Plant viruses versus RNAi: Simple pathogens reveal complex insights on plant antimicrobial defense
Corresponding Author
Feng Qu
Department of Plant Pathology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Ave., Wooster, OH 44691
Department of Plant Pathology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Ave., Wooster, OH 44691Search for more papers by this authorCorresponding Author
Feng Qu
Department of Plant Pathology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Ave., Wooster, OH 44691
Department of Plant Pathology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Ave., Wooster, OH 44691Search for more papers by this authorAbstract
RNA interference (RNAi) and related processes serve as a nucleic-acid-mediated surveillance system conserved in almost all eukaryotic organisms. This surveillance system detects various forms of double-stranded RNA (dsRNA) in cells and initiates a cascade of events that degrades dsRNAs into small interfering RNAs (siRNAs) or microRNAs (miRNAs). These small RNAs in turn serve as sequence-specific guides to interfere with the function of other nucleic acids through degradation or translational repression of homologous RNAs, or modification of homologous genome segments. One of the major roles of RNAi in plants and invertebrates is antiviral defense. Conversely, viruses have also evolved to encode suppressors of RNAi (VSRs), which disrupt RNAi at various steps. Research activities focusing on the relationship between plant viruses and RNAi have been essential to our current understanding of RNAi mechanisms. Copyright © 2010 John Wiley & Sons, Ltd.
This article is categorized under:
- Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action
- RNA in Disease and Development > RNA in Disease
RELATED WIREs ARTICLES
REFERENCES
- 1Fire A, Albertson D, Harrison S, Moerman D. Production of antisense RNA leads to effective and specific inhibition of gene expression in C. elegans muscle. Development 1991, 113: 503–514.
- 2Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391: 806–811.
- 3van der Krol AR, Lenting PE, Veenstra J, van der Meer IM, Koes RE, et al. An antisense chalcone synthase gene in transgenic plants inhibits flower pigmentation. Nature 1988, 333: 866–869.
- 4Napoli C, Lemieux C, Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 1990, 2: 279–289.
- 5Hamilton AJ, Baulcombe DC. A species of small antisense RNA in post-transcriptional gene silencing in plants. Science 1999, 276: 1558–1560.
- 6Gil J, Esteban M. Induction of apoptosis by the dsRNA-dependent protein kinase (PKR): mechanism of action. Apoptosis 2000, 5: 107–114.
- 7Paddison PJ, Caudy AA, Bernstein E, Hannon GJ, Conklin DS. Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev 2002, 16: 948–958.
- 8Baulcombe DC. Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 1996, 8: 1833–1844.
- 9Lindbo JA, Dougherty WG. Untranslatable transcripts of the tobacco etch virus coat protein gene sequence can interfere with tobacco etch virus replication in transgenic plants and protoplasts. Virology 1992, 189: 725–733.
- 10Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 1993, 5: 1749–1759.
- 11Goodwin J, Chapman K, Swaney S, Parks TD, Wernsman EA, et al. Genetic and biochemical dissection of transgenic RNA-mediated virus resistance. Plant Cell 1996, 8: 95–105.
- 12Schiebel W, Haas B, Marinkovic S, Klanner A, Sanger HL. RNA-directed RNA polymerase from tomato leaves. II. Catalytic in vitro properties. J Biochem Mol Biol Biophys 1993, 268: 11858–11867.
- 13Hobbs SLA, Warkentin TD, DeLong CMO. Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol Biol 1993, 21: 17–26.
- 14de Carvalho niebel F, Frendo P, van Montagu M, Cornelissen M. Post-transcriptional cosuppression of β-1,3-glucanase genes does not affect accumulation of transgene nuclear mRNA. Plant Cell 1995, 7: 347–358.
- 15Chuang C-F, Meyerowitz EM. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc Natl Acad Sci USA 2000, 97: 4985–4990.
- 16Jacobson SE, Running MP, Meyerowitz EM. Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 1999, 126: 5231–5243.
