Previous resistance analyses of mutants knocked out for eukaryotic translation initiation factors showed that disruption of the or both the and genes resulted in resistance against turnip mosaic virus (TuMV). This study selected TuMV virulent variants that overcame this resistance and showed that two independent mutations in the region coding for the viral genome-linked protein (VPg) were sufficient to restore TuMV virulence in - and × knockout plants. As a VPg–eIF(iso)4E interaction has been shown previously to be critical for TuMV infection, a systematic analysis of the interactions between eIF4Es and VPgs of virulent and avirulent TuMVs was performed. The results suggest that virulent TuMV variants may use an eIF4F-independent pathway.


Article metrics loading...

Loading full text...

Full text loading...



  1. Abdul-Razzak, A., Guiraud, T., Peypelut, M., Walter, J., Houvenaghel, M. C., Candresse, T., Le Gall, O. & German-Retana, S.(2009). Involvement of the cylindrical inclusion (CI) protein in the overcoming of an eIF4E-mediated resistance against Lettucemosaic potyvirus. Mol Plant Pathol 10, 109–113.[CrossRef] [Google Scholar]
  2. Adams, M. J., Antoniw, J. F. & Fauquet, C. M.(2005). Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150, 459–479.[CrossRef] [Google Scholar]
  3. Ayme, V., Souche, S., Caranta, C., Jacquemond, M., Chadoeuf, J., Palloix, A. & Moury, B.(2006). Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol Plant Microbe Interact 19, 557–563.[CrossRef] [Google Scholar]
  4. Basso, J., Dallaire, P., Charest, P. J., Devantier, Y. & Laliberté, J. F.(1994). Evidence for an internal ribosome entry site within the 5′ non-translated region of turnip mosaic potyvirus RNA. J Gen Virol 75, 3157–3165.[CrossRef] [Google Scholar]
  5. Beauchemin, C., Boutet, N. & Laliberté, J. F.(2007). Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor iso 4E in planta. J Virol 81, 775–782.[CrossRef] [Google Scholar]
  6. Browning, K. S.(2004). Plant translation initiation factors: it is not easy to be green. Biochem Soc Trans 32, 589–591.[CrossRef] [Google Scholar]
  7. Charron, C., Nicolai, M., Gallois, J. L., Robaglia, C., Moury, B., Palloix, A. & Caranta, C.(2008). Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54, 56–68.[CrossRef] [Google Scholar]
  8. Duprat, A., Caranta, C., Revers, F., Menand, B., Browning, K. S. & Robaglia, C.(2002). The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32, 927–934.[CrossRef] [Google Scholar]
  9. Gallie, D. R.(2001). Cap-independent translation conferred by the 5′ leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J Virol 75, 12141–12152.[CrossRef] [Google Scholar]
  10. Gallie, D. R. & Browning, K. S.(2001). eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J Biol Chem 276, 36951–36960.[CrossRef] [Google Scholar]
  11. Gao, Z., Johansen, E., Eyers, S., Thomas, C. L., Noel Ellis, T. H. & Maule, A. J.(2004). The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40, 376–385.[CrossRef] [Google Scholar]
  12. German-Retana, S., Walter, J., Doublet, B., Roudet-Tavert, G., Nicaise, V., Lecampion, C., Houvenaghel, M. C., Robaglia, C., Michon, T. & Le Gall, O.(2008). Mutational analysis of plant cap-binding protein eIF4E reveals key amino acids involved in biochemical functions and potyvirus infection. J Virol 82, 7601–7612.[CrossRef] [Google Scholar]
  13. Hjulsager, C. K., Olsen, B. S., Jensen, D. M., Cordea, M. I., Krath, B. N., Johansen, I. E. & Lund, O. S.(2006). Multiple determinants in the coding region of Pea seed-borne mosaic virus P3 are involved in virulence against sbm-2 resistance. Virology 355, 52–61.[CrossRef] [Google Scholar]
  14. Jenner, C. E., Sánchez, F., Nettleship, S. B., Foster, G. D., Ponz, F. & Walsh, J. A.(2000). The cylindrical inclusion gene of Turnip mosaic virus encodes a pathogenic determinant to the Brassica resistance gene TuRB01. Mol Plant Microbe Interact 13, 1102–1108.[CrossRef] [Google Scholar]
  15. Kang, B. C., Yeam, I., Frantz, J. D., Murphy, J. F. & Jahn, M. M.(2005). The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobaccoetchvirus VPg. Plant J 42, 392–405.[CrossRef] [Google Scholar]
