1887

Abstract

This study investigated the effects of silencing suppressors derived from six different viruses (P1, P19, P25, HcPro, AC2 and 2b), expressed in transgenic and plants, on the infection pattern of tobacco ringspot virus (TRSV) potato calico strain. In , this virus produced an initial infection with severe systemic symptoms, but the infection was strongly reduced within a few weeks as the plant recovered from the infection. P25 and HcPro silencing suppressors effectively prevented recovery in this host, allowing continuous accumulation of the viral RNA as well as of the virus-specific small interfering RNAs, in the systemically infected leaves. In the P1-, P19-, AC2- or 2b-expressing transgenic , the recovery was not complete. Susceptibility of to this virus was temperature sensitive. At lower temperatures, up to 25 °C, the plants became systemically infected, but at higher temperatures, the infections were limited to the inoculated leaves. In these preventative conditions, all silencing suppressor transgenes (except P25, which was expressed at very low levels) allowed the establishment of systemic infections. Very strong and consistent systemic infections were observed in HcPro- and AC2-expressing plants.

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2008-06-01
2024-04-19
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References

  1. Al-Kaff N. S., Covey S. N., Kreike M. M., Page A. M., Pinder R., Dale P. J. 1998; Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science 279:2113–2115 [CrossRef]
    [Google Scholar]
  2. Brigneti G., Voinnet O., Li W.-X., Ji L.-H., Ding S.-W., Baulcombe D. C. 1998; Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana . EMBO J 17:6739–6746 [CrossRef]
    [Google Scholar]
  3. Brunt A. A., Crabtree K., Dallwitz M. J., Gibbs A. J., Watson L., Zurcher E. J. editors 1996 onwards Plant viruses online: descriptions and lists from the VIDE database. Version 20 August 1996 http://biology.anu.edu.au/Groups/MES/vide
    [Google Scholar]
  4. Buchon N., Vaury C. 2006; RNAi: a defensive RNA-silencing against viruses and transposable elements. Heredity 96:195–202 [CrossRef]
    [Google Scholar]
  5. Close R. 1964; Some effects of other viruses and temperature on the multiplication of potato virus X. Ann Appl Biol 53:151–164 [CrossRef]
    [Google Scholar]
  6. Deleris A., Gallego-Bartolome J., Bao J., Kasschau K. D., Carrington J. C., Voinnet O. 2006; Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68–71 [CrossRef]
    [Google Scholar]
  7. Foster T. M., Lough T. J., Emerson S. J., Lee R. H., Bowman J. L., Forster R. L., Lucas W. J. A. 2002; A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508 [CrossRef]
    [Google Scholar]
  8. Fribourg C. E., Jones R. A. C., Koening R. 1977; Andean potato mottle, a new member of the cowpea mosaic virus group. Phytopathology 67:969–974
    [Google Scholar]
  9. Frison E. A., Stace-Smith R. 1992; Cross-reacting and heterospecific monoclonal anti-bodies produced against arabis mosaic nepovirus. J Gen Virol 73:2525–2530 [CrossRef]
    [Google Scholar]
  10. González-Jara P., Atencio F. A., Martínez-García B., Barajas D., Tenllado F., Díaz-Ruíz J. R. 2005; A single amino acid mutation in the plum pox virus helper component-proteinase gene abolishes both synergistic and RNA silencing suppression activities. Phytopathology 95:894–901 [CrossRef]
    [Google Scholar]
  11. 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 [CrossRef]
    [Google Scholar]
  12. Guo H. S., Ding S. W. 2002; A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21:398–407 [CrossRef]
    [Google Scholar]
  13. Hamilton A., Voinnet O., Chappell L., Baulcombe D. 2002; Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679 [CrossRef]
    [Google Scholar]
  14. Harris A., Gibbs A. J., Gibbs M. J. 2002 Nepovirus and their Diagnosis in Plants – a Novel Polymerase Chain Reaction Diagnostic Test for Nepovirus in Nursery Stock . Consultancy report Australia: Agriculture Fisheries and Forestry;
    [Google Scholar]
  15. 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 [CrossRef]
    [Google Scholar]
  16. Kasschau K. D., Carrington J. C. 1998; A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470 [CrossRef]
    [Google Scholar]
  17. Lecellier C.-H., Voinnet O. 2004; RNA silencing: no mercy for viruses?. Immunol Rev 198:285–303 [CrossRef]
    [Google Scholar]
  18. Lehto K., Siddiqui S. A. 2005; RNA-silencing in plant endogene regulation, and its disturbance caused by viral suppressors. Recent Res Dev Plant Sci 3:47–68
    [Google Scholar]
  19. Lewsey M., Robertson F. C., Canto T., Palukaitis P., Carr J. P. 2007; Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J 50:240–252 [CrossRef]
