European Journal of Plant Pathology

, Volume 125, Issue 1, pp 1–22 | Cite as

Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability

  • P. Gómez
  • A.M. Rodríguez-Hernández
  • B. Moury
  • M.A. Aranda
Article

Abstract

Plant viruses are important agricultural pathogens, and are responsible for a significant number of commercially relevant plant diseases. There are very few efficient control measures for viral diseases, but the use of genetic resistance appears to be the most promising strategy, often conferring effective protection without additional costs or labour during the growing season, and without damaging the environment. Sources of virus resistance have been identified for most crop species, and many resistant cultivars are already commercially available and of widespread cultivation; however, much remains to be learned about genetic resistance. This review article considers three main aspects that require intense investigation. First, we review the identification of sources of resistance and how plant breeders and pathologists have focused on aspects of the breeding process particularly relevant to viruses, such as germplasm screening and the dissection of resistance phenotypes. Second, we review how molecular mechanisms controlling resistance have been unravelled, looking at case studies where resistance mechanisms are now understood in detail for each stage of the infection cycle. Third, we turn to the durability of resistance in a global context, examining factors that influence durability and how this can be predicted. We conclude with a short discussion of the technological and scientific opportunities provided by recent advances in the field.

Keywords

Genetic resources Plant breeding Plant virus Resistance durability Resistance genes Resistance mechanisms 

Notes

Acknowledgements

P.G. was supported by a “Juan de la Cierva” post-doctoral contract from Ministerio de Ciencia e Innovación (Spain). A.M.R-H. is the recipient of a fellowship from Consejo Nacional de Ciencia y Tecnología (Mexico). Financial support was provided by the EU-FP6 Co-ordination action ResistVir “Co-ordination of Research on Genetic resistance to Plant Pathogenic Viruses and their Vectors in European Crops”, Contract No. FOOD-CT-2005-514048.

