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Jasmonate-inducible plant defences cause increased parasitism of herbivores

Abstract

In many plants, defence systems against herbivores are induced through the octadecanoid pathway1,2, which may also be involved in recruiting natural enemies of herbivores3. This pathway can beinduced by treating plants with jasmonic acid4 or by natural herbivory, and increases resistance against herbivorous insects intomato plants5, in part by causing production of toxic and antinutritive proteinase inhibitors and oxidative enzymes6,7,8. Herbivore-infested tomato plants release increased amounts of volatiles9 and attract natural enemies of the herbivores10, as do other plants11,12,13,14,15. The octadecanoid pathway may regulate production of these volatiles, which attract host-seeking parasitic wasps16,17. However, plant resistance compounds can adversely affect parasitoids as well as herbivores18. It is unclear whether the combination of increased retention and/or attractiveness of parasitic wasps to induced plants and the adverse effects of plant defence compounds on both caterpillars and parasitoids results in a net increase in parasitization of herbivores feeding on induced plants.Here I show that inducing plants with jasmonic acid increases parasitism of caterpillar pests in an agricultural field twofold. Thus, elicitors of plant resistance may become useful in agriculture.

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Figure 1: The effects of jasmonate-induced plant responses on the parasitism of caterpillars.
Figure 2: Indirect effects of jasmonate-induced plant responses on parasitoid performance due to changes in the caterpillar host.

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References

  1. Karban, R. & Baldwin, I. T. Induced Responses to Herbivory(Univ. of Chicago Press, Chicago, Illinois, 1997).

    Book  Google Scholar 

  2. Meyer, A., Miersch, O., Buttner, C., Dathe, W. & Sembdner, G. Occurrence of the plant growth regulator jasmonic acid in plants. J. Plant Growth Regul. 3, 1–8 (1984).

    Article  CAS  Google Scholar 

  3. Farmer, E. E. New fatty acid based signals: a lesson from the plant world. Science 276, 912–913 (1997).

    Article  CAS  Google Scholar 

  4. McConn, M., Creelman, R. A., Bell, E., Mullet, J. E. & Browse, J. Jasmonate is essential for insect defense in Arabidopsis . Proc. Natl Acad. Sci. USA 93, 5473–5477 (1997).

    Article  ADS  Google Scholar 

  5. Thaler, J. S., Stout, M. J., Karban, R. & Duffey, S. S. Exogenous jasmonates simulate insect wounding intomato plants, Lycopersicon esculentum, in the laboratory and field. J. Chem. Ecol. 22, 1767–1781 (1996).

    Article  CAS  Google Scholar 

  6. Broadway, R. M., Duffey, S. S., Pearce, G. & Ryan, C. A. Plant proteinase inhibitors: a defense against herbivorous insects? Entomol. Exp. Appl. 41, 33–38 (1986).

    Article  CAS  Google Scholar 

  7. Felton, G. W., Donato, K., del Vecchio, R. J. & Duffey, S. S. Activation of plant foliar oxidases by feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15, 2667–2694 (1989).

    Article  CAS  Google Scholar 

  8. Orozco-Cardenas, M., McGurl, B. & Ryan, C. A. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl Acad. Sci. USA 90, 8273 8276 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Dicke, M., Takabayashi, J., Posthumus, M. A., Schutte, C. & Krips, O. E. Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp. Appl. Acarol. 22, 311–333 (1998).

    Article  CAS  Google Scholar 

  10. Dicke, M. & Sabelis, M. W. How plants obtain predatory mites as bodyguards. Netherlands J. Zool. 38, 148–165 (1988).

    Article  Google Scholar 

  11. Turlings, T. C. J., McCall, P. J., Alborn, H. T. & Tumlinson, J. H. An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. J. Chem. Ecol. 19, 411–425 (1993).

    Article  CAS  Google Scholar 

  12. Hopke, J., Donath, J., Blechert, S. & Boland, W. Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a β-glucosidase and jasmonic acid. FEBS Lett. 352, 146–150 (1994).

    Article  CAS  Google Scholar 

  13. Drukker, B., Scutareanu, P. & Sabelis, M. W. Do anthocorid predators respond to synomones from Psylla -infested pear trees under field conditions? Entomol. Exp. Appl. 77, 193–203 (1995).

    Article  Google Scholar 

  14. Shimoda, T., Takabayashi, J., Ashihara, W. & Takafuji, A. Response of predatory insect Scolothrips takahashii toward herbivore-induced plant volatiles under laboratory and field conditions. J. Chem. Ecol. 23, 2033–2048 (1997).

    Article  CAS  Google Scholar 

  15. De Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T. & Tumlinson, J. H. Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–572 (1998).

    Article  ADS  CAS  Google Scholar 

  16. Boland, W., Hopke, J., Donath, J., Nuske, J. & Bublitz, F. Jasmonic acid and coronatin induce odor production in plants. Angew. Chem. Int. Ed. Engl. 34, 1600–1602 (1995).

    Article  CAS  Google Scholar 

  17. Alborn, H. T. et al. . An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945–949 (1997).

    Article  CAS  Google Scholar 

  18. Campbell, B. C. & Duffey, S. S. Tomatine and parasitic wasps: Potential incompatibility of plant-antibiosis with biological control. Science 205, 700–702 (1979).

    Article  ADS  CAS  Google Scholar 

  19. Strand, L. L. Integrated Pest Management for Tomatoes(Division of Agriculture and Natural Resources Communication Services—Publications, Oakland, 1998).

    Google Scholar 

  20. Takabayashi, J. & Dicke, M. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1, 109–113 (1996).

    Article  Google Scholar 

  21. Clancy, K. M. & Price, P. W. Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68, 733–737 (1987).

    Article  Google Scholar 

  22. Benrey, B. & Denno, R. F. The slow-growth–high-mortality hypotheses: a test using the cabbage butterfly. Ecology 78, 987–999 (1997).

    Google Scholar 

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

    Article  Google Scholar 

  24. Bell, E. & Mullet, J. E. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant. Physiol. 103, 1133–1137 (1993).

    Article  CAS  Google Scholar 

  25. Siedow, J. N. Plant lipoxygenase: structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 145–188 (1991).

    Article  CAS  Google Scholar 

  26. Paré, P. W., Alborn, H. T. & Tumlinson, J. H. Concerted biosynthesis of an insect elicitor of plant volatiles. Proc. Natl Acad. Sci. USA 95, 13971–13975 (1998).

    Article  ADS  Google Scholar 

  27. Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J. & Posthumus, M. A. Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application to pest control. J. Chem. Ecol. 16, 3091–3118 (1990).

    Article  CAS  Google Scholar 

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Acknowledgements

I thank C. Wardlaw and C. Black for help in the field; M. Stout and C. De Moraes for discussion; and A. Agrawal, R. Karban, M. Dicke, J. Rosenheim, L. Adler, C. Black, R. Kimura and J.Granett for comments on the manuscript. This research was supported by the USDA-NRI.

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Correspondence to Jennifer S. Thaler.

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Thaler, J. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399, 686–688 (1999). https://doi.org/10.1038/21420

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