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Induction of Hypericins and Hyperforins in Hypericum perforatum in Response to Damage by Herbivores

Abstract

Plants respond to herbivore and pathogen attack by a variety of direct and indirect mechanisms that include the induction of secondary metabolites. The phytomedicinal plant Hypericum perforatum L. produces two different classes of secondary metabolites:hyperforins, a family of antimicrobial acylphloroglucinols; and hypericins, a family of phototoxic anthraquinones exhibiting antimicrobial, antiviral, and antiherbivore properties in vitro. To determine whether these compounds are part of the herbivore-specific inducible plant defense system, we used an in vitro detached assay to assess the effects of specialist and generalist herbivore damage on the levels of hypericins and hyperforin. Greenhouse-grown H. perforatum plant sections were challenged with the specialist, Chrysolina quadrigemina, or with one of the following generalist feeders: Spilosoma virginica, Spilosoma congrua,or Spodoptera exigua. Feeding by the specialist beetle or mechanical wounding caused little change in phytochemical levels in plant tissue, whereas the small amount of feeding by the generalists caused 30–100% increases in hypericins and hyperforin as compared to control levels. Although the leaf damage index of the specialist feeding was 2.7 times greater, C. quadrigemina had little effect on H. perforatum chemical defenses in response to feeding damage in comparison to generalist feeding.

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References

  1. Agrawal, A. A. 1999. Induced responses to herbivory in wild radish: Effects on several herbivores and plant fitness. Ecology 80:1713–1723.

    Google Scholar 

  2. Arnason, J. T., Towers, G. H. N., Philogene, B. J. R., and Lambert, J. D. H. 1983. The role of natural photosensitizers in plant resistance to insects, pp. 139–151, in P. Hedin (ed.). Plant Resistance to Insects. American Chemical Society, Washington, DC.

    Google Scholar 

  3. Baldwin, I. T. and Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Plant. Berl. 208:137–145.

    Google Scholar 

  4. Bennett, R.-N. and Wallsgrove, R.-M. 1994. Tansley review No. 72: Secondary metabolites in plant defence mechanisms. N. Phytol. 127:617–633.

    Google Scholar 

  5. Berenbaum, M. R. 1983. Coumarins and caterpillars: A case for coevolution. Evolution 37:163–179.

    Google Scholar 

  6. Berenbaum, M. R. 1990. Evolution of specialization in insect-umbellifer associations. Annu. Rev. Entomol. 35:319–343.

    Google Scholar 

  7. Bieri, S., Potrykus, I., and Futterer, J. 2003. Effects of combined expression of antifungal barley seed proteins in transgenic wheat on powdery mildew infection. Mol. Breedings 11:37–48.

    Google Scholar 

  8. Bowles, D. J. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem. 59:873–907.

    Google Scholar 

  9. Brody, A. K. and Karban, R. 1992. Lack of a tradeoff between constitutive and induced defenses among varieties of cotton. Oilos 65:301–306.

    Google Scholar 

  10. Büter, B., Orlacchio C., Soldati, A., and Berger, K. 1998. Significance of genetic and environmental aspects in the field cultivation of Hypericum perforatum Plant Med. 64:431–437.

    Google Scholar 

  11. Campbell, C. 1988. Assessment of Biological Control of St. John's Wort (Hypericum perforatum L.) in Northern Idaho. Department of Entomology, University of Idaho, Moscow, ID.

    Google Scholar 

  12. Campbell, M. H., May, C. E., Southwell, I. A., Tumlinson, J. D., and Michael, P. W. 1997. Variation in Hypericum perforatum L. (St. John's wort) in New South Wales. Plant Protein Q. 12:64–66.

    Google Scholar 

  13. Clayton, B. D. 1978. Escape of Hypericum perforatum L. from an Insect Herbivore at Clearwater Junction, Montana. Department of Botany, University of Montana, Missoula, MT.

    Google Scholar 

  14. Constabel, C. P. 1999. A survey of herbivore-inducible defensive proteins and phytochemicals, pp. 137–166, in A. Agrawal, S. Tuzun, and E. Bent (Eds.). Induced Defenses Against Pathogens and Herbivores. APS, St. Paul, MN.