References

  1. Agudelo-Romero, P., de la Iglesia, F., & Elena, S. F. (2008). The pleiotropic cost of host-specialization in Tobacco etch potyvirus. Infection, Genetics and Evolution, 8, 806–814. doi: 10.1016/j.meegid.2008.07.010.PubMedGoogle Scholar
  2. Albar, L., Bangratz-Reyser, M., Hebrard, E., Ndjiondjop, M. N., Jones, M., & Ghesquiere, A. (2006). Mutations in the eIF4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. The Plant Journal, 47, 417–426. doi: 10.1111/j.1365-313X.2006.02792.x.PubMedGoogle Scholar
  3. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., & Daszak, P. (2004). Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution, 19, 535–544. doi: 10.1016/j.tree.2004.07.021.Google Scholar
  4. Arroyo, R., Soto, M. J., Martinez-Zapater, J. M., & Ponz, F. (1996). Impaired cell-to-cell movement of Potato virus Y in pepper plants carrying the y(a)(pr2(1)) resistance gene. Molecular Plant-Microbe Interactions, 9, 314–318.Google Scholar
  5. Ayme, V., Souche, S., Caranta, C., Jacquemond, M., Chadœuf, J., Palloix, A., et al. (2006). Different mutations in the VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Molecular Plant-Microbe Interactions, 19, 557–563. doi: 10.1094/MPMI-19-0557.PubMedGoogle Scholar
  6. Babcock, C., Chen, X., Crous, P. W., Dugan, F. M., Goates, B., & Green, P. N. (2007). Plant germplasm centers and microbial culture collections. A user’s guide to key genetic resources for plant pathology. Plant Disease, 91(5), 476–484. doi: 10.1094/PDIS-91-5-0476.Google Scholar
  7. Bailiss, K. W., & Offei, S. K. (1990). Alfalfa mosaic virus in lucerne seed during seed maturation and storage, and in seedlings. Plant Pathology, 39, 539–547. doi: 10.1111/j.1365-3059.1990.tb02531.x.Google Scholar
  8. Baker, B., Zambryski, P., Staskawicz, B., & Dinesh-Kumar, S. P. (1997). Signaling in plant-microbe interactions. Science, 276, 726–733. doi: 10.1126/science.276.5313.726.PubMedGoogle Scholar
  9. Barker, H., & Harrison, B. D. (1984). Expression of genes for resistance to Potato virus Y in potato plants and protoplasts. The Annals of Applied Biology, 105, 539–545. doi: 10.1111/j.1744-7348.1984.tb03080.x.Google Scholar
  10. Baulcombe, D. (2004). RNA silencing in plants. Nature, 431, 356–363. doi: 10.1038/nature02874.PubMedGoogle Scholar
  11. Bayer, E. M., Bottrill, A. R., Walshaw, J., Vigouroux, M., Naldrett, M. J., Thomas, C. L., et al. (2006). Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics, 6, 301–311. doi: 10.1002/pmic.200500046.PubMedGoogle Scholar
  12. Bendahmane, A., Kohm, B. A., Dedi, C., & Baulcombe, D. C. (1995). The coat protein of Potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. The Plant Journal, 8, 933–941.PubMedGoogle Scholar
  13. Bendahmane, M., Fitchen, J. H., Zhang, G., & Beachy, R. N. (1997). Studies of coat protein-mediated resistance to Tobacco mosaic tobamovirus: correlation between assembly of mutant coat proteins and resistance. Journal of Virology, 71, 7942–7950.PubMedGoogle Scholar
  14. Bendahmane, M., Koo, M., Karrer, E., & Beachy, R. N. (1999). Display of epitopes on the surface of Tobacco mosaic virus: impact of charge and isoelectric point of the epitope on virus-host interactions. Journal of Molecular Biology, 290, 9–20. doi: 10.1006/jmbi.1999.2860.PubMedGoogle Scholar
  15. Bhattarai, K. K., Li, Q., Liu, Y., Dinesh-Kumar, S. P., & Kaloshian, I. (2007). The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiology, 144, 312–323. doi: 10.1104/pp. 107.097246.PubMedGoogle Scholar
  16. Blackman, R. L., & Eastop, V. F. (2000). Aphids on the World’s Crop, 466. pp. Chichester: Wiley.Google Scholar
  17. Borgstrom, B., & Johansen, I. E. (2001). Mutations in Pea seedborne mosaic virus genome-linked protein VPg after pathotype-specific virulence in Pisum sativum. Molecular Plant-Microbe Interactions, 14, 707–714. doi: 10.1094/MPMI.2001.14.6.707.PubMedGoogle Scholar
  18. Buck, K. W. (1996). Comparison of the replication of positive-stranded RNA viruses of plants and animals. Advances in Virus Research, 47, 159–251. doi: 10.1016/S0065-3527(08)60736-8.PubMedGoogle Scholar
  19. Buck, K. W. (1999). Replication of Tobacco mosaic virus RNA. Philosophical Transactions of the Royal Society B. Biological Sciences, 354, 613–627. doi: 10.1098/rstb.1999.0413.Google Scholar
  20. Canto, T., Aranda, M. A., & Fereres, A. (2009). Climate change effects on physiology and population processes of hosts and vectors that influence the spread of hemipteran-borne plant viruses. Global Change Biology. doi: 10.1111/j.1365-2486.2008.01820.x.
  21. Caplan, J., & Dinesh-Kumar, S. P. (2006). Recognition and signal transduction associated with R gene-mediated resistance. In G. Loebenstein & J. P. Carr (Eds.), Natural resistance mechanisms of plants to viruses, 73–98. pp. Netherlands: Kluwer Academic.Google Scholar
  22. Caplan, J. L., Mamillapalli, P., Burch-Smith, T. M., Czymmek, K., & Dinesh-Kumar, S. P. (2008). Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell, 132, 449–462. doi: 10.1016/j.cell.2007.12.031.PubMedGoogle Scholar
  23. Carrington, J. C., Kasschau, K. D., Mahajan, S. K., & Schaad, M. C. (1996). Cell-to-cell and long-distance transport of viruses in plants. The Plant Cell, 8, 1669–1681.PubMedGoogle Scholar
  24. Carroll, T. W., & Mayhew, D. E. (1976). Occurrence of virions in developing ovules and embryo sacs of barley in relation to seed transmissibility of Barley stripe mosaic virus. Canadian Journal Botany-Revue Canadienne De Botanique, 54, 2497–2512. doi: 10.1139/b76-268.Google Scholar
  25. Carroll, T. W., Zaske, S. K., & Hockett, E. A. (1981). Development of a barley germ plasm resistant to the seed transmission of Barley stripe mosaic virus. Phytopathology, 71, 865–865.Google Scholar
  26. Chain, F., Riault, G., Trottet, M., & Jacquot, E. (2007). Evaluation of the durability of the Barley yellow dwarf virus resistant Zhong ZH and TC14 wheat lines. European Journal of Plant Pathology, 117, 35–43. doi: 10.1007/s10658-006-9066-8.Google Scholar
  27. Charron, C., Nicolai, M., Gallois, J.-L., Robaglia, C., Moury, B., Palloix, A., et al. (2008). Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. The Plant Journal, 54, 56–68. doi: 10.1111/j.1365-313X.2008.03407.x.PubMedGoogle Scholar
  28. Chemo, R., Maoz, I., & Yarden, G. (2000). Screening pathogenicity of pathogens for screening disease resistance of plants. Patent WO200042835-A.Google Scholar
  29. Chen, H., Wang, S., Xing, Y., Xu, C., Hayes, P. M., & Zhang, Q. (2003). Comparative analysis of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proceedings of the National Academy of Sciences of the United States of America, 100, 2544–2549. doi: 10.1073/pnas.0437898100.PubMedGoogle Scholar
