Skip to main content
SpringerLink
Log in

The triple gene block movement proteins of a grape virus in the genus Foveavirus confer limited cell-to-cell spread of a mutant Potato virus X

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Grapevine rupestris stem pitting-associated virus (GRSPaV) is a member of the genus Foveavirus in the family Betaflexiviridae. The genome of GRSPaV encodes five proteins, among which are three movement proteins designated the triple gene block (TGB) proteins. The TGB proteins of GRSPaV are highly similar to their counterparts in Potato virus X (PVX), as reflected in size, modular structure, conservation of critical amino acid sequence motifs, as well as similar cellular localization. Based on these similarities, we predicted that the TGB proteins of these two viruses would be interchangeable. To test this hypothesis, we replaced the entire or partial sequence of PVX TGB with the corresponding regions from GRSPaV, creating chimeric viruses that contain the PVX backbone and different sequences from GRSPaV TGB. These chimeric constructs were delivered into plants of Nicotiana benthamiana through agro-infiltration to test whether they were capable of cell-to-cell and systemic movement. To our surprise, viruses derived from pPVX.GFP(CH3) bearing GRSPaV TGB in place of PVX TGB lost the ability to move either cell-to-cell or systemically. Interestingly, another chimeric virus resulting from pPVX.GFP(HY2) containing four TGB genes (TGB1 from PVX and TGB1-3 from GRSPaV), exhibited limited cell-to-cell, but not systemic, movement. Our data question the notion that analogous movement proteins encoded by even distantly related viruses are functionally interchangeable and can be replaced by each other. These data suggest that other factors, besides the TGB proteins, may be required for successful intercellular and/or systemic movement of progeny viruses. This is the first experimental demonstration that the GRSPaV TGB function as movement proteins in the context of a chimeric virus and that four TGB genes were required to support the intercellular movement of the chimeric virus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. J.G. Atabekov, N.P. Rodionova, O.V. Karpova, S.V. Kozlovsky, V.Y. Poljakov, Virology 271, 259 (2000)

    Article  PubMed  CAS  Google Scholar 

  2. D.C. Baulcombe, S. Chapman, S. Santa Cruz, Plant J 7, 1045–1053 (1995)

    Article  PubMed  CAS  Google Scholar 

  3. S. Chapman, T. Kavanagh, D. Baulcome, Plant J. 2, 549–557 (1992)

    PubMed  CAS  Google Scholar 

  4. C.M. Deom, X.Z. He, R.N. Beachy, A.K. Weissinger, Virology 205, 198–209 (1994)

    Article  PubMed  CAS  Google Scholar 

  5. O. Fedorkin, A. Solovyev, N. Yelina, A. Zamyatnin, R. Zinovkin, K. Makinen, J. Schiemann, S. Yu Morozov, J. Gen. Virol. 82, 449–458 (2001)

    PubMed  CAS  Google Scholar 

  6. C.A. Fenczik, H.S. Padgett, C.A. Holt, S.J. Casper, R.N. Beachy, Mol. Plant Microbe Interact. 8, 666–673 (1995)

    Article  PubMed  CAS  Google Scholar 

  7. D. Giesman-Cookmeyer, S. Silver, A.A. Vaewhongs, S.A. Lommel, C.M. Deom, Virology 213, 38–45 (1995)

    Article  PubMed  CAS  Google Scholar 

  8. S. Haupt, G.H. Cowan, A. Ziegler, A.G. Roberts, K.J. Oparka, L. Torrance, Plant Cell 17, 164–181 (2005)

    Article  PubMed  CAS  Google Scholar 

  9. A.R. Howard, M.L. Heppler, H.J. Ju, K. Krishnamurthy, M.E. Payton, J. Verchot-Lubicz, Virology 328, 185–197 (2004)

    Article  PubMed  CAS  Google Scholar 

  10. A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz. Virus taxonomy: 9th Report of the international committee on the taxonomy of viruses. Academic Press

  11. E.V. Koonin, V.V. Dolja, Crit. Rev. Biochem. Mol. Biol. 28, 375–430 (1993)

    Article  PubMed  CAS  Google Scholar 

  12. E. Lauber, C. Bleykasten-Grosshans, M. Erhardt, S. Bouzoubaa, G. Jonard, K.E. Richards, H. Guilley, Mol. Plant Microbe Interact. 11, 618–625 (1998)

    Article  PubMed  CAS  Google Scholar 

  13. J.A. Lindbo, BMC Biotechnol. 7, 52 (2007)

    Article  PubMed  Google Scholar 

  14. T.J. Lough, N.E. Netzler, S.J. Emerson, P. Sutherland, F. Carr, D.L. Beck, W.J. Lucas, R.L. Forster, Mol. Plant Microbe Interact. 13, 962–974 (2000)

