microRNA-directed chromatin silencing

(Tang 2005; Zofall and Grewal 2006; Aravin, Hannon et al. 2007; Brennecke, Aravin et al. 2007; Buker, Iida et al. 2007; Ding and Voinnet 2007; Brennecke, Malone et al. 2008; Hutvagner and Simard 2008; White and Allshire 2008; Csorba, Pantaleo et al. 2009; David-Rus, Mukhopadhyay et al. 2009; Braun, Cannella et al. 2010; Chellappan, Xia et al. 2010; Grewal 2010; Mukhopadhyay, Nagaraj et al. 2010; Djuranovic, Nahvi et al. 2011; Gagnon and Corey 2012; Huang and Li 2012; Wu, Mao et al. 2012; Zhang and Zhu 2012; Handler, Meixner et al. 2013).

Table 1. Genome immunity by microRNA targeting of mobile DNA

(see also http://shapiro.bsd.uchicago.edu/TableII.9.shtml for earlier references).


microRNA targets



Transposable elements

(Rigal and Mathieu 2011; Ng, Lu et al. 2012; Nuthikattu, McCue et al. 2013)



(Mirouze, Reinders et al. 2009; Slotkin 2010)



(Tian, Yu et al. 2011)



(Zhang, Ge et al. 2013)


Transposable elements

(McCue, Nuthikattu et al. 2012)


Transposable elements

(Barber, Zhang et al. 2012; He, Chen et al. 2013)


Viruses and viroids

(Navarro, Pantaleo et al. 2009; Pantaleo 2011; Zhu and Guo 2012; Ramesh, Ratnaparkhe et al. 2014)

Rice, tobacco and Laodelphgax striatellus insect vector

Rice stripe virus

(Xu, Huang et al. 2012)



(Vanitharani, Chellappan et al. 2005; Raja, Jackel et al. 2013)

Caenorhabditis elegans germ-line


(Sijen and Plasterk 2003; Buckley, Burkhart et al. 2012; Lee, Gu et al. 2012)



(van Rij, Saleh et al. 2006)

Drosophila somatic cells


(Kawamura, Saito et al. 2008)

Drosophila male germ-line


(Kalmykova, Klenov et al. 2005)

Drosophila female germ-line

Transposons, retrotransposons and retroviruses

(Brennecke, Aravin et al. 2007; Brennecke, Malone et al. 2008)

Drosophila female germ-line

Telomeric retrotransposons

(Shpiz, Kwon et al. 2009)

Drosophila gonads


(Sienski, Donertas et al. 2012)

Drosophila somatic and germ-line cells

Transposons, retrotransposons and retroviruses

(Handler, Meixner et al. 2013)

Drosophila tissue culture cells


(Chung, Okamura et al. 2008)


White spot syndrome DNA virus

(Huang and Zhang 2013; Sabin and Cherry 2013)

Mammalian cells

EMCV and NoV RNA viruses

(Maillard, Ciaudo et al. 2013)

Human tissue culture cells

LINE retrotransposons

(Yang and Kazazian 2006)




Aravin, A. A., G. J. Hannon, et al. (2007). "The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race." Science 318(5851): 761-764. http://www.ncbi.nlm.nih.gov/pubmed/17975059.

Barber, W. T., W. Zhang, et al. (2012). "Repeat associated small RNAs vary among parents and following hybridization in maize." Proc Natl Acad Sci U S A 109(26): 10444-10449. http://www.ncbi.nlm.nih.gov/pubmed/22689990.

Braun, L., D. Cannella, et al. (2010). "A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii." PLoS Pathog 6(5): e1000920. http://www.ncbi.nlm.nih.gov/pubmed/20523899.

Brennecke, J., A. A. Aravin, et al. (2007). "Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila." Cell 128(6): 1089-1103. http://www.ncbi.nlm.nih.gov/pubmed/17346786.

Brennecke, J., C. D. Malone, et al. (2008). "An epigenetic role for maternally inherited piRNAs in transposon silencing." Science 322(5906): 1387-1392. http://www.ncbi.nlm.nih.gov/pubmed/19039138.

Buckley, B. A., K. B. Burkhart, et al. (2012). "A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality." Nature. http://www.ncbi.nlm.nih.gov/pubmed/22810588.

Buker, S. M., T. Iida, et al. (2007). "Two different Argonaute complexes are required for siRNA generation and heterochromatin assembly in fission yeast." Nat Struct Mol Biol 14(3): 200-207. http://www.ncbi.nlm.nih.gov/pubmed/17310250.

Chellappan, P., J. Xia, et al. (2010). "siRNAs from miRNA sites mediate DNA methylation of target genes." Nucleic Acids Res\. http://www.ncbi.nlm.nih.gov/pubmed/20621980%22.