  30. Chiba, S., Miyanishi, M., Andika, I. B., Kondo, H., & Tamada, T. (2008). Identification of amino acids of the Beet necrotic yellow vein virus p25 protein required for induction of the resistance response in leaves of Beta vulgaris plants. The Journal of General Virology, 89, 1314–1323. doi: 10.1099/vir.0.83624-0.PubMedGoogle Scholar
  31. Chisholm, S. T., Mahajan, S. K., Whitham, S. A., Yamamoto, M. L., & Carrington, J. C. (2000). Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of Tobacco etch virus. Proceedings of the National Academy of Sciences of the United States of America, 97, 489–494. doi: 10.1073/pnas.97.1.489.PubMedGoogle Scholar
  32. Chisholm, S. T., Parra, M. A., Anderberg, R. J., & Carrington, J. C. (2001). Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of Tobacco etch virus. Plant Physiology, 127, 1667–1675. doi: 10.1104/pp. 010479.PubMedGoogle Scholar
  33. Citovsky, V., & Zambryski, P. (1991). How do plant virus nucleic acids move through intercellular connections? BioEssays, 13, 373–379. doi: 10.1002/bies.950130802.PubMedGoogle Scholar
  34. Collard, C. Y. B., & Mackill, D. J. (2008). Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society B. Biological Sciences, 363, 557–572. doi: 10.1098/rstb.2007.2170.Google Scholar
  35. Cooley, M. B., Pathirana, S., Wu, H. J., Kachroo, P., & Klessig, D. F. (2000). Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. The Plant Cell, 12, 663–676.PubMedGoogle Scholar
  36. Coudriet, D. L., Kishaba, A. N., & Bohn, G. W. (1981). Inheritance of resistance to Muskmelon necrotic spot virus in a melon aphid-resistant breeding line of muskmelon. The American Society for Horticultural Science, 106, 789–791.Google Scholar
  37. Covey, S. N., Al-Kaff, N. S., Langara, A., & Turner, D. S. (1997). Plants combat infection by gene silencing. Nature, 385, 781–782. doi: 10.1038/385781a0.Google Scholar
  38. Culver, J. N., & Padmanabhan, M. S. (2007). Virus-induced disease: altering host physiology one interaction at a time. Annual Review of Phytopathology, 45, 221–243. doi: 10.1146/annurev.phyto.45.062806.094422.PubMedGoogle Scholar
  39. Dangl, J. L., & Jones, J. D. G. (2001). Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833. doi: 10.1038/35081161.PubMedGoogle Scholar
  40. Decroocq, V., Sicard, O., Alamillo, J. M., Lansac, M., Eyquard, J. P., Garcia, J. A., et al. (2006). Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 19, 541–549. doi: 10.1094/MPMI-19-0541.PubMedGoogle Scholar
  41. Dempsey, D. A., Pathirana, M. S., Wobbe, K. K., & Klessig, D. F. (1997). Identification of an Arabidopsis locus required for resistance to Turnip crinkle virus. The Plant Journal, 11, 301–311. doi: 10.1046/j.1365-313X.1997.11020301.x.PubMedGoogle Scholar
  42. Desbiez, C., Gal-On, A., Girard, M., Wipf-Scheibel, C., & Lecoq, H. (2003). Increase in Zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology, 93, 1478–1484. doi: 10.1094/PHYTO.2003.93.12.1478.PubMedGoogle Scholar
  43. Díaz, J., Nieto, C., Moriones, E., Truniger, V., & Aranda, M. A. (2004). Molecular characterization of a Melon necrotic spot virus strain that overcomes the resistance in melon and non-host plants. Molecular Plant-Microbe Interactions, 17, 668–675. doi: 10.1094/MPMI.2004.17.6.668.PubMedGoogle Scholar
  44. Diaz-Pendon, J. A., Truniger, V., Nieto, C., Garcia-Mas, J., Bendahmane, A., & Aranda, M. A. (2004). Advances in understanding recessive resistance to plant viruses. Molecular Plant Pathology, 5, 223–233. doi: 10.1111/j.1364-3703.2004.00223.x.Google Scholar
  45. Dietrich, C., & Maiss, E. (2003). Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. The Journal of General Virology, 84, 2871–2876. doi: 10.1099/vir.0.19245-0.PubMedGoogle Scholar
  46. Dinesh-Kumar, S. P., & Baker, B. J. (2000). Alternatively spliced N resistance gene transcripts: their possible role in Tobacco mosaic virus resistance. Proceedings of the National Academy of Sciences of the United States of America, 97, 1908–1913. doi: 10.1073/pnas.020367497.PubMedGoogle Scholar
  47. Dinesh-Kumar, S. P., Whitham, S., Choi, D., Hehl, R., Corr, C., & Baker, B. (1995). Transposon tagging of Tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proceedings of the National Academy of Sciences of the United States of America, 92, 4175–4180. doi: 10.1073/pnas.92.10.4175.PubMedGoogle Scholar
  48. Ding, S. W., & Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell, 130, 413–426. doi: 10.1016/j.cell.2007.07.039.PubMedGoogle Scholar
  49. Dogimont, C., Chovelon, V., Tual, S., Boissot, N., Rittener-Rüff, V., Giovinazzo, N., et al. (2008). Molecular diversity at the Vat/Pm-W resistance locus in melon. In M. Pitrat (Ed), Cucurbitaceae, Proceedings of the IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae (pp. 219–228). Avignon (France), May 21–24th, 2008.Google Scholar
  50. Dropkin, V. H. (1969). Necrotic reaction of tomatoes and other hosts resistant to meloidogyne—reversal by temperature. Phytopathology, 59, 1632.Google Scholar
  51. Edwards, M. C. (1995). Mapping of the seed transmission determinants of Barley stripe mosaic virus. Molecular Plant-Microbe Interactions, 8, 906–915.PubMedGoogle Scholar
  52. Edwards, M. C., & Steffenson, B. J. (1996). Genetics and mapping of Barley stripe mosaic virus resistance in barley. Phytopathology, 86, 184–187. doi: 10.1094/Phyto-86-184.Google Scholar
  53. Elena, S. F., & Sanjuán, R. (2007). Virus evolution: insights from an experimental approach. Annual Review of Ecology Evolution and Systematics, 38, 27–52. doi: 10.1146/annurev.ecolsys.38.091206.095637.Google Scholar
  54. Fargette, D., Konate, G., Fauquet, C., Muller, E., Peterschmitt, M., & Thresh, J. M. (2006). Molecular ecology and emergence of tropical plant viruses. Annual Review of Phytopathology, 44, 235–260. doi: 10.1146/annurev.phyto.44.120705.104644.PubMedGoogle Scholar
  55. Ferguson, A. R. (2007). The need for characterisation and evaluation of germplasm: kiwifruit as an example. Euphytica, 154, 371–382. doi: 10.1007/s10681-006-9188-2.Google Scholar
  56. Fraser, R. S. S. (1990). The genetics of resistance to plant-viruses. Annual Review of Phytopathology, 28, 179–200. doi: 10.1146/annurev.py.28.090190.001143.Google Scholar
  57. French, R., & Stenger, D. C. (2003). Evolution of Wheat streak mosaic virus: dynamics of population growth within plants may explain limited variation. Annual Review of Phytopathology, 41, 199–214. doi: 10.1146/annurev.phyto.41.052002.095559.PubMedGoogle Scholar
  58. Gao, Z., Eyers, S., Thomas, C., Ellis, N., & Maule, A. (2004a). Identification of markers tightly linked to sbm recessive genes for resistance to Pea seed-borne mosaic virus. Theoretical and Applied Genetics, 109, 488–494.Google Scholar
