Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum

Plant Journal

Volumn 23, Issue 3, 2000, Pages 305-318

  Brading, Penny A ^a,c   Hammond Kosack, Kim E ^a,d   Parr, Adrian ^b   Jones, Jonathan D G ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c JOHN INNES CENTRE   (United Kingdom)

^d Cereal Technology Group   (United Kingdom)

Author keywords

Catechol; Cladosporium fulvum; Disease resistance; Salicylate hydroxylase (nahG); Salicylic acid

Indexed keywords

BACTERIAL GENE; CATECHOL; CELL DEATH; CHLOROSIS; CLADOSPORIUM FULVUM; COTYLEDON; DISEASE RESISTANCE; GENETIC SUSCEPTIBILITY; NECROSIS; PEPTIDE ELICITOR; RESISTANCE GENE; SALICYLATE 1 MONOOXYGENASE; SALICYLIC ACID; TOBACCO; TOMATO; WILD RELATIVE;

CATECHOLS; CLADOSPORIUM; GENES, BACTERIAL; LYCOPERSICON ESCULENTUM; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACID;

EID: 0033862495     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2000.00778.x     Document Type: Article

References (48)

1. Ashfield, T.A., Hammond-Kosack, K.E., Harrison, K. and Jones, J.D.G. (1994) Cf gene-dependent induction of a β-1,3-glucanase promoter in tomato plants infected with Cladosporium fulvum. Mol. Plant-Microbe Interact. 7, 645-657.
2. Bent, A.F., Innes, R.W., Ecker, J.R. and Staskawicz, B.J. (1992) Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol. Plant-Microbe Interact. 5, 372-378.
3. Bi, Y.-M., Kenton, P., Mur, L., Darby, R. and Draper, J. (1995) Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 8, 235-245.
4. Brading, P.A. (1997) Functional analysis of Cf gene-dependent defence responses in tomato. PhD Dissertation. Norwich: University of East Anglia.
5. De Wit, P.J.G.M. (1977) A light and scanning-electron microscopic study of infection of tomato plants by virulent and avirulent races of Cladosporium fulvum. Neth. J. Plant Pathol. 83, 109-122.
6. De Wit, P.J.G.M. (1992) Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu. Rev. Phytopathol. 30, 391-418.
7. De Wit, P.J.G.M. and Spikman, G. (1982) Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiol. Plant Pathol. 21, 1-11.
8. Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
9. Dixon, M.S., Jones, D.A., Keddie, J.S., Thomas, C.M., Harrison, K. and Jones, J.D.G. (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell, 84, 451-459.
10. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabelling DNA restriction enclonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
11. Feys, B.J.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
12. Fillatti, J.J., Kiser, J., Rose, R. and Comai, L. (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bio/Technology, 5, 726-730.
13. Flor, H.H. (1971) Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275-296.
14. Gaffney, T., Friedrich, L., Vernooij, B., Negroto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261, 754-756.
15. Glazebrook, J., Rogers, E.E. and Ausubel, F.M. (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics, 143, 973-1382.
16. Hall, T.J. (1980) Resistance at the Tm-2 locus in the tomato to tomato mosaic virus. Euphytica, 29, 189-197.
17. Hammond-Kosack, K.E. and Jones, J.D.G. (1994) Incomplete dominance of tomato Cf genes for resistance to Cladosporium fulvum. Mol. Plant-Microbe Interact. 7, 58-70.
18. Hammond-Kosack, K.E. and Jones, J.D.G. (1997) Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 575-607.
19. Hammond-Kosack, K.E., Silverman, P., Raskin, I. and Jones, J.D.G. (1996) Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance genes. Plant Physiol. 110, 1381-1394.
20. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J. and Schilperoort, R.A. (1983) A binary plant vector strategy based on separation of virand T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature, 303, 179-180.
21. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl Acad. Sci. USA, 94, 4800-4805.
22. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
