Skip to main content

Advertisement

Log in

VPg of Potato virus A alone does not suppress RNA silencing but affects virulence of a heterologous virus

  • Original Article
  • Published:
Virus Genes Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

The viral genome-linked protein (VPg) is a well-known virulence factor in potyviruses (genus Potyvirus), including Potato virus A (PVA). Its ability to suppress onset and signalling of transgene-mediated RNA silencing and accumulation of small interfering RNA (siRNA) was studied using cross-protection and Agrobacterium infiltration assays and green fluorescent protein (GFP) and PVA VPg protein-expressing transgenic Nicotiana benthamiana plants. N. benthamiana plants were also transformed with a transgene comprising the cylindrical inclusion protein (CI), nuclear inclusion protein a (NIa) and coat protein (CP) encoding regions of PVA. This transgene mRNA was expressed in the T1 progeny of the transgenic lines but all were susceptible to PVA. This result contrasted the plants transformed with the PVA P1, VPg (N-proximal part of NIa) or CP encoding regions that expressed various forms of resistance. There was little evidence for direct involvement of VPg in suppression of silencing, while other mechanisms by which VPg might interfere with transgenic resistance could not be excluded. Expression of the wild-type PVA VPg from the genome of Potato virus X (PVX, genus Potexvirus) increased symptom severity in N. benthamiana, whereas a single point mutation introduced to the VPg enhanced accumulation of the PVX chimera. These data demonstrated previously unknown virulence functions controlled by the VPg of a potyvirus.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. D.M. Stark, R.N. Beachy, Bio-Technology 7, 1257 (1989)

    Google Scholar 

  2. C. Lawson, W. Kaniewski, L. Haley, R. Rozman, C. Newell, P. Sanders, N.E. Tumer, Bio-Technology 8, 127 (1990)

    CAS  PubMed  Google Scholar 

  3. J.A. Lindbo, W.G. Dougherty, Mol. Plant-Microbe Interact. 5, 144 (1992)

    Article  CAS  PubMed  Google Scholar 

  4. M.-L. Rajamäki, T. Mäki-Valkama, K. Mäkinen, J.P.T. Valkonen, in Plant-Pathogen Interactions, ed. by N.J. Talbot (Blackwell Publishing, Oxford, UK, 2004), pp. 68–91