  59. Gao, Z. H., Johansen, E., Eyers, S., Thomas, C. L., Noel Ellis, T. H., & Maule, A. (2004b). The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. The Plant Journal, 40, 376–385. doi: 10.1111/j.1365-313X.2004.02215.x.Google Scholar
  60. García-Arenal, F., & McDonald, B. A. (2003). An analysis of the durability of resistance to plant viruses. Phytopathology, 93, 941–952. doi: 10.1094/PHYTO.2003.93.8.941.PubMedGoogle Scholar
  61. German-Retana, S., Walter, J., Doublet, B., Roudet-Tavert, G., Nicaise, V., Lecampion, C., et al. (2008). Mutational analysis of a plant cap-binding protein eIF4E reveals key amino-acids involved in biochemical functions and potyvirus infection. Journal of Virology, 82, 7601–7612. doi: 10.1128/JVI.00209-08.PubMedGoogle Scholar
  62. Gilbert, J. C., & McGuire, D. C. (1956). Inheritance of resistance to severe root-knot from Meloidogyne incognita in commercial-type tomatoes. Proceedings of the American Society for Horticultural Science, 68, 437–442.Google Scholar
  63. Goulden, M. G., Köhm, B. A., Santa Cruz, S., Kavanagh, T. A., & Baulcombe, D. C. (1993). A feature of the coat protein of Potato virus X affects both induced virus resistance in potato and viral fitness. Virology, 197, 293–302. doi: 10.1006/viro.1993.1590.PubMedGoogle Scholar
  64. Gray, S. M., & Banerjee, N. (1999). Mechanisms of arthropod transmission of plant and animal viruses. Microbiology and Molecular Biology Reviews, 63, 128–148.PubMedGoogle Scholar
  65. Hajimorad, M. R., & Hill, J. H. (2001). Rsv1-mediated resistance against Soybean mosaic virus-N is hypersensitive response-independent at inoculation site, but has the potential to initiate a hypersensitive response-like mechanism. Molecular Plant-Microbe Interactions, 14, 587–598. doi: 10.1094/MPMI.2001.14.5.587.PubMedGoogle Scholar
  66. Harrison, B. D. (2002). Virus variation in relation to resistance breaking in plants. Euphytica, 124, 181–192. doi: 10.1023/A:1015630516425.Google Scholar
  67. Haseloff, J., Goelet, P., Zimmern, D., Ahlquist, P., Dasgupta, R., & Kaesberg, P. (1984). Striking similarities in amino-acid-sequence among nonstructural proteins encoded by rna viruses that have dissimilar genomic organization. Proceedings of the National Academy of Sciences of the United States of America, 81, 4358–4362. doi: 10.1073/pnas.81.14.4358.PubMedGoogle Scholar
  68. Hoffmann, K., Qiu, W. P., & Moyer, J. W. (2001). Overcoming host- and pathogen-mediated resistance in tomato and tobacco maps to the M RNA of Tomato spotted wilt virus. Molecular Plant-Microbe Interactions, 14, 242–249. doi: 10.1094/MPMI.2001.14.2.242.PubMedGoogle Scholar
  69. Hull, R. (2002). Matthews’ plant virology (4th ed.). San Diego, CA: Academic.Google Scholar
  70. Innes, N. L. (1992). Gene banks and their contribution to the breeding of disease resistant cultivars. Euphytica, 63, 23–31. doi: 10.1007/BF00023909.Google Scholar
  71. Ishibashi, K., Masuda, K., Naito, S., Meshi, T., & Ishikawa, M. (2007). An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proceedings of the National Academy of Sciences of the United States of America, 104, 13833–13838. doi: 10.1073/pnas.0703203104.PubMedGoogle Scholar
  72. Janda, M., & Ahlquist, P. (1993). RNA-dependent replication, transcription, and persistence of Brome mosaic virus RNA replicons in S. cerevisiae. Cell, 72, 961–970. doi: 10.1016/0092-8674(93)90584-D.PubMedGoogle Scholar
  73. Jenner, C. E., Wang, X., Ponz, F., & Walsh, J. A. (2002). A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Research, 86, 1–6. doi: 10.1016/S0168-1702(02)00031-X.PubMedGoogle Scholar
  74. Johansen, E., Edwards, M. C., & Hampton, R. O. (1994). Seed transmission of viruses—current perspectives. Annual Review of Phytopathology, 32, 363–386. doi: 10.1146/annurev.py.32.090194.002051.Google Scholar
  75. Johnson, R. (1981). Durable resistance: definition of, genetic control and attainment in plant breeding. Phytopathology, 71, 567–568. doi: 10.1094/Phyto-71-567.Google Scholar
  76. Jovel, J., Walker, M., & Sanfacon, H. (2007). Recovery of Nicotiana benthamiana plants from a necrotic response induced by a nepovirus is associated with rna silencing but not with reduced virus titer. Journal of Virology, 81(22), 12285–12297. doi: 10.1128/JVI.01192-07.PubMedGoogle Scholar
  77. Jridi, C., Martin, J. F., Marie-Jeanne, V., Labonne, G., & Blanc, S. (2006). Distinct viral populations differentiate and evolve independently in a single perennial host plant. Journal of Virology, 80, 2349–2357. doi: 10.1128/JVI.80.5.2349-2357.2006.PubMedGoogle Scholar
  78. Kachroo, P., Yoshioka, K., Shah, J., Dooner, H. K., & Klessig, D. F. (2000). Resistance to Turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. The Plant Cell, 12, 677–690.PubMedGoogle Scholar
  79. Kaloshian, I., Lange, W. H., & Williamson, V. M. (1995). An aphid-resistance locus is tightly linked to the nematode-resistance gene, mi, in tomato. Proceedings of the National Academy of Sciences of the United States of America, 92, 622–625. doi: 10.1073/pnas.92.2.622.PubMedGoogle Scholar
  80. Kaloshian, I., Kinsey, M. G., Williamson, V. M., & Ullman, D. E. (2000). Mi-mediated resistance against the potato aphid Macrosiphum euphorbiae (Hemiptera: Aphididae) limits sieve element ingestion. Environmental Entomology, 29, 690–695.CrossRefGoogle Scholar
  81. Kang, B. C., Yeam, I., & Jahn, M. M. (2005). Genetics of plant virus resistance. Annual Review of Phytopathology, 43, 581–621. doi: 10.1146/annurev.phyto.43.011205.141140.PubMedGoogle Scholar
  82. Kanyuka, K., Druka, A., Caldwell, D. G., Tymon, A., McCallum, N., Waugh, R., et al. (2005). Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Molecular Plant Pathology, 6, 449–458. doi: 10.1111/j.1364-3703.2005.00294.x.Google Scholar
  83. Khetarpal, R. K., Maisonneuve, B., Maury, Y., Chalhoub, B., Dianant, S., Lecoq, H., et al. (1998). Breeding for resistance to plant viruses. In Plant virus disease control, 14–33. pp. St. Paul, Minnesota: APS.Google Scholar
  84. Kido, K., Tanaka, C., Mochizuki, T., Kubota, K., Ohki, T., Ohnishi, J., et al. (2008). High temperatures activate local viral multiplication and cell-to-cell movement of Melon necrotic spot virus but restrict expression of systemic symptoms. Phytopathology, 98, 181–186. doi: 10.1094/PHYTO-98-2-0181.PubMedGoogle Scholar
  85. Klingler, J., Creasy, R., Gao, L., Nair, R. M., & Calix, A. S. (2005). Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiology, 137, 1445–1455. doi: 10.1104/pp. 104.051243.PubMedGoogle Scholar
