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.
Similar content being viewed by others
References
Ahmad A, Zhang Y, Cao X F (2010). Decoding the epigenetic language of plant development. Mol Plant, 3(4): 719–728
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
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
Bartel D P (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2): 281–297
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
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
Carthew R W, Sontheimer E J (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136(4): 642–655
Chan SW, Henderson I R, Jacobsen S E (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet, 6(5): 351–360
Chapman E J, Carrington J C (2007). Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet, 8(11): 884–896
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
Chen X (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303(5666): 2022–2025
Chinnusamy V, Zhu J K (2009). Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol, 12(2): 133–139
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
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
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
Ghildiyal M, Zamore P D (2009). Small silencing RNAs: an expanding universe. Nat Rev Genet, 10(2): 94–108
Gonzalez S, Pisano D G, Serrano M (2008). Mechanistic principles of chromatin remodeling guided by siRNAs and miRNAs. Cell Cycle, 7(16): 2601–2608
Henderson I R, Jacobsen S E (2007). Epigenetic inheritance in plants. Nature, 447(7143): 418–424
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Ronemus M, Martienssen R (2005). RNA interference: methylation mystery. Nature, 433(7025): 472–473
Sunkar R, Girke T, Jain P K, Zhu J K (2005a). Cloning and characterization of microRNAs from rice. Plant Cell, 17(5): 1397–1411
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
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
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
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
Voinnet O (2009). Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4): 669–687
Wolffe A P, Matzke M A (1999). Epigenetics: regulation through repression. Science, 286(5439): 481–486
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
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
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
Xie Z, Qi X (2008). Diverse small RNA-directed silencing pathways in plants. Biochim Biophys Acta, 1779(11): 720–724
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
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
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
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-011-1136-4