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RNA Interference-Mediated Intrinsic Antiviral Immunity in Plants

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Book cover Intrinsic Immunity

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 371))

Abstract

RNA interference (RNAi) is an evolutionarily conserved, sequence-specific gene-inactivation system that plays an essential role in many biological processes, such as genome defense against mobile DNA elements or regulation of factors involved in plant and animal development. In higher plants and invertebrates, it also functions as a powerful antiviral mechanism. To overcome antiviral RNAi, viruses have evolved suppressor proteins which counteract host RNAi-based antiviral processes and target one or more key points in the RNAi machinery. Here, we review recent progress in our understanding of the mechanism and function of antiviral RNAi in plants and on the viral responses through the expression of silencing suppressor proteins. As a counter-attack RNAi may also regulate innate immunity in plants and contribute to a novel layer of defense against pathogen attack. We also discuss emerging evidence that viruses use RNAi to manipulate host gene expression to modify the cellular environment for the benefit of invading viruses.

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References

  • Ahlquist P (2002) RNA-dependent RNA polymerases, viruses, and RNA silencing. Science 296:1270–1273

    PubMed  CAS  Google Scholar 

  • Akbergenov R, Si-Ammour A, Blevins T, Amin I, Kutter C, Vanderschuren H, Zhang P, Gruissem W, Meins F Jr, Hohn T, Pooggin MM (2006) Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res 34:462–471

    PubMed  CAS  Google Scholar 

  • Al-Kaff NS, Covey SN, Kreike MM, Page AM, Pinder R, Dale PJ (1998) Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science 279:2113–2115

    PubMed  CAS  Google Scholar 

  • Almeida R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 15:251–258

    PubMed  CAS  Google Scholar 

  • Ameres SL, Martinez J, Schroeder R (2007) Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130:101–112

    PubMed  CAS  Google Scholar 

  • Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95:13079–13084

    PubMed  CAS  Google Scholar 

  • Aregger M, Borah BK, Seguin J, Rajeswaran R, Gubaeva EG, Zvereva AS, Windels D, Vazquez F, Blevins T, Farinelli L, Pooggin MM (2012) Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathog 8:e1002941

    PubMed  Google Scholar 

  • Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, Garcia S, Braun L, Bergdoll M, Hakimi MA, Lagrange T, Voinnet O (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev 24:904–915

    PubMed  CAS  Google Scholar 

  • Bao H, Guo H, Wang J, Zhou R, Lu X, Shi S (2009) MapView: visualization of short reads alignment on a desktop computer. Bioinformatics 25:1554–1555

    PubMed  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    PubMed  CAS  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    PubMed  CAS  Google Scholar 

  • Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC (2007) The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 17:1609–1614

    PubMed  CAS  Google Scholar 

  • Becker A, Lange M (2010) VIGS–genomics goes functional. Trends Plant Sci 15:1–4

    PubMed  CAS  Google Scholar 

  • Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20:1885–1898

    PubMed  CAS  Google Scholar 

  • Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366

    PubMed  CAS  Google Scholar 

  • Bhattacharjee S, Zamora A, Azhar MT, Sacco MA, Lambert LH, Moffett P (2009) Virus resistance induced by NB-LRR proteins involves Argonaute4-dependent translational control. Plant J 58:940–951

    PubMed  CAS  Google Scholar 

  • Bies-Etheve N, Pontier D, Lahmy S, Picart C, Vega D, Cooke R, Lagrange T (2009) RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep 10:649–654

    PubMed  CAS  Google Scholar 

  • Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park HS, Vazquez F, Robertson D, Meins F Jr, Hohn T, Pooggin MM (2006) Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246

    PubMed  CAS  Google Scholar 

  • Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M, Baerlocher L, Farinelli L, Meins F Jr, Hohn T, Pooggin MM (2011) Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res 39:5003–5014

    PubMed  CAS  Google Scholar 

  • Bortolamiol D, Pazhouhandeh M, Marrocco K, Genschik P, Ziegler-Graff V (2007) The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr Biol 17:1615–1621

