Scholar
  23. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crété P, Voinnet O, Robaglia C (2009). Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell, 21(6): 1762–1768PubMedCrossRefGoogle Scholar
  24. Lee Y, Jeon K, Lee J T, Kim S, Kim V N (2002). MicroRNA maturation: stepwise processing and subcellular localization. EMBO J, 21(17): 4663–4670PubMedCrossRefGoogle Scholar
  25. Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M(2009). Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell, 21(9): 2780–2796PubMedCrossRefGoogle Scholar
  26. Li C F, Pontes O, El-Shami M, Henderson I R, Bernatavichute Y V, Chan S W, Lagrange T, Pikaard C S, Jacobsen S E (2006). An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell, 126(1): 93–106PubMedCrossRefGoogle Scholar
  27. Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005). Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol, 139(1): 296–305PubMedCrossRefGoogle Scholar
  28. Llave C, Xie Z, Kasschau K D, Carrington J C (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science, 297(5589): 2053–2056PubMedCrossRefGoogle Scholar
  29. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke A J (2009). RNAmediated chromatin-based silencing in plants. Curr Opin Cell Biol, 21(3): 367–376PubMedCrossRefGoogle Scholar
  30. Onodera Y, Haag J R, Ream T, Nunes P C, Pontes O, Pikaard C S (2005). Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120(5): 613–622PubMedCrossRefGoogle Scholar
  31. Park W, Li J, Song R, Messing J, Chen X (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol, 12(17): 1484–1495PubMedCrossRefGoogle Scholar
  32. Pontes O, Costa-Nunes P, Vithayathil P, Pikaard C S (2009). RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Mol Plant, 2(4): 700–710PubMedCrossRefGoogle Scholar
  33. Qi Y, He X, Wang X J, Kohany O, Jurka J, Hannon G J (2006). Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature, 443(7114): 1008–1012PubMedCrossRefGoogle Scholar
  34. Ronemus M, Martienssen R (2005). RNA interference: methylation mystery. Nature, 433(7025): 472–473PubMedCrossRefGoogle Scholar
  35. Sunkar R, Girke T, Jain P K, Zhu J K (2005a). Cloning and characterization of microRNAs from rice. Plant Cell, 17(5): 1397–1411PubMedCrossRefGoogle Scholar
  36. Sunkar R, Girke T, Zhu J K (2005b). Identification and characterization of endogenous small interfering RNAs from rice. Nucleic Acids Res, 33(14): 4443–4454PubMedCrossRefGoogle Scholar
  37. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu J K (2008). Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol, 8(1): 25PubMedCrossRefGoogle Scholar
  38. Tang G, Reinhart B J, Bartel D P, Zamore P D (2003). A biochemical framework for RNA silencing in plants. Genes Dev, 17(1): 49–63PubMedCrossRefGoogle Scholar
  39. Vazquez F, Blevins T, Ailhas J, Boller T, Meins F Jr (2008). Evolution of Arabidopsis MIR genes generates novel microRNA classes. Nucleic Acids Res, 36(20): 6429–6438PubMedCrossRefGoogle Scholar
  40. Voinnet O (2009). Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4): 669–687PubMedCrossRefGoogle Scholar
  41. Wolffe A P, Matzke M A (1999). Epigenetics: regulation through repression. Science, 286(5439): 481–486PubMedCrossRefGoogle Scholar
  42. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009). Rice microRNA effector complexes and targets. Plant Cell, 21(11): 3421–3435PubMedCrossRefGoogle Scholar
  43. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010). DNA methylation mediated by a microRNA pathway. Mol Cell, 38(3): 465–475PubMedCrossRefGoogle Scholar
  44. Xie Z, Johansen L K, Gustafson A M, Kasschau K D, Lellis A D, Zilberman D, Jacobsen S E, Carrington J C (2004). Genetic and functional diversification of small RNA pathways in plants. PloS Biol, 2(5): E104PubMedCrossRefGoogle Scholar
  45. Xie Z, Qi X (2008). Diverse small RNA-directed silencing pathways in plants. Biochim Biophys Acta, 1779(11): 720–724PubMedGoogle Scholar
  46. Zheng B, Wang Z, Li S, Yu B, Liu J Y, Chen X (2009). Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev, 23(24): 2850–2860PubMedCrossRefGoogle Scholar
  47. Zhu Q H, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008). A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res, 18(9): 1456–1465PubMedCrossRefGoogle Scholar
  48. Zilberman D, Cao X, Jacobsen S E (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science, 299(5607): 716–719PubMedCrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.College of Life ScienceShanxi Agricultural UniversityTaiguChina
  2. 2.Gene Suppression Laboratory, Department of Plant and Soil Sciences and KTRDCUniversity of KentuckyLexingtonUSA

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