  86. Kogan, M., & Ortman, E. E. (1978). Antixenosis—a new term proposed to replace painter’s ‘nonpreference’ modality of resistance. Bulletin of the Entomological Society of America, 24, 175–176.Google Scholar
  87. Köhm, B. A., Goulden, M. G., Gilbert, J. E., Kavanagh, T. A., & Baulcombe, D. C. (1993). A Potato virus X resistance gene mediates an induced, nonspecific resistance in protoplasts. The Plant Cell, 5, 913–620.PubMedGoogle Scholar
  88. Koorneneef, M., & Stam, P. (2001). Changing paradigms in plant breeding. Plant Physiology, 125, 156–159. doi: 10.1104/pp. 125.1.156.Google Scholar
  89. Kumar, L. S. (1999). DNA markers in plant improvement: an overview. Biotechnology Advances, 17, 143–182. doi: 10.1016/S0734-9750(98)00018-4.PubMedGoogle Scholar
  90. Kushner, D. B., Lindenbach, B. D., Grdzelishvili, V. Z., Noueiry, A. O., Paul, S. M., & Ahlquist, P. (2003). Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proceedings of the National Academy of Sciences of the United States of America, 100, 15764–15769. doi: 10.1073/pnas.2536857100.PubMedGoogle Scholar
  91. Lanfermeijer, F. C., Dijkhuis, J., Sturre, M. J. G., Haan, P., & Hille, J. (2003). Cloning and characterization of the durable Tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Molecular Biology, 52, 1039–1051. doi: 10.1023/A:1025434519282.Google Scholar
  92. Lanfermeijer, F. C., Jiang, G. Y., Ferwerda, M. A., Dijkhuis, J., de Haan, P., Yang, R. C., et al. (2004). The durable resistance gene Tm-2(2) from tomato confers resistance against ToMV in tobacco and preserves its viral specificity. Plant Science, 167, 687–692. doi: 10.1016/j.plantsci.2004.04.027.Google Scholar
  93. Lee, W. M., Ishikawa, M., & Ahlquist, P. (2001). Mutation of host Delta 9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. Journal of Virology, 75, 2097–2106. doi: 10.1128/JVI.75.5.2097-2106.2001.PubMedGoogle Scholar
  94. Lellis, A. D., Kasschau, K. D., Whitham, S. A., & Carrington, J. C. (2002). Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF4E during potyvirus infection. Current Biology, 12, 1046–1051. doi: 10.1016/S0960-9822(02)00898-9.PubMedGoogle Scholar
  95. Leonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M. G., & Laliberte, J. F. (2000). Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. Journal of Virology, 74, 7730–7737. doi: 10.1128/JVI.74.17.7730-7737.2000.PubMedGoogle Scholar
  96. Leonard, S., Chisholm, J., Laliberte, J. F., & Sanfacon, H. (2002). Interaction in vitro between the proteinase of Tomato ringspot virus (genus Nepovirus) and the eukaryotic translation initiation factor iso4E from Arabidopsis thaliana. The Journal of General Virology, 83, 2085–2089.PubMedGoogle Scholar
  97. Leonard, S., Viel, C., Beauchemin, C., Daigneault, N., Fortin, M. G., & Laliberte, 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. The Journal of General Virology, 85, 1055–1063. doi: 10.1099/vir.0.19706-0.PubMedGoogle Scholar
  98. Levy, M., Edelbaum, O., & Sela, I. (2004). Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiology, 135, 2392–2397. doi: 10.1104/pp.104.044859.PubMedGoogle Scholar
  99. Li, L., Zhao, Y., McCaig, B. C., Wingerd, B. A., Wang, J., Whalon, M. E., et al. (2004). The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. The Plant Cell, 16, 126–143. doi: 10.1105/tpc.017954.PubMedGoogle Scholar
  100. Li, Y., Hill, C., Carlson, S., Diers, B., & Hartman, G. (2007). Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Molecular Breeding, 19, 25–34. doi: 10.1007/s11032-006-9039-9.Google Scholar
  101. Lindhout, P. (2002). The perspectives of polygenic resistance in breeding for durable resistance. Euphytica, 124, 217–229. doi: 10.1023/A:1015686601404.Google Scholar
  102. Liu, Y., Schiff, M., Marathe, R., & Dinesh-Kumar, S. P. (2002). Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to Tobacco mosaic virus. The Plant Journal, 30, 415–429. doi: 10.1046/j.1365-313X.2002.01297.x.PubMedGoogle Scholar
  103. Lopez-Perez, J. A., Le Strange, M., Kaloshian, I., & Ploeg, A. T. (2006). Differential response of Mi gene-resistant tomato rootstocks to root-knot nematodes (Meloidogyne incognita). Crop Protection (Guildford, Surrey), 25, 382–388. doi: 10.1016/j.cropro.2005.07.001.Google Scholar
  104. Lucas, W. J. (2006). Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology, 344, 169–184. doi: 10.1016/j.virol.2005.09.026.PubMedGoogle Scholar
  105. Lunello, P., Mansilla, C., Sanchez, F., & Ponz, F. (2007). A developmentally linked, dramatic, and transient loss of virus from roots of Arabidopsis thaliana plants infected by either of two RNA viruses. Molecular Plant-Microbe Interactions, 20, 1589–1595. doi: 10.1094/MPMI-20-12-1589.PubMedGoogle Scholar
  106. Mahajan, S. K., Chisholm, S. T., Whitham, S. A., & Carrington, J. C. (1998). Identification and characterization of a locus (RTM1) that restricts long-distance movement of Tobacco etch virus in Arabidopsis thaliana. The Plant Journal, 14, 177–186. doi: 10.1046/j.1365-313X.1998.00105.x.PubMedGoogle Scholar
  107. Malcuit, I., Marano, M. R., Kavanagh, T. A., De Jong, W., Forsyth, A., & Baulcombe, D. C. (1999). The 25-kDa movement protein of PVX elicits Nb-mediated hypersensitive cell death in potato. Molecular Plant-Microbe Interactions, 12, 536–543. doi: 10.1094/MPMI.1999.12.6.536.Google Scholar
  108. Mallor, C., Alvarez, J. M., & Arteaga, M. L. (2003). A resistance to systemic symptom expression of Melon necrotic spot virus in melon. Journal of the American Society for Horticultural Science, 128(4), 541–547.Google Scholar
  109. Marco, C. F., Aguilar, J. M., Abad, J., Gómez-Guillamón, M. L., & Aranda, M. A. (2003). Melon resistance to Cucurbit yellow stunting disorder virus is characterized by reduced virus accumulation. Phytopathology, 93, 844–852. doi: 10.1094/PHYTO.2003.93.7.844.PubMedGoogle Scholar
  110. Margaria, P., Ciuffo, M., & Turina, M. (2004). Resistance breaking strains of Tomato spotted wilt virus (Tospovirus-Bunyaviridae) on resistant pepper cultivars in Almeria (Spain). Plant Pathology, 53, 795. doi: 10.1111/j.1365-3059.2004.01082.x.Google Scholar
  111. Martinez de Ilarduya, O., Xie, Q., & Kaloshian, I. (2003). Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions, 16, 699–708. doi: 10.1094/MPMI.2003.16.8.699.PubMedGoogle Scholar
  112. Maule, A. J. (2008). Plasmodesmata: structure, function and biogenesis. Current Opinion in Plant Biology, 11, 680–686. doi: 10.1016/j.pbi.2008.08.002.PubMedGoogle Scholar
  113. Maule, A. J., & Wang, D. (1996). Seed transmission of plant viruses: a lesson in biological complexity. Trends in Microbiology, 4, 153–158. doi: 10.1016/0966-842X(96) 10016-0.PubMedGoogle Scholar
