A plant RNA virus suppresses RNA silencing through viral RNA replication

EMBO Journal

Volumn 24, Issue 17, 2005, Pages 3147-3157

  Takeda, Atsushi ^a   Tsukuda, Misato ^a   Mizumoto, Hiroyuki ^a   Okamoto, Kimiyuki ^a   Kaido, Masanori ^a   Mise, Kazuyuki ^a   Okuno, Tetsuro ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Dicer; Plant virus; Replication; RNAi; Suppressor; Virus

Indexed keywords

DOUBLE STRANDED RNA; MICRORNA; RNA DIRECTED RNA POLYMERASE; SMALL INTERFERING RNA; VIRUS RNA; ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; DCL1 PROTEIN, ARABIDOPSIS; PLANT RNA; RIBONUCLEASE III;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENZYMOLOGY; GENE SILENCING; INFECTION SENSITIVITY; MOLECULAR DYNAMICS; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; RED CLOVER NECROTIC MOSAIC VIRUS; RNA ANALYSIS; RNA INTERFERENCE; RNA REPLICATION; RNA STRUCTURE; RNA SYNTHESIS; VIRUS INFECTION; 3' UNTRANSLATED REGION; BIOSYNTHESIS; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; RNA VIRUS; VIROLOGY;

ARABIDOPSIS; EUKARYOTA; RED CLOVER NECROTIC MOSAIC VIRUS; RNA VIRUSES;

3' UNTRANSLATED REGIONS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; MICRORNAS; MUTATION; PLANT VIRUSES; RIBONUCLEASE III; RNA INTERFERENCE; RNA REPLICASE; RNA VIRUSES; RNA, PLANT; RNA, SMALL INTERFERING; RNA, VIRAL;

EID: 27144499282     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600776     Document Type: Article

References (56)

1. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT (2003) Host factors in positive-strand RNA virus genome replication. J Virol 77: 8181-8186
2. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297
3. Bates HJ, Farjah M, Osman TA, Buck KW (1995) Isolation and characterization of an RNA-dependent RNA polymerase from Nicotiana clevelandii plants infected with red clover necrotic mosaic dianthovirus. J Gen Virol 76: 1483-1491
4. Baulcombe D (2004) RNA silencing in plants. Nature 431: 356-363
5. Beclin C, Boutet S, Waterhouse P, Vaucheret H (2002) A branched pathway for transgene-induced RNA silencing in plants. Curr Biol 12: 684-688
6. Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47: 159-251
7. 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
8. Dalmay T, Hamilton AJ, 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
9. 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
10. Ding SW, Anderson BJ, Haase HR, Symons RH (1994) New overlapping gene encoded by the cucumber mosaic virus genome. Virology 198: 593-601
11. 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
12. Finnegan EJ, Margis R, Waterhouse PM (2003) Posttranscriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-LIKE1) mutant, a homolog of Dicer-1 from Drosophila. Curr Biol 13: 236-240
13. Fujisaki K, Hagihara F, Kaido M, Mise K, Okuno T (2003) Complete nucleotide sequence of Spring beauty latent virus, a bromovirus infectious to Arabidopsis thaliana. Arch Virol 148: 165-175
14. Guo HS, Ding SW (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21: 398-407
15. Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671-4679
16. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22: 4523-4533
17. 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 function. Dev Cell 4: 205-217
18. Kim KH, Lommel SA (1994) Identification and analysis of the site of -1 ribosomal frameshifting in red clover necrotic mosaic virus. Virology 200: 574-582
19. Koonin EV, Dolja VV (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28: 375-430
20. Kurihara Y, Watanabe Y (2003) Cross-protection in Arabidopsis against crucifer tobamovirus Cg by an attenuated strain of the virus. Mol Plant Pathol 4: 259-270
21. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101: 12753-12758
22. Lakatos L, Szittya G, Silhavy D, Burgyán J (2004) Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J 23: 876-884
23. Lecellier CH, Voinnet O (2004) RNA silencing: no mercy for viruses? Immunol Rev 198: 285-303
24. Li H, Li WX, Ding SW (2002) Induction and suppression of RNA silencing by an animal virus. Science 296: 1319-1321
25. Li WX, Li H, Lu R, Li F, Dus M, Atkinson P, Brydon EWA, Johnson KL, García-Sastre A, Ball LA, Palese P, Ding SW (2004) Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc Natl Acad Sci USA 101: 1350-1355
26. Lommel SA (1999) Dianthoviruses. In Encyclopedia of Virology, Granoff A, Webster RG (eds) 2nd edn, Vol. 1, pp 403-409. San Diego, CA: Academic Press
27. Lu S, Cullen BR (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J Virol 78: 12868-12876
28. Matsuda D, Bauer L, Tinnesand K, Dreher TW (2004) Expression of the two nested overlapping reading frames of turnip yellow mosaic virus RNA is enhanced by a 5′ cap and by 5′ and 3′ viral sequences. J Virol 78: 9325-9335
29. Mizumoto H, Hikichi Y, Okuno T (2002) The 3′-untranslated region of RNA1 as a primary determinant of temperature sensitivity of Red clover necrotic mosaic virus Canadian strain. Virology 293: 320-327
30. Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T (2003) Cap-independent translational enhancement by the 3′ untranslated region of Red clover necrotic mosaic virus. J Virol 77: 12113-12121
31. Moissiard G, Voinnet O (2004) Viral suppression of RNA silencing in plants. Mol Plant Pathol 5: 71-82
32. Mori M, Zhang GH, Kaido M, Okuno T, Furusawa I (1993) Efficient production of human gamma interferon in tobacco protoplasts by genetically engineered brome mosaic virus RNAs. J Gen Virol 74: 1255-1260
33. Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542
34. Noueiry AO, Ahlquist P (2003) Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annu Rev Phytopathol 41: 77-98
35. Osman TAM, Buck KW (1987) Replication of red clover necrotic mosaic virus RNA in cowpea protoplasts: RNA-1 replicates independently of RNA-2. J Gen Virol 68: 289-296
36. Papp I, Mette MF, Aufsatz W, Daxinger L, Schauer SE, Ray A, van der Winden J, Matzke M, Matzke AJ (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol 132: 1382-1390
37. Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18: 2237-2242
38. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102: 3691-3696
39. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16: 1616-1626
40. Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Alabidopsis development. Trends Plant Sci 7: 487-491
41. Silhavy D, Burgyán J (2004) Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci 9: 76-83
42. Sit TL, Vaewhongs AA, Lommel SA (1998) RNA-mediated trans-activation of transcription from a viral RNA. Science 281: 829-832
43. Sun JH, Adkins S, Faurote G, Kao CC (1996) Initiation of (-)-strand RNA synthesis catalyzed by the BMV RNA-dependent RNA polymerase: synthesis of oligonucleotides. Virology 226: 1-12
44. Sun JH, Kao CC (1997) RNA synthesis by the brome mosaic virus RNA-dependent RNA polymerase: transition from initiation to elongation. Virology 233: 63-73
45. Tahbaz N, Kolb FA, Zhang H, Jaronczyk K, Filipowicz W, Hobman TC (2004) Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO Rep 5: 189-194
46. Takeda A, Sugiyama K, Nagano H, Mori M, Kaido M, Mise K, Tsuda S, Okuno T (2002) Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett 532: 75-79
47. Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17: 49-63
48. Tatsuta M, Mizumoto H, Kaido M, Mise K, Okuno T (2005) The Red clover necrotic mosaic virus RNA2 traits-activator is also a cis- acting RNA2 replication element. J Virol 79: 978-986
49. Turner KA, Sit TM, Callaway AS, Allen NS, Lommel SA (2004) Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 320: 276-290
50. Turner RL, Buck KW (1999) Mutational analysis of cis-acting sequences in the 3′- and 5′-untranslated regions of RNA2 of red clover necrotic mosaic virus. Virology 253: 115-124
51. Vargason JM, Szittya G, Burgyán J, Hall TMT (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115: 799-811
52. Vastenhouw NL, Plasterk RH (2004) RNAi protects the Caenorhabditis elegans germline against transposition. Trends Genet 20: 314-319
53. Voinnet O, Lederer C, Baulcombe DC (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157-167
54. Watanabe Y, Meshi T, Okada Y (1987) Infection of tobacco protoplasts with in vitro transcribed tobacco mosaic virus RNA using an improved electroporation method. FEBS Lett 219: 65-69
55. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: e104
56. Xiong Z, Kim K, Kendall TL, Lommel SA (1993) Synthesis of the putative red clover necrotic mosaic virus RNA polymerase by ribosomal frameshifting in vitro. Virology 193: 213-221