  16. Khan, M. A., Miyoshi, H., Gallie, D. R. & Goss, D. J.(2008). Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J Biol Chem 283, 1340–1349.[CrossRef] [Google Scholar]
  17. Lehmann, P., Petrzik, K., Jenner, C., Greenland, A., Spak, J., Kozubek, E. & Walsh, J. A.(1997). Nucleotide and amino acid variation in the coat protein coding region of turnip mosaic virus isolates and possible involvement in the interaction with the brassica resistance gene TuRB01. Physiol Mol Plant Pathol 51, 195–208.[CrossRef] [Google Scholar]
  18. Léonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M. G. & Laliberté, J. F.(2000). Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74, 7730–7737.[CrossRef] [Google Scholar]
  19. Léonard, S., Viel, C., Beauchemin, C., Daigneault, N., Fortin, M. G. & Laliberté, J. F.(2004). Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J Gen Virol 85, 1055–1063.[CrossRef] [Google Scholar]
  20. Marcotrigiano, J., Gingras, A.-C., Sonenberg, N. & Burley, S. K.(1999). Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3, 707–716.[CrossRef] [Google Scholar]
  21. Moury, B., Morel, C., Johansen, E., Guilbaud, L., Souche, S., Ayme, V., Caranta, C., Palloix, A. & Jacquemond, M.(2004). Mutations in potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersiconhirsutum. Mol Plant Microbe Interact 17, 322–329.[CrossRef] [Google Scholar]
  22. Murphy, J. F., Rychlik, W., Rhoads, R. E., Hunt, A. G. & Shaw, J. G.(1991). A tyrosine residue in the small nuclear inclusion protein of tobacco vein mottling virus links the VPg to the viral RNA. J Virol 65, 511–513. [Google Scholar]
  23. Nicaise, V., Gallois, J. L., Chafiai, F., Allen, L. M., Schurdi-Levraud, V., Browning, K. S., Candresse, T., Caranta, C., Le Gall, O. & German-Retana, S.(2007). Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsisthaliana. FEBS Lett 581, 1041–1046.[CrossRef] [Google Scholar]
  24. Okade, H., Fujita, Y., Miyamoto, S., Tomoo, K., Muto, S., Miyoshi, H., Natsuaki, T., Rhoads, R. E. & Ishida, T.(2009). Turnip mosaic virus genome-linked protein VPg binds C-terminal region of cap-bound initiation factor 4E orthologue without exhibiting host cellular specificity. J Biochem 145, 299–307.[CrossRef] [Google Scholar]
  25. Revers, F., Le Gall, O., Candresse, T. & Maule, A. J.(1999). New advances in understanding the molecular biology of plant/potyvirus interactions. Mol Plant Microbe Interact 12, 367–376.[CrossRef] [Google Scholar]
  26. Robaglia, C. & Caranta, C.(2006). Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11, 40–45. [Google Scholar]
  27. Ruud, K. A., Kuhlow, C., Goss, D. J. & Browning, K. S.(1998). Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. J Biol Chem 273, 10325–10330.[CrossRef] [Google Scholar]
  28. Sánchez, F., Martinez-Herrera, D., Aguilar, I. & Ponz, F.(1998). Infectivity of turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. Virus Res 55, 207–219.[CrossRef] [Google Scholar]
  29. Sánchez, F., Wang, X., Jenner, C. E., Walsh, J. A. & Ponz, F.(2003). Strains of Turnip mosaic potyvirus as defined by the molecular analysis of the coat protein gene of the virus. Virus Res 94, 33–43.[CrossRef] [Google Scholar]
  30. Sato, M., Nakahara, K., Yoshii, M., Ishikawa, M. & Uyeda, I.(2005). Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett 579, 1167–1171.[CrossRef] [Google Scholar]
  31. Shukla, D. D., Ward, C. W. & Brunt, A. A.(1994).The Potyviridae. Wallingford, UK: CAB International.
  32. Tan, Z., Gibbs, A. J., Tomitaka, Y., Sánchez, F., Ponz, F. & Ohshima, K.(2005). Mutations in Turnip mosaic virus genomes that have adapted to Raphanus sativus. J Gen Virol 86, 501–510.[CrossRef] [Google Scholar]
  33. Yeam, I., Cavatorta, J. R., Ripoll, D. R., Kang, B. C. & Jahn, M. M.(2007). Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19, 2913–2928.[CrossRef] [Google Scholar]
  34. Yoshii, M., Nishikiori, M., Tomita, K., Yoshioka, N., Kozuka, R., Naito, S. & Ishikawa, M.(2004). The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol 78, 6102–6111.[CrossRef] [Google Scholar]

Data & Media loading...


vol. , part 1, pp. 288 - 293

Oligonucleotides used for PCR fusion-based mutagenesis experiments

Oligonucleotides used for cloning [Single PDF file](64 KB)


Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error