Complementary functions of two recessive R-genes determine resistance durability of tobacco 'Virgin A Mutant' (VAM) to Potato virus Y

Virology

Volumn 379, Issue 2, 2008, Pages 275-283

  Acosta Leal, Rodolfo ^a   Xiong, Zhongguo ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Cytoplasmic inheritance; eIF4E; Gene pyramiding; Genome linked protein; Pathogenesis; Pepper pvr2 gene; Picornavirus; Protoplast printing; Tolerance; VPg

Indexed keywords

ARTICLE; CELL MOTION; CONTROLLED STUDY; GENE FUNCTION; GENE LOCUS; GENETIC ANALYSIS; NONHUMAN; POTYVIRUS; PRIORITY JOURNAL; VIRUS RESISTANCE;

GENES, PLANT; GENES, RECESSIVE; GENOTYPE; HOST-PATHOGEN INTERACTIONS; MUTATION; PHENOTYPE; PLANT DISEASES; POTYVIRUS; TOBACCO; VARIATION (GENETICS); VIRULENCE;

NICOTIANA TABACUM; PICORNAVIRIDAE; POTATO VIRUS Y;

EID: 50349085805     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.06.026     Document Type: Article

References (58)

1. . A plant resistance mechanism that promotes the emergence of resistance breaking variants of potato Y potyvirus. Ph.D. Dissertation, Dept. Plant Pathology, University of Arizona, 248 p.
2. Acosta-Leal R., Fawley M.W., and Rush C.M. Changes in the intraisolate genetic structure of Beet necrotic yellow vein virus populations associated with plant resistance breakdown. Virology 376 (2008) 60-68
3. Acosta-Leal R., and Rush C.M. Mutations associated with resistance-breaking isolates of Beet necrotic yellow vein virus and their allelic discrimination using TaqMan technology. Phytopathology 97 (2007) 325-330
4. Andrade M., Sato M., and Uyeda I. Two resistance modes to Clover yellow vein virus in pea characterized by a green fluorescent protein-tagged virus. Phytopathology 97 (2007) 544-550
5. Athow K.L., Laviolette F.A., Wilcox J.R., and Abney T.S. Registration of 'TN 86' burley tobacco. Crop Sci. 27 (1987) 365-366
6. Berk K.N. Data analysis with Student SYSTAT Windows edition (1994), Course Technology, Inc., Cambridge, MA 495p
7. Burk L.G., Chaplin J.F., Gooding G.V., and Powell N.T. Quantity production of anther-derived haploids from a multiple disease resistant tobacco hybrid. I. Frequency of plants with resistance or susceptibility to tobacco mosaic virus (TMV), potato virus Y (PVY) and root knot (RK). Euphytica 28 (1979) 201-208
8. Candresse T., Le Gall O., Maisonneuve B., German-Retana S., and Redondo E. The use of green fluorescent protein-tagged recombinant viruses to test Lettuce mosaic virus resistance in lettuce. Phytopathology 92 (2002) 169-176
9. Carrington J.C., and Morris T.J. Complementary DNA cloning and analysis of carnation mottle virus RNA. Virology 139 (1984) 22-31
10. Chachulska A.M., Fakhfakh H., Robaglia C., Granier F., Zagorski W., and Vilaine F. Synthesis of full-length potyvirus cDNA copies suitable for the analysis of genome polymorphism. J. Virol. Methods 67 (1997) 189-197
11. Chaplin J.F., Burk L.G., Gooding G.V., and Powell N.T. Registration of NC 744 tobacco germplasm. Crop Sci. 20 (1980) 677
12. Crespi S., Accotto G.P., Caciagli P., and Gronenborg B. Use of digoxigenin-labelled probes for detection and host-range studies of tomato yellow leaf curl geminivirus. Res. Virol. 142 (1991) 283-288
13. Diaz-Pendon J.A., Truniger V., Nieto C., Garcia-Mas J., Bendahmane A., and Aranda M.A. Advances in understanding recessive resistance to plant viruses. Mol. Plant Pathol. 5 (2004) 223-233
14. Dunoyer P., Thomas C., Harrison S., Revers F., and Maule A. A cysteine-rich plant protein potentiates potyvirus movement through an interaction with the virus genome-linked protein VPg. J. Virol. 78 (2004) 2301-2309
15. Galbraith D. Isolation and flow cytometric characterization of plant protoplasts. In: Darzynkiewicz Z., and Crissman H.A. (Eds). Methods in Cell Biology 33 (1990), Academic Press, New York 527-547
