1887

Abstract

(TuMV, genus , family ) infects mainly cruciferous plants. Isolates Tu-3 and Tu-2R1 of TuMV exhibit different infection phenotypes in cabbage ( L.) and Japanese radish ( L.). Infectious full-length cDNA clones, pTuC and pTuR1, were constructed from isolates Tu-3 and Tu-2R1, respectively. Progeny virus derived from infections with pTuC induced systemic chlorotic and ringspot symptoms in infected cabbage, but no systemic infection in radish. Virus derived from plants infected with pTuR1 induced a mild chlorotic mottle in cabbage and infected radish systemically to induce mosaic symptoms. By exchanging genome fragments between the two virus isolates, the P3-coding region was shown to be responsible for systemic infection by TuMV and the symptoms it induces in cabbage and radish. Moreover, exchanges of smaller parts of the P3 region resulted in recombinants that induced complex infection phenotypes, especially the combination of pTuC-derived N-terminal sequence and pTuR1-derived C-terminal sequence. Analysis by tissue immunoblotting of the inoculated leaves showed that the distributions of P3-chimeric viruses differed from those of the parents, and that the origin of the P3 components affected not only virus accumulation, but also long-distance movement. These results suggest that the P3 protein is an important factor in the infection cycle of TuMV and in determining the host range of this and perhaps other potyviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.79825-0
2004-07-01
2024-03-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/85/7/vir852087.html?itemId=/content/journal/jgv/10.1099/vir.0.79825-0&mimeType=html&fmt=ahah