    PubMed  CAS  Google Scholar 

  • Bouche N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25:3347–3356

    PubMed  CAS  Google Scholar 

  • Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17:6739–6746

    PubMed  CAS  Google Scholar 

  • Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280

    PubMed  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    PubMed  CAS  Google Scholar 

  • Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83:5005–5013

    PubMed  CAS  Google Scholar 

  • Buhler M, Verdel A, Moazed D (2006) Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 125:873–886

    PubMed  CAS  Google Scholar 

  • Burgyan J, Havelda Z (2011) Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272

    PubMed  CAS  Google Scholar 

  • Burgyan J, Rubino L, Russo M (1996) The 5′-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. J Gen Virol 77:1967–1974

    PubMed  CAS  Google Scholar 

  • Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA, Nguyen T, Cuperus JT, Carrington JC (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:3613–3629

    PubMed  CAS  Google Scholar 

  • Chao JA, Lee JH, Chapados BR, Debler EW, Schneemann A, Williamson JR (2005) Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nat Struct Mol Biol 12:952–957

    PubMed  CAS  Google Scholar 

  • Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896

    PubMed  CAS  Google Scholar 

  • Chapman EJ, Prokhnevsky AI, Gopinath K, Dolja VV, Carrington JC (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18:1179–1186

    PubMed  CAS  Google Scholar 

  • Chellappan P, Vanitharani R, Fauquet CM (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. Proc Natl Acad Sci U S A 102:10381–10386

    PubMed  CAS  Google Scholar 

  • Chen HY, Yang J, Lin C, Yuan YA (2008) Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep 9:754–760

    PubMed  CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    PubMed  CAS  Google Scholar 

  • Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554

    PubMed  CAS  Google Scholar 

  • Csorba T, Bovi A, Dalmay T, Burgyan J (2007) The p122 subunit of Tobacco Mosaic Virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J Virol 81:11768–11780

    PubMed  CAS  Google Scholar 

  • Csorba T, Pantaleo V, Burgyan J (2009) RNA silencing: an antiviral mechanism. Adv Virus Res 75:35–71

    PubMed  CAS  Google Scholar 

  • Csorba T, Lozsa R, Hutvagner G, Burgyan J (2010) Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J 62:463–472

    PubMed  CAS  Google Scholar 

  • Cuellar WJ, Kreuze JF, Rajamaki ML, Cruzado KR, Untiveros M, Valkonen JP (2009) Elimination of antiviral defense by viral RNase III. Proc Natl Acad Sci U S A 106:10354–10358

    PubMed  Google Scholar 

  • Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553

    PubMed  CAS  Google Scholar 

  • Dalmay T, Horsefield R, Braunstein TH, Baulcombe DC (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20:2069–2078

    PubMed  CAS  Google Scholar 

  • Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68–71

    PubMed  CAS  Google Scholar 

  • Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci U S A 109:15942–15946

    PubMed  CAS  Google Scholar 

  • Diaz-Pendon JA, Ding SW (2008) Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu Rev Phytopathol 46:303–326

    PubMed  CAS  Google Scholar 

  • Diaz-Pendon JA, Li F, Li WX, Ding SW (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:2053–2063

    PubMed  CAS  Google Scholar 

  • Ding SW (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644

    PubMed  CAS  Google Scholar 

  • Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426

    PubMed  CAS  Google Scholar 

  • Donaire L, Barajas D, Martinez-Garcia B, Martinez-Priego L, Pagan I, Llave C (2008) Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J Virol 82:5167–5177

    PubMed  CAS  Google Scholar 

  • Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214

    PubMed  CAS  Google Scholar 

  • Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16:1235–1250

    PubMed  CAS  Google Scholar 

  • Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–916

    PubMed  CAS  Google Scholar 

  • Eamens A, Vaistij FE, Jones L (2008) NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J 55:596–606