  114. Maule, A. J., Caranta, C., & Boulton, M. I. (2007). Sources of natural resistance to plant viruses: status and prospects. Molecular Plant Pathology, 8, 223–231. doi: 10.1111/j.1364-3703.2007.00386.x.Google Scholar
  115. Mensah, C., Di Fonzo, C., & Wang, D. (2008). Inheritance of soybean aphid resistance in PI567541B and PI567598B. Crop Science, 48, 1759–1763. doi: 10.2135/cropsci2007.09.0535.Google Scholar
  116. Milligan, S. B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P., & Williamson, V. M. (1998). The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. The Plant Cell, 10, 1307–1319.PubMedGoogle Scholar
  117. Moffett, P., Farnham, G., Peart, J., & Baulcombe, D. C. (2002). Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. The EMBO Journal, 21, 4511–4519. doi: 10.1093/emboj/cdf453.PubMedGoogle Scholar
  118. Moore, C. J., & MacDiarmid, R. M. (2006). Dark green islands: the phenomenon. In G. Loebenstein & J. P. Carr (Eds.), Natural resistance mechanisms of plants to viruses, pp. 187–209. The Netherlands: Springer, Dordrecht.Google Scholar
  119. Moury, B., Morel, C., Johansen, E., Guilbaud, L., Souche, S., Ayme, V., et al. (2004). Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Molecular Plant-Microbe Interactions, 17, 322–329. doi: 10.1094/MPMI.2004.17.3.322.PubMedGoogle Scholar
  120. Moury, B., Fabre, F., & Senoussi, R. (2007). Estimation of the number of virus particles transmitted by an insect vector. Proceedings of the National Academy of Sciences of the United States of America, 104, 17891–17896. doi: 10.1073/pnas.0702739104.PubMedGoogle Scholar
  121. Nagy, P. D., & Pogany, J. (2006). Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology, 344, 211–220. doi: 10.1016/j.virol.2005.09.017.PubMedGoogle Scholar
  122. Nault, L. R. (1997). Arthropod transmission of plant viruses: a new synthesis. Annals of the Entomological Society of America, 90, 521–541.Google Scholar
  123. Ng, J. C., & Falk, B. W. (2006). Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annual Review of Phytopathology, 44, 183–212. doi: 10.1146/annurev.phyto.44.070505.143325.PubMedGoogle Scholar
  124. Nieto, C., Morales, M., Orjeda, G., Clepet, C., Monfort, A., Sturbois, B., et al. (2006). An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. The Plant Journal, 48, 452–462. doi: 10.1111/j.1365-313X.2006.02885.x.PubMedGoogle Scholar
  125. Noueiry, A. O., & Ahlquist, P. (2003). Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annual Review of Phytopathology, 41, 77–98. doi: 10.1146/annurev.phyto.41.052002.095717.PubMedGoogle Scholar
  126. Oleykowsky, C. A., Bronson Mullins, C. R., Godwin, A. K., & Yeung, A. T. (1998). Mutation detection using a novel plant endonuclease. Nucleic Acids Research, 26, 4597–4602. doi: 10.1093/nar/26.20.4597.Google Scholar
  127. Padgett, H. S., & Beachy, R. N. (1993). Analysis of a Tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. The Plant Cell, 5, 577–586.PubMedGoogle Scholar
  128. Palloix, A., Ayme, V., & Moury, B. (2009). Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytologist, doi: 10.1111/j.1469-8137.2009.02827.x.
  129. Palukaitis, P., & Carr, J. P. (2008). Plant resistance responses to viruses. Journal of Plant Pathology, 90(2), 153–171.Google Scholar
  130. Panavas, T., & Nagy, P. D. (2003). Yeast as a model host to study replication and recombination of defective interfering RNA of Tomato bushy stunt virus. Virology, 314, 315–325. doi: 10.1016/S0042-6822(03) 00436-7.PubMedGoogle Scholar
  131. Pascual, S., Avilés, M., Nombela, G., Muñiz, M., & Beitia, F. (2000). Development of Bemisia tabaci (biotype Q) on tomato cultivars with / without the Mi gene. Medical Faculty Landbouww, University Gent, 65, 291–292.Google Scholar
  132. Pitrat, M., & Lecoq, H. (1980). Inheritance of resistance to Cucumber mosaic virus transmission by Aphis gossypii in Cucumis melo. Phytopathology, 70, 958–961. doi: 10.1094/Phyto-70-958.Google Scholar
  133. Pokorny, R., & Porubova, M. (2006). Heritability of resistance in maize to the Czech isolate of Sugarcane mosaic virus. Cereal Research Communications, 34, 1081–1086. doi: 10.1556/CRC.34.2006.2-3.241.Google Scholar
  134. Ponz, F., Russell, M. L., Rowhani, A., & Bruening, G. (1988). A cowpea line has distinct genes for resistance to Tobacco ringspot virus and Cowpea mosaic-virus. Phytopathology, 78, 1124–1128. doi: 10.1094/Phyto-78-1124.Google Scholar
  135. Prins, M., & Goldbach, R. (1998). The emerging problem of tospovirus infection and nonconventional methods of control. Trends in Microbiology, 6, 31–35. doi: 10.1016/S0966-842X(97) 01173-6.PubMedGoogle Scholar
  136. Prins, M., Laimer, M., Noris, E., Schubert, J., Wassenegger, M., & Tepfer, M. (2008). Strategies for antiviral resistance in transgenic plants. Molecular Plant Pathology, 9, 73–83.PubMedGoogle Scholar
  137. Qiu, W., & Moyer, J. W. (1999). Tomato spotted wilt tospovirus adapts to the TSWV N gene-derived resistance by genome reassortment. Phytopathology, 89, 575–582. doi: 10.1094/PHYTO.1999.89.7.575.PubMedGoogle Scholar
  138. Rairdan, G. J., & Moffett, P. (2006). Distinct domains in the ARC region of the potato resistance protein Rx Mediate LRR binding and inhibition of activation. The Plant Cell, 18, 2082–2093. doi: 10.1105/tpc.106.042747.PubMedGoogle Scholar
  139. Rairdan, G. J., Collier, S. M., Sacco, M. A., Baldwin, T. T., Boettrich, T., & Moffett, P. (2008). The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. The Plant Cell, 20, 739–751. doi: 10.1105/tpc.107.056036.PubMedGoogle Scholar
  140. Ratcliff, F., Harrison, B. D., & Baulcombe, D. C. (1997). A similarity between viral defense and gene silencing in plants. Science, 276, 1558–1560. doi: 10.1126/science.276.5318.1558.PubMedGoogle Scholar
  141. Ratcliff, F. G., MacFarlane, S. A., & Baulcombe, D. C. (1999). Gene silencing without DNA: RNA-mediated cross-protection between viruses. The Plant Cell, 11, 1207–1215.PubMedGoogle Scholar
  142. Revers, F., Guiraud, T., Houvenaghel, M. C., Mauduit, T., Le Gall, O., & Candresse, T. (2003). Multiple resistance phenotypes to Lettuce mosaic virus among Arabidopsis thaliana accessions. Molecular Plant-Microbe Interactions, 16, 608–616. doi: 10.1094/MPMI.2003.16.7.608.PubMedGoogle Scholar
  143. Robaglia, C., & Caranta, C. (2006). Translation initiation factors: a weak link in plant RNA virus infection. Trends in Plant Science, 11, 40–45. doi: 10.1016/j.tplants.2005.11.004.PubMedGoogle Scholar
  144. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., & Williamson, V. W. (1998). The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the United States of America, 95, 9750–9754. doi: 10.1073/pnas.95.17.9750.PubMedGoogle Scholar
