Abstract
In tomato, infections by tomato mosaic virus are controlled by durable Tm-22 resistance. In order to gain insight into the processes underlying disease resistance and its durability, we cloned and analysed the Tm-22 resistance gene and the susceptible allele, tm-2. The Tm-22 gene was isolated by transposon tagging using a screen in which plants with a destroyed Tm-22 gene survive. The Tm-22 locus consists of a single gene that encodes an 861 amino acid polypeptide, which belongs to the CC-NBS-LRR class of resistance proteins. The putative tm-2 allele was cloned from susceptible tomato lines via PCR with primers based on the Tm-22 sequence. Interestingly, the tm-2 gene has an open reading frame that is comparable to the Tm-22 allele. Between the tm-2 and the Tm-22 polypeptide 38 amino acid differences are present of which 26 are located in the second half of the LRR-domain. Susceptible tomato plants, which were transformed with the Tm-22 gene, displayed resistance against ToMV infection. In addition, virus specificity, displayed by the Tm-22 resistance was conserved in these transgenic lines. To explain the durability of this resistance, it is proposed that the Tm-22-encoded resistance is aimed at the Achilles' heel of the virus.
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Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.
Bittner-Eddy, P.D., Crute, I.R., Holub, E.B. and Beynon, J.L. 2000. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 21: 177–188.
Brading, P.A., Hammond-Kosack, K.E., Parr, A. and Jones, J.D. 2000. Salicylic acid is not required for Cf-2-and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J. 23: 305–318.
Brommonschenkel, S.H., Frary, A., Frary, A. and Tanksley, S.D. 2000. The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol. Plant-Microbe Interact. 13: 1130–1138.
Bryan, G.T., Wu, K.S., Farrall, L., Jia, Y., Hershey, H.P., McAdams, S.A., Faulk, K.N., Donaldson, G.K., Tarchini, R. and Valent, B. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12: 2033–2046.
Calder, V.L. and Palukaitis, P. 1992. Nucleotide sequence analysis of the movement genes of resistance breaking strains of tomato mosaic virus. J. Gen. Virol. 73: 165–168.
Citovsky, V. and Zambryski, P. 2000. Systemic transport of RNA in plants. Trends Plant Sci. 5: 52–54.
Dinesh-Kumar, S.P., Whitham, S., Choi, D., Hehl, R., Corr, C. and Baker, B. 1995. Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proc. Natl. Acad. Sci. USA 92: 4175–4180.
Ellis, J., Dodds, P. and Pryor, T. 2000. The generation of plant disease resistance gene specificities. Trends Plant Sci. 5: 373–379.
Fraser, R.S.S., Gerwitz, A. and Betti, L. 1989. Deployment of resistance genes: implications from studies on resistance-breaking isolates of tobacco mosaic virus. In: Proceedings of the Fourth International Plant Virus Epidemiology Workshop (Montpellier), ISPP, pp. 154–155.
Gidoni, D., Fuss, E., Burbidge, A., Speckmann, G.J., James, S., Nijkamp, D., Mett, A., Feiler, J., Smoker, M., de Vroomen, M.J., Leader, D., Liharska, T., Groenendijk, J., Coppoolse, E., Smit, J.J.M., Levin, I., de Both, M., Schuch, W., Jones, J.D.G., Taylor, I.B., Theres, K. and van Haaren, M.J.J. 2003. Multi-functional TDNA/Ds tomato lines designed for gene cloning and molecular and physical dissection of the tomato genome. Plant Mol. Biol. 51: 83–98.
Glazebrook, J. 2001. Genes controlling expression of defense responses in Arabidopsis: 2001 status. Curr. Opin. Plant Biol. 4: 301–308.
Hall, T.J. 1980. Resistance at the Tm-2 locus in the tomato to tomato mosaic virus. Euphytica 29: 189–197.
Hammond-Kosack, K.E. and Jones, J.D.G. (1997) Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 575–607.
Horsch, R.B., Fry, J., Hoffman, N., Eichholtz, D., Rogers, D. and Fraley, R. 1985. A simple and general method for transferring genes into plants. Science 227: 1229–1231.
Jones, D.A. and Jones, J.D.G. 1997. The role of leucine-rich repeat proteins in plant defences. Adv. Bot. Res. Adv. Plant Pathol. 24: 89–167.
Khush, G.S., Rick, C.M. and Robinson, R.W. 1964. Genetic activity in a heterochromatic chromosome segment of the tomato. Science 145: 1432–1434.
Lartey, R.T., Voss, T.C. and Melcher, U. 1996. Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol. Biol. Evol. 13: 1327–1338.
Meshi, T., Motoyoshi, F., Adachi, A., Watanabe, Y., Takamatsu, N. and Okada, Y. 1988. Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J. 7: 1575–1581.
Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and 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. Plant Cell 10: 1307–1319.
Motoyoshi, F., Ohmori, T. and Murata, M. 1996. Molecular characterization of heterochromatic regions around the Tm-2 locus in chromosome 9 of tomato. Symp. Soc. Exp. Biol. 50: 65–70.
Ohmori, T., Murata, M. and Motoyoshi, F. 1995. Identification of RAPD markers linked to the Tm-2 locus in tomato. Theor. Appl. Genet. 90: 307–311.
Ohmori, T., Murata, M. and Motoyoshi, F. 1998. Characterization of disease resistance gene-like sequences in near-isogenic lines of tomato. Theor. Appl. Genet. 96: 331–338.
Ori, N., Eshed, Y., Paran, I., Presting, G., Aviv, D., Tanksley, S., Zamir, D. and Fluhr, R. 1997. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9: 521–532.
Pelham, J. 1966. Resistance in tomato to tobacco mosaic virus. Euphytica 15: 258–267.
Pillen, K., Ganal, M.W. and Tanksley, S.D. 1996. Construction of a high-resolution genetic map and YAC-contigs in the tomato Tm-2a region. Theor. Appl. Genet. 93: 228–233.
Pilowsky, M., Frankel, R. and Cohen, S. 1981. Studies of the variable reaction at high temperature of F1 hybrid tomato plants resistant to tobacco mosaic virus. Phytopathology 71: 319–323.
Rommens, C.M., Rudenko, G.N., Dijkwel, P.P., van Haaren, M.J., Ouwerkerk, P.B., Blok, K.M., Nijkamp, H.J. and Hille, J. 1992. Characterization of the Ac/Ds behaviour in transgenic tomato plants using plasmid rescue. Plant Mol. Biol. 20: 61–70.
Salmeron, J.M., Oldroyd, G.E., Rommens, C.M., Scofield, S.R., Kim, H.S., Lavelle, D.T., Dahlbeck, D. and Staskawicz, B.J. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86: 123–133.
Sambrook, L., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Schroeder, W.T., Provividenti, R. and Robinson, R.W. 1967.Incubation temperature and virus strains important in evaluating tomato genotypes for tobacco mosaic virus reactions. Tomato Genet. Co-Op. Rep. 17: 47–48.
Sobir, Ohmori, T., Murata, M. and Motoyoshi, F. 2000. Molecular characterization of the SCAR markers tightly linked to the Tm-2 locus of the genus Lycopersicon. Theor. Appl. Genet. 101: 64–69.
Spassova, M.I., Prins, T.W., Folkertsma, R.T., Klein-Lankhorst, R.M., Hille, J., Goldbach, R.W. and Prins, M. 2001. The tomato gene Sw5 is a member of the coiled coil, nucleotide binding, leucine-rich repeat class of plant resistance genes and confers resistance to TSWV in tobacco. Mol. Breed. 7: 151–161.
Takken, F.L., Schipper, D., Nijkamp, H.J. and Hille, J. 1998. Identification and Ds-tagged isolation of a new gene at the Cf-4 locus of tomato involved in disease resistance to Cladosporium fulvum race 5. Plant J. 14: 401–411.
Tanksley, S.D., Ganal, M.W., Prince, J.P., de Vicente, M.C., Bonierbale, M.W., Broun, P., Fulton, T.M., Giovannoni, J.J., Grandillo, S. and Martin, G.B. 1992. High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141–1160.
Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.
van der Beek, J.G., Verkerk, R., Zabel, P. and Lindhout, P. 1992. Mapping strategy for resistance genes in tomato based on RFLPs between cultivars: Cf9 (resistance to Cladosporium fulvum) on chromosome 1. Theor. Appl. Genet. 84: 106–112.
van der Biezen, E.A. and Jones, J.D. 1998. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals [letter]. Curr. Biol. 8: R226–R227.
van der Hoorn, R.A., deWit, P.J. and Joosten, M.H. 2002. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7: 67–71.
Weber, H. and Pfitzner, A.J. 1998. Tm-2(2) resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Mol. Plant-Microbe. Interact. 11: 498–503.
Weber, H., Schultze, S. and 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. J. Virol. 67: 6432–6438.
Zaitlin, M. and Palukaitis, P. 2000. Advances in understanding plant viruses and virus diseases. Annu. Rev. Phytopathol. 38: 117–143.
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Lanfermeijer, F.C., Dijkhuis, J., Sturre, M.J. et al. Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum . Plant Mol Biol 52, 1039–1051 (2003). https://doi.org/10.1023/A:1025434519282
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DOI: https://doi.org/10.1023/A:1025434519282