The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in brassicas

Molecular Plant-Microbe Interactions

Volumn 16, Issue 9, 2003, Pages 777-784

  Jenner, Carol E ^a   Wang, Xiaowu ^b,d   Tomimura, Kenta ^c   Ohshima, Kazusato ^c   Ponz, Fernando ^b   Walsh, John A ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b INIA   (Spain)

^c SAGA UNIVERSITY   (Japan)

^d INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRASSICA; BRASSICA JUNCEA; BRASSICA NAPUS; BRASSICA RAPA SUBSP. RAPA; POTYVIRUS; TURNIP MOSAIC VIRUS;

EID: 0041692684     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2003.16.9.777     Document Type: Article

References (50)

1. Bateson, M. F., Henderson, J., Chaleeprom, W., Gibbs, A. J., and Dale, J. L. 1994. Papaya ringspot potyvirus: Isolate variability and the origin of PRSV type P (Australia). J. Gen. Virol. 75:3547-3553.
2. Chu, M., Lopez-Moya, J. J., Llave-Correas, C., and 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.
3. Dallot, S., Quiot-Douine, L.. Sáenz, P., Cervera, M. T., García, J. A., and Quiot, J.-B. 2001. Identification of Plum pox virus determinants implicated in specific interactions with different Prunus spp. Phytopathology 91:159-164.
4. Fellers, J. P., Tremblay, D., Handest, M. F., and Lommel, S. A. 2002. The Potato virus Y MSNR NIb-replicase is the elicitor of a veinal necrosis-hypersensitive response in root knot nematode resistant tobacco. Mol. Plant Pathol. 3:145-152.
5. Gabriel, D. W. 1999. Why do pathogens carry avirulence genes? Physiol. Mol. Plant Pathol. 55:205-214.
6. Glasa, M., Marie-Jeanne, V., Moury, B., Kúdela, O., and Quiot, J.-B. 2002. Molecular variability of the P3-6K1 genomic region among geographically and biologically distinct isolates of Plum pox virus. Arch. Virol. 147:563-575.
7. Guo, D., Rajamäki, M.-L., Saarma, M., and 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.
8. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K., and Pease. L. R. 1989. Engineering hybrid genes without the use of restriction enzymes: Gene splicing by overlap extension. Gene 77:61-68.
9. Hughes, S. L., Green, S. K., Lydiate, D. J., and 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.
10. Hughes, S. L., Hunter, P. J., Sharpe, A. G., Kearsey, M. J., Lydiate, D. J., and Walsh, J. A. Genetic mapping of the novel Turnip mosaic virus resistance gene TuRB03 in Brassica napus. Theor. Appl. Genet. In press.
11. Jenner, C. E., Keane, G. J., Jones, J. E., and Walsh, J. A. 1999. Serotypic variation in turnip mosaic virus. Plant Pathol. 48:101-108.
12. Jenner, C. E., Sánchez, F., Nettleship, S. B., Foster, G. D., Ponz, F., and 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.
13. Jenner, C. E., Tomimura, K., Ohshima, K., Hughes, S. L., and Walsh, J. A. 2002a. Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300:50-59.
14. Jenner, C. E., and Walsh, J. A. 1996. Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathol. 45:848-856.
15. Jenner, C. E., Wang, X., Ponz, F., and Walsh, J. A. 2002b. A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res. 86:1-6.
16. Johansen, I. E., Lund, O. S., Hjulsager, C. K., and 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.
17. Keller, K. E., Johansen, I. E., Martin, R. R., and 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.
18. Klein, P. G., Klein, R. R., Rodríguez-Cerezo, E., Hunt, A. G., and Shaw, J. G. 1994. Mutational analysis of the tobacco vein mottling virus genome. Virology 204:759-769.
19. Krause-Sakate, R., Le Gall, O., Fakhfakh, H., Peypelut, M., Marrakchi, M., Varveri, C., Pavan, M. A., Souche, S., Lot, H., Zerbini, M., and Candresse, T. 2002. Molecular and biological characterization of Lettuce mosaic virus (LMV) isolates reveals a distinct and widespread type of resistance-breaking isolate: LMV-Most. Phytopathology 92:563-572.
20. Laín, S., Riechmann, J. L., and García, J. A. 1990. RNA helicase - a novel activity associated with a protein encoded by a positive strand RNA virus. Nucleic Acids Res. 18:7003-7006.
21. Langenberg, W. G., and Zhang, L. 1997. Immunocytology shows the presence of tobacco etch virus P3 protein in nuclear inclusions. J. Struct. Biol. 118:243-247.
22. Lehmann, P., Petrzik, K., Jenner, C., Greenland, A., Špak, J., Kozubek, E., and 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.
23. Masuta, C., Nishimura, M., Morishita, H., and Hataya, T. 1999. A single amino acid change in viral genome-associated protein of potato virus Y correlates with resistance breaking in 'Virgin A mutant' tobacco. Phytopathology 89:118-123.
24. Merits, A., Guo, D., Järvekülg, L., and 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.