- 17Bernstein E, Caudy AA, Hammond SC, Hannon GJ. Role of a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409: 363–366.
- 18Brodersen P, Voinnet O. The diversity of RNA silencing pathways in plants. Trends Genet 2006, 22: 268–280.
- 19Chapman EJ, Carrington JC. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 2007, 8: 884–896.
- 20Kurihara Y, Watanabe Y. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 2004, 101: 12753–12758.
- 21Qi Y, Denli AM, Hannon GJ. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol Cell 2005, 19: 421–428.
- 22Baumberger N, Baulcombe DC. Arabidopsis Argonaute1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 2005, 102: 11928–11933.
- 23Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, et al. Specificity of Argonaute7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 2008, 133: 128–141.
- 24Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Sieburth L, et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320: 1185–1190.
- 25Han MH, Goud S, Song L, Fedoroff N. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 2004, 101: 1093–1098.
- 26Yu B, Yang Z, Li J, Minakhina S, Yang M, et al. Methylation as a crucial step in plant microRNA biogenesis. Science 2005, 307: 932–935.
- 27Kurihara Y, Takashi Y, Watanabe Y. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 2006, 12: 206–212.
- 28Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J. SERRATE: a new player on the plant microRNA scene. EMBO Rep 2006, 7: 1052–1058.
- 29Ramachandran V, Chen X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 2008, 321: 1490–1492.
- 30Mallory AC, Elmayan T, Vaucheret H. MicroRNA maturation and action the expanding roles of ARGONAUTEs. Curr Opin Plant Biol 2008, 11: 560–566.
- 31Sunkar R, Kapoor A, Zhu J-K. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 2006, 18: 2051–2065.
- 32Sunkar R, Chinnusamy V, Zhu J, Zhu J-K. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 2007, 12: 301–309.
- 33Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312: 436–439.
- 34Navarro L, Jay F, Nomura K, He SY, Voinnet O. Suppression of the microRNA pathway by bacterial effector proteins. Science 2008, 321: 964–967.
- 35Qu F, Ye X, Morris TJ. Arabidopsis DRB4, AGO1, and AGO7 participate in a DCL4-initiated antiviral RNA silencing pathway that is negatively regulated by DCL1. Proc Natl Acad Sci U S A 2008, 105: 14732–14737.
- 36Allen E, Xie Z, Gustafson AM, Carrington JC. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 2005, 121: 207–221.
- 37Yoshikawa M, Peragine A, Park MY, Poethig RC. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 2005, 19: 2164–2175.
- 38Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 2004, 18: 2368–2379.
- 39Vazquez F, Vaucheret H, Rajagopala R, Lepers C, Gasciolli V, et al. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 2004, 16: 69–79.
- 40Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, et al. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 2006, 16: 927–932.
- 41Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, et al. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 2006, 16: 939–944.
- 42Garcia D, Collier SA, Byrne ME, Martienssen RA. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 2006, 16: 933–938.
- 43Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutierrez-Nava M, et al. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 2006, 133: 2973–2981.
- 44Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, et al. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat Genet 2006, 38: 721–725.
- 45Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, et al. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 2007, 5: e57. DOI:10.1371/journal.pbio.0050057.
- 46Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. RNA polymerase IV directs silencing of endogenous DNA. Science 2005, 308: 118–120.
- 47Onodera Y, Haag JR, Ream T, Nunes PC, Pontes O, et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterchromatin formation. Cell 2005, 120: 613–622.
- 48Zheng X, Zhu J, Kapoor A, Zhu J-K. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 2007, 26: 1691–1701.
- 49Wierzbicki AT, Haag JR, Pikaard CS. Noncoding transcription by RNA polymerase PolIVb/PolV mediates transcriptional silencing of overlapping and adjacent genes. Cell 2008, 135: 635–648.
- 50Raja P, Sanville BC, Buchmann RC, Bisaro DM. Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 2008, 82: 8997–9007.
