Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV-infected tobacco

Plant Journal

Volumn 12, Issue 5, 1997, Pages 1113-1126

  Mur, Luis A J ^a   Bi, Yong Mei ^a   Darby, Robert M ^a   Firek, Simon ^a   Draper, John ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTIANA TABACUM; TOBACCO MOSAIC VIRUS;

EID: 0031280182     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1997.12051113.x     Document Type: Article

References (54)

1. Apostol, I., Heinstein, P.F. and Low, P.S. (1989) Rapid stimulation of an oxidative burst during elrcitation of cultured plant cells. Plant Physiol. 90, 109-116.
2. 2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241-1247.
3. Assinder, S.J. and Williams, P.A. (1988) Comparison of the meta pathway operons on NAH plasmid pWW60-22 and TOL plasmid pWW53-4 and its evolutionary significance. J. Gen. Microbiol. 134, 2769-2778.
4. Bi, Y.-M., Kenton, P., Mur, L., Darby, R. and Draper, J. (1995) Hydrogen peroxide functions upstream of salicylic acid in the induction of PR protein expression. Plant J. 8, 252-245.
5. Bowles, D. (1990) Defense-related proteins in higher plants. Annu. Rev. Biochem. 59, 873-907.
6. Bowling, S.A., Guo, A., Cao, H., Gordon, S., Klessig, D.F. and Dong, X. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845-1857.
7. Bradley, D.J., Kjellbm, P. and Lamb, C.J. (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell, 70, 21-30.
8. Chester, K.S. (1933) The problem of acquired physiological immunity in plants. Q. Rev. Biol. 8, 275-324.
9. Chivasa, S., Murphy, A.M., Naylor, M. and Carr J.P. (1997) Salicylic acid interferes with Tobacco Mosaic Virus replication via a novel, salicylhydroxamic acid-sensitive mechanism. Plant Cell, 9, 547-557.
10. Dawson, W.O. and Lehto, K. M. (1990) Regulation of tobamovirus gene expression. Adv. Virus Res. 38, 307-341.
11. Dangl, J.L. (1995) Piece de resistance: Novel classes of plant disease resistance genes. Cell, 80, 363-366.
12. Dangl, J.L., Dietrich, R.A. and Richberg, M.H. (1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell, 8, 1793-1807.
13. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
14. Deom, C.M., Wolf, S., Holt, C.A., Lucas, W.J. and Beachy, R.N. (1991) Altered function of the tobacco mosiac virus movement protein in a hypersentive host. Virology, 180, 251-256.
15. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A. and Dangl, J.L. (1994) Arabidopsis mutants simulating disease resistance response. Cell, 77, 565-577.
16. Enyedi, A.J., Yalpani, N., Silverman, P. and Raskin, I. (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl Acad. Sci. USA, 89, 2480-2484.
17. 2 in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol. 110, 347-354.
18. Firek, S., Ozcan, S., Warner, S.A. and Draper, J. (1993) A wound induced promoter driving npt-II expression limited to dedifferentiated cells at wound sites is sufficient to allow selection of transgenic shoots. Plant Mol. Biol. 22, 129-142.
19. Friedrich, L., Vernooij, B., Gaffney, T., Morse, A. and Ryals, J. (1995) Characterisation of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol. Biol. 29, 959-968.
20. Gaffney, T., Friedrich, L., Vernooji, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylic acid for the induction of systemic aquired resistance. Science, 261, 754-756.
21. Goodrick, B.J., Kuhn, C.W. and Hussey, R.S. (1991) Restricted systemic movement of cowpea chorotic mottle virus in soybean with non necrotic resistance. Phytopathology, 81, 1426-1431.
22. Greenberg, J.T., Guo, A., Klessig, D.F. and Ausubel, F.M. (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defence functions. Cell, 77, 551-563.
23. Guerineau, F., Brooks, L. and Mullineaux, P. (1991) Effects of deletions in the cauliflower mosaic virus polyadenylation sites in tobacco protoplasts. Mol. Gen. Genetics, 226, 141-144.
24. Hammond-Kosack, K. and Jones, J.D.G. (1996) Resistance gene-dependent plant defence responses. Plant Cell, 8, 1773-1791.
25. 2. Plant Physiol. 108, 1171-1178.
26. Keen, N.T. (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24, 447-463.
27. Klement, Z., Farkas, G.L. and Lovrekovich, L. (1964) Hypersensitive reaction induced by phytopathogenic bacteria in the tobacco leaf. Phytopathology, 54, 474-477.
28. Lamb, C. (1994) Plant disease resistance genes in signal perception and transduction. Cell, 76, 419-422.
29. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 1-20.
30. 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, 1001-1004.
31. Malamy, J., Hennig, J. and Klessig, D.F. (1992) Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell, 4, 359-366.
32. Massala, R., Legrand, M. and Fritig, B. (1987) Comparative effects of two competitive inhibitors of phenylalanine ammonia-lyase on the hypersensitive resistance of tobacco to tobacco mosiac virus. Plant Physiol. Biochem. 25, 217-225.
33. Mehdy, M. (1994) Active oxygen species in plant defence against pathogens. Plant Physiol. 105, 467-472.
34. Metraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdoorf, K., Schmid, E., Blum, W. and Inverardi, B. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250, 1004-1006.
35. 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 leaf tissue exhibiting acquired resistance to pathogen attack. Plant J. 9, 559-571.
36. Padgett, H.S. and Beachy, R.N. (1993) Analysis of a tobacco mosaic-virus strain capable of overcoming N gene-mediated resistance. Plant Cell, 5, 577-586.
37. Peng, M. and Kuc, J. (1992) Peroxidase-generated hydrogen peroxide as a source of anti-fungal activity in vitro and on tobacco leaf discs. Phytopathology, 82, 696-699.
38. Rasmussen, J.B., Hammerschmidt, R. and Zook, M.N. (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342-1347.
39. Ross, A.F. (1961) Systemic acquired resistance induced by localized virus infections in plants. Virology, 14, 340-358.
40. Ryals, J., Uknes, S. and Ward, E. (1996) Systemic acquired resistance. Plant Cell, 8, 1809-1819.
41. Sanger, M., Passmore, B., Falk, C.J., Bruening, G., Ding, B. and Lucas, W.J. (1994) Severity of beet western yellow virus strain ST9 is conferred by the ST9-associated RNA and is not associated with the release of the infection from the phloem. Virology, 200, 48-55.
42. Shirasu, K., Nakajima, H., Krishnamachari, R., 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, 261-270.
43. Shulaev, V., Leon, J. and Raskin, I. (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell, 7, 1691-1701.
44. Uknes, S., Dincher, S., Friedrich, L., Negrotto, D., Williams, S., Thompson-Taylor, H., Potter, S., Ward, E. and Ryals, J. (1993a) Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell, 5, 159-169.
45. Uknes, S., Winter, A.M., Delaney, T., Vernooij, B., Morse, A., Friedrich, L., Nye, G., Potter, S., Ward, E. and Ryals, J. (1993b) Biological induction of systemic acquired resistance in Arabidopsis. Mol. Plant-Microbe Interact. 6, 692-698.
46. Van Loon, L.C. and Van Kammen, A. (1970) Polyacrylamide disc electrophoresis of the soluble proteins from Nicotiana tabacum var. 'Samsun' and 'Samsun NN'. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 199-211.
47. Ward, E.R., Uknes, S.J., Williams, S.C., Dincher, S.S., Wiederhold, D.L., Alexander, D.C., Ahl-Goy, P., Métraux, J.-P. and Ryals, J.A. (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell, 3, 1085-1094.
48. Warner, S.A.J., Scott, R. and Draper, J. (1993) Isolation of an asparagus intracellular PR gene (AoPR1) wound-responsive promoter by the inverse polymerase chain reaction and its characterisation in transgenic tobacco. Plant J 3, 191-201.
49. Warner, S.A.J., Gill, A. and Draper, J. (1994) Developmental expression of the asparagus intracellular PR protein (AoPR1) gene correlates with sites of phenylpropanoid biosynthesis. Plant J. 6, 31-43.
50. Weymann, K., Hunt, M., Uknes, S. Neuenschwander, U., Lawton, K. Steiner, H.-Y. and Ryals, J. (1995) Suppression and restoration of lesion formation in arabidopsis Isd mutants. Plant Cell, 7, 2013-2022.
51. Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C. and Baker, B. (1994) The product of the tobacco mosaic virus resistance gene N: Similarity to Toll and the interleukin-1 receptor. Cell, 78, 1101-1115.
52. Yalpani, N., Shulaev, V. and Raskin, I. (1993) Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco. Phytopathology, 83, 702-708.
53. Yamamoto, S., Katagiri, M., Maeno, H. and Hayaishi, O. (1965) Salicylate hydroxylase, a monooxygenase requiring flavin adenine dinucleotide. I. Purification and general properties. J. Biol. Chem. 240, 3408-3413.
54. You, I.-S., Murray, R.I., Jollic, D. and Gunsalus I.C. (1990) Purification and characterization of salicylate hydroxylase from Pseudomonas putida PpG7. Biochem. Biophys. Res. Commun. 169, 1049-1054.