MicroRNA-mediated DNA methylation in plants

Abstract

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.

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References

  1. Ahmad A, Zhang Y, Cao X F (2010). Decoding the epigenetic language of plant development. Mol Plant, 3(4): 719–728

    PubMed  Article  CAS  Google 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): 1750–1769

    PubMed  Article  CAS  Google 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): 653–662

    PubMed  Article  CAS  Google Scholar 

  4. Bartel D P (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2): 281–297

    PubMed  Article  CAS  Google 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): 1185–1190

    PubMed  Article  CAS  Google 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): 1138–1144

    PubMed  Article  CAS  Google Scholar 

  7. Carthew R W, Sontheimer E J (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136(4): 642–655

    PubMed  Article  CAS  Google Scholar 

  8. Chan SW, Henderson I R, Jacobsen S E (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet, 6(5): 351–360

    PubMed  Article  CAS  Google Scholar 

  9. Chapman E J, Carrington J C (2007). Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet, 8(11): 884–896

    PubMed  Article  CAS  Google 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): 6883–6894

    PubMed  Article  CAS  Google Scholar 

  11. Chen X (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303(5666): 2022–2025

    PubMed  Article  CAS  Google Scholar 

  12. Chinnusamy V, Zhu J K (2009). Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol, 12(2): 133–139

    PubMed  Article  CAS  Google 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): 215–219

    PubMed  Article  CAS  Google 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): 7874–7881

    PubMed  Article  CAS  Google 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): 13

    PubMed  Article  Google Scholar 

  16. Ghildiyal M, Zamore P D (2009). Small silencing RNAs: an expanding universe. Nat Rev Genet, 10(2): 94–108

    PubMed  Article  CAS  Google Scholar 

  17. Gonzalez S, Pisano D G, Serrano M (2008). Mechanistic principles of chromatin remodeling guided by siRNAs and miRNAs. Cell Cycle, 7(16): 2601–2608

    PubMed  Article  CAS  Google Scholar 

  18. Henderson I R, Jacobsen S E (2007). Epigenetic inheritance in plants. Nature, 447(7143): 418–424

    PubMed  Article  CAS  Google 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): 118–120

    PubMed  Article  CAS  Google 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): 761–765

    PubMed  Article  CAS  Google 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): 111–122

    PubMed  Article  CAS  Google 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): 16230–16235

    PubMed  Article  CAS  Google 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): 1762–1768

    PubMed  Article  CAS  Google 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): 4663–4670

    PubMed  Article  CAS  Google 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): 2780–2796

    PubMed  Article  CAS  Google 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): 93–106

    PubMed  Article  CAS  Google 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): 296–305

    PubMed  Article  CAS  Google 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): 2053–2056

    PubMed  Article  CAS  Google 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): 367–376

    PubMed  Article  CAS  Google 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): 613–622

    PubMed  Article  CAS  Google 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): 1484–1495

    PubMed  Article  CAS  Google 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): 700–710

    PubMed  Article  CAS  Google 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): 1008–1012

    PubMed  Article  Google Scholar 

  34. Ronemus M, Martienssen R (2005). RNA interference: methylation mystery. Nature, 433(7025): 472–473

    PubMed  Article  CAS  Google Scholar 

  35. Sunkar R, Girke T, Jain P K, Zhu J K (2005a). Cloning and characterization of microRNAs from rice. Plant Cell, 17(5): 1397–1411

    PubMed  Article  CAS  Google 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): 4443–4454

    PubMed  Article  CAS  Google 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): 25

    PubMed  Article  Google 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): 49–63

    PubMed  Article  CAS  Google 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): 6429–6438

    PubMed  Article  CAS  Google Scholar 

  40. Voinnet O (2009). Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4): 669–687

    PubMed  Article  CAS  Google Scholar 

  41. Wolffe A P, Matzke M A (1999). Epigenetics: regulation through repression. Science, 286(5439): 481–486

    PubMed  Article  CAS  Google 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): 3421–3435

    PubMed  Article  CAS  Google 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): 465–475

    PubMed  Article  CAS  Google 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): E104

    PubMed  Article  Google Scholar 

  45. Xie Z, Qi X (2008). Diverse small RNA-directed silencing pathways in plants. Biochim Biophys Acta, 1779(11): 720–724

    PubMed  CAS  Google 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): 2850–2860

    PubMed  Article  CAS  Google 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): 1456–1465

    PubMed  Article  CAS  Google 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): 716–719

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Guiliang Tang.

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Jia, X., Yan, J. & Tang, G. MicroRNA-mediated DNA methylation in plants. Front. Biol. 6, 133–139 (2011). https://doi.org/10.1007/s11515-011-1136-4

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Keywords

  • miRNA Gene
  • miRNA Binding Site
  • Transcriptional Gene Silence
  • Target Gene Locus
  • Canonical miRNAs