    PubMed  CAS  Google Scholar 

  • Ebhardt HA, Thi EP, Wang MB, Unrau PJ (2005) Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc Natl Acad Sci U S A 102:13398–13403

    PubMed  CAS  Google Scholar 

  • El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, Hakimi MA, Jacobsen SE, Cooke R, Lagrange T (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21:2539–2544

    PubMed  CAS  Google Scholar 

  • Eulalio A, Huntzinger E, Izaurralde E (2008) GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat Struct Mol Biol 15:346–353

    PubMed  CAS  Google Scholar 

  • Fukunaga R, Doudna JA (2009) dsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J 28:545–555

    PubMed  CAS  Google Scholar 

  • Fusaro AF, Matthew L, Smith NA, Curtin SJ, Dedic-Hagan J, Ellacott GA, Watson JM, Wang MB, Brosnan C, Carroll BJ, Waterhouse PM (2006) RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep 7:1168–1175

    PubMed  CAS  Google Scholar 

  • Fusaro AF, Correa RL, Nakasugi K, Jackson C, Kawchuk L, Vaslin MF, Waterhouse PM (2012) The Enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing through AGO1 degradation. Virology 426:178–187

    PubMed  CAS  Google Scholar 

  • Garcia D, Garcia S, Pontier D, Marchais A, Renou JP, Lagrange T, Voinnet O (2012) Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol Cell 48:109–120

    PubMed  CAS  Google Scholar 

  • Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22:481–496

    PubMed  CAS  Google Scholar 

  • Gerik JS, Duffus JE, Perry R, Stenger DC, Van Maren AF (1990) Etiology of tomato plant decline in the California desert. Phytopathology 80:1352–1356

    Google Scholar 

  • Giner A, Lakatos L, Garcia-Chapa M, Lopez-Moya JJ, Burgyan J (2010) Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog 6:e1000996

    PubMed  Google Scholar 

  • Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, Belausov E, Citovsky V, Gafni Y (2008) Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci U S A 105:157–161

    PubMed  CAS  Google Scholar 

  • Goto K, Kobori T, Kosaka Y, Natsuaki T, Masuta C (2007) Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol 48:1050–1060

    PubMed  CAS  Google Scholar 

  • Guo HS, Ding SW (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21:398–407

    PubMed  CAS  Google Scholar 

  • Haas G, Azevedo J, Moissiard G, Geldreich A, Himber C, Bureau M, Fukuhara T, Keller M, Voinnet O (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 27:2102–2112

    PubMed  CAS  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    PubMed  CAS  Google Scholar 

  • Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296

    PubMed  CAS  Google Scholar 

  • Harvey JJ, Lewsey MG, Patel K, Westwood J, Heimstadt S, Carr JP, Baulcombe DC (2011) An antiviral defense role of AGO2 in plants. PLoS ONE 6:e14639

    PubMed  CAS  Google Scholar 

  • He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, Liu HL, Wang CS, Jin H, Zhu JK (2009) An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137:498–508

    PubMed  CAS  Google Scholar 

  • Hine RB, Osborne WE, Dennis RE (1970) Elevation and temperature effects on severity of maize dwarf mosaic virus in sorghum in Arizona. Plant Disease Reporter 54:1064–1068

    Google Scholar 

  • Ho T, Pallett D, Rusholme R, Dalmay T, Wang H (2006) A simplified method for cloning of short interfering RNAs from Brassica juncea infected with Turnip mosaic potyvirus and Turnip crinkle carmovirus. J Virol Methods 136:217–223

    PubMed  CAS  Google Scholar 

  • Hull R (2002) Matthews’ Plant Virology, 4th edn. Academic Press, San Diego

    Google Scholar 

  • Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32

    PubMed  CAS  Google Scholar 

  • Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39:282–291

    PubMed  CAS  Google Scholar 

  • Iki T, Yoshikawa M, Meshi T, Ishikawa M (2011) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J 31:267–278