16. Gamborg O.L., Miller R.A., and Ojima K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50 (1968) 151-158
17. Gao Z.H., Johansen E., Eyers S., Thomas C.L., Noel Ellis T.H., and Maule A.J. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J. 40 (2004) 376-385
18. Gibb K.S., Hellmann G.M., and Pirone T.P. Nature of resistance of a tobacco cultivar to tobacco vein mottling virus. Mol. Plant-Microbe Interact. 2 (1989) 332-339
19. Gooding Jr. G.V. Relationship between strains of potato virus Y and breeding for resistance, cross protection, and interference. Tob. Sci. 29 (1985) 99-104
20. Gooding Jr. G.V., and Tolin S.A. Strain of potato virus Y affecting flue-cured tobacco in the southeastern United States. Plant Dis. Rep. 57 (1973) 200-203
21. Gupton C.L. Registration of Greeneville 107 burley tobacco germplasm. Crop Sci. 20 (1980) 116
22. Gupton C.L., and Burk L.G. Location of the factor for resistance to potato virus Y in tobacco. J. Heredity 64 (1973) 289-290
23. Hebrard E., Pinel-Galzi A., Bersoult A., Sire C., and Fargette D. Emergence of a resistance-breaking isolate of Rice yellow mottle virus during serial inoculations is due to a single substitution in the genome-linked viral protein VPg. J. Gen. Virol. 87 (2006) 1369-1373
24. ICTVdB- The Universal Virus Database, version 4, 2006. http://www.ncbi.nlm.nih.gov/ICTVdb/ICTVdB/.
25. Jung J.L., Bouzoubaa S., Gilmer D., and Habne G. Visualization of transgene expression at the single protoplast level. Plant Cell Rep. 11 (1992) 346-350
26. Kang B.C., Yeam I., and Jahn M.M. Genetic of plant virus resistance. Annu. Rev. Phytopathol. 43 (2005) 581-621
27. Keller K.E., Johansen E., Martin R.R., and Hampton R.O. Potyvirus genome-linked protein (VPg) determines Pea seed-borne mosaic virus pathotype-specific virulence in Pisum sativum. Mol. Plant-Microbe Interact. 11 (1998) 124-130
28. Koelle G. Genetische analyse einer Y-virus (Rippenbraune) resistenten mutante der tabaksorte Virgin A. Zuchter 31 (1961) 71-72
29. Kuhn C.W., Wyatt S.D., and Brantley B.B. Genetic control of symptoms, movement, and virus accumulation in cowpea plants infected with cowpea chlorotic mottle virus. Phytopathology 71 (1981) 1310-1315
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
31. Lommel S.A., McCain A.H., and Morris T.J. Evaluation of indirect enzyme-linked immunosorbent assay for the detection of plant viruses. Phytopathology 72 (1982) 1018-1022
32. Masuta C., Nishimura M., Morishita H., and Hataya T. A single amino acid change in the viral genome-associated protein of potato virus Y correlates with resistance breaking in "Virgin A Mutant" tobacco. Phytopathology 89 (1999) 118-123
33. Murphy J.F., Blauth J.R., Livingstone K.D., Lackney V.K., and Jahn M.K. 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 (1998) 943-951
34. Negrutiu I., Shillito R., Potrykus I., Biasini G., and Sala F. Hybrid genes in the analysis of transformation conditions I. Setting up a simple method for direct gene transfer in plant protoplasts. Pl. Mol. Biol. 8 (1987) 363-373
35. Nicaise V., Gallois J.L., Chafiai F., Allen L.M., Schurdi-Levraud V., Browning K.S., Candresse T., Caranta C., Le Gall O., and German-Retana S. Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsis thaliana. FEBS Letters 581 (2007) 1041-1046
36. Nicaise V., German-Retana S., Sanjuan R., Dubrana M.P., Mazier M., Maisonneuve B., Candresse T., Caranta C., and LeGall O. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol. 132 (2003) 1272-1282
37. Nicolai M., Duprat A., Sormani R., Rodriguez C., Roncato M.A., Rolland N., and Robaglia C. Higher plant chloroplasts import the mRNA coding for the eukaryotic translation initiation factor 4E. FEBS Letters 581 (2007) 3921-3926