  5. E.I. Savenkov, J.P.T. Valkonen, J. Gen. Virol. 82, 2275 (2001)

    Article  CAS  PubMed  Google Scholar 

  6. P. Audy, P. Palukaitis, S.A. Slack, M. Zaitlin, Mol. Plant-Microbe Interact. 7, 15 (1994)

    Article  CAS  PubMed  Google Scholar 

  7. T. Pehu, T. Mäki-Valkama, J.P.T. Valkonen, K. Koivu, K. Lehto, E. Pehu, Am. Potato J. 72, 523 (1995)

    Article  CAS  Google Scholar 

  8. T. Mäki-Valkama, J.P.T. Valkonen, J.F. Kreuze, E. Pehu, Mol. Plant-Microbe Interact. 13, 366 (2000)

    Article  PubMed  Google Scholar 

  9. E.I. Savenkov, J.P.T. Valkonen, J. Gen. Virol. 83, 2325 (2002)

    Article  CAS  PubMed  Google Scholar 

  10. T. Van den Boogaart, A.J. Maule, J.W. Davies, G.P. Lomonossoff, Mol. Plant Pathol. 5, 37 (2004)

    Article  Google Scholar 

  11. J.A. Lindbo, W.G. Dougherty, Ann. Rev. Phytopathol. 43, 191 (2005)

    Article  CAS  Google Scholar 

  12. O. Voinnet, Nature Rev Genet 6, 206 (2005)

    Article  CAS  PubMed  Google Scholar 

  13. W.G. Dougherty, T.D. Parks, Curr. Opinion Cell. Biol. 7, 399 (1995)

    Article  CAS  PubMed  Google Scholar 

  14. A. Fire, S. Xu, M.K. Montgomery, S.A. Kostas, S.E. Driver, C.C. Mello, Nature 391, 806 (1998)

    Article  CAS  PubMed  Google Scholar 

  15. E.A. Bernstein, A. Caudy, S.M. Hammond, G.J. Hannon, Nature 409, 363 (2001)

    Article  CAS  PubMed  Google Scholar 

  16. P. Dunoyer, C. Himber, O. Voinnet, Nat. Genet 37, 1356 (2005)

    Article  CAS  PubMed  Google Scholar 

  17. J.C. Palaqui, T. Elmayan, J.-M. Pollien, H. Vaucheret, EMBO J. 16, 4738 (1997)

    Article  Google Scholar 

  18. O. Voinnet, P. Vain, S. Angell, D.C. Baulcombe, Cell 95, 177 (1998)

    Article  CAS  Google Scholar 

  19. R.N. Beachy, Philos. Transact. Royal Soc. London B Biol. Sci. 354, 659 (1999)

    Article  CAS  Google Scholar 

  20. J.C. Carrington, R. Haldeman, V.V. Dolja, M.A. Restrepo-Hartwig, J. Virol. 67, 6995 (1993)

    CAS  PubMed  Google Scholar 

  21. J.F. Murphy, W. Rychlik, R.A. Rhoads, A.G. Hunt, J.G. Shaw, J. Virol. 65, 511 (1991)

    CAS  PubMed  Google Scholar 

  22. I. Oruetxebarria, D. Guo, A. Merits, K. Mäkinen, M. Saarma, J.P.T. Valkonen, Virus Res. 73, 103 (2001)

    Article  CAS  PubMed  Google Scholar 

  23. P. Puustinen, M.-L. Rajamäki, K. Ivanov, J.P.T. Valkonen, K. Mäkinen, J. Virol. 76, 12703 (2002)

    Article  CAS  PubMed  Google Scholar 

  24. M.-L. Rajamäki, J.P.T. Valkonen, Mol. Plant-Microbe Interact. 15, 138 (2002)

    Article  PubMed  Google Scholar 

  25. C. Robaglia, C. Caranta, Trends Plant Sci. 11, 40 (2006)

    Article  CAS  PubMed  Google Scholar 

  26. E. Vardi, I. Sela, O. Edelbaum, O. Livneh, L. Kuznetsova, Y. Stram, PNAS 90, 7513 (1993)

    Article  CAS  PubMed  Google Scholar 

  27. M.C. Schaad, R. Haldeman-Cahill, S. Cronin, J.C. Carrington, J. Virol. 70, 7039 (1996)

    CAS  PubMed  Google Scholar 

  28. J.P. Fellers, G.B. Collins, A.G. Hunt, Crop Sci. 38, 1309 (1998)

    Article  CAS  Google Scholar 

  29. I.B. Maiti, C. Von Lanken, Y.L. Hong, N. Dey, A.G. Hunt, J. Plant Biochem. Biotechnol. 8, 67 (1999)

    Article  CAS  Google Scholar 

  30. H.S. Guo M., Cervera, J.A. Garcia, Gene 206, 263 (1998)

    Article  CAS  PubMed  Google Scholar 

  31. A. Germundsson, J.P.T. Valkonen, Virus Res. 116, 208 (2006)

    Article  CAS  PubMed  Google Scholar 

  32. G. Brigneti, O. Voinnet, W.X. Li, L.H. Ji, S.W. Ding, D.C. Baulcombe, EMBO J. 17, 6739 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. A.C. Mallory, L. Ely, T.H. Smith, R. Marathe, R. Anandalakshmi, M. Fagard, Vaucheret H., Pruss G., Bowman L., Vance V.B., Plant Cell 13, 571 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. J.F. Kreuze, E.I. Savenkov, W. Cuellar, X. Li, J.P.T. Valkonen, J. Virol. 79, 7227 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ü. Puurand, J.P.T. Valkonen, K. Mäkinen, F. Rabenstein, M. Saarma, Virus Res. 40, 135 (1996)

    Article  CAS  PubMed  Google Scholar 

  36. K.O. Holmström, PhD thesis, Acta Universitatis Agriculturae Sueciae, Series Agraria, Uppsala, Sweden (1998)

  37. R. Deblaere, B. Bytebier, H. De Greve, F. Deboeck, J. Schnell, M. Van Montagu, J. Leemans, Nucl. Acids Res. 13, 477 (1985)

    Article  Google Scholar 

  38. D. Mattanovich, F. Ruker, A. de Camara Machado, M. Laimer, F. Regner, H. Steinkellner, G. Himmler, H. Katinger, Nucl. Acids Res. 17, 6747 (1989)

    Article  CAS  PubMed  Google Scholar 

  39. E.I. Savenkov, J.P.T. Valkonen, Virology 283, 285 (2001)

    Article  CAS  PubMed  Google Scholar 

  40. G. Vancanneyt, R. Schmidt, A. O´Connor-Sanchez, L. Willmitzer, M. Rocha-Sosa, Mol. Gen. Genet. 220, 245 (1990)

    Article  CAS  PubMed  Google Scholar 

  41. T. Murishage, F. Skoog, Physiol. Plant 15, 473 (1962)

    Article  Google Scholar 

  42. M. Erhardt, E. Herzog, E. Lauber, C. Fritsch, H. Guilley, G. Jonard, K. Richards, S. Bouzoubaa, Plant Cell Rep. 18, 614 (1999)