    PubMed  Google Scholar 

  • Itaya A, Zhong X, Bundschuh R, Qi Y, Wang Y, Takeda R, Harris AR, Molina C, Nelson RS, Ding B (2007) A structured viroid RNA serves as a substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complex-mediated degradation. J Virol 81:2980–2994

    PubMed  CAS  Google Scholar 

  • Jaubert M, Bhattacharjee S, Mello AF, Perry KL, Moffett P (2011) ARGONAUTE2 mediates RNA-silencing antiviral defenses against Potato virus X in Arabidopsis. Plant Physiol 156:1556–1564

    PubMed  CAS  Google Scholar 

  • Jay F, Wang Y, Yu A, Taconnat L, Pelletier S, Colot V, Renou JP, Voinnet O (2011) Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog 7:e1002035

    PubMed  CAS  Google Scholar 

  • Johnson J (1922) The relation of air temperature to the mosaic disease of potatoes and other plants. Phytopathology 12:438–440

    Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    PubMed  CAS  Google Scholar 

  • Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11:2291–2301

    PubMed  CAS  Google Scholar 

  • Jones L, Ratcliff F, Baulcombe DC (2001) RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 11:747–757

    PubMed  CAS  Google Scholar 

  • Karlowski WM, Zielezinski A, Carrere J, Pontier D, Lagrange T, Cooke R (2010) Genome-wide computational identification of WG/GW Argonaute-binding proteins in Arabidopsis. Nucleic Acids Res 38:4231–4245

    PubMed  CAS  Google Scholar 

  • Kasschau KD, Carrington JC (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470

    PubMed  CAS  Google Scholar 

  • Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev Cell 4:205–217

    PubMed  CAS  Google Scholar 

  • Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R, Watanabe Y (2009) SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett 583:1261–1266

    PubMed  CAS  Google Scholar 

  • Lakatos L, Szittya G, Silhavy D, Burgyan J (2004) Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J 23:876–884 Epub 2004 Feb 2019

    PubMed  CAS  Google Scholar 

  • Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, Liu YP, Dolja VV, Calvino LF, Lopez-Moya JJ, Burgyan J (2006) Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J 25:2768–2780

    PubMed  CAS  Google Scholar 

  • Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crete P, Voinnet O, Robaglia C (2009) Biochemical Evidence for Translational Repression by Arabidopsis MicroRNAs. Plant Cell 21:1762–1768

    PubMed  CAS  Google Scholar 

  • Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 15:1501–1507

    PubMed  CAS  Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci U S A 109:1790–1795

    PubMed  CAS  Google Scholar 

  • Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–1441

    PubMed  CAS  Google Scholar 

  • Liu J, Rivas FV, Wohlschlegel J, Yates JR 3rd, Parker R, Hannon GJ (2005) A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7:1261–1266

    PubMed  Google Scholar 

  • Llave C (2010) Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci 15:701–707

    PubMed  CAS  Google Scholar 

  • Love AJ, Laird J, Holt J, Hamilton AJ, Sadanandom A, Milner JJ (2007) Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J Gen Virol 88:3439–3444

    PubMed  CAS  Google Scholar 

  • Lozsa R, Csorba T, Lakatos L, Burgyan J (2008) Inhibition of 3′ modification of small RNAs in virus-infected plants require spatial and temporal co-expression of small RNAs and viral silencing-suppressor proteins. Nucleic Acids Res 36:4099–4107

    PubMed  CAS  Google Scholar 

  • Mallory AC, Reinhart BJ, Bartel D, Vance VB, Bowman LH (2002) A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc Natl Acad Sci U S A 99:15228–15233

    PubMed  CAS  Google Scholar 

  • Manganaris GA, Economou AS, Boubourakas IN, Katis NI (2003) Elimination of PPV and PNRSV through thermotherapy and meristem-tip culture in nectarine. Plant Cell Rep 22:195–200