Chung, W. J., K. Okamura, et al. (2008). "Endogenous RNA interference provides a somatic defense against Drosophila transposons." Curr Biol 18(11): 795-802. http://www.ncbi.nlm.nih.gov/pubmed/18501606.

Csorba, T., V. Pantaleo, et al. (2009). "RNA silencing: an antiviral mechanism." Adv Virus Res 75: 35-71. http://www.ncbi.nlm.nih.gov/pubmed/20109663.

David-Rus, D., S. Mukhopadhyay, et al. (2009). "Inheritance of epigenetic chromatin silencing." J Theor Biol 258(1): 112-120. http://www.ncbi.nlm.nih.gov/pubmed/19174167.

Ding, S. W. and O. Voinnet (2007). "Antiviral immunity directed by small RNAs." Cell 130(3): 413-426. http://www.ncbi.nlm.nih.gov/pubmed/17693253.

Djuranovic, S., A. Nahvi, et al. (2011). "A Parsimonious Model for Gene Regulation by miRNAs." Science 331(6017): 550-553. .

Gagnon, K. T. and D. R. Corey (2012). "Argonaute and the nuclear RNAs: new pathways for RNA-mediated control of gene expression." Nucleic Acid Ther 22(1): 3-16. http://www.ncbi.nlm.nih.gov/pubmed/22283730.

Grewal, S. I. (2010). "RNAi-dependent formation of heterochromatin and its diverse functions." Curr Opin Genet Dev 20(2): 134-141. http://www.ncbi.nlm.nih.gov/pubmed/20207534.

Handler, D., K. Meixner, et al. (2013). "The Genetic Makeup of the Drosophila piRNA Pathway." Mol Cell 50(5): 762-777. http://www.ncbi.nlm.nih.gov/pubmed/23665231.

He, G., B. Chen, et al. (2013). "Conservation and divergence of transcriptomic and epigenomic variation in maize hybrids." Genome Biol 14(6): R57. http://www.ncbi.nlm.nih.gov/pubmed/23758703.

Huang, T. and X. Zhang (2013). "Host defense against DNA virus infection in shrimp is mediated by the siRNA pathway." Eur J Immunol 43(1): 137-146. http://www.ncbi.nlm.nih.gov/pubmed/23065729.

Huang, V. and L. C. Li (2012). "miRNA goes nuclear." RNA Biol 9(3): 269-273. http://www.ncbi.nlm.nih.gov/pubmed/22336708.

Hutvagner, G. and M. J. Simard (2008). "Argonaute proteins: key players in RNA silencing." Nat Rev Mol Cell Biol 9(1): 22-32. http://www.ncbi.nlm.nih.gov/pubmed/18073770.

Kalmykova, A. I., M. S. Klenov, et al. (2005). "Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline." Nucleic Acids Res 33(6): 2052-2059. http://www.ncbi.nlm.nih.gov/pubmed/15817569.

Kawamura, Y., K. Saito, et al. (2008). "Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells." Nature 453(7196): 793-797. http://www.ncbi.nlm.nih.gov/pubmed/18463636.

Lee, H. C., W. Gu, et al. (2012). "C. elegans piRNAs Mediate the Genome-wide Surveillance of Germline Transcripts." Cell 150(1): 78-87. http://www.ncbi.nlm.nih.gov/pubmed/22738724.

Maillard, P. V., C. Ciaudo, et al. (2013). "Antiviral RNA interference in mammalian cells." Science 342(6155): 235-238. http://www.ncbi.nlm.nih.gov/pubmed/24115438.

McCue, A. D., S. Nuthikattu, et al. (2012). "Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA." PLoS Genet 8(2): e1002474. http://www.ncbi.nlm.nih.gov/pubmed/22346759.

Mirouze, M., J. Reinders, et al. (2009). "Selective epigenetic control of retrotransposition in Arabidopsis." Nature 461(7262): 427-430. http://www.ncbi.nlm.nih.gov/pubmed/19734882.

Mukhopadhyay, S., V. H. Nagaraj, et al. (2010). "Locus dependence in epigenetic chromatin silencing." Biosystems 102(1): 49-54. http://www.ncbi.nlm.nih.gov/pubmed/20655355.

Navarro, B., V. Pantaleo, et al. (2009). "Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction." PLoS One 4(11): e7686. http://www.ncbi.nlm.nih.gov/pubmed/19890399.

Ng, D. W., J. Lu, et al. (2012). "Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility." Curr Opin Plant Biol 15(2): 154-161. http://www.ncbi.nlm.nih.gov/pubmed/22326630.

Nuthikattu, S., A. D. McCue, et al. (2013). "The Initiation of Epigenetic Silencing of Active Transposable Elements Is Triggered by RDR6 and 21-22 Nucleotide Small Interfering RNAs." Plant Physiol 162(1): 116-131. http://www.ncbi.nlm.nih.gov/pubmed/23542151.

