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Effect of Nitrogen Availability on Expression of Constitutive and Inducible Chemical Defenses in Tomato, Lycopersicon esculentum

Abstract

Young tomato plants (Lycopersicon esculentum) grown in sand in a greenhouse and subjected to different fertilization regimes were used to test the effects of nitrogen availability on constitutive levels of phenolics and on constitutive and inducible activities of polyphenol oxidase and proteinase inhibitors. Theories that emphasize physiological constraints on the expression of phytochemicals predict an increase in levels of carbon-based allelochemicals under moderate nitrogen stress but predict, under the same conditions, an attenuation of chemical responses involving nitrogen-containing compounds such as proteinase inhibitors and polyphenol oxidase. We found that nitrogen availability had a strong effect on constitutive levels of phenolics; weaker effects on constitutive polyphenol oxidase activity, constitutive proteinase inhibitor activity, and inducible polyphenol oxidase activity; and no effect on inducible proteinase inhibitor activity. These results point to a need for the integration of theories that emphasize physiological influences on secondary metabolism with those that emphasize ecological influences on secondary metabolism and suggest that current theories of plant defense do not adequately account for enzymatic and proteinaceous defenses against arthropods.

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REFERENCES

  • Baldwin, I. T. 1994. Chemical changes rapidly induced by folivory, pp. 1–23, in E. A. Bemays (ed.). Insect-Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Baldwin, I. T., Oesch, R. C., Merhige, P. M., and Hayes, K. 1993. Damage-induced root nitrogen metabolism in Nicotiana sylvestris: Testing C/N predictions for alkaloid production. J. Chem. Ecol. 19:3029–3043.

    Google Scholar 

  • Berenbaum, M. R. 1995. The chemistry of defense: Theory and practice. Proc. Natl. Acad. Sci. U.S.A. 92:2–8.

    Google Scholar 

  • Berenbaum, M. B., and Rosenthal, G. A. 1992. Plant Secondary Metabolites: Vol. 1. The Chemical Participants. Academic Press, New York.

    Google Scholar 

  • Blankendaal, M., Hodgson, R. H., Davis, D. G., Hoerauf, R. A., and Shimabukuro, R. H. 1972. Growing plants without soil for experimental use. United States Department of Agriculture, Miscellaneous publication 1251.

  • Bongue-Bartelsman, M., and Phillips, D. A. 1995. Nitrogen stress regulates expression of enzymes in the flavonoid biosynthetic pathway of tomato. Plant Physiol. Biochem. 33:539–546.

    Google Scholar 

  • Coley, P. D., Byrant, J. P., and Chapin, S. III. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.

    Google Scholar 

  • Denno, R. F., and McClure, M. S. 1983. Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.

    Google Scholar 

  • Duffey, S. S., and Felton, G. W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects, pp. 167–197, in P. A. Hedin (ed.). Naturally Occurring Pest Bioregulators. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Duffey, S. S., and Stout, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3–38.

    Google Scholar 

  • Edwards, P. J. 1992. Resistance and defence: The role of secondary plant substances, pp. 69–84, in P. G. Ayers (ed.). Pests and Pathogens: Plant Responses to Foliar Attack. BioScientific Publishers, Oxford.

    Google Scholar 

  • Farmer, E. E., Johnson, R. R., and Ryan, C. A. 1992. Regulation of expression of proteinase inhibitor genes by methyl jasmonic acid. Plant Physiol. 98:995–1002.

    Google Scholar 

  • Frischknecht, P. M., Ulmer-Dufek, J., and Baumann, T. W. 1986. Purine alkaloid formation in buds and developing leaflets of Coffea arabica: Expression of an optimal defence strategy? Phytochemistry 25:613–616.

    Google Scholar 

  • Gershenzon, J. 1994. The cost of chemical defense against herbivory: A biochemical perspective, pp. 105–174, in E. A. Bernays (ed.). Insect-Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Harborne, J. B. 1988. Introduction to Ecological Biochemistry. Academic Press, London.

    Google Scholar 

  • Hedin, P. A. 1983. Plant Resistance to Insects. American Chemical Society Symposium Series, Vol. 208. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Herms, D. A., and Mattson, W. J. 1992. The dilemma of plants: To grow or defend. Q. Rev. Biol. 67:283–335.

    Google Scholar 

  • Hugentobler, U., and Renwick, J. A. A. 1995. Effects of plant nutrition on the balance of insect relevant cardenolides and glucosinolates in Erysimum cheriranthoides. Oecologia 102:95–101.