    Article  PubMed  CAS  Google Scholar 

  15. W.J. Lucas, Virology 344, 169–184 (2006)

    Article  PubMed  CAS  Google Scholar 

  16. J. Matousek, J. Schubert, P. Dedic, Virus Res. 146, 81–88 (2009)

    Article  PubMed  CAS  Google Scholar 

  17. B. Meng, D. Gonsalves, Plant Viruses 1, 52–62 (2007)

    Google Scholar 

  18. B. Meng, S.Z. Pang, P.L. Forsline, J.R. McFerson, D. Gonsalves, J. Gen. Virol. 79, 2059–2069 (1998)

    PubMed  CAS  Google Scholar 

  19. B. Meng, R. Credi, N. Petrovic, I. Tomazic, D. Gonsalves, Plant Dis. 87, 515–522 (2003)

    Article  CAS  Google Scholar 

  20. B. Meng, S. Venkataraman, C. Li, W. Wang, C. Dayan-Glick, M. Mawassi, Virology 435, 453–462 (2013)

    Article  PubMed  CAS  Google Scholar 

  21. K. Mise, R.F. Allison, M. Janda, P. Ahlquist, J. Virol. 67, 2815–2823 (1993)

    PubMed  CAS  Google Scholar 

  22. S.Y. Morozov, A.G. Solovyev, J. Gen. Virol. 84, 1351–1366 (2003)

    Article  PubMed  CAS  Google Scholar 

  23. S.Y. Morozov, A.G. Solovyev, N.O. Kalinina, O.N. Fedorkin, O.V. Samuilova, J. Schiemann, J.G. Atabekov, Virology 260, 55–63 (1999)

    Article  PubMed  CAS  Google Scholar 

  24. A. Nejidat, F. Cellier, A. Holt, R. Gafny, A.L. Eggenberger, R.N. Beachy, Virology 180, 318–326 (1991)

    Article  PubMed  CAS  Google Scholar 

  25. K.J. Oparka, A.G. Roberts, P. Boevink, S. Santa Cruz, I. Roberts, K.S. Pradel, A. Imlau, G. Kotlizky, n. Cell 97, 743–754 (1999)

    Article  PubMed  CAS  Google Scholar 

  26. N. Petrovic, B. Meng, M. Ravnikar, I. Mavric, D. Gonsalves, Plant Dis. 87, 510–514 (2003)

    Article  CAS  Google Scholar 

  27. I.T. Petty, A.O. Jackson, Virology 179, 712–718 (1990)

    Article  PubMed  CAS  Google Scholar 

  28. A.L. Rao, B. Cooper, C.M. Deom, Phytopathology 88, 666–672 (1998)

    Article  PubMed  CAS  Google Scholar 

  29. A.R. Rebelo, S. Niewiadomski, S.W. Prosser, P. Krell, B. Meng, Virus Res. 138, 57–69 (2008)

    Article  PubMed  CAS  Google Scholar 

  30. J. Sambrook, D.W. Russell, Molecular cloning: a laboratory manual (Cold Spring Harbor Laboratory, New York, 2001)

    Google Scholar 

  31. H.B. Scholthof, Trends Plant Sci. 10, 376–382 (2005)

    Article  PubMed  CAS  Google Scholar 

  32. A.G. Solovyev, E.I. Savenkov, V.Z. Grdzelishvili, N.O. Kalinina, S.Y. Morozov, J. Schiemann, J.G. Atabekov, Virology 253, 278–287 (1999)

    Article  PubMed  CAS  Google Scholar 

  33. M. Taliansky, L. Torrance, N.O. Kalinina, Methods Mol. Biol. 451, 33–54 (2008)

    Article  PubMed  CAS  Google Scholar 

  34. A. Tamai, K. Kubota, H. Nagano, M. Yoshii, M. Ishikawa, K. Mise, T. Meshi, Virology 315, 56–67 (2003)

    Article  PubMed  CAS  Google Scholar 

  35. J. Verchot-Lubicz, L. Torrance, A.G. Solovyev, S.Y. Morozov, A.O. Jackson, D. Gilmer, Mol. Plant Microbe Interact. 23, 1231–1247 (2010)

    Article  PubMed  CAS  Google Scholar 

  36. E. Waigmann, S. Ueki, K. Trutnyeva, V. Citovsky, Crit. Rev. Plant Sci. 23, 195–250 (2004)

    Article  CAS  Google Scholar 

  37. C. Xiang, P. Han, I. Lutziger, K. Wang, D.J. Oliver, Plant Mol. Biol. 40, 711–717 (1999)

    Article  PubMed  CAS  Google Scholar 

  38. Y. Zhang, J.K. Uyemoto, D. Golino, A. Rowhani, Phytopathology 88, 1231–1237 (1998)

    Article  PubMed  CAS  Google Scholar 

  39. V. Ziegler-Graff, P.J. Guilford, D.C. Baulcombe, Virology 182, 145–155 (1991)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study is supported by an NSERC Discovery Grant (400163) awarded to B. Meng. The authors thank Dr. S. Venkataraman for help with Northern blotting, Dr. J. Verchot-Lubicz (Oklahoma State University) for the PVX infectious clone, and Dr. D. J. Oliver (Iowa State University) for the binary plasmid vector pCB301.

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, University of Guelph, 50 Stone Road, Guelph, ON, N1G 2W1, Canada

    Krinpreet Mann & Baozhong Meng

Authors
  1. Krinpreet Mann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Baozhong Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Baozhong Meng.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mann, K., Meng, B. The triple gene block movement proteins of a grape virus in the genus Foveavirus confer limited cell-to-cell spread of a mutant Potato virus X . Virus Genes 47, 93–104 (2013). https://doi.org/10.1007/s11262-013-0908-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-013-0908-0

Keywords

Search

Navigation