1887

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Volume 95, Issue 12

A viral transcription factor exhibits antiviral RNA silencing suppression activity independent of its nuclear localization Free

Abstract

Viral suppressors of RNA silencing (VSRs) are critical for the success of virus infection and efficient accumulation of virus progeny. The chrysanthemum virus B p12 protein acts as a transcription factor to regulate cell size and proliferation favourable for virus infection. Here, we showed that the p12 protein suppressed RNA silencing and was able to complement a VSR-deficient unrelated virus. Moreover, p12 counter-silencing activity could be uncoupled from its function as a transcription factor in the nucleus. The altered p12 protein, which lacked a nuclear localization signal and was not imported into the nucleus, was able to suppress RNA silencing as efficiently as the native protein. The data revealed new aspects of p12 functioning and identified a novel role for this viral zinc-finger transcription factor. The results provided a general insight into one of the activities of the p12 protein, which appeared to possess more than one function.

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
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2014-12-01
2024-04-18
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References

  1. Bragg J. N., Jackson A. O. 2004; The C-terminal region of the Barley stripe mosaic virusγb protein participates in homologous interactions and is required for suppression of RNA silencing. Mol Plant Pathol 5:465–481 [View Article][PubMed]
     [Google Scholar]
  2. Burgyán J., Havelda Z. 2011; Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272 [View Article][PubMed]
     [Google Scholar]
  3. Ding S. W. 2010; RNA-based antiviral immunity. Nat Rev Immunol 10:632–644 [View Article][PubMed]
     [Google Scholar]
  4. Donald R. G., Jackson A. O. 1994; The barley stripe mosaic virus 2b gene encodes a multifunctional cysteine-rich protein that affects pathogenesis. Plant Cell 6:1593–1606[PubMed]
     [Google Scholar]
  5. Du Z., Chen A., Chen W., Liao Q., Zhang H., Bao Y., Roossinck M. J., Carr J. P. 2014; Nuclear-cytoplasmic partitioning of cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J Virol 88:5228–5241 [View Article][PubMed]
     [Google Scholar]
  6. Dunoyer P., Herzog E., Hemmer O., Ritzenthaler C., Fritsch C. 2001; Peanut clump virus RNA-1-encoded P15 regulates viral RNA accumulation but is not abundant at viral RNA replication sites. J Virol 75:1941–1948 [View Article][PubMed]
     [Google Scholar]
  7. Dunoyer P., Pfeffer S., Fritsch C., Hemmer O., Voinnet O., Richards K. E. 2002; Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J 29:555–567 [View Article][PubMed]
     [Google Scholar]
  8. González I., Rakitina D., Semashko M., Taliansky M., Praveen S., Palukaitis P., Carr J. P., Kalinina N., Canto T. 2012; RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA 18:771–782 [View Article][PubMed]
     [Google Scholar]
  9. Ham B. K., Lee T. H., You J. S., Nam Y. W., Kim J. K., Paek K. H. 1999; Isolation of a putative tobacco host factor interacting with cucumber mosaic virus-encoded 2b protein by yeast two-hybrid screening. Mol Cells 9:548–555[PubMed]
     [Google Scholar]
  10. Incarbone M., Dunoyer P. 2013; RNA silencing and its suppression: novel insights from in planta analyses. Trends Plant Sci 18:382–392 [View Article][PubMed]
     [Google Scholar]
  11. Liu H. B., Reavy B., Swanson M., MacFarlane S. A. 2002; Functional replacement of the tobacco rattle virus cysteine-rich protein by pathogenicity proteins from unrelated plant viruses. Virology 298:232–239 [View Article][PubMed]
     [Google Scholar]
  12. Lukhovitskaya N. I., Yelina N. E., Zamyatnin A. A. Jr, Schepetilnikov M. V., Solovyev A. G., Sandgren M., Morozov S. Y., Valkonen J. P., Savenkov E. I. 2005; Expression, localization and effects on virulence of the cysteine-rich 8 kDa protein of Potato mop-top virus. J Gen Virol 86:2879–2889 [View Article][PubMed]
     [Google Scholar]
  13. Lukhovitskaya N. I., Ignatovich I. V., Savenkov E. I., Schiemann J., Morozov S. Y., Solovyev A. G. 2009; Role of the zinc-finger and basic motifs of chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector. J Gen Virol 90:723–733 [View Article][PubMed]