    Google Scholar 

  15. Cornell, H. V. and Hawkins, B. A. 2003. Herbivore responses to plant secondary compounds: A test of phytochemical coevolution theory. Am. Nat. 161:507–522.

    Google Scholar 

  16. Creelman, R.-A. and Mullet, J.-E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:355–381.

    Google Scholar 

  17. Dixon, R. A. and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.

    Google Scholar 

  18. Duffey, S. S. and Pasteels, J. M. 1993. Transient uptake of hypericin by chrysomelids is regulated by feeding behavior. Physiol. Entomol. 18:119–129.

    Google Scholar 

  19. Duffey, S. S. and Stout, M. J. 1996. Anti-nutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3–37.

    Google Scholar 

  20. Ehrlich, P. and Raven, P. H. 1964. Butterflies and plants: A study in coevolution. Evolution 18:586–608.

    Google Scholar 

  21. Fields, P. G., Arnason, J. T., and Philogene, B. J. R. 1990. Behavioral and physical adaptations of three insects that feed on the phototoxic plant Hypericum perforatum. Can. J. Zool. 68:339–346.

    Google Scholar 

  22. Fitches, E., Gatehouse, A. M. R., and Gatehouse, J. A. 1997. Effects of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on the development of tomato moth (Lacanobia oleracea) larvae in laboratory and glasshouse trials. J. Insect Physiol. 43:727–739.

    Google Scholar 

  23. Gershenzon, J. and Croteau, R. 1991. Terpenoids, pp. 165–219, in G. A. Rosenthal and M. R. Berenbaum (Eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic, San Diego, CA.

    Google Scholar 

  24. Grünwald, J. 1999. The world market for Hypericum products. Nutr. World. 2:22–25.

    Google Scholar 

  25. Guillet, G. 1997. Ecophysiological Importance of Phototoxins in Plant–Insect Relationships. Department of Ottawa-Carleton Institute of Biology, University of Ottawa, Ottawa, Ontario.

    Google Scholar 

  26. Guillet, G., Podenszfinski, C., Regnault-Roger, C., Arnason, J. T., and Philogéne, B. J. R. 2000. Behavioral and biochemical adaptations of generalist and specialist herbivorous insects feeding on Hypericum perforatum (Guttiferae). Environ. Entomol. 29:135–139.

    Google Scholar 

  27. Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and Baldwin I. 2001. Molecular interaction between the specialist herbivore Maduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid–amino acid conjugated in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol. 125:711–717.

    Google Scholar 

  28. Hammond-Kosack, K. E. and Jones, J. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791.

    Google Scholar 

  29. Hartmann, T. 1991. Alkaloids, pp. 79–121, in G. A. Rosenthal and M. R. Berenbaum (Eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic, San Diego, CA.

    Google Scholar 

  30. Hersmeier, D., Schittko, U., and Baldwin, I. 2001. Molecular interaction between the specialist herbivore Maduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth and defense-related plant mRNAs. Plant Physiol. 125:683–700.

    Google Scholar 

  31. Jensen, K. I. N., Gaul, S. O., Specht, E. G., and Doohan, D. J. 1995. Hypericin content of Nova Scotia biotypes of Hypericum perforatum L. Can. J. Plant Sci. 75:923–926.

    Google Scholar 

  32. Karban, R., Agrawal, A., and Mangel, M. 1997. The benefits of induced defenses against herbivores. Ecology 78:1351–1355.

    Google Scholar 

  33. Karban, R. and Kúc, J. 1999. Induced resistance against pathogens and herbivores: An overview, pp. 1–16, in A. Agrawal, S. Tuzun, and E. Bent (Eds.). Induced Defenses Against Pathogens and Herbivores. APS, St. Paul, MN.

    Google Scholar 

  34. Kirakosyan, A. B., Gibson, D. M., and Sirvent, T. M. 2003. A comparative survey of Hypericum perforatum plants as sources of hypericins and hyperforin. J. Herbs Spices Med. Plants. 11(1).

  35. Melikian, E., Boroyan, R., Karaguezian, A., Charchoglian, A., Gabrielian, E., and Panossian, A. 1998. Hypericin content in St. John's wort (Hypericum perforatum L.) growing in Armenia. Pharm. Pharmacol. Lett. 8:101–102.