38. Nicolas O., Dunnington S.W., Gotow L.F., Pirone T.P., and Hellmann G.M. Variations in the VPg protein allow a potyvirus to overcome va gene resistance in tobacco. Virology 237 (1997) 452-459
39. Nieto C., Morales M., Orjeda G., Clepet C., Monfort A., Sturbois B., Puigdomenech P., Pitrat M., Caboche M., Dogimont C., Garcia-Mas J., Aranda M.A., and Bendahmane A. An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J. 48 (2006) 452-462
40. Revers F., Le Gall O., Candresse T., and Maule A.J. New advances in understanding the molecular biology of plant/potyvirus interactions. Mol. Plant-Microbe Interact. 12 (1999) 367-376
41. Robaglia C., and Caranta C. Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 11 (2006) 40-45
42. Robaglia C., Duran-Tardif M., Tronchet M., Boudazin G., Astier-Manifacier S., and Casse-Delbart F. Nucleotide sequence of potato virus Y (N strain) genomic RNA. J. Gen. Virol. 70 (1989) 935-947
43. Ruffel S., Dussault M.H., Palloix A., Moury B., Bendahmane A., Robaglia C., and Caranta C. A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J. 32 (2002) 1067-1075
44. Ruffel S., Gallois J.L., Moury B., Robaglia C., Palloix A., and Caranta C. Simultaneous mutations in translation initiation factors elF4E and elF(iso)4E are required to prevent Pepper veinal mottle virus infection of pepper. J. Gen. Virol. 87 (2006) 2089-2098
45. Salinovich O., and Montelaro R. Reversible staining and peptide mapping of proteins transferred to nitrocellulose after separation by SDS-PAGE. Anal. Biochem. 156 (1986) 341-347
46. Sato M., Nakahara K., Yoshii M., Ishikawa M., and Uyeda I. Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Letters 579 (2005) 1167-1171
47. Schaad M.C., Lellis A.D., and Carrington J.C. VPg of Tobacco etch potyvirus is a host genotype-specific determinant for long-distance movement. J. Virol. 71 (1997) 8624-8631
48. Shillito R.D., and Saul M.W. Protoplast isolation and transformation. In: Shaw C.H. (Ed). Plant Molecular Biology: A Practical Approach (1988), IRL Press, Washington, DC 161-186
49. Shukla D.D., Ward C.W., and Brunt A.A. The Potyviridae (1994), CAB International 516p
50. Sudarsono S.L., Woloshuk S.L., Xiong Z., Hellmann G.M., Wernsman E.A., Weissenger A.K., and Lommel S.A. Nucleotide sequence of the capsid protein cistrons from six potato virus Y (PVY) isolates infecting tobacco. Arch. Virol. 132 (1993) 161-170
51. Stavely J.R. Disease Resistance. Nicotiana: Procedures for Experimental Use (1979), US Dep. Agric. Tech. Bull No 1586
52. Thole V., Dalmay T., Burgyan J., and Balazs E. Cloning and sequencing of potato virus Y (Hungarian isolate) genomic RNA. Gene 123 (1993) 149-156
53. Tordo V.M.J., Chachulska A.M., Kakhfakh H., Le Romancer M., Robaglia C., and Astier-Manifacier S. Sequence polymorphism in the 5' NTR and in the P1 coding region of potato virus Y genomic RNA. J. Gen. Virol. 76 (1995) 939-949
54. Wittmann S., Chatel H., Fortin M.G., and Laliberte J.F. Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234 (1997) 84-92
55. Wyatt S.D., and Wilkinson T.C. Increase and spread of cowpea chlorotic mottle virus in resistant and fully susceptible cowpeas. Physiol. Plant Pathol. 24 (1984) 339-345
56. Xiong Z., and Lommel S.A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro from full-length cDNA clones. Virology 182 (1991) 388-392
57. Yeam I., Cavatorta J.R., Ripoll D.R., Kang B.C., and Jahn M.M. Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19 (2007) 2913-2928
58. Yoshii M., Nishikiori M., Tomita K., Yoshioka N., Kozuka R., Naito S., and Ishikawa M. The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J. Virol. 78 (2004) 6102-6111