- 51Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM. Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 2009, 83: 5005–5013.
- 52Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu J-K. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 2005, 123: 1279–1291.
- 53Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H. A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 2006, 103: 18002–18007.
- 54Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, et al. A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 2007, 21: 3123–3134.
- 55Covey SN, Al-Kaff NS, Langara A, Turner DS. Plants combat infection by gene silencing. Nature 1997, 385: 781–782.
- 56Ratcliff F, Harrison BD, Baulcombe DC. A similarity between viral defense and gene silencing. Science 1997, 276: 1558–1560.
- 57Baulcombe D. RNA silencing in plants. Nature 2004, 431: 356–363.
- 58Ding SW, Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130: 413–426.
- 59Bouche N, Lauressergues D, Gasciolli V, Vaucheret H. An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 2006, 25: 3347–3356.
- 60Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, et al. Hierachical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 2006, 313: 68–71.
- 61Diaz-Pendon JA, Li F, Li W-X, Ding S-W. 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 2006, 19: 2053–2063.
- 62Donaire L, Barajas D, Martinez-Garcia B, Martinez-Priego L, Pagan I, et al. Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J Virol 2008, 82: 5167–5177.
- 63Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Meins MM, et al. Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 2006, 34: 6233–6246.
- 64Moissiard G, Voinnet O. RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins. Proc Natl Acad Sci USA 2006, 103: 19593–19598.
- 65Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 2005, 6: 206–220.
- 66Li F, Ding S-W. Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 2006, 60: 503–531.
- 67Scholthof HB, Scholthof K-BG, Kikkert M, Jackson AO. Tomato bushy stunt virus spread is regulated by two nested genes that function in cell-to-cell movement and host-dependent systemic invasion. Virology 1995, 213: 425–438.
- 68Voinnet O, Pinto YM, Baulcombe DC. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci USA 1999, 96: 14147–14152.
- 69Qu F, Morris TJ. Efficient infection of Nicotiana benthamiana by Tomato bushy stunt virus is facilitated by the coat protein and maintained by p19 through suppression of gene silencing. Mol Plant-Microbe Interact 2002, 15: 193–202.
- 70Qiu W, Park J-W, Scholthof HB. Tombusvirus P19-mediated suppression of virus-induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol Plant-Microbe Interact 2002, 15: 269–280.
- 71Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, et al. A viral protein suppresses RNA silencing and binds silencing-generated, 21-to 25-nucleotide double-stranded RNAs. EMBO J 2002, 21: 3070–3080.
- 72Vargason JM, Szittya G, Burgyán J, Hall TMT. Size selective recognition of siRNA by an RNA silencing suppressor. Cell 2003, 115: 799–811.
- 73Ye K, Malinina L, Patel DJ. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 2003, 426: 874–878.
- 74Dunoyer P, Lecellier C-H, Parizotto EA, Himber C, Voinnet O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 2004, 16: 1235–1250.
- 75Chapman EJ, Prokhnevsky AI, Gopinath K, Dojia VV, Carrington JC. Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 2004, 18: 1179–1186.
- 76Lakatos L, Szittya G, Silhavy D, Burgyán J. Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J 2004, 23: 876–884.
- 77Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, et al. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J 2006, 25: 2768–2780.
- 78Cuellar WJ, Kreuze JF, Rajamaki M-L, Cruzado KR, Untiveros M, et al. Elimination of antiviral defense by viral RNase III. Proc Natl Acad Sci USA 2009, 106: 10354–10358.
- 79Zhang X, Yuan Y-R, Pei Y, Lin S-S, Tuschl T, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 2006, 20: 3255–3268.
- 80Baumberger N, Tsai C-H, Lie M, Havecker E, Baulcombe DC. The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 2007, 17: 1609–1614.
- 81Bortolamiol D, Pazhouhandeh M, Marrocco K, Genschik P, Ziegler-Graff V. The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr Biol 2007, 17: 1615–1621.
