Antagonism Between Jasmonate- and Salicylate-Mediated Induced Plant Resistance: Effects of Concentration and Timing of Elicitation on Defense-Related Proteins, Herbivore, and Pathogen Performance in Tomato
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.Get Access
The jasmonate (JA) and salicylate (SA) signaling pathways in plants provide resistance to herbivorous insects and pathogens. It is known that these pathways interact, sometimes resulting in antagonism between the pathways. We tested how the timing and concentration of elicitation of each pathway influenced the interaction between the jasmonate and salicylate pathways measured in terms of five biochemical responses and biological resistance to caterpillars and bacteria. The salicylate pathway had a stronger effect on the jasmonate pathway than did the reverse. The negative signal interaction was generated by two distinct paths in the plant. A negative interaction in the biochemical expression of the two pathways was most consistent in the simultaneous elicitation experiments compared to when the elicitors were temporally separated by two days. Herbivore bioassays with Spodoptera exigua also consistently reflected an interaction between the two pathways in the simultaneous elicitation experiments. The negative signal interaction reducing biological resistance to the herbivore was also demonstrated in some temporally separated treatment combinations where attenuation of the biochemical response was not evident. Concentration of the elicitors had an effect on the pathway interaction with consistent biochemical and biological antagonism in the high concentration experiments and inconsistent antagonism in the low concentration experiments. The bacterial pathogen, Pseudomonas syringae pv. tomato (Pst), consistently showed reduced lesion development on plants with SA responses activated and, in some experiments, on JA-elicited plants. Resistance to Pst was not reduced or enhanced in dual-elicited plants. Thus, signal interaction is most consistent when elicitors are applied at the same time or when applied at high doses. Signal interaction affected the herbivore S. exigua, but not the pathogen Pst.
- Broadway, R. M., Duffey, S. S., Pearce, G., and Ryan, C. A. 1986. Plant proteinase inhibitors: A defense against herbivorous insects? Entomol. Exp. Appl. 41:33–38.
- Choi, D., Bostock, R. M., Avdiushko, S., and Hildebrand, D. F. 1994. Lipid-derived signals that discriminate wound-and pathogen-responsive isoprenoid pathways in plants: Methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes antimicrobial isoprenoids in Solanum tuberosum L. Proc. Natl. Acad. Sci. USA 91:2329–2333.
- Conconi, A., Miquel, M., Browse, J. A., and Ryan, C. A. 1996. Intracellular levels of free linolenic and linolenic acids increase in tomato leaves in response towounding. Plant Physiol. 111:797–803.
- Creelman, R. A., and Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Ann. Rev. of Plant Physiol. Plant Mol. Biol. 48:355–381.
- Doares, S. H., Narvaez-Vasquez, J., Conconi, A., and Ryan, C. A. 1995a. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108:1741–1746.
- Doares, S. H., Syrovets, T., Weiler, E. W., and Ryan, C. A. 1995b. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 92:4095–4098.
- Doherty, H. M., Selvendran, R. R., and Bowles, D. J. 1988. The wound response of tomato plants can be inhibited by aspirin and related hydroxybenzoic acids. Physiol. Mol. Plant Path. 33:377–384.
- Duffey, S. S. and Felton, G. W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects pp. 166–197, in P. A. Hedin, (ed.). ACS Symp. Series, 449. Naturally Occurring Pest Bioregulators. American Chemical Society: Washington, DC.
- Engelberth, J., Koch, T., Schuler, G., Bachmann, N., Rechtenbach, J., and Boland, W. 2001. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol. 125:369– 377.
- Enyedi, A. J., Yalpani, N., Silverman, P., and Raskin, I. 1992. Signal molecules in systemic plant resistance to pathogens and pests. Cell 70:879–886. CrossRef
- Felton, G. and Korth, K. 2000. Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3:309–314.
- Felton, G. W., Donato, K., Del Vecchio, R. J., and Duffey, S. S. 1989. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667–2694.
- Felton, G. W., Korth, K. L., Bi, J. L., Wesley, S. V., Huhman, D. V., Matthews, M. C., and Murphy, J. B. 1999. Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr. Biol. 9:317–320.
- Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: Expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathl. 54:97–114.
- Howe, G. A., Lightner, J., Browse, J., and Ryan, C. A. 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signalling for defense against insect attack. Plant Cell 8:2067–2077.
- Inbar, M., Doostdar, H., Sonoda, R. M., Leibee, G. L., and Mayer, R. T. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. J. Chem. Ecol. 24:135–149.
- Jones, C. G., Hare, J. D., and Compton, S. J. 1989. Measuring plant protein with the bradford assay.J. Chem. Ecol. 15:979–992.
- Karban, R. and English-Loeb, G. M. 1988. Effects of herbivory and plant conditioning on the population dynamics of spider mites. Exp. Appl. Acarol. 4:225–246.
- McDowell, J. M. and Dangl, J. L. 2000. Signal transduction in the plant immune response. Trends Plant Sci. 25:79–82.
- Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N., and Ohashi, Y. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39:500–507.
- O'Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H.M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917.
- Oldroyd, G. E. D. and Staskawicz, B. J. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. USA 95:10300–10305.
- Pena-Cortes, H., Albrecht, T., Prat, S., Weiler, E.W., and Willmitzer, L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128. CrossRef
- Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., and Manners, J.M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97:11655–11660.
- Seo, S., Okamato, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi Y. 1995. TobaccoMAPkinase: A possible mediator in wound signal transduction pathways. Science 270:1988–1992.
- Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998. Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol. Exp. Appl. 86:267–279.
- Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767–1781.
- Thaler, J. S., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 1999. Trade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistance. J. Chem. Ecol. 25:1597–1609.
- Underwood, A. J. 1997. Experiments in Ecology. Cambridge University Press, Cambridge.
- Waldbauer, G. B. 1968. PThe consumption and utilization of food by insects. Adv. Insect Physiol. 5:229–289.
- Zhu-Salzman, K., Salzman, R. A., Koiwa, H., Murdock, L. L., Bressan, R. A., and Hasegawa, P. M. 1998. Ethylene negatively regulates local expression of plant defense lectin genes. Plant Physiol. 104:6365–372.
- Antagonism Between Jasmonate- and Salicylate-Mediated Induced Plant Resistance: Effects of Concentration and Timing of Elicitation on Defense-Related Proteins, Herbivore, and Pathogen Performance in Tomato
Journal of Chemical Ecology
Volume 28, Issue 6 , pp 1131-1159
- Cover Date
- Print ISSN
- Online ISSN
- Kluwer Academic Publishers-Plenum Publishers
- Additional Links
- Signal interaction
- induced defense
- Spodoptera exigua
- Pseudomonas syringae pv. tomato
- polyphenol oxidase
- Industry Sectors