References

  1. Berger P. H., Barnett O. W., Brunt A. A. 14 other authors 2000; Family Potyviridae . In Virus Taxonomy : Seventh Report of the International Committee on Taxonomy of Viruses . pp  703–724 Edited by van Regenmortel M. H. V., Fauquet C. M., L D. H. Bishop and 8 others San Diego: Academic Press;
    [Google Scholar]
  2. Borgstrøm B., Johansen I. E. 2001; Mutations in Pea seedborne mosaic virus genome-linked protein VPg alter pathotype-specific virulence in Pisum sativum . Mol Plant Microbe Interact 14:707–714 [CrossRef]
    [Google Scholar]
  3. Carrington J. C., Kasschau K. D., Mahajan S. K., Schaad M. C. 1996; Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669–1681 [CrossRef]
    [Google Scholar]
  4. Carrington J. C., Jensen P. E., Schaad M. C. 1998; Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14:393–400 [CrossRef]
    [Google Scholar]
  5. 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 Physiol 127:1667–1675 [CrossRef]
    [Google Scholar]
  6. Chu M., Lopez-Moya J. J., Llave-Correas C., Pirone T. P. 1997; Two separate regions in the genome of the tobacco etch virus contain determinants of the wilting response of tabasco pepper. Mol Plant Microbe Interact 10:472–480 [CrossRef]
    [Google Scholar]
  7. Cronin S., Verchot J., Haldeman-Cahill R., Schaad M. C., Carrington J. C. 1995; Long-distance movement factor: a transport function of the potyvirus helper component proteinase. Plant Cell 7:549–559 [CrossRef]
    [Google Scholar]
  8. Dallot S., Quiot-Douine L., Sáenz P., Cervera M. T., García J.-A., Quiot J.-B. 2001; Identification of Plum pox virus determinants implicated in specific interactions with different Prunus spp. Phytopathology 91:159–164 [CrossRef]
    [Google Scholar]
  9. Dawson W. O., Hilf M. E. 1992; Host-range determinants of plant viruses. Annu Rev Plant Physiol Plant Mol Biol 43:527–555 [CrossRef]
    [Google Scholar]
  10. Dolja V. V., Haldeman R., Robertson N. L., Dougherty W. G., Carrington J. C. 1994; Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13:1482–1491
    [Google Scholar]
  11. Dolja V. V., Haldeman-Cahill R., Montgomery A. E., Vandenbosch K. A., Carrington J. C. 1995; Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 206:1007–1016 [CrossRef]
    [Google Scholar]
  12. Fraser R. S. S. 1992; The genetics of plant–virus interactions: implications for plant breeding. Euphytica 63:175–185 [CrossRef]
    [Google Scholar]
  13. Fujisawa I. 1990; Turnip mosaic virus strains in cruciferous crops in Japan. Jpn Agric Res Q 23:289–293
    [Google Scholar]
  14. Gómez-Campo C. 1999; Taxonomy. In Biology of Brassica coenospecies pp  3–32 Edited by Gómez-Campo C. Amsterdam: Elsevier Science;
    [Google Scholar]
  15. Green S. K., Deng T. C. 1985; Turnip mosaic virus strains in cruciferous hosts in Taiwan. Plant Dis 69:28–31 [CrossRef]
    [Google Scholar]
  16. Guo D., Rajamäki M.-L., Saarma M., Valkonen J. P. T. 2001; Towards a protein interaction map of potyviruses: protein interaction matrixes of two potyviruses based on the yeast two-hybrid system. J Gen Virol 82:935–939
    [Google Scholar]
  17. 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]
  18. Hjulsager C. K., Lund O. S., Johansen I. E. 2002; A new pathotype of Pea seedborne mosaic virus explained by properties of the P3-6K1- and viral genome-linked protein (VPg)-coding regions. Mol Plant Microbe Interact 15:169–171 [CrossRef]
    [Google Scholar]
  19. Hollings M., Brunt A. A. 1981; Potyviruses. In Handbook of Plant Virus Infections and Comparative Diagnosis pp  731–807 Edited by Kurstak E. Amsterdam: Elsevier/North-Holland;
    [Google Scholar]
  20. Hughes S. L., Hunter P. J., Sharpe A. G., Kearsey M. J., Lydiate D. J., Walsh J. A. 2003; Genetic mapping of novel Turnip mosaic virus resistance gene TuRB03 in Brassica napus . Theor Appl Genet 107:1169–1173 [CrossRef]
    [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. Kasschau K. D., Cronin S., Carrington J. C. 1997; Genome amplification and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component-proteinase. Virology 228:251–262 [CrossRef]
    [Google Scholar]
  27. Klein P. G., Klein R. R., Rodríguez-Cerezo E., Hunt A. G., Shaw J. G. 1994; Mutational analysis of the tobacco vein mottling virus genome. Virology 204:759–769 [CrossRef]
    [Google Scholar]
  28. Lucas W. J., Gilbertson R. L. 1994; Plasmodesmata in relation to viral movement within leaf tissues. Annu Rev Phytopathol 32:387–411 [CrossRef]
    [Google Scholar]
  29. 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 . Plant J 14:177–186 [CrossRef]
    [Google Scholar]
  30. Merits A., Guo D., Saarma M. 1998; VPg, coat protein and five non-structural proteins of potato A potyvirus bind RNA in a sequence-unspecific manner. J Gen Virol 79:3123–3127
    [Google Scholar]