    [Google Scholar]
  20. Mallory A. C., Ely L., Smith T. H., Marathe R., Anandalakshmi R., Fagard M., Vaucheret H., Pruss G., Bowman L., Vance V. B. 2001; HC-Pro suppression of transgene silencing eliminates the small RNAs, but not transgene methylation or the mobile signal. Plant Cell 13:571–583 [CrossRef]
    [Google Scholar]
  21. Matzke M., Aufsatz W., Kanno T., Daxinger L., Papp I., Mette M. F., Matzke J. M. 2004; Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim Biophys Acta 1677129–141 [CrossRef]
    [Google Scholar]
  22. Murant A. F., Jones T. A., Martelli G. P., Stace-Smith R. 1996; Nepoviruses: general properties, diseases, and virus identification. In The Plant Viruses, Polyhedral Virions and Bipartite RNA Genomes . , 5th edn. pp 99–138Edited by Harrison B. D., Murant A. F. New York: Plenum Press;
  23. Pruss G., Ge X., Shi X. M., Carrington J. C., Vance V. B. 1997; Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous virus. Plant Cell 9:859–868 [CrossRef]
    [Google Scholar]
  24. Pruss G. J., Lawrence C. B., Bass T., Li Q. Q., Bowman L. H., Vance V. 2004; The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology 320:107–120 [CrossRef]
    [Google Scholar]
  25. Qu F., Morris T. J. 2005; Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS Lett 579:5958–5964 [CrossRef]
    [Google Scholar]
  26. Ratcliff F., Harrison B. D., Baulcombe D. C. 1997; A similarity between viral defense and gene silencing in plants. Science 276:1558–1560 [CrossRef]
    [Google Scholar]
  27. Ratcliff F. G., MacFarlane S. A., Baulcombe D. C. 1999; Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207–1216 [CrossRef]
    [Google Scholar]
  28. Roth B. M., Pruss G. J., Vance V. B. 2004; Plant viral suppressors of RNA silencing. Virus Res 102:97–108 [CrossRef]
    [Google Scholar]
  29. Sarmiento C., Nigul L., Kazantseva J., Buschmann M., Truve E. 2006; AtRLI2 is an endogenous suppressor of RNA silencing. Plant Mol Biol 61:153–163 [CrossRef]
    [Google Scholar]
  30. Schwach F., Vaistij F. E., Jones L., Baulcombe D. C. 2005; An RNA-dependent RNA polymerase prevents meristem invasion by Potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852 [CrossRef]
    [Google Scholar]
  31. Shams-Bakhsh M., Canto T., Palukaitis P. 2007; Enhanced resistance and neutralization of defence responses by suppressors of RNA silencing. Virus Res 130:103–109 [CrossRef]
    [Google Scholar]
  32. Siddiqui S. A., Sarmiento C., Valkonen S., Truve E., Lehto K. 2007; Suppression of infectious TMV genome in young transgenic tobacco plants. Mol Plant Microbe Interact 20:1489–1494 [CrossRef]
    [Google Scholar]
  33. Siddiqui S. A., Sarmiento C., Truve E., Lehto H., Lehto K. 2008; Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum . Mol Plant Microbe Interact 21:178–187 [CrossRef]
    [Google Scholar]
  34. Szittya G., Molnár A., Silhavy D., Hornyik C., Burgyán J. 2002; Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell 14:359–372 [CrossRef]
    [Google Scholar]
  35. Szittya G., Silhavy D., Molnár A., Havelda Z., Lovas A., Lakatos L., Banfalve Z., Burgyan J. 2003; Low temperature inhibits RNA silencing-mediated defense by the control of siRNA generation. EMBO J 22:633–640 [CrossRef]
    [Google Scholar]
  36. Trinks D., Rajeswaran R., Shivaprasad P. V., Akbergenov R., Oakeley E. J., Veluthambi K., Hohn T., Pooggin M. 2005; Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 79:2517–2527 [CrossRef]
    [Google Scholar]
  37. Vargason J. M., Szittya G., Burgyan J., Tanaka H. T. M. 2003; Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115:799–811 [CrossRef]
    [Google Scholar]
  38. Voinnet O. 2005a; Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220 [CrossRef]
    [Google Scholar]
  39. Voinnet O. 2005b; Non-cell autonomous RNA silencing. FEBS Lett 579:5858–5871 [CrossRef]
    [Google Scholar]
  40. Voinnet O., Pinto Y. M., Baulcombe D. C. 1999; Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96:14147–14152 [CrossRef]
    [Google Scholar]
  41. Waterhouse P. M., Wang M.-B., Lough T. 2001; Gene silencing as an adaptive defense against viruses. Nature 411:834–842 [CrossRef]
    [Google Scholar]
  42. Wingard S. A. 1928; Hosts and symptoms of ring spot, a virus disease of plants. J Agric Res 37:127–153
    [Google Scholar]
  43. Xie Z., Fan B., Chen C., Chen Z. 2001; An important role of an inducible RNA-dependent RNA polymerase in antiviral defence. Proc Natl Acad Sci U S A 11:6516–6521
    [Google Scholar]
  44. Zhang X., Yuan Y.-R., Pei Y., Shih-Shun Lin S.-S., Tuschl T., Patel D. J., Chua N.-H. 2006; Cucumber mosaic virus -encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20:3255–3268 [CrossRef]
    [Google Scholar]
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