Abstract
Since its discovery in the late 1980s, the status of the Tombusvirus-encoded p19 protein (P19) changed from being thought obsolete to its identification a decade later as an important viral pathogenicity factor. The recent finding that P19 suppresses RNA interference (RNAi) by appropriating short interfering RNAs led to its widespread use as an RNAi-probing tool in various plant and animal models. Here, I discuss how our knowledge of p19 has developed over the years, with emphasis on the relevance of understanding its biological roles during Tombusvirus infection of plants.
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References
Hull, R. Matthews' Plant Virology (Academic Press, London, 2002).
Hillman, B. I. et al. A defective interfering RNA that contains a mosaic of a plant virus genome. Cell 51, 427–433 (1987).
Yamamura, Y. & Scholthof, H. B. Pathogen profile: tomato bushy stunt virus: a resilient model system for studying virus–plant interactions. Mol. Plant Pathol. 6, 491–502 (2005).
Russo, M. et al. Molecular biology of Tombusviridae. Adv. Virus Res. 44, 381–428 (1994).
Martelli, G. P. et al. in The Plant Viruses (ed. Koenig, R.) 13–72 (Plenum Press, New York, 1988).
Grieco, F. et al. Nucleotide sequence of the 3′-terminal region of cymbidium ringspot virus RNA. J. Gen. Virol. 70, 2533–2538 (1989).
Hayes, R. J. et al. Gene mapping and expression of tomato bushy stunt virus. J. Gen. Virol. 69, 3047–3057 (1988).
Hillman, B. I. et al. Organization of tomato bushy stunt virus genome: characterization of the coat protein gene and the 3′ terminus. Virology 169, 42–50 (1989).
Tavazza, M. et al. Nucleotide sequence, genomic organization and synthesis of infectious transcripts from a full-length clone of artichoke mottle crinkle virus. J. Gen. Virol. 75, 1515–1524 (1994).
Rubino, L. et al. Molecular cloning and complete nucleotide sequence of carnation italian ringspot tombusvirus genomic and defective interfering RNAs. Arch. Virol. 140, 2027–2039 (1995).
Burgyan, J. et al. Synthesis of infectious RNA from full-length cloned cDNA to RNA of cymbidium ringspot tombusvirus. J. Gen. Virol. 71, 1857–1860 (1990).
Hearne, P. Q. et al. The complete genome structure and synthesis of infectious RNA from clones of tomato bushy stunt virus. Virology 177, 141–151 (1990).
Rochon, D. M. & Johnston, J. C. Infectious transcripts from cloned cucumber necrosis virus cDNA: evidence for a bifunctional subgenomic mRNA. Virology 181, 656–665 (1991).
White, K. A. & Nagy, P. D. Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog. Nucleic Acid Res. Mol. Biol. 78, 187–226 (2004).
Choi, I. R. et al. Regulatory activity of distal and core RNA elements in Tombusvirus subgenomic mRNA2 transcription. J. Biol. Chem. 276, 41761–41768 (2001).
Wu, B. & White, K. A. A primary determinant of cap-independent translation is located in the 3′-proximal region of the tomato bushy stunt virus genome. J. Virol. 73, 8982–8988 (1999).
Johnston, J. C. & Rochon, D. M. Both codon context and leader length contribute to efficient expression of two overlapping open reading frames of a cucumber necrosis virus bifunctional subgenomic mRNA. Virology 221, 232–239 (1996).
Johnston, J. C. & Rochon, D. M. Deletion analysis of the promoter for the cucumber necrosis virus 0.9-kb subgenomic RNA. Virology 214, 100–109 (1995).
Scholthof, H. B. et al. The biological activity of two tombusvirus proteins translated from nested genes is influenced by dosage control via context-dependent leaky scanning. Mol. Plant Microbe Interact. 12, 670–679 (1999).
Scholthof, H. B. et al. Identification of tomato bushy stunt virus host-specific symptom determinants by expression of individual genes from a potato virus X vector. Plant Cell 7, 1157–1172 (1995).
Qiu, W. & Scholthof, H. B. Effects of inactivation of the coat protein and movement genes of Tomato bushy stunt virus on early accumulation of genomic and subgenomic RNAs. J. Gen. Virol. 82, 3107–3114 (2001).
Rochon, D. M. Rapid de novo generation of defective interfering RNA by cucumber necrosis mutants that do not express the 20-kDa nonstructural protein. Proc. Natl Acad. Sci. USA 88, 11153–11157 (1991).
Dalmay, T. et al. Functional analysis of cymbidium ringspot virus genome. Virology 194, 697–704 (1993).
Scholthof, H. B. et al. Tomato bushy stunt virus spread is regulated by two nested genes that function in cell-to-cell movement and host-dependent systemic invasion. Virology 213, 425–438 (1995).
Chu, M. et al. Genetic dissection of tomato bushy stunt virus p19-protein-mediated host-dependent symptom induction and systemic invasion. Virology 266, 79–87 (2000).
Turina, M. et al. A newly identified role for the Tomato bushy stunt virus P19 in short distance spread. Molec. Plant Pathol. 4, 67–72 (2003).