    PubMed  CAS  Google Scholar 

  • Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376

    PubMed  CAS  Google Scholar 

  • Mayers CN, Palukaitis P, Carr JP (2000) Subcellular distribution analysis of the cucumber mosaic virus 2b protein. J Gen Virol 81:219–226

    PubMed  CAS  Google Scholar 

  • Mayo MA, Ziegler-Graff V (1996) Molecular biology of luteoviruses. Adv Virus Res 46:413–460

    PubMed  CAS  Google Scholar 

  • Merai Z, Kerenyi Z, Molnar A, Barta E, Valoczi A, Bisztray G, Havelda Z, Burgyan J, Silhavy D (2005) Aureusvirus P14 is an efficient RNA silencing suppressor that binds double-stranded RNAs without size specificity. J Virol 79:7217–7226

    PubMed  CAS  Google Scholar 

  • Merai Z, Kerenyi Z, Kertesz S, Magna M, Lakatos L, Silhavy D (2006) Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J Virol 80:5747–5756

    PubMed  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    PubMed  CAS  Google Scholar 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    PubMed  CAS  Google Scholar 

  • Miozzi L, Gambino G, Burgyan J, Pantaleo V (2013) Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol Plant Pathol 14:30–43

    PubMed  CAS  Google Scholar 

  • Moissiard G, Voinnet O (2006) RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins. Proc Natl Acad Sci U S A 103:19593–19598

    PubMed  CAS  Google Scholar 

  • Molnar A, Csorba T, Lakatos L, Varallyay E, Lacomme C, Burgyan J (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79:7812–7818

    PubMed  CAS  Google Scholar 

  • Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–639

    PubMed  CAS  Google Scholar 

  • Navarro B, Pantaleo V, Gisel A, Moxon S, Dalmay T, Bisztray G, Di Serio F, Burgyan J (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:e7686

    PubMed  Google Scholar 

  • Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F (2012) Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J 70:991–1003

    PubMed  CAS  Google Scholar 

  • Omarov RT, Ciomperlik JJ, Scholthof HB (2007) RNAi-associated ssRNA-specific ribonucleases in Tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc Natl Acad Sci U S A 104:1714–1719

    PubMed  CAS  Google Scholar 

  • Pantaleo V, Szittya G, Burgyan J (2007) Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J Virol 81:3797–3806

    PubMed  CAS  Google Scholar 

  • Pantaleo V, Saldarelli P, Miozzi L, Giampetruzzi A, Gisel A, Moxon S, Dalmay T, Bisztray G, Burgyan J (2010) Deep sequencing analysis of viral short RNAs from an infected Pinot Noir grapevine. Virology 408:49–56

    PubMed  CAS  Google Scholar 

  • Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 102:3691–3696

    PubMed  CAS  Google Scholar 

  • Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, Hemmer O, Kretsch T, Richards KE, Genschik P, Ziegler-Graff V (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci U S A 103:1994–1999

    PubMed  CAS  Google Scholar 

  • Pfeffer S, Dunoyer P, Heim F, Richards KE, Jonard G, Ziegler-Graff V (2002) P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. J Virol 76:6815–6824

    PubMed  CAS  Google Scholar 

  • Pham JW, Pellino JL, Lee YS, Carthew RW, Sontheimer EJ (2004) A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117:83–94

    PubMed  CAS  Google Scholar 

  • Qi X, Bao FS, Xie Z (2009) Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLoS ONE 4:e4971

    PubMed  Google Scholar 

  • Qu F (2010) Antiviral role of plant-encoded RNA-dependent RNA polymerases revisited with deep sequencing of small interfering RNAs of virus origin. Mol Plant Microbe Interact 23:1248–1252

    PubMed  CAS  Google Scholar 

  • Qu F, Ye X, Hou G, Sato S, Clemente TE, Morris TJ (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J Virol 79:15209–15217

    PubMed  CAS  Google Scholar 

  • Qu F, Ye X, Morris TJ (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A 105:14732–14737