  31. Merits A., Guo D., Järvekülg L., Saarma M. 1999; Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263:15–22 [CrossRef]
    [Google Scholar]
  32. Moreno M., Bernal J. J., Jiménez I., Rodríguez-Cerezo E. 1998; Resistance in plants transformed with the P1 or P3 gene of tobacco vein mottling potyvirus. J Gen Virol 79:2819–2827
    [Google Scholar]
  33. 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 νa gene resistance in tobacco. Virology 237:452–459 [CrossRef]
    [Google Scholar]
  34. 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]
  35. Ohshima K., Yamaguchi Y., Hirota R. 10 other authors 2002; Molecular evolution of Turnip mosaic virus : evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521
    [Google Scholar]
  36. Provvidenti R. 1980; Evaluation of Chinese cabbage cultivars from Japan and the People's Republic of China for resistance to turnip mosaic virus and cauliflower mosaic virus. J Am Soc Hortic Sci 105:571–573
    [Google Scholar]
  37. Rajamäki M.-L., Valkonen J. P. T. 1999; The 6K2 protein and the VPg of potato virus A are determinants of systemic infection in Nicandra physaloides . Mol Plant Microbe Interact 12:1074–1081 [CrossRef]
    [Google Scholar]
  38. Rao A. L. N. 1999; Molecular basis of symptomatology. In Molecular Biology of Plant Viruses pp  201–210 Edited by Mandahar C. L. Norwell: Kluwer Academic;
    [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. 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. Mol Plant Microbe Interact 16:608–616 [CrossRef]
    [Google Scholar]
  41. Riechmann J. L., Laín S., García J. A. 1992; Highlights and prospects of potyvirus molecular biology. J Gen Virol 73:1–16 [CrossRef]
    [Google Scholar]
  42. Rodríguez-Cerezo E., Shaw J. G. 1991; Two newly detected nonstructural viral proteins in potyvirus-infected cells. Virology 185:572–579 [CrossRef]
    [Google Scholar]
  43. Rojas M. R., Zerbini F. M., Allison R. F., Gilbertson R. L., Lucas W. J. 1997; Capsid protein and helper component-proteinase functions as potyvirus cell-to-cell movement proteins. Virology 237:283–295 [CrossRef]
    [Google Scholar]
  44. Sáenz P., Cervera M. T., Dallot S., Quiot L., Quiot J.-B., Riechmann J. L., García J. A. 2000; Identification of a pathogenicity determinant of Plum pox virus in the sequence encoding the C-terminal region of protein P3+6K1 . J Gen Virol 81:557–566
    [Google Scholar]
  45. Sáenz P., Salvador B., Simón-Mateo C., Kasschau K. D., Carrington J. C., García J. A. 2002; Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J Virol 76:1922–1931 [CrossRef]
    [Google Scholar]
  46. Sako N. 1980; Loss of aphid transmissibility of turnip mosaic virus. Phytopathology 70:647–649 [CrossRef]
    [Google Scholar]
  47. Sambrook J., Fritsch E. F., Maniatis T. A. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  48. 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]
  49. Schaad M. C., Lellis A. D., Carrington J. C. 1997; VPg of tobacco etch potyvirus is a host genotype-specific determinant for long-distance movement. J Virol 71:8624–8631
    [Google Scholar]
  50. Srinivasan I., Tolin S. A. 1992; Detection of three viruses of clovers by direct tissue immunoblotting. Phytopathology 82:721
    [Google Scholar]
  51. Stavolone L., Alioto D., Ragozzino A., Laliberté J.-F. 1998; Variability among turnip mosaic potyvirus isolates. Phytopathology 88:1200–1204 [CrossRef]
    [Google Scholar]
  52. Stobbs L. W., Shattuck V. I. 1989; Turnip mosaic virus strains in southern Ontario, Canada. Plant Dis 73:208–212 [CrossRef]
    [Google Scholar]
  53. Tóbiás I., Palkovics L., Tzekova L., Balázs E. 2001; Replacement of the coat protein gene of plum pox potyvirus with that of zucchini yellow mosaic potyvirus: characterization of the hybrid potyvirus. Virus Res 76:9–16 [CrossRef]
    [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. Tomlinson J. A., Ward C. M. 1978; The reactions of swede ( Brassica napus ) to infection by turnip mosaic virus. Ann Appl Biol 89:61–69 [CrossRef]
    [Google Scholar]
  56. Urcuqui-Inchima S., Haenni A.-L., Bernardi F. 2001; Potyvirus proteins: a wealth of functions. Virus Res 74:157–175 [CrossRef]
    [Google Scholar]
  57. Walsh J. A. 1989; Genetic control of immunity to turnip mosaic virus in winter oilseed rape ( Brassica napus ssp. oleifera ) and the effect of foreign isolates of the virus. Ann Appl Biol 115:89–99 [CrossRef]
    [Google Scholar]
  58. 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]
  59. Whitham S. A., Yamamoto M. L., Carrington J. C. 1999; Selectable viruses and altered susceptibility mutants in Arabidopsis thaliana . Proc Natl Acad Sci U S A 96:772–777 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.79825-0
Loading
/content/journal/jgv/10.1099/vir.0.79825-0
Loading

Data & Media loading...

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