  145. Sacco, M. A., Shahid, M., & Moffett, P. (2007). A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance. The Plant Journal, 52, 82–93. doi: 10.1111/j.1365-313X.2007.03213.x.PubMedGoogle Scholar
  146. Sacristán, S., Malpica, J. M., Fraile, A., & García-Arenal, F. (2003). Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. Journal of Virology, 77, 9906–9911. doi: 10.1128/JVI.77.18.9906-9911.2003.PubMedGoogle Scholar
  147. Sadasivam, S., & Thayumanavan, B. B. (2003). Molecular host plant resistance to pests (pp. 479). New York.Google Scholar
  148. Sanjuán, R., Moya, A., & Elena, S. F. (2004). The contribution of epistasis to the architecture of fitness in an RNA virus. Proceedings of the National Academy of Sciences of the United States of America, 101, 15376–15379. doi: 10.1073/pnas.0404125101.PubMedGoogle Scholar
  149. Sanjuán, R., Cuevas, J. M., Moya, A., & Elena, S. F. (2005). Epistasis and the adaptability of an RNA virus. Genetics, 170, 1001–1008. doi: 10.1534/genetics.105.040741.PubMedGoogle Scholar
  150. 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. doi: 10.1006/viro.2000.0416.PubMedGoogle Scholar
  151. Schirmer, A., Link, D., Cognat, V., Moury, B., Beuve, M., Meunier, A., et al. (2005). Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. The Journal of General Virology, 86, 2897–2911. doi: 10.1099/vir.0.81167-0.PubMedGoogle Scholar
  152. Scholthof, H. B. (2005). Plant virus transport: motions of functional equivalence. Trends in Plant Science, 10, 376–382. doi: 10.1016/j.tplants.2005.07.002.PubMedGoogle Scholar
  153. Schurnbusch, T., Paillard, S., Schori, A., Messner, M., Schachermayr, G., Winzeler, M., et al. (2004). Dissection of quantitative and durable leaf rust resistance in Swiss winter wheat reveals a major resistance QTL in the Lr34 chromosomal region. Theoretical and Applied Genetics, 108, 477–784. doi: 10.1007/s00122-003-1444-4.Google Scholar
  154. Seifers, D. L., Martin, T. J., Harvey, T. L., Haber, S., & Haley, S. D. (2006). Temperature sensitivity and efficacy of Wheat streak mosaic virus resistance derived from CO960293 wheat. Plant Disease, 90, 623–628. doi: 10.1094/PD-90-0623.Google Scholar
  155. Sekine, K. T., Ishihara, T., Hase, S., Kusano, T., Shah, J., & Takahashi, H. (2006). Single amino acid alterations in Arabidopsis thaliana RCY1 compromise resistance to Cucumber mosaic virus, but differentially suppress hypersensitive response-like cell death. Plant Molecular Biology, 62, 669–682. doi: 10.1007/s11103-006-9048-4.PubMedGoogle Scholar
  156. Serva, S., & Nagy, P. D. (2006). Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. Journal of Virology, 80, 2162–2169. doi: 10.1128/JVI.80.5.2162-2169.2006.PubMedGoogle Scholar
  157. Singer, A. C., Crowley, D. E., & Thompson, I. P. (2003). Secondary plant metabolites in phytoremediation and biotransformation. Trends in Biotechnology, 21, 123–130. doi: 10.1016/S0167-7799(02) 00041-0.PubMedGoogle Scholar
  158. Slade, A. J., Fuerstenberg, S. I., Loeffler, D., Steine, M. N., & Facciotti, D. (2005). A reverse genetic, non-transgenic approach to wheat crop improvement by TILLING. Nature Biotechnology, 23, 75–81. doi: 10.1038/nbt1043.PubMedGoogle Scholar
  159. Smith, C. M. (1989). Plant resistance to insects: A fundamental approach. New York: Wiley.Google Scholar
  160. Soler, S., Díez, M. J., & Nuez, F. (1998). Effect of temperature regime and growth stage interaction on pattern of virus presence in TSWV-resistant accessions of Capsicum chinense. Plant Disease, 82, 1199–1204. doi: 10.1094/PDIS.1998.82.11.1199.Google Scholar
  161. Soosaar, J. L., Burch-Smith, T. M., & Dinesh-Kumar, S. P. (2005). Mechanisms of plant resistance to viruses. Nature Reviews Microbiology, 3, 789–798. doi: 10.1038/nrmicro1239.PubMedGoogle Scholar
  162. Sorho, F., Pinel, A., Traore, O., Bersoult, A., Ghesquiere, A., Hébrard, E., et al. (2005). Durability of natural and transgenic resistances in rice to Rice yellow mottle virus. European Journal of Plant Pathology, 112, 349–359. doi: 10.1007/s10658-005-6607-5.Google Scholar
  163. Stacesmith, R., & Hamilton, R. I. (1988). Inoculum thresholds of seedborne pathogens-viruses. Phytopathology, 78, 875–880. doi: 10.1094/Phyto-78-875.Google Scholar
  164. Stein, N., Perovic, D., Kumlehn, J., Pellio, B., Stracke, S., Streng, S., et al. (2005). The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). The Plant Journal, 42, 912–922. doi: 10.1111/j.1365-313X.2005.02424.x.PubMedGoogle Scholar
  165. Strange, R. N., & Scott, P. R. (2005). Plant disease: a threat to global food security. Annual Review of Phytopathology, 43, 83–116. doi: 10.1146/annurev.phyto.43.113004.133839.PubMedGoogle Scholar
  166. Szittya, G., & Burgyan, J. (2001). Cymbidium ringspot tombusvirus coat protein coding sequence acts as an avirulent RNA. Journal of Virology, 75, 2411–2420. doi: 10.1128/JVI.75.5.2411-2420.2001.PubMedGoogle Scholar
  167. Takahashi, G. N., & Ehara, Y. (1994). Hypersensitive response in Cucumber mosaic virus-inoculated Arabidopsis thaliana. The Plant Journal, 6, 369–377.Google Scholar
  168. Takahashi, H., Suzuki, M., Natsuaki, K., Shigyo, T., Hino, K., Teraoka, T., et al. (2001). Mapping the virus and host genes involved in the resistance response in Cucumber mosaic virus-infected Arabidopsis thaliana. Plant & Cell Physiology, 42, 340–347. doi: 10.1093/pcp/pce039.Google Scholar
  169. Takahashi, H., Miller, J., Nozaki, Y., Takeda, M., Shah, J., Hase, S., et al. (2002). RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to Cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. The Plant Journal, 32, 655–667. doi: 10.1046/j.1365-313X.2002.01453.x.PubMedGoogle Scholar
  170. Takahashi, H., Kanayama, Y., Zheng, M. S., Kusano, T., Hase, S., Ikegami, M., et al. (2004). Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to Cucumber mosaic virus. Plant & Cell Physiology, 45, 803–809. doi: 10.1093/pcp/pch085.Google Scholar
  171. Takken, F. L. W., Albrech, T. M., & Tameling, W. I. L. (2006). Resistance proteins: molecular switches of plant defence. Current Opinion in Plant Biology, 9, 383–390. doi: 10.1016/j.pbi.2006.05.009.PubMedGoogle Scholar
  172. Tameling, W. I. L., & Baulcombe, D. C. (2007). Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. The Plant Cell, 19, 1682–1694. doi: 10.1105/tpc.107.050880.PubMedGoogle Scholar
  173. Thomas, C. L., Bayer, E. M., Ritzenthaler, C., Fernandez-Calvino, L., & Maule, A. J. (2008). Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology, 6, e7. doi: 10.1371/journal.pbio.0060007.PubMedGoogle Scholar
  174. Thompson, G. A., & Goggin, F. L. (2006). Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany, 57, 755–766. doi: 10.1093/jxb/erj135.PubMedGoogle Scholar
