1887

Abstract

The line RLR22 was resistant to eight diverse turnip mosaic virus (TuMV) isolates. A genetic map based on 213 marker loci segregating in 120 first back-cross (B) individuals was established and aligned with the genome reference map using some of the RFLP probes. B individuals were self-pollinated to produce BS families. The existence of two loci controlling resistance to TuMV isolate CDN 1 was established from contrasting patterns of segregation for resistance and susceptibility in the BS families. The first gene, (), had a recessive allele for resistance, was located on the upper portion of chromosome R4 and was epistatic to the second gene. The second gene, (), possessed a dominant allele for resistance and was located on the upper portion of chromosome R8. These genes also controlled resistance to TuMV isolate CZE 1 and might be sufficient to explain the broad-spectrum resistance of RLR22. The dominant resistance gene, , was coincident with one of the three eukaryotic initiation factor 4E () loci of and possibly one of the loci of . The recessive resistance gene was apparently coincident with one of the three loci of in the A genome of and therefore, by inference, in the genome. This suggested a mode of action for the resistance that is based on denying the viral RNA access to the translation initiation complex of the plant host. The gene is the first reported example of a recessive resistance gene mapped in a species.

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2007-11-01
2019-12-09
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References

  1. Anonymous ( 1996; ). Asian Vegetable Research and Development Centre Annual Report. Asian Vegetable Research and Development Centre, Shanhua, Tainan, Taiwan.
  2. Bendahmane, A., Kanyuka, K. & Baulcombe, D. C. ( 1999; ). The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11, 781–791.[CrossRef]
    [Google Scholar]
  3. Bergelson, J., Kreitman, M., Stahl, E. A. & Tian, D. ( 2001; ). Evolutionary dynamics of plant R-genes. Science 292, 2281–2285.[CrossRef]
    [Google Scholar]
  4. Browning, K. S. ( 1996; ). The plant translational apparatus. Plant Mol Biol 32, 107–143.[CrossRef]
    [Google Scholar]
  5. Carrington, J. C. & Freed, D. D. ( 1990; ). Cap-independent enhancement of translation by a plant potyvirus 5′ non-translated region. J Virol 64, 1590–1597.
    [Google Scholar]
  6. Chisholm, S. T., Para, 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 Physiol 127, 1667–1675.[CrossRef]
    [Google Scholar]
  7. Dangl, J. L. & Jones, J. D. G. ( 2001; ). Plant pathogens and integrated defense responses to infection. Nature 411, 826–833.[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. Edwardson, J.R. & Christie, R.G. ( 1991; ). The Potyvirus Group. Volumes I–IV, Florida Agricultural Experiment Station Monograph 16.
  10. Erickson, F. L., Dinesh-Kumar, S. P., Holzberg, S., Ustach, C. V., Dutton, M., Handley, V., Corr, C. & Baker, B. J. ( 1999; ). Interactions between tobacco mosaic virus and the tobacco N gene. Philos Trans R Soc Lond B Biol Sci 354, 653–658.[CrossRef]
    [Google Scholar]
  11. Gao, Z., Johansen, E., Eyres, S., Thomas, C. L., Ellis, T. H. N. & Maule, A. J. ( 2004; ). The potyvirus recessive 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. Hämäläinen, J. H., Kekarainen, T., Gebhardt, C., Watanabe, K. N. & Valkonen, J. P. T. ( 2000; ). Recessive and dominant genes interfere with the vascular transport of potato virus A in diploid potatoes. Mol Plant Microbe Interact 13, 402–412.[CrossRef]
    [Google Scholar]
  13. Hughes, S. L., Green, S. K., Lydiate, D. J. & Walsh, J. A. ( 2002; ). Resistance to turnip mosaic virus in Brassica rapa and B. napus and the analysis of genetic inheritance in selected lines. Plant Pathol 51, 567–573.[CrossRef]
    [Google Scholar]
  14. Hughes, S. L., Hunter, P. J., Sharpe, A. G., Kearsey, M. J., Lydiate, D. J. & Walsh, J. A. ( 2003; ). Genetic mapping of a novel turnip mosaic virus resistance gene in Brassica napus. Theor Appl Genet 107, 1169–1173.[CrossRef]
    [Google Scholar]
  15. Jenner, C. E. & Walsh, J. A. ( 1996; ). Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathol 45, 848–856.[CrossRef]
    [Google Scholar]
  16. Jenner, C. E., Keane, G. J., Jones, J. E. & Walsh, J. A. ( 1999; ). Serotypic variation in turnip mosaic virus. Plant Pathol 48, 101–108.[CrossRef]
    [Google Scholar]
  17. Jenner, C. E., Sanchez, 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]
  18. Jenner, C. E., Tomimura, K., Ohshima, K., Hughes, S. L. & Walsh, J. A. ( 2002; ). Mutations in turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300, 50–59.[CrossRef]
    [Google Scholar]
  19. Jenner, C. E., Wang, X., Tomimura, K., Ohshima, K., Ponz, F. & Walsh, J. A. ( 2003; ). The dual role of the potyvirus P3 protein of turnip mosaic virus as a symptom and avirulence determinant in brassicas. Mol Plant Microbe Interact 16, 777–784.[CrossRef]
    [Google Scholar]
  20. Johansen, I. E., Lund, O. S., Hjulsager, C. K. & Laursen, J. ( 2001; ). Recessive resistance in Pisum sativum and potyvirus pathotype resolved in a gene-for-cistron correspondence between host and virus. J Virol 75, 6609–6614.[CrossRef]
    [Google Scholar]
  21. Keller, K. E., Johanssen, I. E., Martin, R. R. & Hampton, R. O. ( 1998; ). Potyvirus genome-linked protein (VPg) determines pea seed-borne mosaic virus pathotype-specific virulence in Pisum sativum. Mol Plant Microbe Interact 11, 124–130.[CrossRef]
    [Google Scholar]
  22. 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. Plant Cell 5, 913–920.[CrossRef]
    [Google Scholar]