    Google Scholar 

  • Johnson, N. D., Rigney, L. P., and Bentley, B. L. 1989. Short-term induction of alkaloid production in lupines: Differences between N2-fixing and nitrogen-limited plants. J. Chem. Ecol. 15:2425–2433.

    Google Scholar 

  • Jones, C. G., Hare, J. D., and Compton, S. J. 1989. Measuring plant protein with the bradford assay. 1. Evaluation and standard method. J. Chem. Ecol. 15:979–992.

    Google Scholar 

  • Karban, R. 1992. Plant variation: Its effects on populations of herbivorous insects, pp. 195–215, in R. S. Fritz and E. L. Simms (eds.). Plant Resistance to Herbivores and Pathogens. University of Chicago Press, Chicago.

    Google Scholar 

  • Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • Kuwabara, T., Masuda, T., and Aizawa, S. 1997. A dithiothreitol-sensitive tetrameric protease from spinach thylakoids has polyphenol oxidase activity. Plant Cell Physiol. 38:179–187.

    Google Scholar 

  • Lerdau, M., Litvak, M., and Monson, R. 1994. Plant chemical defense: Monoterpenes and the growth-differentiation balance hypothesis. Trends Ecol. Evol. 9:58–61.

    Google Scholar 

  • Reichardt, P. B., Chapin, F. S., III, Bryant, J. P., Mattes, B. R., and Clausen, T. P. 1991. Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: Potential importance of metabolite turnover. Oecologia 88:401–406.

    Google Scholar 

  • Reinbothe, S. B., Mollenhauer, B., and Reinbothe, C. 1994. JIPs and RIPs: The regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209.

    Google Scholar 

  • Ryan, C. A., Bishop, P. D., Graham, J. S., Broadway, R. M., and Duffey, S. S. 1986. Plant and fungal cell wall fragments activate expression of proteinase inhibitor genes for plant defense. J. Chem. Ecol. 12:1025–1036.

    Google Scholar 

  • Schaller, A., and Ryan, C. A. 1995. Systemin—a polypeptide defense signal in plants. BioEssays 18:27–33.

    Google Scholar 

  • Stout, M. J., and Duffey, S. S. 1996. Characterization of induced resistance in tomato plants. Entomol. Exp. Appl. 79:273–283.

    Google Scholar 

  • Stout, M. J., Workman, K. V., and Duffey, S. S. 1996a. Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomol. Exp. Appl. 79:255–271.

    Google Scholar 

  • Stout, M. J., Workman, K. V., Workman, J. S., and Duffey, S. S. 1996b. Temporal and ontogenetic aspects of protein induction in foliage of the tomato, Lycopersicon esculentum. Biochem. System. Ecol. 24:611–625.

    Google Scholar 

  • Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998a. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81.

    Google Scholar 

  • Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998b. Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol. Exp. Appl. 86:267–279.

    Google Scholar 

  • Tallamy, D. W., and Raupp, M. J. (eds.). 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York.

    Google Scholar 

  • 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.

    Google Scholar 

  • Waterman, P. G., and Mole, S. 1989. Extrinsic factors influencing production of secondary metabolites in plants, pp. 107–134, in E. A. Bernays (ed.). Insect-Plant Interactions. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Waterman, P. G., and Mole, S. 1994. Analysis of Phenolic Plant Metabolites. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Wilkens, R. T., Shea, G. O., Halbreich, S., and Stamp, N. E. 1996a. Resource availability and the trichome defenses of tomato plants. Oecologia 106:181–191.

    Google Scholar 

  • Wilkens, R. T., Spoerke, J. M., and Stamp, N. E. 1996b. Differential responses of growth and two soluble phenolics of tomato to resource availability. Ecology 77:247–258.

    Google Scholar 

  • Zangerl, A. R., and Berenbaum, M. R. 1995. Spatial, temporal, and environmental limits on xanthotoxin induction in wild parsnip foliage. Chemoecology 1:37–42.

    Google Scholar 

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Stout, M.J., Brovont, R.A. & Duffey, S.S. Effect of Nitrogen Availability on Expression of Constitutive and Inducible Chemical Defenses in Tomato, Lycopersicon esculentum . J Chem Ecol 24, 945–963 (1998). https://doi.org/10.1023/A:1022350100718

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  • DOI: https://doi.org/10.1023/A:1022350100718

  • Lycopersicon esculentum
  • Helicoverpa zea
  • induced resistance
  • inducible chemistry
  • phenolics
  • proteinase inhibitors
  • polyphenol oxidase
  • nitrogen availability