  175. Tomita, Y., Mizuno, T., Diez, J., Naito, S., Ahlquist, P., & Ishikawa, M. (2003). Mutation of host Dna homolog inhibits Brome mosaic virus negative-strand RNA synthesis. Journal of Virology, 77, 2990–2997. doi: 10.1128/JVI.77.5.2990-2997.2003.PubMedGoogle Scholar
  176. Traw, M. B., Kim, J., Enright, S., Cipollini, D. F., & Bergelson, J. (2003). Negative cross-talk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Molecular Ecology, 12, 1125–1135. doi: 10.1046/j.1365-294X.2003.01815.x.PubMedGoogle Scholar
  177. Truniger, V., Nieto, C., González-Ibeas, D., & Aranda, M. A. (2008). Mechanism of plant eIF4E-mediated virus resistance: Cap-independent translation of a viral RNA controlled in cis by an (a) virulence determinant. The Plant Journal, 56, 716–727. doi: 10.1111/j.1365-313X.2008.03630.x.PubMedGoogle Scholar
  178. Tsujimoto, Y., Numaga, T., Ohshima, K., Yano, M. A., Ohsawa, R., Goto, D. B., et al. (2003). Arabidopsis tobamovirus multiplication (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. The EMBO Journal, 22, 335–343. doi: 10.1093/emboj/cdg034.PubMedGoogle Scholar
  179. Turkensteen, L. J. (1993). Durable resistance of potatoes against Phytophthora infestans. In T. Jacobs & J. E. Parlevliet (Eds.), Durability of disease resistance, pp. 115–124. Dordrecht, The Netherlands: Academic.Google Scholar
  180. Ueda, H., Yamaguchi, Y., & Sano, H. (2006). Direct recognition of Tobacco mosaic virus by the tobacco N factor. Plant & Cell Physiology, 47, S48–S48.Google Scholar
  181. Ueki, S., & Citovsky, V. (2002). The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nature Cell Biology, 4, 478–486.PubMedGoogle Scholar
  182. Vazquez, F. (2006). Arabidopsis endogenous small RNAs: highways and byways. Trends in Plant Science, 11, 460–468. doi: 10.1016/j.tplants.2006.07.006.PubMedGoogle Scholar
  183. Waigmann, E. (2004). Screening for mutant virus movement proteins (MP), useful in producing virus-resistant transgenic plants, comprises carrying a mutation at the carboxyterminal end of the virus MP. Patent WO2004023137-A2; AU2003273818-A1.Google Scholar
  184. Wang, D., & Maule, A. J. (1992). Early embryo invasion as a determinant in pea of the seed transmission of Pea seed-borne mosaic virus. The Journal of General Virology, 73, 1615–1620. doi: 10.1099/0022-1317-73-7-1615.PubMedGoogle Scholar
  185. Wang, D., & Maule, A. J. (1994). A model for seed transmission of a plant virus: genetic and structural analyses of pea embryo invasion by Pea seed-borne mosaic virus. The Plant Cell, 6, 777–787.PubMedGoogle Scholar
  186. Wang, D., MacFarlane, S. A., & Maule, A. J. (1997). Viral determinants of Pea early browning virus seed transmission in pea. Virology, 234, 112–117. doi: 10.1006/viro.1997.8637.PubMedGoogle Scholar
  187. Weber, H., Schultze, S., & Pfitzner, A. J. (1993). Two amino acid substitutions in the Tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-2(2) resistance gene in the tomato. Journal of Virology, 67, 6432–6438.PubMedGoogle Scholar
  188. Weiland, J. J., & Edwards, M. C. (1996). A single nucleotide substitution in the alpha a gene confers oat pathogenicity to Barley stripe mosaic virus strain ND18. Molecular Plant-Microbe Interactions, 9, 62–67.PubMedGoogle Scholar
  189. Whitham, S. A., & Wang, Y. (2004). Roles for host factors in plant viral pathogenicity. Current Opinion in Plant Biology, 7, 365–371. doi: 10.1016/j.pbi.2004.04.006.PubMedGoogle Scholar
  190. Whitham, S., Dinesh-Kumar, S. P., Choi, D., Hehl, R., Corr, C., & Baker, B. (1994). The product of the Tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell, 78, 1101–1115. doi: 10.1016/0092-8674(94)90283-6.PubMedGoogle Scholar
  191. Whitham, S. A., Yamamoto, M. L., & Carrington, J. C. (1999). Selectable viruses and altered susceptibility mutants in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 96, 772–777. doi: 10.1073/pnas.96.2.772.PubMedGoogle Scholar
  192. Whitham, S. A., Anderberg, R. J., Chisholm, S. T., & Carrington, J. C. (2000). Arabidopsis RTM2 gene is necessary for specific restriction of Tobacco etch virus and encodes an unusual small heat shock-like protein. The Plant Cell, 12, 569–582.PubMedGoogle Scholar
  193. Wintermantel, W. M., Banerjee, N., Oliver, J. C., Paolillo, D. J., & Zaitlin, M. (1997). Cucumber mosaic virus is restricted from entering minor veins in transgenic tobacco exhibiting replicase-mediated resistance. Virology, 231, 248–257. doi: 10.1006/viro.1997.8533.PubMedGoogle Scholar
  194. Wise, R. P., Moscou, M. J., Bogdanove, A. J., & Whitham, S. A. (2007). Transcript profiling in host-pathogen interactions. Annual Review of Phytopathology, 45, 329–369. doi: 10.1146/annurev.phyto.45.011107.143944.PubMedGoogle Scholar
  195. Wittmann, S., Chatel, H., Fortin, M. G., & Laliberte, J. F. (1997). Interaction of the viral protein genome linked of Turnip mosaic potyvirus with the translational eukaryotic initiation factor 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology, 234, 84–92. doi: 10.1006/viro.1997.8634.PubMedGoogle Scholar
  196. Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O., & Michelmore, R. W. (2007). Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. The Plant Journal, 51, 803–818. doi: 10.1111/j.1365-313X.2007.03182.x.PubMedGoogle Scholar
  197. Yamanaka, T., Imai, T., Satoh, R., Kawashima, A., Takahashi, M., Tomita, K., et al. (2002). Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. Journal of Virology, 76, 2491–2497. doi: 10.1128/jvi.76.5.2491-2497.2002.PubMedGoogle Scholar
  198. Yoshii, M., Yoshioka, N., Ishikawa, M., & Naito, S. (1998). Isolation of an Arabidopsis thaliana mutant in which accumulation of Cucumber mosaic virus coat protein is delayed. The Plant Journal, 13, 211–219. doi: 10.1046/j.1365-313X.1998.00024.x.PubMedGoogle Scholar
  199. Yoshii, M., Nishikiori, M., Tomita, K., Yoshioka, N., Kozuka, R., Naito, S., et al. (2004). The Arabidopsis cucumovirus multiplication 1 and 2 loci encode tip translation initiation factors 4E and 4G. Journal of Virology, 78, 6102–6111. doi: 10.1128/JVI.78.12.6102-6111.2004.PubMedGoogle Scholar
  200. Zheng, Y., & Edwards, M. C. (1990). Expression of resistance to Barley stripe mosaic virus in barley and oat protoplasts. The Journal of General Virology, 71, 1865–1868. doi: 10.1099/0022-1317-71-8-1865.PubMedGoogle Scholar

Copyright information

© KNPV 2009

Authors and Affiliations

  • P. Gómez
    • 1
  • A.M. Rodríguez-Hernández
    • 1
  • B. Moury
    • 2
  • M.A. Aranda
    • 1
  1. 1.Centro de Edafología y Biología Aplicada del Segura (CEBAS)Consejo Superior de Investigaciones Científicas (CSIC)Espinardo (Murcia)Spain
  2. 2.INRAUR407 Pathologie VégétaleMontfavetFrance

Personalised recommendations