This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mérai, Z.
Right arrow Articles by Silhavy, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mérai, Z.
Right arrow Articles by Silhavy, D.

 Previous Article  |  Next Article 

Journal of Virology, June 2006, p. 5747-5756, Vol. 80, No. 12
0022-538X/06/$08.00+0     doi:10.1128/JVI.01963-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Double-Stranded RNA Binding May Be a General Plant RNA Viral Strategy To Suppress RNA Silencing

Zsuzsanna Mérai,1,2 Zoltán Kerényi,1 Sándor Kertész,1 Melinda Magna,1 Lóránt Lakatos,1 and Dániel Silhavy1*

Agricultural Biotechnology Center, Gödöllö, Hungary,1 Department of Genetics, Eötvös Loránd University, Budapest, Hungary2

Received 15 September 2005/ Accepted 25 January 2006

In plants, RNA silencing (RNA interference) is an efficient antiviral system, and therefore successful virus infection requires suppression of silencing. Although many viral silencing suppressors have been identified, the molecular basis of silencing suppression is poorly understood. It is proposed that various suppressors inhibit RNA silencing by targeting different steps. However, as double-stranded RNAs (dsRNAs) play key roles in silencing, it was speculated that dsRNA binding might be a general silencing suppression strategy. Indeed, it was shown that the related aureusvirus P14 and tombusvirus P19 suppressors are dsRNA-binding proteins. Interestingly, P14 is a size-independent dsRNA-binding protein, while P19 binds only 21-nucleotide ds-sRNAs (small dsRNAs having 2-nucleotide 3' overhangs), the specificity determinant of the silencing system. Much evidence supports the idea that P19 inhibits silencing by sequestering silencing-generated viral ds-sRNAs. In this study we wanted to test the hypothesis that dsRNA binding is a general silencing suppression strategy. Here we show that many plant viral silencing suppressors bind dsRNAs. Beet yellows virus Peanut P21, clump virus P15, Barley stripe mosaic virus {gamma}B, and Tobacco etch virus HC-Pro, like P19, bind ds-sRNAs size-selectively, while Turnip crinkle virus CP is a size-independent dsRNA-binding protein, which binds long dsRNAs as well as ds-sRNAs. We propose that size-selective ds-sRNA-binding suppressors inhibit silencing by sequestering viral ds-sRNAs, whereas size-independent dsRNA-binding suppressors inactivate silencing by sequestering long dsRNA precursors of viral sRNAs and/or by binding ds-sRNAs. The findings that many unrelated silencing suppressors bind dsRNA suggest that dsRNA binding is a general silencing suppression strategy which has evolved independently many times.


* Corresponding author. Mailing address: Agricultural Biotechnology Center, H-2101 Gödöllö, P. O. Box. 411, Hungary. Phone: 36-28-526-194. Fax: 36-28-526-145. E-mail: silhavy{at}abc.hu.