    Article  CAS  Google Scholar 

  43. M.L. Rajamäki, J.P.T. Valkonen, Mol. Plant-Microbe Interact. 12, 1074 (1999)

    Article  PubMed  Google Scholar 

  44. S. Shivprasad, G.P. Pogue, D.J. Lewandowski, J. Hidalgo, J. Donson, J.K. Grill, W.P. Dawson, Virology 255, 312 (1999)

    Article  CAS  PubMed  Google Scholar 

  45. P. Boevink, S. Santa Cruz, C. Hawes, N. Harris, K.J. Oparka, Plant J. 10, 935 (1996)

    Article  CAS  Google Scholar 

  46. N.E. Yelina, E.I. Savenkov, A.G. Solovyev, S.Y. Morozov, J.P.T. Valkonen, J. Virol. 317, 73 (2002)

    Google Scholar 

  47. I.T. Petty, B.G. Hunter, N. Wei, A.O. Jackson, Virology 171, 341 (1989)

    Article  Google Scholar 

  48. J.H. Hämäläinen, T. Kekarainen, C. Gebhardt, K.N. Watanabe, J.P.T. Valkonen, Mol. Plant-Microbe Interact. 13, 402 (2000)

    Article  PubMed  Google Scholar 

  49. M.-L. Rajamäki, A. Merits, F. Rabenstein, J. Andrejeva, L. Paulin, T. Kekarainen, J.F. Kreuze, R.L.S. Forster, J.P.T. Valkonen, Phytopathology 88, 311 (1998)

    Article  PubMed  Google Scholar 

  50. A.J. Hamilton, D.C. Baulcombe, Science 286, 950 (1999).

    Article  CAS  PubMed  Google Scholar 

  51. J. Sambrook, D.W. Russel, Molecular Cloning: A Laboratory Manual, 3rd edn. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 2001)

    Google Scholar 

  52. A. Merits, M.-L. Rajamäki, P. Lindholm, P. Runeberg-Roos, T. Kekarainen, P. Puustinen, K. Mäkeläinen, J.P.T. Valkonen, M. Saarma, J. Gen. Virol. 83, 1211 (2002)

    Article  CAS  PubMed  Google Scholar 

  53. P. Dunoyer, C. Thomas, S. Harrison, F. Revers, A.J. Maule, J. Virol. 78, 2301 (2004)

    Article  CAS  PubMed  Google Scholar 

  54. S. Léonard, D. Plante, S. Wittmann, N. Daigneault, M.G. Fortin, J.F. Laliberté, J. Virol. 74, 7730 (2000)

    Article  PubMed  Google Scholar 

  55. J.F. Murphy, P.G. Klein, A.G. Hunt, J.G. Shaw, Virology 220, 535 (1996)

    Article  CAS  PubMed  Google Scholar 

  56. F.G. Ratcliff, S.A. MacFarlane, D.C. Baulcombe, Plant Cell 11, 1207 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. H.S. Guo, S.W. Ding, EMBO J. 21, 398 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. L.K. Johansen, J.C. Carrington, Plant Physiol. 126, 930 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. J.A. Lindbo, L. Silva-Rosales, W.M. Proebsting, W.G. Dougherty, Plant Cell 5, 1749 (1993)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. A. Wittner, L. Palkovics, E. Balázs, Virus Res. 53, 97 (1998)