Vargason, J. M. et al. Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115, 799–811 (2003).
Scholthof, K. -B. G. et al. The effect of defective interfering RNAs on the accumulation of tomato bushy stunt virus proteins and implications for disease attenuation. Virology 211, 324–328 (1995).
Voinnet, O. Induction and suppression of RNA silencing: insights from viral infections. Nature Rev. Genetics 6, 206–220 (2005).
Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13079–13084 (1998).
Brigneti, G. et al. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739–6746 (1998).
Kasschau, K. D. & Carrington, J. C. A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95, 461–470 (1998).
Voinnet, O. et al. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl Acad. Sci. USA 96, 14147–14152 (1999).
Roth, B. M. et al. Plant viral suppressors of RNA silencing. Virus Res. 102, 97–108 (2004).
Scholthof, H. B. Plant virus transport: motions of functional equivalence. Trends Plant Sci. 10, 376–382 (2005).
Qu, F. & Morris, T. J. Suppressors of RNA silencing encoded by plant viruses and their role in virus infection. FEBS Lett. 579, 5958–5964 (2005).
Silhavy, D. & Burgyan, J. Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci. 9, 76–83 (2004).
Li, H. W. & Ding, S. W. Antiviral silencing in animals. FEBS Lett. 579, 5965–5973 (2005).
Baulcombe, D. RNA silencing in plants. Nature 431, 356–363 (2004).
Szittya, G. et al. Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell 14, 1–15 (2002).
Qu, F. & Morris, T. J. 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. 15, 193–202 (2002).
Qiu, W. P. et al. Tombusvirus P19-mediated suppression of virus induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol. Plant Microbe Interact. 15, 269–280 (2002).
Havelda, Z. et al. In situ characterization of cymbidium ringspot tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana. J. Virol. 77, 6082–6086 (2003).
Silhavy, D. et al. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21, 3070–3080 (2002).
Szittya, G. et al. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J. 22, 633–640 (2003).
Papp, I. et al. Evidence for nuclear processing of plant microRNA and short-interfering RNA precursors. Plant Physiol. 132, 1382–1390 (2003).
Uhrig, J. F. et al. Relocalization of nuclear ALY proteins to the cytoplasm by the tomato bushy stunt virus P19 pathogenicity protein. Plant Physiol. 135, 2411–2423 (2004).
Park, J. -W. et al. The multifunctional plant viral suppressor of gene silencing P19 interacts with itself and an RNA binding host protein. Virology 323, 49–58 (2004).
Lakatos, L. et al. Molecular mechanism of RNA silencing suppression mediated by the P19 protein of tombusviruses. EMBO J. 23, 876–884 (2004).
Desvoyes, B. et al. A novel plant homeodomain protein interacts in a functionally relevant manner with a virus movement protein. Plant Physiol. 129, 1521–1532 (2002).
Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104 (2004).
Dunoyer, P. et al. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nature Genet. 37, 1356–1360 (2005).
Molnar, A. et al. Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol. 79, 7812–7818 (2005).
Ye, K. et al. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426, 874–878 (2003).
Chapman, E. et al. Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18, 1179–1186 (2004).
Dunoyer, P. et al. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16, 1235–1250 (2004).
Li, W. X. et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl Acad. Sci. USA 101, 1350–1355 (2004).
Lecellier, C. H. et al. A cellular microRNA mediates antiviral defense in human cells. Science 308, 557–560 (2005).
Lu, R. et al. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436, 1040–1043 (2005).
Voinnet, O. et al. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003).
Burgyan, J. et al. The ORF1 products of tombusviruses play a crucial role in lethal necrosis of virus-infected plants. J. Virol. 74, 10873–10881 (2000).
Omarov, R. et al. Biological relevance of a stable interaction between the tombusvirus-encoded P19 and siRNAs. J. Virol. (in the press).
Scholthof, H. B. et al. The capsid protein gene of tomato bushy stunt virus is dispensable for systemic movement and can be replaced for localized expression of foreign genes. Mol. Plant Microbe Interact. 6, 309–322 (1993).
Zamore, P. D. Plant RNAi: how a viral silencing suppressor inactivates siRNA. Curr. Biol. 14, 198–200 (2004).
Havelda, Z. et al. Defective interfering RNA hinders the activity of a tombusvirus-encoded posttranscriptional gene silencing suppressor. J. Virol. 79, 450–457 (2005).
Rochon, D. M. & Tremaine, J. H. Complete nucleotide sequence of the cucumber necrosis virus genome. Virology 169, 251–259 (1989).
Acknowledgements
I thank R. Omarov and K.-B. G. Scholthof for providing helpful suggestions, and J. Hsieh for customizing the P19 structure representation. Funding for our TBSV work was provided by the National Science Foundation.
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Scholthof, H. The Tombusvirus-encoded P19: from irrelevance to elegance. Nat Rev Microbiol 4, 405–411 (2006). https://doi.org/10.1038/nrmicro1395
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DOI: https://doi.org/10.1038/nrmicro1395
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