    PubMed  CAS  Google Scholar 

  • Raja P, Sanville BC, Buchmann RC, Bisaro DM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82:8997–9007

    PubMed  CAS  Google Scholar 

  • Ratcliff F, Harrison BD, Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276:1558–1560

    PubMed  CAS  Google Scholar 

  • Ratcliff FG, MacFarlane SA, Baulcombe DC (1999) Gene silencing without DNA. rna-mediated cross-protection between viruses. Plant Cell 11:1207–1216

    PubMed  CAS  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    PubMed  CAS  Google Scholar 

  • Scholthof HB, Alvarado VY, Vega-Arreguin JC, Ciomperlik J, Odokonyero D, Brosseau C, Jaubert M, Zamora A, Moffett P (2011) Identification of an ARGONAUTE for antiviral RNA silencing in Nicotiana benthamiana. Plant Physiol 156:1548–1555

    PubMed  CAS  Google Scholar 

  • Schott G, Mari-Ordonez A, Himber C, Alioua A, Voinnet O, Dunoyer P (2012) Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. EMBO J 31:2553–2565

    PubMed  CAS  Google Scholar 

  • Schuck J, Gursinsky T, Pantaleo V, Burgyán J, Behrens SE (2013) AGO/RISC-mediated antiviral RNA silencing in a plant in vitro system. Nucleic Acids Res doi:10.1093/nar/gkt193

  • Shen B, Goodman HM (2004) Uridine addition after microRNA-directed cleavage. Science 306:997

    PubMed  CAS  Google Scholar 

  • Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J, Sueda K, Burgyan J, Masuta C (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog 7:e1002021

    PubMed  CAS  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    PubMed  CAS  Google Scholar 

  • Silhavy D, Burgyan J (2004) Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci 9:76–83

    PubMed  CAS  Google Scholar 

  • Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, Tavazza M, Burgyan J (2002) A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080

    PubMed  CAS  Google Scholar 

  • Smith NA, Eamens AL, Wang MB (2011) Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog 7:e1002022

    PubMed  CAS  Google Scholar 

  • Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434–1437

    PubMed  CAS  Google Scholar 

  • Szittya G, Molnar A, Silhavy D, Hornyik C, Burgyan J (2002) Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell 14:359–372

    PubMed  CAS  Google Scholar 

  • Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A, Lakatos L, Banfalvi Z, Burgyan J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640

    PubMed  CAS  Google Scholar 

  • Szittya G, Moxon S, Pantaleo V, Toth G, Rusholme Pilcher RL, Moulton V, Burgyan J, Dalmay T (2010) Structural and functional analysis of viral siRNAs. PLoS Pathog 6:e1000838

    PubMed  Google Scholar 

  • Takeda A, Tsukuda M, Mizumoto H, Okamoto K, Kaido M, Mise K, Okuno T (2005) A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J 24:3147–3157

    PubMed  CAS  Google Scholar 

  • Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49:493–500

    PubMed  CAS  Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    PubMed  CAS  Google Scholar 

  • Till S, Ladurner AG (2007) RNA Pol IV plays catch with Argonaute 4. Cell 131:643–645

    PubMed  CAS  Google Scholar 

  • Tomari Y, Zamore PD (2005) Perspective: machines for RNAi. Genes Dev 19:517–529

    PubMed  CAS  Google Scholar 

  • Vaistij FE, Jones L (2009) Compromised virus-induced gene silencing in RDR6-deficient plants. Plant Physiol 149:1399–1407

    PubMed  CAS  Google Scholar 

  • van Wezel WR, Dong X, Liu H, Tien P, Stanley J, Hong Y (2002) Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Mol Plant Microbe Interact 15:203–208

    Google Scholar 

  • Varallyay E, Valoczi A, Agyi A, Burgyan J, Havelda Z (2010) Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J 29:3507–3519

    PubMed  CAS  Google Scholar 

  • Vargason J, Szittya G, Burgyan J, Hall TM (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115:799–811

