Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus

Plant Journal

Volumn 10, Issue 2, 1996, Pages 281-293

  Pallas, Jacqueline A ^a,b   Paiva, Nancy L ^a   Lamb, Chris ^b   Dixon, Richard A ^a  

^a PLANT BIOLOGY DIVISION   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; PHASEOLUS (ANGIOSPERM); TABACUM; TOBACCO MOSAIC VIRUS;

EID: 0030512252     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1996.10020281.x     Document Type: Review

References (39)

1. Bate, N.J., Orr, J., Ni, W., Meromi, A., Nadler-Hassar, T., Doerner, P.W., Dixon, R.A., Lamb, C.J. and Elkind, Y. (1994) Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc. Natl Acad. Sci. USA, 91, 7608-7612.
2. Bell, A.A. (1981) Biochemical mechanisms of disease resistance. Ann. Rev. Plant Physiol. 32, 21-81.
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. Bowling, S.A., Guo, A., Cao, H., Gordon, A.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.
5. Brederode, F.T., Linthorst, H.J.M. and Bol, J.F. (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol. Biol. 17, 1117-1125.
6. Cameron, R.K., Dixon, R.A. and Lamb, C.J. (1994) Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5, 715-725.
7. Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6, 1583-1592.
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. Delaney, T.P., Friedrich, L. and Ryals, J.A. (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl Acad. Sci. USA, 92, 6602-6606.
10. De Vries, S., Hoge, H. and Bisseling, T. (1988) Isolation of total and polysomal RNA from plant tissues. In Plant Molecular Biology Manual, B6 (Gelvin, S.B., Schilperoort, R.A. and Verma, D.P.S., eds). Dordrecht: Kluwer Academic Publishers, pp. 1-13.
11. Dixon, R.A. and Paiva, N.L. (1995) Stress-induced phenylpropanoid metabolism. Plant Cell, 7, 1085-1097.
12. - generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol. Mol. Plant Pathol. 32, 163-175.
13. Elkind, Y., Edwards, R., Mavandad, M., Hedrick, S.A., Ribak, O., Dixon, R.A. and Lamb, C.J. (1990) Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc. Natl Acad. Sci. USA, 87, 9057-9061.
14. Fraser, R.S.S. (1982) Are 'pathogenesis-related proteins' involved in acquired systemic resistance of tobacco plants to tobacco mosaic virus? J. Gen. Virol. 58, 305-313.
15. Friedrich, L., Vernooij, B., Gaffney, T., Morse, A. and Ryals, J. (1995) Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol. Biol. 29, 959-968.
16. Fritig, B., Gosse, J., Legrand, M. and Hirth, L. (1973) Changes in phenytalanine ammonia-lyase during the hypersensitive reaction of tobacco to TMV. Virology, 55, 371-379.
17. Fritig, B., Kauffmann, S., Dumas, B., Geoffroy, P., Kopp, M. and Legrand, M. (1987) Mechanism of the hypersensitivity response of plants. In Plant Resistance to Viruses (Evered, D. and Harnett, S., eds). Chichester: Wiley, pp. 92-108.
18. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, 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.
19. Klessig, D.F. and Malamy, J. (1994) The salicylic acid signal in plants. Plant Mol. Biol. 26, 1439-1458.
20. Lawton, K., Ward, E., Payne, G., Moyer, M. and Ryals, J. (1992) Acidic and basic class III chitinase mRNA accumulation in response to TMV infection of tobacco. Plant Mol. Biol 19, 735-743.
21. Legrand, M., Fritig, B. and Hirth, L. (1976) Enzymes of the phenylpropanoid pathway and the necrotic reaction of hypersensitive tobacco to tobacco mosaic virus. Phytochemistry, 15, 1353-1359.
22. Liang, X., Dron, M., Cramer, C.L., Dixon, R.A. and Lamb, C.J. (1939) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J. Biol. Chem. 264, 14 486-14 492.
23. Linthorst, H.J.M., van Loon, L.C., van Rossum, C.M.A., Mayer, A., Bol, J.F., van Roekel, J.S.C., Meulenhoff, E.J.S. and Cornelissen, B.J.C. (1990) Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. Mol. Plant-Microbe Interact. 3, 252-258.
24. Maher, E.A., Bate, N.J., Ni, W., Elkind, Y., Dixon, R.A. and Lamb, C.J. (1994) Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc. Natl Acad. Sci. USA, 91, 7802-7806.
25. 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.
26. Massala, R., Legrand, M. and Fritig, B. (1980) Effect of α-aminooxyacetate, a competitive inhibitor of phenylalanine ammonia-lyase, on the hypersensitive resistance of tobacco to tobacco mosaic virus. Physiol. Plant Pathol. 16, 213-226.
27. 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 mosaic virus. Plant Physiol. Biochem. 25, 217-225.
28. Mauch-Mani, B. and Slusarenko, A.J. (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonialyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell, 8, 203-212.
29. Métraux, J.-P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Scmid, E., Blum, W. and Inverardi, B. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250, 1004-1006.
30. Pellegrini, L., Rohfritsch, O., Fritig, B. and Legrand, M. (1994) Phenylalanine ammonia-lyase in tobacco. Molecular cloning and gene expression during the hypersensitive reaction to tobacco mosaic virus and the response to a fungal elicitor. Plant Physiol. 106, 877-886.
31. Rüffer, M., Steipe, B. and Zenk, M.H. (1995) Evidence against specific binding of salicylic acid to plant catalase. FEBS Lett. 377, 175-180.
32. Ryals, J., Ukness, S. and Ward, E. (1994) Systemic acquired resistance. Plant Physiol. 104, 1109-1112.
33. Shulaev, V., Leon, J. and Raskin, I. (1995) Is salicylic acid a translocated signal of systemic resistance in tobacco? Plant Cell, 7, 1691-1701.
34. Uknes, S., Dincher, S., Friedrich, L., Negrotto, D., Williams, S., Thompson-Taylor, H., Potter, S., Ward, E. and Ryals, J. (1993) Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell, 5, 159-169.
35. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jahwar, R., Ward, E., Uknes, S., Kessmann, H. and Ryals, J. (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell, 6, 959-965.
36. Vernooij, B., Friedrich, L., Ahl Goy, P., Staub, T., Kessmann, H. and Ryals, J. (1995) 2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 8, 228-234.
37. Walter, M. (1992) Regulation of lignification in defense. In Plant Gene Research. Genes Involved in Plant Defense (Boller, T. and Meins, F., eds). New York: Springer Verlag, pp. 326-352.
38. 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.
39. Yalpani, N., Leon, J., Lawton, M.A. and Raskin, I. (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 103, 315-321.