- 82Haas G, Azevedo J, Moissiard G, Geldreich A, Himber C, et al. Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 2008, 27: 2102–2112.
- 83Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, et al. Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci USA 2008, 105: 157–161.
- 84Fukunaga R, Doudna JA. dsRNA with 5' overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J 2009, 28: 545–555.
- 85Trinks D, Rajeswaran R, Shivaprasad V, Akbergenov R, Oakeley EJ, et al. Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 2005, 79: 2517–2527.
- 86Sun Q, Choi GH, Nuss DL. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc Natl Acad Sci USA 2009, 106: 17929–17932.
- 87Anandalakshmi R, Marathe R, Ge X, Herr JM Jr, Mau C, Mallory VB, et al. A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 2000, 290: 142–144.
- 88Canto T, Uhrig JF, Swanson M, Wright KM, MacFarlane SA. Translocation of Tomato bushy stunt virus P19 by ALY proteins compromises its silencing suppressor activity. J Virol 2006, 80: 9064–9072.
- 89Goto K, Kobori T, Kosaka Y, Natsuaki T, Masuta C. Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol 2007, 48: 1050–1060.
- 90Lu R, Folomonov A, Shintaku M, Li W-X, Falk BW, et al. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc Natl Acad Sci USA 2004, 101: 15742–15747.
- 91Kreuze JF, Savenkov EI, Cuellar W, Li X, Valkonen JPT. Viral class 1 RNase III involved in suppression of RNA silencing. J Virol 2005, 79: 7227–7238.
- 92Hagiwara-Komoda Y, Hirai K, Mochizuki A, Nishiguchi M, Meshi T, et al. Overexpression of a host factor TOM1 inhibits tomato mosaic virus propagation and suppression of RNA silencing. Virology 2008, 376: 132–139.
- 93Lu S, Cullen BR. Adenovirus VA1 non-coding RNA can inhibit small interfering RNA and microRNA biogenesis. J Virol 2004, 78: 12868–12876.
- 94Pruss G, Ge X, Shi XM, Carrington JC, Vance VB. Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 1997, 9: 859–868.
- 95Szittya G, Molnar A, Silhavy D, Hornyik C, Burgyan J. Short defective interfering RNAs of tombusviruses are not targeted by trigger post-transcriptional gene silencing against their helper virus. Plant Cell 2002, 14: 359–372.
- 96Souret FF, Kastenmayer JP, Green PJ. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 2004, 15: 173–183.
- 97Gy I, Gasiolli V, Lauressergues D, Morel J-B, Gombert J, et al. Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 2007, 19: 3451–3461.
- 98Herr AJ, Molnar A, Jones A, Baulcombe DC. Defective RNA processing enhances RNA silencing and influences flowering of Arabidopsis. Proc Natl Acad Sci USA 2006, 103: 14994–15001.
- 99Zhu J, Kapoor A, Sridhar VV, Agius F, Zhu JK. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr Biol 2007, 17: 54–59.
- 100Aliyari R, Wu Q, Li H-W, Wang X-H, Li F, et al. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 2008, 4: 387–397.
- 101Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, et al. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 2005, 436: 1040–1043.
- 102Li H, Li WX, Ding SW. Induction and suppression of RNA silencing by an animal virus. Science 2002, 296: 1319–1321.
- 103Umbach JL, Cullen BR. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev 2009, 23: 1151–1164.
- 104Lecellier CH, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S, et al. A cellular microRNA mediates antiviral defense in human cells. Science 2005, 308: 557–560.
- 105Triboulet R, Mari B, Lin YL, Chable-Bessia C, Bennasser Y, et al. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 2007, 315: 1579–1582.
- 106Schnettler E, De Vries W, Hemmes H, Haasnoot J, Kornelink R, et al. The NS3 protein Eof rice hoja blanca virus complements the RNAi suppressor function of HIV-1 Tat. EMBO Rep 2009, 10: 258–263.
- 107Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, et al. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139: 845–956.