  23. Kosambi, D. D. ( 1944; ). The estimation of map distances from recombination values. Ann Eugen 12, 172–175.
    [Google Scholar]
  24. Lander, E. S., Green, P., Abrahamson, J., Barlow, A., Daly, M. J., Lincoln, S. E. & Newberg, L. ( 1987; ). mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181.[CrossRef]
    [Google Scholar]
  25. Lartey, R. T., Ghoshroy, S. & Citovsky, V. ( 1998; ). Identification of an Arabidopsis thaliana mutation (vsm1) that restricts systemic movement of tobamoviruses. Mol Plant Microbe Interact 11, 706–709.[CrossRef]
    [Google Scholar]
  26. 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]
  27. Lellis, A. D., Kasschau, K. D., Whitham, S. A. & Carrington, J. ( 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]
  28. Léonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M. G. & Laliberté, J.-F. ( 2000; ). Complex formation between potyvirus VPg and translation initiation factor 4E correlates with virus infectivity. J Virol 74, 7730–7737.[CrossRef]
    [Google Scholar]
  29. Levis, C. & Astier-Manifacier, S. ( 1993; ). The 5′ untranslated region of PVY RNA, even located in an internal position, enables initiation of translation. Virus Genes 7, 367–379.[CrossRef]
    [Google Scholar]
  30. Liu, X. P., Lu, W. C., Liu, Y. K., Wei, S. Q., Xu, J. B., Liu, Z. R., Zhang, H. J., Li, J. L., Ke, G. L. & other authors ( 1996; ). Occurrence and strain differentiation of turnip mosaic potyvirus and sources of resistance in Chinese cabbage in China. Acta Hortic 407, 431–440.
    [Google Scholar]
  31. Michon, T., Estevez, Y., Walter, J., German-Retana, S. & Le Gall, O. ( 2006; ). The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J 273, 1312–1322.[CrossRef]
    [Google Scholar]
  32. Murphy, J. F., Blauth, J. R., Livingstone, K. D., Lackney, V. K. & Jahn, M. K. ( 1998; ). Genetic mapping of the pvr1 locus in Capsicum spp. and evidence that distinct potyvirus resistance loci control responses that differ at the whole plant and cellular levels. Mol Plant Microbe Interact 11, 943–951.[CrossRef]
    [Google Scholar]
  33. Naom, I. S., Mathew, C. G. & Town, M. M. ( 1995; ). Genetic mapping with microsatellites. In DNA Cloning: a Practical Approach 3: Complex Genomes, pp.195–217. Edited by D. M. Glover & B. D. Hames. Oxford: IRL Press.
  34. Nicolas, O. & Laliberté, J.-F. ( 1992; ). The complete nucleotide sequence of turnip mosaic potyvirus RNA. J Gen Virol 73, 2785–2793.[CrossRef]
    [Google Scholar]
  35. Nicolas, O., Dunnington, S. W., Gotow, L. F., Pirone, T. P. & Hellmann, G. M. ( 1997; ). Variations in the VPg protein allow a potyvirus to overcome va gene resistance in tobacco. Virology 237, 452–459.[CrossRef]
    [Google Scholar]
  36. Ohshima, K., Tanaka, M. & Sako, N. ( 1996; ). The complete nucleotide sequence of turnip mosaic virus RNA Japanese strain. Arch Virol 141, 1991–1997.[CrossRef]
    [Google Scholar]
  37. Parkin, I. A. P., Sharpe, A. G., Keith, D. J. & Lydiate, D. J. ( 1995; ). Identification of the A and C genome of amphidiploid Brassica napus (oilseed rape). Genome 38, 1122–1131.[CrossRef]
    [Google Scholar]
  38. Parkin, I. A. P., Gulden, S. M., Sharpe, A. G., Lukens, L., Trick, M., Osborn, T. C. & Lydiate, D. J. ( 2005; ). Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171, 765–781.[CrossRef]
    [Google Scholar]
  39. 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]
  40. Robaglia, C. & Caranta, C. ( 2006; ). Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11, 40–45.
    [Google Scholar]
  41. Robbins, M. A., Witsenboer, H., Michelmore, R. W., Laliberte, J. F. & Fortin, M. G. ( 1994; ). Genetic mapping of turnip mosaic virus resistance in Lactuca sativa. Theor Appl Genet 89, 583–589.
