1887

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Volume 87, Issue 2

Host-induced avirulence of hibiscus chlorotic ringspot virus mutants correlates with reduced gene-silencing suppression activity Free

Abstract

Post-transcriptional gene silencing (PTGS) and virus-encoded gene-silencing suppressors are defence and counterdefence strategies developed by host and pathogens during evolution. Using a green fluorescence protein-based transient suppression system, the coat protein (CP) of (HCRSV) was identified as a strong gene-silencing suppressor. CP suppressed sense RNA-induced but not dsRNA-induced local and systemic PTGS. This is different from another virus in the genus , (TCV), the CP of which strongly suppresses dsRNA-induced PTGS. HCRSV CP domain deletion mutants lost their suppression function, indicating that the complete CP is essential for suppression of PTGS. When CP was expressed from a (PVX) vector, it was able to enhance the symptom severity and to increase the accumulation of PVX RNA. Here, it is proposed that HCRSV CP suppresses PTGS at the initiation step, which is different from TCV CP. In addition, a previous study demonstrated that CP mutants resulting from serial passage of HCRSV in its local lesion host also showed a significantly reduced suppression function, indicating that host-induced mutations that lead to avirulence of HCRSV in kenaf correlate with its reduced ability to suppress PTGS.

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2006-02-01
2024-04-27
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References

  1. Allen E., Xie Z., Gustafson A. M., Carrington J. C. 2005; microRNA-directed phasing during trans -acting siRNA biogenesis in plants. Cell 121:207–221 [CrossRef]
     [Google Scholar]
  2. Anandalakshmi R., Pruss G. J., Ge X., Marathe R., Mallory A. C., Smith T. H., Vance V. B. 1998; A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95:13079–13084 [CrossRef]
     [Google Scholar]
  3. Choi C. W., Qu F., Ren T., Ye X., Morris T. J. 2004; RNA silencing-suppressor function of Turnip crinkle virus coat protein cannot be attributed to its interaction with the Arabidopsis protein TIP. J Gen Virol 85:3415–3420 [CrossRef]
     [Google Scholar]
  4. Cogoni C., Macino G. 1999; Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169 [CrossRef]
     [Google Scholar]
  5. Doan D. N., Lee K. C., Laurinmäki P., Butcher S., Wong S.-M., Dokland T. 2003; Three-dimensional reconstruction of hibiscus chlorotic ringspot virus. J Struct Biol 144:253–261 [CrossRef]
     [Google Scholar]
  6. Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. 1998; Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans . Nature 391:806–811 [CrossRef]
     [Google Scholar]
  7. 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]
  8. 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]
  9. Hannon G. J. 2002; RNA interference. Nature 418:244–251 [CrossRef]
     [Google Scholar]
  10. Huang M., Koh D. C.-Y., Weng L.-J., Chang M.-L., Yap Y.-K., Zhang L., Wong S.-M. 2000; Complete nucleotide sequence and genome organization of Hibiscus chlorotic ringspot virus, a new member of the genus Carmovirus : evidence for the presence and expression of two novel open reading frames. J Virol 74:3149–3155 [CrossRef]
     [Google Scholar]
  11. Hurtt S. S. 1987; Detection and comparison of electrophorotypes of hibiscus chlorotic ringspot virus. Phytopathology 77:845–850 [CrossRef]
     [Google Scholar]
  12. 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]
  13. Lee K.-C., Lim D., Wong S.-M., Dokland T. 2003; Purification, crystallization and X-ray analysis of Hibiscus chlorotic ringspot virus. Acta Crystallogr D Biol Crystallogr 59:1481–1483 [CrossRef]
     [Google Scholar]
  14. Li H.-W., Lucy A. P., Guo H.-S., Li W.-X., Ji L.-H., Wong S.-M., Ding S.-W. 1999; Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. EMBO J 18:2683–2691 [CrossRef]
     [Google Scholar]
  15. Liang X.-Z., Lee B. T. K., Wong S.-M. 2002a; Covariation in the capsid protein of hibiscus chlorotic ringspot virus induced by serial passaging in a host that restricts movement leads to avirulence in its systemic host. J Virol 76:12320–12324 [CrossRef]
     [Google Scholar]
  16. Liang X.-Z., Lucy A. P., Ding S.-W., Wong S.-M. 2002b; The p23 protein of hibiscus chlorotic ringspot virus is indispensable for host-specific replication. J Virol 76:12312–12319 [CrossRef]
     [Google Scholar]
  17. Lu R., Folimonov A., Shintaku M., Li W.-X., Falk B. W., Dawson W. O., 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 [CrossRef]
     [Google Scholar]
  18. Mlotshwa S., Voinnet O., Mette M. F., Matzke M., Vaucheret H., Ding S. W., Pruss G., Vance V. B. 2002; RNA silencing and the mobile silencing signal. Plant Cell 14 (Suppl.), S289–S301 [CrossRef]
     [Google Scholar]
  19. Napoli C., Lemieux C., 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 [CrossRef]
     [Google Scholar]
  20. Palauqui J.-C., Elmayan T., Pollien J.-M., Vaucheret H. 1997; Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745 [CrossRef]
     [Google Scholar]
  21. Peragine A., Yoshikawa M., Wu G., Albrecht H. L., Poethig R. S. 2004; SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans -acting siRNAs in Arabidopsis . Genes Dev 18:2368–2379 [CrossRef]
     [Google Scholar]
  22. 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 viruses. Plant Cell 9:859–868 [CrossRef]
     [Google Scholar]
  23. Qi Y., Zhong X., Itaya A., 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:e179 [CrossRef]
     [Google Scholar]
  24. Qu F., Ren T., 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 [CrossRef]
     [Google Scholar]
  25. Silhavy D., Molnár A., Lucioli A., Szittya G., Hornyik C., Tavazza M., Burgyán J. 2002; A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080 [CrossRef]
     [Google Scholar]
  26. 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 [CrossRef]
     [Google Scholar]
  27. Te J., Melcher U., Howard A., Verchot-Lubicz J. 2005; Soilborne wheat mosaic virus (SBWMV) 19K protein belongs to a class of cysteine rich proteins that suppress RNA silencing. Virol J 2:18 [CrossRef]
     [Google Scholar]
  28. Thomas C. L., Leh V., Lederer C., Maule A. J. 2003; Turnip crinkle virus coat protein mediates suppression of RNA silencing in Nicotiana benthamiana . Virology 306:33–41 [CrossRef]
     [Google Scholar]
  29. Vance V., Vaucheret H. 2001; RNA silencing in plants – defense and counterdefense. Science 292:2277–2280 [CrossRef]
     [Google Scholar]
  30. Van der Krol A. R., Mur L. A., Beld M., Mol J. N. M., Stuitje A. R. 1990; Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299 [CrossRef]
     [Google Scholar]
  31. Voinnet O. 2005; Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220 [CrossRef]
     [Google Scholar]
  32. Voinnet O., Baulcombe D. C. 1997; Systemic signalling in gene silencing. Nature 389:553 [CrossRef]
     [Google Scholar]
  33. 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]
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Host-induced avirulence of hibiscus chlorotic ringspot virus mutants correlates with reduced gene-silencing suppression activity
J. Gen. Virol. 87, 451 (2006); https://doi.org/10.1099/vir.0.81578-0
/content/journal/jgv/10.1099/vir.0.81578-0
/content/journal/jgv/10.1099/vir.0.81578-0
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