     [Google Scholar]
  14. Lukhovitskaya N. I., Thaduri S., Garushyants S. K., Torrance L., Savenkov E. I. 2013a; Deciphering the mechanism of defective interfering RNA (DI RNA) biogenesis reveals that a viral protein and the DI RNA act antagonistically in virus infection. J Virol 87:6091–6103 [View Article][PubMed]
     [Google Scholar]
  15. Lukhovitskaya N. I., Solovieva A. D., Boddeti S. K., Thaduri S., Solovyev A. G., Savenkov E. I. 2013b; An RNA virus-encoded zinc-finger protein acts as a plant transcription factor and induces a regulator of cell size and proliferation in two tobacco species. Plant Cell 25:960–973 [View Article][PubMed]
     [Google Scholar]
  16. Lukhovitskaya N. I., Gushchin V. A., Solovyev A. G., Savenkov E. I. 2013c; Making sense of nuclear localization: a zinc-finger protein encoded by a cytoplasmically replicating plant RNA virus acts a transcription factor: a novel function for a member of large family of viral proteins. Plant Signal Behav 8:e25263 [View Article][PubMed]
     [Google Scholar]
  17. Martín-Hernández A. M., Baulcombe D. C. 2008; Tobacco rattle virus 16-kilodalton protein encodes a suppressor of RNA silencing that allows transient viral entry in meristems. J Virol 82:4064–4071 [View Article][PubMed]
     [Google Scholar]
  18. Martínez-Priego L., Donaire L., Barajas D., Llave C. 2008; Silencing suppressor activity of the Tobacco rattle virus-encoded 16-kDa protein and interference with endogenous small RNA-guided regulatory pathways. Virology 376:346–356 [View Article][PubMed]
     [Google Scholar]
  19. Powers J. G., Sit T. L., Qu F., Morris T. J., Kim K. H., Lommel S. A. 2008; A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement. Mol Plant Microbe Interact 21:879–890 [View Article][PubMed]
     [Google Scholar]
  20. Pumplin N., Voinnet O. 2013; RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760 [View Article][PubMed]
     [Google Scholar]
  21. Savenkov E. I., Valkonen J. P. 2001; Potyviral helper-component proteinase expressed in transgenic plants enhances titers of Potato leaf roll virus but does not alleviate its phloem limitation. Virology 283:285–293 [View Article][PubMed]
     [Google Scholar]
  22. Senshu H., Yamaji Y., Minato N., Shiraishi T., Maejima K., Hashimoto M., Miura C., Neriya Y., Namba S. 2011; A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol 85:10269–10278 [View Article][PubMed]
     [Google Scholar]
  23. Sueda K., Shimura H., Meguro A., Uchida T., Inaba J., Masuta C. 2010; The C-terminal residues of the 2b protein of Cucumber mosaic virus are important for efficient expression in Escherichia coli and DNA-binding. FEBS Lett 584:945–950 [View Article][PubMed]
     [Google Scholar]
  24. Szittya G., Burgyán J. 2013; RNA interference-mediated intrinsic antiviral immunity in plants. Curr Top Microbiol Immunol 371:153–181[PubMed]
     [Google Scholar]
  25. Wang Y., Tzfira T., Gaba V., Citovsky V., Palukaitis P., Gal-On A. 2004; Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J Gen Virol 85:3135–3147 [View Article][PubMed]
     [Google Scholar]
  26. Yelina N. E., Savenkov E. I., Solovyev A. G., Morozov S. Y., Valkonen J. P. 2002; Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei- and potyviruses: complementary functions between virus families. J Virol 76:12981–12991 [View Article][PubMed]
     [Google Scholar]
  27. Yelina N. E., Erokhina T. N., Lukhovitskaya N. I., Minina E. A., Schepetilnikov M. V., Lesemann D. E., Schiemann J., Solovyev A. G., Morozov S. Y. 2005; Localization of Poa semilatent virus cysteine-rich protein in peroxisomes is dispensable for its ability to suppress RNA silencing. J Gen Virol 86:479–489 [View Article][PubMed]
     [Google Scholar]
  28. Zamyatnin A. A. Jr, Solovyev A. G., Bozhkov P. V., Valkonen J. P., Morozov S. Y., Savenkov E. I. 2006; Assessment of the integral membrane protein topology in living cells. Plant J 46:145–154 [View Article][PubMed]
     [Google Scholar]
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A viral transcription factor exhibits antiviral RNA silencing suppression activity independent of its nuclear localization
J. Gen. Virol. 95, 2831 (2014); https://doi.org/10.1099/vir.0.067884-0
/content/journal/jgv/10.1099/vir.0.067884-0
/content/journal/jgv/10.1099/vir.0.067884-0
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