Abstract
Transgenic tobacco plants that express the bacterial nahG gene encoding salicylate hydroxylase have been shown to accumulate very little salicylic acid and to be defective in their ability to induce systemic acquired resistance (SAR). In recent experiments using transgenic NahG tobacco and Arabidopsis plants, we have also demonstrated that salicylic acid plays a central role in both disease susceptibility and genetic resistance. In this paper, we further characterize tobacco plants that express the salicylate hydroxylase enzyme. We show that tobacco mosaic virus (TMV) inoculation of NahG tobacco leaves induces the accumulation of the nahG mRNA in the pathogen infected leaves, presumably due to enhanced stabilization of the bacterial mRNA. SAR-associated genes are expressed in the TMV-infected leaves, but this is localized to the area surrounding necrotic lesions. Localized acquired resistance (LAR) is not induced in the TMV-inoculated NahG plants suggesting that LAR, like SAR, is dependent on SA accumulation. When SA is applied to nahG-expressing leave's SAR gene expression does not result. We have confirmed earlier reports that the salicylate hydroxylase enzyme has a narrow substrate specificity and we find that catechol, the breakdown product of salicylic acid, neither induces acquired resistance nor prevents the SA-dependent induction of the SAR genes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Comai L, Moran P, Maslyar D: Novel and useful properties of a chimeric promoter combining 35S and MAS elements. Plant Mol Biol 15: 373–381 (1990).
Delaney T, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J: A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250 (1994).
Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J: Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756 (1993).
Löffelhardt W, Kindl H: The conversion of L-Phenylalanine into benzoic acid on the thylakoid membrane of higher plants. Hoppe-Seyler's Z Physiol Chem 356: 487–493 (1975).
Malamy J, Carr JP, Klessig DF, Raskin I: Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002–1004 (1990).
Métraux J-P, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B: Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006 (1990).
Murray EE, Rocheleau T, Eberle M, Stock C, Sehar V, Adang M: Analysis of unstable RNA transcripts of insecticidal crystal protein genes of Bacillus thuringiensis in transgenic plants and electroporated protoplasts. Plant Mol Biol 16: 1035–1050 (1991).
Qin X-F, Holuigue L, Horvath DM, Chua N-H: Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6: 863–874 (1994).
Ranjeva R, Alibert G, Boudot AM: Métabolisme des composés phénoliques chez le pétunia VI. Intervention des chloroplastes dans la biosynthèse de la naringénine et de l'acide chlorogénique. Plant Sc Lett 10: 235–242 (1977).
Rasmussen JB, Hammerschmidt R, Zook MN: Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol 97: 1342–1347 (1991).
Ross AF: Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14: 329–339 (1961).
Uknes S, Mauch-Mani B, Moyer M, Williams S, Dincher S, Chandler D, Potter S, Slusarenko A, Ward E, Ryals J: Acquired resistance in Arabidopsis. Plant Cell 4: 645–656 (1992).
Uknes S, Winter A, Delaney T, Vernooij B, Morse A, Friedrich L, Potter S, Ward E, Ryals J: Biological induction of systemic acquired resistance in Arabidopsis. Mol Plant-Microbe Interact 6: 680–685 (1993).
Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jowhar R, Ward E, Uknes S, Kessmann H, Ryals J: Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959–965 (1994).
Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux J-P, Ryals JA: Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094 (1991).
White RF: Acetylsalicylic acid (aspirin) induces resitance to tobacco mosaic virus in tobacco. Virology 99: 410–412 (1979).
White-Stevens R, Kamin H: Studies of a flavoprotein, salicylate hydroxylase. J Biol Chem 247: 2358–2370 (1972).
Williams S, Friedrich L, Dincher S, Carozzi N, Kessmann H, Ward E, Ryals J: Chemical regulation of Bacillus thuringiensis delta-endotoxin expression in transgenic plants. Bio/technology 10: 540–543 (1992).
Yalpani N, Shulaev V, Raskin I: Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco. Phytopathology 83: 702–708 (1993).
Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J: Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant-Microbe Interact, in press.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Friedrich, L., Vernooij, B., Gaffney, T. et al. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol 29, 959–968 (1995). https://doi.org/10.1007/BF00014969
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00014969