1887

Abstract

resistance to (PVMV) results from complementation between the and resistance genes: recessive alleles at these two loci are necessary for resistance, whereas any dominant allele confers susceptibility. In line with previous results showing that resistance alleles encode mutated versions of the eukaryotic translation initiation factor 4E (eIF4E), the involvement of other members of the multigenic family in PVMV resistance was investigated. It was demonstrated that corresponds to an gene, predicted to encode the second cap-binding isoform identified in plants. Comparative genetic mapping in pepper and tomato indicated that maps in the same genomic region as . Sequence analysis revealed an 82 nt deletion in cDNAs from genotypes with the resistance allele, leading to a truncated protein. This deletion was shown to co-segregate with in doubled haploid and F progeny. Transient expression in a PVMV-resistant genotype of derived from a genotype with the susceptibility allele resulted in loss of resistance to subsequent PVMV inoculation, confirming that encodes the translation factor eIF(iso)4E. Similarly, transient expression of from a genotype with the susceptibility allele also resulted in loss of resistance, demonstrating that wild-type eIF4E and eIF(iso)4E are susceptibility factors for PVMV and that resistance results from the combined effect of mutations in the two cap-binding isoforms. Thus, whilst most potyviruses specifically require one eIF4E isoform to perform their replication cycle, PVMV uses either eIF4E or eIF(iso)4E for infection of pepper.

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2006-07-01
2019-10-21
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References

  1. Baulcombe, D. C., Chapman, S. & Santa Cruz, S. ( 1995; ). Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7, 1045–1053.[CrossRef]
    [Google Scholar]
  2. Browning, K. S. ( 1996; ). The plant translational apparatus. Plant Mol Biol 32, 107–144.[CrossRef]
    [Google Scholar]
  3. Caranta, C., Palloix, A., Gebre-Selassie, K., Lefebvre, V., Moury, B. & Daubèze, 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]
  4. 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]
  5. 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]
  6. Gallie, D. R. & Browning, K. ( 2001; ). eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structure mRNAs. J Biol Chem 276, 36951–36960.[CrossRef]
    [Google Scholar]
  7. Gao, Z., Johansen, E., Eyers, S., Thomas, C. L., Ellis, T. H. N. & 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]
  8. Guerini, M. N. & Murphy, J. F. ( 1999; ). Resistance of Capsicum annuum ‘Avelar’ to pepper mottle potyvirus and alleviation of this resistance by co-infection with cucumber mosaic cucumovirus are associated with virus movement. J Gen Virol 80, 2785–2792.
    [Google Scholar]
  9. Kang, B. C., Yeam, I., Frantz, J. D., Murphy, J. D. & Jahn, M. M. ( 2005; ). 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]
  10. Lefebvre, V., Pflieger, S., Thabuis, A., Caranta, C., Blattes, A., Chauvet, J. C., Daubèze, A. M. & Palloix, A. ( 2002; ). Toward the saturation of the pepper linkage map by alignment of three intraspecific maps including known-function genes. Genome 45, 839–854.[CrossRef]
    [Google Scholar]
  11. Lellis, A. D., Kasschau, K. D., Whitham, S. A. & Carrington, J. S. ( 2002; ). Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12, 1046–1051.[CrossRef]
    [Google Scholar]
  12. Léonard, S., Plante, D., Wittman, 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]
  13. Liu, Y.-S. & Zamir, D. ( 1999; ). Second generation L. pennellii introgression lines and the concept of bin mapping. Tomato Genet Coop Rep 49, 26–30.
    [Google Scholar]
  14. Livingstone, K. D., Lackney, V. K., Blauth, J. R., van Wijk, R. & Kyle Jahn, M. ( 1999; ). Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152, 1183–1202.
    [Google Scholar]
  15. Marcotrigiano, J., Gingras, A.-C., Sonenberg, N. & Burley, S. K. ( 1997; ). Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89, 951–961.[CrossRef]
    [Google Scholar]
  16. Matsuo, H., Li, H., McGuire, A. M., Fletcher, C. M., Gingras, A.-C., Sonenberg, N. & Wagner, G. ( 1997; ). Structure of translation initiation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol 4, 717–724.[CrossRef]
    [Google Scholar]
  17. Moury, B., Palloix, A., Caranta, C., Gognalons, P., Souche, S., Gebre Selassie, K. & Marchoux, G. ( 2005; ). Serological, molecular and pathotype diversity of Pepper veinal mottle virus and Chilli veinal mottle virus. Phytopathology 95, 227–232.[CrossRef]
    [Google Scholar]
  18. Nicaise, V., German-Retana, S., Sanjuán, R., Dubrana, M.-P., Mazier, M., Maisonneuve, B., Candresse, T., Caranta, C. & LeGall, O. ( 2003; ). The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132, 1272–1282.[CrossRef]
    [Google Scholar]
  19. Robaglia, C. & Caranta, C. ( 2006; ). Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11, 40–45.
    [Google Scholar]
  20. Rodriguez, C. M., Freire, M. A., Camilleri, C. & Robaglia, C. ( 1998; ). The Arabidopsis thaliana cDNAs coding for eIF4E and eIF(iso)4E are not functionally equivalent for yeast complementation and are differentially expressed during plant development. Plant J 13, 465–473.[CrossRef]
    [Google Scholar]
  21. 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]
  22. Ruffel, S., Dussault, M.-H., Duprat, A., 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 Interactions: New Bridges Between Past and Future, pp. 81–83. Edited by I. Tikhonovich, B. Lugtenberg & N. Provorov. St Paul, MN: International Society for Molecular Plant–Microbe Interactions.
  23. Ruffel, S., Gallois, J. L., Lesage, M. L. & Caranta, C. ( 2005; ). The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genom 274, 346–353.[CrossRef]
    [Google Scholar]
  24. 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]
  25. Schaad, M. C., Anderberg, R. J. & Carrington, J. C. ( 2000; ). Strain-specific interaction of the tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. Virology 273, 300–306.[CrossRef]
    [Google Scholar]
  26. Stein, N., Perovic, D., Kumlehn, J., Pellio, B., Stracke, S., Streng, S., Ordon, F. & Graner, A. ( 2005; ). The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42, 912–922.[CrossRef]
    [Google Scholar]
  27. Tanksley, S. D., Ganal, M. W., Prince, J. P. & 16 other authors ( 1992; ). High density molecular linkage maps of the tomato and potato genomes. Genetics 132, 1141–1160.
    [Google Scholar]
  28. Urcuqui-Inchima, S., Haenni, A. L. & Bernardi, F. ( 2001; ). Potyvirus proteins: a wealth of functions. Virus Res 74, 157–175.[CrossRef]
    [Google Scholar]
  29. Whitham, S. A. & Wang, Y. ( 2004; ). Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7, 365–371.[CrossRef]
    [Google Scholar]
  30. Wittmann, S., Chatel, H., Fortin, M. G. & Laliberté, J.-F. ( 1997; ). Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234, 84–92.[CrossRef]
    [Google Scholar]
  31. 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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