25. Merits, A., Rajamäki, M.-L., Lindholm, P., Runeberg-Roos, P., Kekarainen, T., Puustinen, P., Mäkeläinen, K., Valkonen, J. P. T., and Saarma, M. 2002. Proteolytic processing of potyviral proteins and polyprotein processing intermediates in insect and plant cells. J. Gen. Virol. 83:1211-1221.
26. Mestre, P., Brigneti, G., and Baulcombe, D. C. 2000. An Ry-mediated resistance response in potato requires the intact active site of the NIa proteinase from potato virus Y. Plant J. 23:653-661.
27. Nicolas, O., Dunnington, S. W., Gotow, L. F., Pirone, T. P., and Hellmann, G. M. 1997. Variations in the VPg protein allow a poty virus to overcome va gene resistance in tobacco. Virology 237:452-459.
28. Ohshima, K., Yamaguchi, Y., Hirota, R., Hamamoto, T., Tomimura, K., Tan, Z., Sano, T., Azuhata, F., Walsh, J. A., Fletcher, J., Chen, J., Gera, A., and Gibbs, A. 2002. Molecular evolution of Turnip mosaic virus: Evidence of host adaptation, genetic recombination and geographical spread. J. Gen. Virol. 83:1511-1521.
29. 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.
30. Revers, F., Le Gall, O., Candresse, T., and Maule, A. J. 1999. New advances in understanding the molecular biology of plant/potyvirus interactions. Mol. Plant-Microbe Interact. 12:367-376.
31. Riechmann, J. L., Cervera, M. T., and García, J. A. 1995. Processing of the plum pox virus polyprotein at the P3-6K1 junction is not required for virus viability. J. Gen. Virol. 76:951-956.
32. Robbins, M. A., Witsenboer, H., Michelmore, R. W., Laliberté, J.-F., and Fortin, M. G. 1994. Genetic mapping of turnip mosaic virus resistance in Lactuca sativa. Theor. Appl. Genet. 89:583-589.
33. Rodríguez-Cerezo, E., Aramar, E. D., Pirone, T. P., and Shaw, I. G. 1993. Association of the nonstructural P3 viral protein with cylindrical inclusions in potyvirus-infected cells. J. Gen. Virol. 74:1945-1949.
34. Rodríguez-Cerezo, E., and Shaw, J. G. 1991. Two newly detected non-structural viral proteins in potyvirus-infected cells. Virology 185:572-579.
35. Romero, A., Blanco-Urgoiti, B., and Ponz, F. 1997. Amplification and cloning of a long RNA virus genome using immunocapture-long-RT-PCR. J. Virol. Methods 66:159-163.
36. Sáenz, P., Cervera, M. T., Dallot, S., Quiot, L., Quiot, J.-B., Riechmann, J. L., and 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.
37. Sánchez, F., Martinez-Herrera, D., Aguilar, I., and Ponz, F. 1998. Infectivity of turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. Virus Res. 55:207-219.
38. Sharpe, A. G., Parkin, I. A. P., Keith, D. J., and Lydiate, D. J. 1995. Frequent non-reciprocal translocations in the amphidiploid genome of oil-seed rape (Brassica napus). Genome 38:1112-1121.
39. Shattuck, V. I. 1992. The biology, epidemiology, and control of turnip mosaic virus. Plant Breed. Rev. 14:199-238.
40. Shukla, D. D., Frenkel, M. J., and Ward, C. W. 1991. Structure and function of the potyvirus genome with special reference to the coat protein coding region. Can. J. Plant Pathol. 13:178-191.
41. Shukla, D. D., Ward, C. W., and Brunt, A. A. 1994. The Potyviridae. CAB International, Wallingford, U.K.
42. Tomimura, K., Gibbs, A. J., Jenner, C. E., Walsh, J. A., and Ohshima, K. 2003. The phylogeny of Turnip mosaic virus; comparisons of thirty-eight genomic sequences reveal a Eurasian origin and a recent 'emergence' in east Asia. Mol. Ecol. 12:2099-2112.
43. Tomlinson, J. A. 1987. Epidemiology and control of virus diseases of vegetables. Ann. Appl. Biol. 110:661-681.
44. Ullah, Z., and Grumet, R. 2002. Localization of Zucchini yellow mosaic virus to the veinal regions and role of viral coat protein in veinal chlorosis conditioned by the zym potyvirus resistance locus in cucumber. Physiol. Mol. Plant Pathol. 60:79-89.
45. Urcuqui-Inchima, S., Haenni, A.-L., and Bernardi, F. 2001. Potyvirus proteins: A wealth of functions. Virus Res. 74:157-175.
46. van't Slot, K. A. E., and Knogge, W. 2002. A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Crit. Rev. Plant Sci. 21:229-271.
47. 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.
48. Walsh, J. A., and Jenner, C. E. 2002. Turnip mosaic virus and the quest for durable resistance. Mol. Plant Pathol. 3:289-300.
49. Walsh, J. A., Rusholme, R. L., Hughes, S. L., Jenner, C. E., Bambridge, J. M., Lydiate, D. J., and Green, S. K. 2002. Different classes of resistance to turnip mosaic virus in Brassica rapa. Eur. J. Plant Pathol. 108:15-20.
50. Walsh, J. A., Sharpe, A. G., Jenner, C. E., and Lydiate, D. J. 1999. Characterization of resistance to turnip mosaic virus in oilseed rape (Brassica napus) and genetic mapping of TuRB01. Theor. Appl. Genet. 99:1149-1154.