    [Google Scholar]
  42. 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]
  43. Rusholme, R. L., Walsh, J. A. & Lydiate, D. J. ( 2007; ). Genetic control of immunity to turnip mosaic virus (TuMV) pathotype 1 in Brassica rapa (Chinese cabbage). Genome in press
    [Google Scholar]
  44. 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]
  45. Schaad, M. C. & Carrington, J. C. ( 1996; ). Suppression of long-distance movement of tobacco etch virus in a nonsusceptible host. J Virol 70, 2556–2561.
    [Google Scholar]
  46. Sharpe, A. G., Parkin, I. A. P., Keith, D. J. & Lydiate, D. J. ( 1995; ). Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 38, 1112–1121.[CrossRef]
    [Google Scholar]
  47. Shattuck, V. I. ( 1992; ). The biology, epidemiology and control of turnip mosaic virus. Plant Breed Rev 14, 199–238.
    [Google Scholar]
  48. Sillito, D., Parkin, I. A. P., Mayerhofer, R., Lydiate, D. J. & Good, A. G. ( 2000; ). Arabidopsis thaliana: a source of candidate disease-resistance genes for Brassica napus. Genome 43, 452–460.[CrossRef]
    [Google Scholar]
  49. Staskawicz, B. J., Ausubel, F. M., Baker, B. J., Ellis, J. G. & Jones, J. D. G. ( 1995; ). Molecular genetics of plant disease resistance. Science 268, 661–667.[CrossRef]
    [Google Scholar]
  50. Suh, S. K., Green, S. K. & Park, H. G. ( 1995; ). Genetics of resistance to five strains of turnip mosaic virus in Chinese cabbage. Euphytica 81, 71–77.[CrossRef]
    [Google Scholar]
  51. Suh, S. K., Park, H. G. & Green, S. K. ( 1996; ). Interactions among TuMV strains inoculated and their movement in Chinese cabbage. J Kor Hort Sci 37, 392–398.
    [Google Scholar]
  52. Tanksley, S. D., Young, N. D., Paterson, A. H. & Bonierbale, M. W. ( 1989; ). RFLP mapping in plant breeding: new tools for an old science. Biol Technol 7, 257–264.[CrossRef]
    [Google Scholar]
  53. Thormann, C. E., Ferreira, M. E., Camargo, L. E. A., Tivang, J. G. & Osborn, T. C. ( 1994; ). Comparison of RFLP and RAPD markers to estimate genetic relationships within and among cruciferous species. Theor Appl Genet 88, 973–980.
    [Google Scholar]
  54. Tomimura, K., Gibbs, A. J., Jenner, C. E., Walsh, J. A. & Ohshima, K. ( 2003; ). The phylogeny of Turnip mosaic virus; comparisons of 38 genomic sequences reveal a Eurasian origin and a recent ‘emergence’ in east Asia. Mol Ecol 12, 2099–2111.[CrossRef]
    [Google Scholar]
  55. U, N. ( 1935; ). Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilisation. Jpn J Bot 7, 389–452.
    [Google Scholar]
  56. Vance, V. & Vaucheret, H. ( 2001; ). RNA silencing in plants – defense and counterdefense. Science 292, 2277–2280.[CrossRef]
    [Google Scholar]
  57. Walsh, J. A. & Jenner, C. E. ( 2002; ). Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 3, 289–300.[CrossRef]
    [Google Scholar]
  58. Walsh, J. A., Sharpe, A. G., Jenner, C. E. & Lydiate, D. J. ( 1999; ). Characterisation of resistance to turnip mosaic virus in oilseed rape (Brassica napus) and genetic mapping of TuRB01. Theor Appl Genet 99, 1149–1154.[CrossRef]
    [Google Scholar]
  59. Walsh, J. A., Rusholme, R. L., Hughes, S. L., Jenner, C. E., Bambridge, J. M., Lydiate, D. J. & Green, S. K. ( 2002; ). Different classes of resistance to turnip mosaic virus in Brassica rapa. Eur J Plant Pathol 108, 15–20.[CrossRef]
    [Google Scholar]
  60. Wittmann, S., Chatel, H., Fortin, M. G. & Laliberté, J.-F. ( 1997; ). Interaction of the viral protein genome linked of turnip mosaic potyvirus with the transitional eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234, 84–92.[CrossRef]
    [Google Scholar]
  61. Yang, Y., Shah, J. & Klessig, D. F. ( 1997; ). Signal perception and transduction in plant defense responses. Genes Dev 11, 1621–1639.[CrossRef]
    [Google Scholar]
  62. Yoon, J. Y., Green, S. K. & Opena, R. T. ( 1993; ). Inheritance of resistance to turnip mosaic virus in Chinese cabbage. Euphytica 69, 103–108.[CrossRef]
    [Google Scholar]
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