    Article  CAS  PubMed  Google Scholar 

  61. X.H. Li, P. Valdez, R.E. Olvera, J.C. Carrington, J Virol. 71, 1598 (1997)

    CAS  PubMed  Google Scholar 

  62. M.C. Schaad, A.D. Lellis, J.C. Carrington, J Virol. 71, 8624 (1997)

    CAS  PubMed  Google Scholar 

  63. K.E. Keller, I.E. Johansen, R.R. Martin, R.O. Hampton, Mol. Plant-Microbe. Interact 11, 124 (1998)

    Article  CAS  PubMed  Google Scholar 

  64. A. Duprat, C. Caranta, F. Revers, B. Menand, K.S. Browning, C. Robaglia, Plant J. 32, 927 (2002)

    Article  CAS  PubMed  Google Scholar 

  65. Z. Gao, E. Johansen, S. Eyers, C.L. Thomas, T.H.N. Ellis, A.J. Maule, Plant J 40, 376 (2004)

    Article  CAS  PubMed  Google Scholar 

  66. B.C. Kang, I. Yeam, J.D. Frantz, J.F. Murphy, M.M. Jahn Plant J 42, 392 (2005)

    Article  CAS  PubMed  Google Scholar 

  67. M. Sato, K. Nakahara, M. Yoshii, M. Ishikawa, I. Uyeda, FEBS Lett 579, 1167 (2005)

    Article  CAS  PubMed  Google Scholar 

  68. O. Voinnet, C. Lederer, D.C. Baulcombe, Cell 103, 157–167, (2000)

    Article  CAS  Google Scholar 

  69. R. Lu, A. Folimonov, M. Shintaku, W.X. Li, B.W. Falk, W.O. Dawson, S.W. Ding, PNAS 101, 15742 (2004)

    Article  CAS  PubMed  Google Scholar 

  70. J.P.T. Valkonen, M.L. Rajamäki, T. Kekarainen, Mol Plant-Microbe Interact 15, 683 (2002)

    Article  CAS  PubMed  Google Scholar 

  71. G. Pruss, X. Ge, M.X. Shi, J.C. Carrington, V.B. Vance, Plant Cell 9, 859 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. N.I. Lukhovitskaya, N.E. Yelina, A.A. Zamyatnin Jr., M.V. Schepetilnikov A.G., Solovyev, M. Sandgren, S.Yu. Morozov, J.P.T. Valkonen, E.I. Savenkov, J. Gen. Virol. 86, 2879 (2005)

    Article  CAS  PubMed  Google Scholar 

  73. T. Canto, S.A. MacFarlane, P. Palukaitis, J. Gen. Virol. 85, 3123 (2004)

    Article  CAS  PubMed  Google Scholar 

  74. J. Burgyán, C. Hornyik, G. Szittya, D. Silhavy, G. Bisztray, J. Virol. 74, 10873 (2000)

    Article  PubMed  PubMed Central  Google Scholar 

  75. L. Rubino, M. Russo, Virology 252, 431 (1998)

    Article  CAS  PubMed  Google Scholar 

  76. T. Panavas, C.M. Hawkins, Z. Panaviene, P.D. Nagy, Virology 338, 81 (2005)

    Article  CAS  PubMed  Google Scholar 

  77. A.D. Lellis, K.D. Kasschau, S.A. Whitham, J.C. Carrington, Curr. Biol .12, 1046 (2002)

    Article  CAS  PubMed  Google Scholar 

  78. S. Ruffel, M.H. Dussault, A. Palloix, B. Moury, A. Bendahmane, C. Robaglia, C. Caranta, Plant J. 32, 1067 (2002)

    Article  CAS  PubMed  Google Scholar 

  79. V. Nicaise, S. German-Retana, R. Sanjuan, M.P. Dubrana, M. Mazier, B. Maisonneuve, T. Candresse, C. Caranta, O. LeGall, Plant Physiol. 132, 1272 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. D. Plante, C. Viel, S. Léonard, H. Tamp, J.F. Laliberté, M.G. Fortin, Physiol. Mol. Plant Pathol. 64, 219 (2004)

    Article  CAS  Google Scholar 

  81. S. Cotton, P.J. Dufresne, K. Thivierge, C. Ide, M.G. Fortin. Virology 351, 92 (2006)

    Article  CAS  PubMed  Google Scholar 

  82. R. Grzela, L. Strokovska, J.P. Andrieu, B. Dublet, W. Zagorski, J. Chroboczek, Biochimie, 88, 887 (2006)

    Article  CAS  PubMed  Google Scholar 

  83. S. Léonard, C. Viel, C. Beauchemin, N. Daigneault, M.G. Fortin, J.F. Laliberté, J. Gen. Virol. 85, 1055 (2004)

    Article  PubMed  CAS  Google Scholar 

  84. D.D. Bilgin, Y. Liu, M. Schiff, S.P. Dinesh-Kumar, Devel. Cell 4, 651 (2003)

    Article  CAS  Google Scholar 

  85. M. Fagard, S. Boutet, J.B. Morel, C. Bellini, H. Vaucheret, PNAS 97, 11650 (2000)

    Article  CAS  PubMed  Google Scholar 

  86. J.P. Combe, M.E. Petracek, G. Van Eldik, F. Meulewaeter, D. Twell, Plant Mol. Biol. 57, 749 (2005)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Zamyatnin, W.O. Dawson and D.C. Baulcombe for valuable materials. Financial support from Formas, Sweden (grant 22.0/2003-0466), and the Academy of Finland (grant 1102003) is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jari P. T. Valkonen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Germundsson, A., Savenkov, E.I., Ala-Poikela, M. et al. VPg of Potato virus A alone does not suppress RNA silencing but affects virulence of a heterologous virus. Virus Genes 34, 387–399 (2007). https://doi.org/10.1007/s11262-006-0030-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-006-0030-7

Keywords

Navigation