    Google Scholar 

  36. Mitchell-Olds, T. and Pedersen, D. 1998. The molecular basis of quantitative genetic variation in central and secondary metabolism in Arabidopsis. Genetics 149:739–747.

    Google Scholar 

  37. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719.

    Google Scholar 

  38. Ryan, C. A. 1990. Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425–449.

    Google Scholar 

  39. Schappert, P. and Shore, J. 1999. Cyanogenesis, herbivory and plant defense in Turnera ulmifolia on Jamaica. Ecoscience 6:511–520.

    Google Scholar 

  40. Sirvent, T. and Gibson, D. 2000. Rapid isocratic analysis of hypericins. J. Liq. Chromatogr 23:251–259.

    Google Scholar 

  41. Sirvent, T., Walker, L., Vance, N., and Gibson, D. 2002. Variations of hypericins in wild populations of Hypericum perforatum L. in the Pacific Northwest. Econ. Bot. 56:41–48.

    Google Scholar 

  42. Sirvent, T. M. and Gibson, D. M. 2002. Induction of hypericins and hyperforin in H. perforatum L. in response to biotic and chemical elicitors. Physiol. Mol. Plant Pathol. 60:311–320.

    Google Scholar 

  43. Southwell, I. and Bourke, C. 2001. Seasonal variation in hypericin content of Hypericum perforatum L. (St. John's wort). Phytochemistry 56:437–441.

    Google Scholar 

  44. Southwell, I. A. and Campbell, M. H. 1991. Hypericin content variation in Hypericum perforatum in Australia. Phytochemistry 30:475–478.

    Google Scholar 

  45. Stout, M. and Bostock, R. 1999. Specificity of induced responses to arthropods and pathogens, pp. 183–209, in A. Agrawal, S. Tuzun, and E. Bent (Eds.). Induced Defenses Against Pathogens and Herbivores. APS, St. Paul, MN.

    Google Scholar 

  46. Tebayashi, S. I., Ishihara, A., Tsuda, M., and Iwamura, H. 2000. Induction of clovamide by jasmonic acid in red clover. Phytochemistry 54:387–392.

    Google Scholar 

  47. Traw, M. B. and Dawson, T. E. 2002. Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ. Entomol. 31:714–722.

    Google Scholar 

  48. Upton, R., Graff, A., Williamson, E., Bunting, D., Gatherum, D. M., Walker, E. B., Butterweck, V., Liefländer, U., Nahrstedt, A., Winterhoff, H., and Cott, J. 1997. St. John's Wort, Hypericum perforatum: Quality Control, Analytical and Therapeutic Monograph. American Herbal Pharmacopoeia, Santa Cruz, CA.

    Google Scholar 

  49. VAN DER Meijden, E. 1988. A plant's response to herbivory: The trade off between defence and regrowth, pp. 137–144, in E. S. Delfosse (ed.). Proceedings (VII) of the International Symposium of the Biological Control of Weeds. Ist. Sper. Patol. Veg., Rome, Italy.

  50. Walker, L., Sirvent, T. M., Gibson, D. M., and Vance, N. 2001. Regional differences in hypericin and pseudohypericin concentrations and five morphological traits among Hypericum perforatum plants in the northwestern United States. Can. J. Bot. 79:1248–1255.

    Google Scholar 

  51. Wegulo, S. N., Yang, X. B., and Martinson, C. A. 1998. Soybean cultivar responses to Sclerotinia sclerotiorum in field and controlled environment studies. Plant Dis. 82:1264–1270.

    Google Scholar 

  52. Zangerl, A. R. and Berenbaum, M. R. 1990. Furanocoumarin induction in wild parsnip: Genetics and populational variation. Ecology 71:1933–1940.

    Google Scholar 

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Correspondence to Tara M. Sirvent.

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Sirvent, T.M., Krasnoff, S.B. & Gibson, D.M. Induction of Hypericins and Hyperforins in Hypericum perforatum in Response to Damage by Herbivores. J Chem Ecol 29, 2667–2681 (2003). https://doi.org/10.1023/B:JOEC.0000008011.77213.64

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  • Hypericum perforatum
  • induced resistance
  • Chrysolina quadrigemina
  • hypericins
  • hyperforin
  • herbivory
  • defense response
  • plant–herbivore interactions