    PubMed  CAS  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    PubMed  CAS  Google Scholar 

  • Vaucheret H (2008) Plant Argonautes. Trends Plant Sci 13:350–358

    PubMed  CAS  Google Scholar 

  • Vaucheret H, Mallory AC, Bartel DP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22:129–136

    PubMed  CAS  Google Scholar 

  • Vazquez F (2006) Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci 11:460–468

    PubMed  CAS  Google Scholar 

  • Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676

    PubMed  CAS  Google Scholar 

  • Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Voinnet O, Pinto YM, Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96:14147–14152

    PubMed  CAS  Google Scholar 

  • Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM (2005) Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J Virol 79:7410–7418

    PubMed  CAS  Google Scholar 

  • Wang XB, Wu Q, Ito T, Cillo F, Li WX, Chen X, Yu JL, Ding SW (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:484–489

    PubMed  CAS  Google Scholar 

  • Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011) The 21-Nucleotide, but Not 22-Nucleotide, Viral Secondary Small Interfering RNAs Direct Potent Antiviral Defense by Two Cooperative Argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638

    PubMed  CAS  Google Scholar 

  • Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151

    PubMed  CAS  Google Scholar 

  • Wu Q, Wang X, Ding SW (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8:12–15

    PubMed  CAS  Google Scholar 

  • Xiong R, Wu J, Zhou Y, Zhou X (2009) Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387:29–40

    PubMed  CAS  Google Scholar 

  • Yang LP, Fang YY, An CP, Dong L, Zhang ZH, Chen H, Xie Q, Guo HS (2013) C2-mediated decrease in DNA methylation, accumulation of siRNAs, and increase in expression for genes involved in defense pathways in plants infected with beet severe curly top virus. Plant J 73:910–917

    PubMed  CAS  Google Scholar 

  • Ye K, Malinina L, Patel DJ (2003) Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426:874–878

    PubMed  CAS  Google Scholar 

  • Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    PubMed  CAS  Google Scholar 

  • Yu B, Chapman EJ, Yang Z, Carrington JC, Chen X (2006) Transgenically expressed viral RNA silencing suppressors interfere with microRNA methylation in Arabidopsis. FEBS Lett 580:3117–3120

    PubMed  CAS  Google Scholar 

  • Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, Gonzalez AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    PubMed  CAS  Google Scholar 

  • Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, Chua NH (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20:3255–3268

    PubMed  CAS  Google Scholar 

  • Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366

    PubMed  CAS  Google Scholar 

  • Zhang X, Zhang X, Singh J, Li D, Qu F (2012) Temperature-dependent survival of Turnip crinkle virus-infected arabidopsis plants relies on an RNA silencing-based defense that requires dcl2, AGO2, and HEN1. J Virol 86:6847–6854

    PubMed  CAS  Google Scholar 

  • Zhou Z, Dell’Orco M, Saldarelli P, Turturo C, Minafra A, Martelli GP (2006) Identification of an RNA-silencing suppressor in the genome of Grapevine virus A. J Gen Virol 87:2387–2395

    PubMed  CAS  Google Scholar 

  • Zrachya A, Glick E, Levy Y, Arazi T, Citovsky V, Gafni Y (2007) Suppressor of RNA silencing encoded by Tomato yellow leaf curl virus-Israel. Virology 358:159–165

    PubMed  CAS  Google Scholar 

  • Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4:2578–2597

    PubMed  CAS  Google Scholar 

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Acknowledgments

We apologize to those colleagues whose work we were unable to cite because of space restrictions. GS and JB are funded by grants from OTKA, K-101793 and NK-105850, respectively.

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Correspondence to György Szittya or József Burgyán .

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Szittya, G., Burgyán, J. (2013). RNA Interference-Mediated Intrinsic Antiviral Immunity in Plants. In: Cullen, B. (eds) Intrinsic Immunity. Current Topics in Microbiology and Immunology, vol 371. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-37765-5_6

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