A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement

Molecular Plant-Microbe Interactions

Volumn 21, Issue 7, 2008, Pages 879-890

  Powers, Jason G ^a   Sit, Tim L ^a   Qu, Feng ^b   Morris, T Jack ^b   Kim, Kook Hyung ^c   Lommel, Steven A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c Seoul National University   (South Korea)

Author keywords

IVIS lumina; p8; p9; pPZP212; VSR

Indexed keywords

CAPSID PROTEIN; GREEN FLUORESCENT PROTEIN; RECOMBINANT PROTEIN; VIRUS DNA; VIRUS RNA;

ARABIDOPSIS; ARTICLE; CARMOVIRUS; GENE REPRESSION; GENETIC COMPLEMENTATION; GENETICS; HOST PATHOGEN INTERACTION; MOVEMENT (PHYSIOLOGY); NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; REPORTER GENE; RHIZOBIUM RADIOBACTER; RNA INTERFERENCE; TOBACCO; VIROLOGY;

ARABIDOPSIS; BASE SEQUENCE; CAPSID PROTEINS; CARMOVIRUS; DNA, VIRAL; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; MOVEMENT; PLANT DISEASES; RECOMBINANT PROTEINS; RHIZOBIUM RADIOBACTER; RNA INTERFERENCE; RNA, VIRAL; SUPPRESSION, GENETIC; TOBACCO;

AGROBACTERIUM TUMEFACIENS; BRASSICA RAPA SUBSP. RAPA; NICOTIANA BENTHAMIANA; TURNIP CRINKLE VIRUS;

EID: 47549110190     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-21-7-0879     Document Type: Article

References (52)

1. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H., and Vance, V. B. 1998. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. U.S.A. 95(22):13079-13084.
2. Ball, L. A. 1994. Replication of the genomic RNA of a positive-strand RNA animal virus from negative-sense transcripts. Proc. Natl. Acad. Sci. U.S.A. 91:12443-12447.
3. Baumberger, N., and Baulcombe, D. C. 2005. Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. U.S.A. 102:11928-11933.
4. Bayne, E. H., Rakitina, D. V., Morozov, S. Y., and Baulcombe, D. C. 2005. Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J. 44:471-482.
5. Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-366.
6. Blevins, T., Rajeswaran, R., Shivaprasad, P.V., Beknazariants, D., Si-Ammour, A., Park, H. S., Vazquez, F., Robertson, D., Meins, F., Jr., Hohn, T., and Pooggin, M. M. 2006. Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34:6233-6246.
7. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO (Eur. Mol. Biol. Organ.) J. 17:6739-6746.
8. Carrington, J. C., and Freed, D. D. 1990. Cap-independent enhancement of translation by a plant potyvirus 5′ nontranslated region. J. Virol. 64:1590-1597.
9. Chapman, E. J., and Carrington, J. C. 2007. Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet. 8:884-896.
10. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. 1996. Engineered GFP as a vital reporter in plants. Curr. Biol. 6:325-330.
11. Choi, G. H., Shapira, R., and Nuss, D. L. 1991. Cotranslational autoproteolysis involved in gene expression from a double-stranded RNA genetic element associated with hypovirulence of the chestnut blight fungus. Proc. Natl. Acad. Sci. U.S.A. 88:1167-1171.
12. Cohen, Y., Gisel, A., and Zambryski, P. C. 2000. Cell-to-cell and systemic movement of recombinant green fluorescent protein-tagged turnip crinkle viruses. Virology 273:258-266.
13. Condit, R. C., and Motyczka, A. 1981. Isolation and preliminary characterization of temperature-sensitive mutants of vaccinia virus. Virology 113:224-241.
14. Coutts, R. H., and Buck, K. W. 1985. DNA and RNA polymerase activities of nuclei and hypotonic extracts of nuclei isolated from tomato golden mosaic virus infected tobacco leaves. Nucleic Acids Res. 13:7881-7897.
15. Dasgupta, R., Garcia, B. H., 2nd and Goodman, R. M. 2001. Systemic spread of an RNA insect virus in plants expressing plant viral movement protein genes. Proc. Natl. Acad. Sci. U.S.A. 98:4910-4915.
16. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K. D., Carrington, J. C., and Voinnet, O. 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68-71.
17. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J. A., and Imler, J. L. 2006. Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol. 7:590-597.
18. Hacker, D. L., Petty, I. T., Wei, N., and Morris, T. J. 1992. Turnip crinkle virus genes required for RNA replication and virus movement. Virology 186:1-8.
19. Hajdukiewicz, P., Svab, Z., and Maliga, P. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25:989-994.
20. Heaton, L. A., Carrington, J. C., and Morris, T. J. 1989. Turnip crinkle virus infection from RNA synthesized in vitro. Virology 170:214-218.
21. Himber, C., Dunoyer, P., Moissiard, G., Ritzenthaler, C., and Voinnet, O. 2003. Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO (Eur. Mol. Biol. Organ.) J. 22:4523-4533.
22. Johansen, L. K., and Carrington, J. C. 2001. Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126:930-938.
23. Kasschau, K. D., and Carrington, J. C. 1998. A counterdefensive strategy of plant viruses: Suppression of posttranscriptional gene silencing. Cell 95:461-470.
24. Koonin, E. V., Choi, G. H., Nuss, D. L., Shapira, R., and Carrington, J. C. 1991. Evidence for common ancestry of a chestnut blight hypovirulence- associated double-stranded RNA and a group of positive-strand RNA plant viruses. Proc. Natl. Acad. Sci. U.S.A. 88:10647-10651.
25. Li, F., and Ding, S. W. 2006. Virus counterdefense: Diverse strategies for evading the RNA-silencing immunity. Annu. Rev. Microbiol. 60:503-531.
26. Li, H., Li, W. X., and Ding, S. W. 2002. Induction and suppression of RNA silencing by an animal virus. Science 296:1319-1321.
27. Li, W. X., Li, H., Lu, R., Li, F., Dus, M., Atkinson, P., Brydon, E. W., Johnson, K. L., Garcia-Sastre, A., Ball, L. A., Palese, P., and Ding, S. W. 2004. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. U.S.A. 101:1350-1355.
28. Li, W. Z., Qu, F., and Morris, T. J. 1998. Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans. Virology 244:405-416.
29. Llave, C., Kasschau, K. D., and Carrington, J. C. 2000. Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc. Natl. Acad. Sci. U.S.A. 97:13401-13406.
30. Lu, R., Folimonov, A., Shintaku, M., Li, W. X., Falk, B. W., Dawson, W. O., and Ding, S. W. 2004. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. U.S.A. 101:15742-15747.
31. Morel, J. B., Godon, C., Mourrain, P., Beclin, C., Boutet, S., Feuerbach, F., Proux, F., and Vaucheret, H. 2002. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629-639.
32. Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J. B., Jouette, D., Lacombe, A. M., Nikic, S., Picault, N., Remoue, K., Sanial, M., Vo, T. A., and Vaucheret, H. 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533-542.
33. Napoli, C., Lemieux, C., and Jorgensen, R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289.
34. Qi, Y., Zhong, X., Itaya, A., and Ding, B. 2004. Dissecting RNA silencing in protoplasts uncovers novel effects of viral suppressors on the silencing pathway at the cellular level. Nucleic Acids Res. 32(22):e179. Published online.
35. Qu, F., and Morris, T. J. 2005. Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS (Fed. Eur. Biochem. Soc.) Lett. 579:5958-5964.
36. Qu, F., Ren, T., and Morris, T. J. 2003. The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J. Virol. 77:511-522.
37. Ren, T., Qu, F., and Morris, T. J. 2000. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917-1926.
38. Ren, T., Qu, F., and Morris, T. J. 2005. The nuclear localization of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip crinkle virus. Virology 331:316-324.
39. Segers, G. C., van Wezel, R., Zhang, X., Hong, Y., and Nuss, D. L. 2006. Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot. Cell 5:896-904.
40. Selling, B. H., Allison, R. F., and Kaesberg, P. 1990. Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Proc. Natl. Acad. Sci. U.S.A. 87:434-438.
41. Sit, T. L., Vaewhongs, A. A., and Lommel, S. A. 1998. RNA-mediated trans-activation of transcription from a viral RNA. Science 281:829-832.
42. Song, J. J., Smith, S. K., Hannon, G. J., and Joshua-Tor, L. 2004. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434-1437.
43. Stockley, P. A., Kirsh, A. L., Chow, E. P., Smart, J. E., and Harrison, S. C. 1986. Structure of Turnip crinkle virus. III. Identification of a unique coat protein dimer. J. Mol. Biol. 191:721-725.
44. Suzuki, N., Chen, B., and Nuss, D. L. 1990. Mapping of a hypovirus p29 protease symptom determinant domain with sequence similarity to potyvirus HC-Pro protease. J. Virol. 73:9478-9484.
45. Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A., Timmons, L., Fire, A., and Mello, C. C. 1990. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99:123-132.
46. Takeda, A., Tsukuda, M., Mizumoto, H., Okamoto, K., Kaido, M., Mise, K., and Okuno, T. 2005. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO (Eur. Mol. Biol. Organ.) J. 24:3147-3157.
47. Voinnet, O. 2001. RNA silencing as a plant immune system against viruses. Trends Genet. 17:449-459.
48. Voinnet, O., Lederer, C., and Baulcombe, D. C. 2000. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157-167.
49. Volpe, T. A., Kidner, C., Hall, I. M., Teng, G., Grewal, S. I., and Martienssen, R. A. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837.
50. Wang, H., Buckley, K. J., Yang, X., Buchmann, R. C., and Bisaro, D. M. 2005. Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79:7410-7418.
51. Wang, X. H., Aliyari, R., Li, W. X., Li, H. W., Kim, K., Carthew, R., Atkinson, P., and Ding, S. W. 2006. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452-454.
52. Zhang, X., Yuan, Y. R., Pei, Y., Lin, S. S., Tuschl, T., Patel, D. J., and Chua, N. H. 2006. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20:3255-3268.