Pantaleo, V. (2011). "Plant RNA silencing in viral defence." Adv Exp Med Biol 722: 39-58. http://www.ncbi.nlm.nih.gov/pubmed/21915781.

Raja, P., J. N. Jackel, et al. (2013). "Arabidopsis Double-Stranded RNA Binding Protein DRB3 Participates in Methylation-Mediated Defense against Geminiviruses." J Virol. http://www.ncbi.nlm.nih.gov/pubmed/24352449.

Ramesh, S. V., M. B. Ratnaparkhe, et al. (2014). "Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges." Virus Genes. http://www.ncbi.nlm.nih.gov/pubmed/24445902.

Rigal, M. and O. Mathieu (2011). "A "mille-feuille" of silencing: epigenetic control of transposable elements." Biochim Biophys Acta 1809(8): 452-458. http://www.ncbi.nlm.nih.gov/pubmed/21514406.

Sabin, L. R. and S. Cherry (2013). "Small creatures use small RNAs to direct antiviral defenses." Eur J Immunol 43(1): 27-33. http://www.ncbi.nlm.nih.gov/pubmed/23322691.

Shpiz, S., D. Kwon, et al. (2009). "rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus." Nucleic Acids Res 37(1): 268-278. http://www.ncbi.nlm.nih.gov/pubmed/19036789.

Sienski, G., D. Donertas, et al. (2012). "Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression." Cell 151(5): 964-980. http://www.ncbi.nlm.nih.gov/pubmed/23159368.

Sijen, T. and R. H. Plasterk (2003). "Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi." Nature\ 426\(6964\): 310-314\. http://www.ncbi.nlm.nih.gov/pubmed/14628056%22.

Slotkin, R. K. (2010). "The epigenetic control of the Athila family of retrotransposons in Arabidopsis." Epigenetics 5(6): 483-490. http://www.ncbi.nlm.nih.gov/pubmed/20484989.

Tang, G. (2005). "siRNA and miRNA: an insight into RISCs." Trends Biochem Sci 30(2): 106-114. http://www.ncbi.nlm.nih.gov/pubmed/15691656.

Tian, Z., Y. Yu, et al. (2011). "Exceptional lability of a genomic complex in rice and its close relatives revealed by interspecific and intraspecific comparison and population analysis." BMC Genomics 12: 142. http://www.ncbi.nlm.nih.gov/pubmed/21385395.

van Rij, R. P., M. C. Saleh, et al. (2006). "The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster." Genes Dev 20(21): 2985-2995. http://www.ncbi.nlm.nih.gov/pubmed/17079687.

Vanitharani, R., P. Chellappan, et al. (2005). "Geminiviruses and RNA silencing." Trends Plant Sci 10(3): 144-151. http://www.ncbi.nlm.nih.gov/pubmed/15749473.

White, S. A. and R. C. Allshire (2008). "RNAi-mediated chromatin silencing in fission yeast." Curr Top Microbiol Immunol 320: 157-183. http://www.ncbi.nlm.nih.gov/pubmed/18268844.

Wu, L., L. Mao, et al. (2012). "Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation." Plant Physiol 160(2): 990-999. http://www.ncbi.nlm.nih.gov/pubmed/22846193.

Xu, Y., L. Huang, et al. (2012). "Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus." PLoS One 7(9): e46238. http://www.ncbi.nlm.nih.gov/pubmed/23029445.

Yang, N. and H. H. Kazazian, Jr. (2006). "L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells." Nat Struct Mol Biol 13(9): 763-771. http://www.ncbi.nlm.nih.gov/pubmed/16936727.

Zhang, H. and J. K. Zhu (2012). "Seeing the forest for the trees: a wide perspective on RNA-directed DNA methylation." Genes Dev 26(16): 1769-1773. http://www.ncbi.nlm.nih.gov/pubmed/22895250.

Zhang, X., X. Ge, et al. (2013). "Genomic change, retrotransposon mobilization and extensive cytosine methylation alteration in Brassica napus introgressions from two intertribal hybridizations." PLoS One 8(2): e56346. http://www.ncbi.nlm.nih.gov/pubmed/23468861.

Zhu, H. and H. Guo (2012). "The role of virus-derived small interfering RNAs in RNA silencing in plants." Sci China Life Sci 55(2): 119-125. http://www.ncbi.nlm.nih.gov/pubmed/22415682.

Zofall, M. and S. I. Grewal (2006). "RNAi-mediated heterochromatin assembly in fission yeast." Cold Spring Harb Symp Quant Biol 71: 487-496. http://www.ncbi.nlm.nih.gov/pubmed/17381331.