23. Jones, D.A., Thomas, C.M., Hammond-Kosack, K.E., Balint-Kurti, P.J. and Jones, J.D.G. (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266, 789-793.
24. Jones, J.D.G., Shlumukov, L., Carland, F., English, J., Scofield, S., Bishop, G. and Harrison, K. (1992) Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgen. Res. 1, 285-297.
25. Joosten, M.H.A.J., Hendrickx, L.J.M. and De Wit, P.J.G.M. (1990) Carbohydrate composition of apoplastic fluids isolated from tomato leaves inoculated with virulent or avirulent races of Cladosporium fulvum (syn. Fulvia fulva). Neth. J. Plant. Pathol. 96, 103-112.
26. 2. Plant Physiol. 108, 1171-1178.
27. Keogh, R.C., Deverall, B.J. and McLeod, S. (1980) Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans. Br. Mycol. Soc. 74, 329-333.
28. Kooman-Gersmann, M., Honée, G., Bonnema, G. and De Wit, P.J.G.M. (1996) A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell, 8, 929-938.
29. Lamb, C.J. and Dixon, R.A. (1997) The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
30. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
31. Logemann, J., Schell, J. and Willmitzer, L. (1987) Improved method for the isolation of RNA from plant-tissues. Anal. Biochem. 163, 16-20.
32. McDonnell, R.E., Clark, R.D., Smith, W.A. and Hinchee, M.A. (1987) A simplified method for the detection of neomycin phosphotransferase II activity in transformed plant tissues. Plant Mol. Biol. Rep. 5, 380-386.
33. Malamy, J., Carr, J.P., Klessig, D.F. and Raskin, I. (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002-1004.
34. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
35. May, M.J., Hammond-Kosack, K., E. and Jones, J.D.G. (1996) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110, 1367-1379.
36. Mur, L.A.J., Naylor, G., Warner, S.A.J., Sugars, J.M., White, R.F. and Draper, J. (1996) Salicylic acid potentiates defence gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J. 9, 559-571.
37. Mur, L.A.J., Bi, M.-Y., Darby, R.M., Firek, S. and Draper, J. (1997) Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV-infected tobacco. Plant J. 12, 1113-1126.
38. Nishiguchi, M. and Motoyoshi, F. (1987) Resistance mechanisms of tobacco mosaic virus strains in tomato and tobacco. In Plant Resistance to Viruses (Evered, D. and Harnett, S., eds). Chichester: Wiley, pp. 38-46.
39. Oldroyd, G.E. and Staskawicz, B.J. (1998) Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA, 95, 10300-10305.
40. Penninckx, I.A.M.A., Eggermont, K., Terras, F.R.G., Thomma, B.P.H.J., De Samblanx, G.W., Buchala, A., Métraux, J.-P., Manners, J.M. and Broekaert, W.F. (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 8, 2309-2323.
41. Piedras, P., Hammond-Kosack, K.E., Harrison, K. and Jones, J.D.G. (1998) Rapid, Cf-9-and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Mol. Plant-Microbe Interact. 11, 1155-1166.
42. Pugin, A., Frachisse, J.M., Tavernier, E., Bligny, R., Gout, E., Douce, R. and Guern, J. (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell, 9, 2077-2091.
43. Raskin, I., Turner, I.M. and Melander, W.R. (1989) Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. Proc. Natl Acad. Sci. USA, 86, 2214-2218.
44. Reymond, P. and Farmer, E.E. (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant. Biol. 1, 404-411.
45. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. (1999) Rapid Avr9-and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell, 11, 273-287.
46. Ryals, J.L., Neuenschwander, U.H., Willits, M.C., Molina, A., Steiner, H.-Y. and Hunt, M.D. (1996) Systemic acquired resistance. Plant Cell, 8, 1809-1819.
47. von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U. and Willmitzer, L. (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 9, 3033-3044.
48. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A. and Lamb, C. (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell, 9, 1-10.