Journal of Virology, June 2006, p. 5747-5756, Vol. 80, No. 12
0022-538X/06/$08.00+0     doi:10.1128/JVI.01963-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Hemmes, H., Kaaij, L., Lohuis, D., Prins, M., Goldbach, R., Schnettler, E. (2009). Binding of small interfering RNA molecules is crucial for RNA interference suppressor activity of rice hoja blanca virus NS3 in plants. J. Gen. Virol. 90: 1762-1766 [Abstract] [Full Text]  
  • Senshu, H., Ozeki, J., Komatsu, K., Hashimoto, M., Hatada, K., Aoyama, M., Kagiwada, S., Yamaji, Y., Namba, S. (2009). Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J. Gen. Virol. 90: 1014-1024 [Abstract] [Full Text]  
  • Martinez-Turino, S., Hernandez, C. (2009). Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. J. Gen. Virol. 90: 519-525 [Abstract] [Full Text]  
  • Sun, L., Suzuki, N. (2008). Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14: 2557-2571 [Abstract] [Full Text]  
  • Ghazala, W., Waltermann, A., Pilot, R., Winter, S., Varrelmann, M. (2008). Functional characterization and subcellular localization of the 16K cysteine-rich suppressor of gene silencing protein of tobacco rattle virus. J. Gen. Virol. 89: 1748-1758 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Cuellar, W. J., Tairo, F., Kreuze, J. F., Valkonen, J. P. T. (2008). Analysis of gene content in sweet potato chlorotic stunt virus RNA1 reveals the presence of the p22 RNA silencing suppressor in only a few isolates: implications for viral evolution and synergism. J. Gen. Virol. 89: 573-582 [Abstract] [Full Text]  
  • Valli, A., Dujovny, G., Garcia, J. A. (2008). Protease Activity, Self Interaction, and Small Interfering RNA Binding of the Silencing Suppressor P1b from Cucumber Vein Yellowing Ipomovirus. J. Virol. 82: 974-986 [Abstract] [Full Text]  
  • Schnettler, E., Hemmes, H., Goldbach, R., Prins, M. (2008). The NS3 protein of rice hoja blanca virus suppresses RNA silencing in mammalian cells. J. Gen. Virol. 89: 336-340 [Abstract] [Full Text]  
  • Love, A. J., Laird, J., Holt, J., Hamilton, A. J., Sadanandom, A., Milner, J. J. (2007). Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J. Gen. Virol. 88: 3439-3444 [Abstract] [Full Text]  
  • Shiboleth, Y. M., Haronsky, E., Leibman, D., Arazi, T., Wassenegger, M., Whitham, S. A., Gaba, V., Gal-On, A. (2007). The Conserved FRNK Box in HC-Pro, a Plant Viral Suppressor of Gene Silencing, Is Required for Small RNA Binding and Mediates Symptom Development. J. Virol. 81: 13135-13148 [Abstract] [Full Text]  
  • Scholthof, H. B. (2007). Heterologous Expression of Viral RNA Interference Suppressors: RISC Management. Plant Physiol. 145: 1110-1117 [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Vogler, H., Akbergenov, R., Shivaprasad, P. V., Dang, V., Fasler, M., Kwon, M.-O., Zhanybekova, S., Hohn, T., Heinlein, M. (2007). Modification of Small RNAs Associated with Suppression of RNA Silencing by Tobamovirus Replicase Protein. J. Virol. 81: 10379-10388 [Abstract] [Full Text]  
  • Kurihara, Y., Inaba, N., Kutsuna, N., Takeda, A., Tagami, Y., Watanabe, Y. (2007). Binding of tobamovirus replication protein with small RNA duplexes. J. Gen. Virol. 88: 2347-2352 [Abstract] [Full Text]  
  • Hemmes, H., Lakatos, L., Goldbach, R., Burgyan, J., Prins, M. (2007). The NS3 protein of Rice hoja blanca tenuivirus suppresses RNA silencing in plant and insect hosts by efficiently binding both siRNAs and miRNAs. RNA 13: 1079-1089 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Verchot-Lubicz, J., Ye, C.-M., Bamunusinghe, D. (2007). Molecular biology of potexviruses: recent advances. J. Gen. Virol. 88: 1643-1655 [Abstract] [Full Text]  
  • Diaz-Pendon, J. A., Li, F., Li, W.-X., Ding, S.-W. (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 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Omarov, R. T., Ciomperlik, J. J., Scholthof, H. B. (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. USA 104: 1714-1719 [Abstract] [Full Text]  
  • Blevins, T., Rajeswaran, R., Shivaprasad, P. V., Beknazariants, D., Si-Ammour, A., Park, H.-S., Vazquez, F., Robertson, D., Meins, F. Jr, Hohn, T., Pooggin, M. M. (2006). Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34: 6233-6246 [Abstract] [Full Text]  
  • van Rij, R. P., Saleh, M.-C., Berry, B., Foo, C., Houk, A., Antoniewski, C., Andino, R. (2006). The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster.. Genes Dev. 20: 2985-2995 [Abstract] [Full Text]