1887

Abstract

Molecular cloning of recessive resistance genes to potyviruses in a large range of host species identified the eukaryotic translation initiation factor 4E (eIF4E) as an essential determinant in the outcome of potyvirus infection. Resistance results from a few amino acid changes in the eIF4E protein encoded by the recessive resistance allele that disrupt the direct interaction with the potyviral protein VPg. In plants, several loci encode two protein subfamilies, eIF4E and eIF(iso)4E. While most eIF4E-mediated resistance to potyviruses depends on mutations in a single eIF4E protein, simultaneous mutations in eIF4E (corresponding to the locus) and eIF(iso)4E (corresponding to the locus) are required to prevent pepper veinal mottle virus (PVMV) infection in pepper. We used this model to look for additional alleles at the locus that result in resistance when combined with the resistant allele. Among the 12 resistance alleles sequenced in the pepper gene pool, three were shown to have a complementary effect with for resistance. Two amino acid changes were exclusively shared by these three alleles and were systematically associated with a second amino acid change, suggesting that these substitutions are associated with resistance expression. The availability of new resistant allele combinations increases the possibility for the durable deployment of resistance against this pepper virus which is prevalent in Africa.

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2009-11-01
2024-04-20
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References

  1. Andersen J. R., Lübberstedt T. 2003; Functional markers in plants. Trends Plant Sci 8:554–560 [CrossRef]
    [Google Scholar]
  2. Ayme V., Petit-Pierre J., Souche S., Palloix A., Moury B. 2007; Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J Gen Virol 88:1594–1601 [CrossRef]
    [Google Scholar]
  3. Brunt A. A., Kenten R. H., Phillips S. 1978; Symptomatologically distinct strains of pepper veinal mottle virus from four West African solanaceous crops. Ann Appl Biol 88:115–119 [CrossRef]
    [Google Scholar]
  4. Caranta C., Palloix A. 1996; Both common and specific genetic factors are involved in polygenic resistance of pepper to several potyviruses. Theor Appl Genet 92:15–20 [CrossRef]
    [Google Scholar]
  5. Caranta C., Palloix A., Gebre-Selassie G., Lefebvre V., Moury B., Daubeze A. M. 1996; A complementation of two genes originating from susceptible Capsicum annuum lines confers a new and complete resistance to pepper veinal mottle virus. Phytopathology 86:739–743 [CrossRef]
    [Google Scholar]
  6. Charron C. 2007; Caractérisation fonctionnelle et évolution moléculaire des gènes codant pour les facteurs d'initiation de la traduction eIF4E: des facteurs clés dans la résistance des plantes aux potyvirus . PhD thesis Université Aix-Marseille II, Faculté des Sciences de Luminy;
  7. Charron C., Nicolaï M., Gallois J. L., Robaglia C., Moury B., Palloix A., Caranta C. 2008; Natural variation and functional analyses provide evidence for coevolution between plant eIF4E and potyviral VPg. Plant J 54:56–68 [CrossRef]
    [Google Scholar]
  8. Combe J. P., Petracek M. E., Van Eldik G., Meulewaeter F., Twell D. 2005; Translation initiation factors eIF4E and eIFiso4E are required for polysome formation and regulate plant growth in tobacco. Plant Mol Biol 57:749–760 [CrossRef]
    [Google Scholar]
  9. Djian-Caporalino C., Lefebvre V., Sage-Daubèze A.-M., Palloix A. 2006; Capsicum . In Genetic Resources, Chromosome Engineering, and Crop Improvement Series: Vegetable Crops . vol 3 pp 185–243Edited by Singh R. J. Boca Raton, FL: CRC Press;
  10. 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]
  11. Fulton T. M., Chunwongse J., Tanksley S. D. 1995; Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209 [CrossRef]
    [Google Scholar]
  12. Gallie D. R., Browning K. S. 2001; eIF4G functionally differs from eIF(iso)4G in promoting internal initiation, cap-independent translation and translation of structural mRNAs. J Biol Chem 276:36951–36960 [CrossRef]
    [Google Scholar]
  13. Hammond-Kosack K. E., Parker J. E. 2003; Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193 [CrossRef]
    [Google Scholar]
  14. Kang B. C., Yeam I., Jahn M. M. 2005a; Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621 [CrossRef]
    [Google Scholar]
  15. Kang B. C., Yeam I., Frantz J. D., Murphy J. F., Jahn M. 2005b; The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405 [CrossRef]
    [Google Scholar]
  16. Lecoq H., Moury B., Desbiez C., Palloix A., Pitrat M. 2004; Durable resistance in plants through conventional approaches: a challenge. Virus Res 100:31–39 [CrossRef]
    [Google Scholar]
  17. Maule A. J., Caranta C., Boulton M. I. 2007; Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231 [CrossRef]
    [Google Scholar]
  18. Michelmore R. W. 2003; The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404 [CrossRef]
    [Google Scholar]
  19. Monzingo A. F., Dhaliwal S., Dutt-Chaudhuri A., Lyon A., Sadow J. H., Hoffman D. W. W., Robertus J. D., Browning K. S. 2007; The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Plant Physiol 143:1504–1518 [CrossRef]
    [Google Scholar]
  20. 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 Lycopersicum hirsutum . Mol Plant Microbe Interact 17:322–329 [CrossRef]
    [Google Scholar]
  21. Moury B., Palloix A., Caranta C., Gognalons P., Souche S., Selassie K. G., Marchoux G. 2005; Serological, molecular and pathotype diversity of Pepper veinal mottle virus and Chili veinal mottle virus . Phytopathology 95:227–232 [CrossRef]
    [Google Scholar]
  22. Robaglia C., Caranta C. 2006; Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45
    [Google Scholar]
  23. Rubio M., Caranta C., Palloix A. 2008; Functional markers for selection of potyvirus resistance alleles at the pvr2 -eIF4E locus in pepper using tetra-primer ARMS-PCR. Genome 51:767–771 [CrossRef]
    [Google Scholar]
  24. Ruffel S., Dussault M. H., Palloix A., Moury B., Bendahmane A., Robaglia C., Caranta C. 2002; A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E ( eIF4E ). Plant J 32:1067–1075 [CrossRef]
    [Google Scholar]
  25. Ruffel S., Dussault M. H., Palloix A., Moury B., Revers F., Bendahmane A., Robaglia C., Caranta C. 2004; The key role of the eukaryotic initiation factor 4E ( eIF4E ) in plant–potyvirus interactions. In Biology of Plant–Microbe Interactions vol. 4 Molecular Plant–Microbe Interaction: New Bridges between Past and Future . pp 81–83Edited by Tikhonovich I., Lugtenberg B., Provorov N. St Paul, MN: International Society for Molecular Plant–Microbe Interactions;
    [Google Scholar]
  26. Ruffel S., Gallois J. L., Moury B., Robaglia C., Palloix A., Caranta C. 2006; Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J Gen Virol 87:2089–2098 [CrossRef]
    [Google Scholar]
  27. Sage-Palloix A. M., Jourdan F., Phaly T., Nemouchi G., Lefebvre V., Palloix A. 2007; Structuring genetic diversity in pepper genetic resources: distribution of horticultural and resistance traits in the INRA pepper germplasm. In Progress in Research on Capsicum & Eggplant pp 33–42Edited by Niemirowicz-Szczytt K. Warsaw, Poland: Warsaw University of Life Sciences Press;
    [Google Scholar]
  28. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  29. 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]
  30. 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]
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