Journal of Chemical Ecology

, Volume 15, Issue 12, pp 2667–2694 | Cite as

Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores

  • G. W. Felton
  • K. Donato
  • R. J. Del Vecchio
  • S. S. Duffey


The foliage and fruit of the tomato plantLycopersicon esculentum contains polyphenol oxidases (PPO) and peroxidases (POD) that are compartmentally separated from orthodihydroxyphenolic substrates in situ. However, when leaf tissue is damaged by insect feeding, the enzyme and phenolic substrates come in contact, resulting in the rapid oxidation of phenolics to orthoquinones. When the tomato fruitwormHeliothis zea or the beet army-wormSpodoptera exigua feed on tomato foliage, a substantial amount of the ingested chlorogenic acid is oxidized to chlorogenoquinone by PPO in the insect gut. Additionally, the digestive enzymes of the fruitworm have the potential to further activate foliar oxidase activity in the gut. Chlorogenoquinone is a highly reactive electrophilic molecule that readily binds cova-lently to nucleophilic groups of amino acids and proteins. In particular, the —SH and —NH2 groups of amino acids are susceptible to binding or alkylation. In experiments with tomato foliage, the relative growth rate of the fruitworm was negatively correlated with PPO activity. As the tomato plant matures, foliar PPO activity may increase nearly 10-fold while the growth rate of the fruitworm is severely depressed. In tomato fruit, the levels of PPO are highest in small immature fruit but are essentially negligible in mature fruit. The growth rate of larvae on fruit was also negatively correlated with PPO activity, with the fastest larval growth rate occurring when larvae fed on mature fruit. The reduction in larval growth is proposed to result from the alkylation of amino acids/protein byo-quinones, and the subsequent reduction in the nutritive quality of foliage. This alkylation reduces the digestibility of dietary protein and the bioavailability of amino acids. We believe that this mechanism of digestibility reduction may be extrapolatable to other plant-insect systems because of the ubiquitous cooccurrence of PPO and phenolic substrates among vascular plant species.

Key words

Polyphenol oxidase peroxidase digestibility reduction plant-insect interactions phenolic-protein binding chlorogenic acid Heliothis zea Spodoptera exigua Lepidoptera Noctuidae Lycopersicon esculentum host-plant resistance 


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  1. Asquith, T.N., andButler, L.G. 1986. Interactions of condensed tannins with selected proteins.Phytochemistry 25:1591–1593.Google Scholar
  2. Barbeau, W.E., andKinsella, J.E. 1983. Factors affecting the binding of chlorogenic acid to fraction 1 leaf protein.J. Agric. Food Chem. 31:993–998.Google Scholar
  3. Barbeau, W.E., andKinsella, J.E. 1985. Effects of free and bound chlorogenic acid on the in vitro digestibility of ribulose biphosphate carboxylase from spinach.J. Food Sci. 50:1083–1100.Google Scholar
  4. Berenbaum, M. 1980. Adaptive significance of midgut pH in larval Lepidoptera.Am. Nat. 112:138–146.Google Scholar
  5. Berenbaum, M. 1983. Effects of tannins on growth and digestion in two species of papilionids.Entomol. Exp. Appl. 24:44–53.Google Scholar
  6. Bernays, E.A. 1981. Plant tannins and insect herbivores: an appraisal.Ecol. Entomol. 6:353–360.Google Scholar
  7. Bernays, E.A., Chamberlain, D.J., andWoodhead, S. 1982. Phenols as nutrients for a phytophagous insectAnacridium melanorhodon.J. Insect Physiol. 29:535–539.Google Scholar
  8. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal. Biochem. 72:248–254.Google Scholar
  9. Broadway (-Meyer), R.M. 1985. The effects of dietary protein and plant proteinase inhibitors on the growth and digestive physiology of larvalHeliothis zea (Boddie) andSpodoptera exigua (Hubner) (Lepidoptera: Noctuidae). University of California, Davis. Ph.D. thesis. 134 pp.Google Scholar
  10. Broadway, R.M., andDuffey, S.S. 1986a. The effect of dietary protein on the growth and digestive physiology of larvalHeliothis zea andSpodoptera exigua.J. Insect Physiol. 32:673–680.Google Scholar
  11. Broadway, R.M., andDuffey, S.S. 1986b. Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larvalHeliothis zea andSpodoptera exigua.J. Insect Physiol. 32:827–833.Google Scholar
  12. Broadway, R., Duffey, S.S., Pearce, G., andRyan, C.A. 1986. Plant proteinase inhibitors: A defence against herbivorous insects?Entomol. Exp. Appl. 41:33–38.Google Scholar
  13. Butt, V.S. 1981. Direct oxidases and related enzymes, pp. 81–123,in P.K. Stumpf and E.E. Conn (eds.). The Biochemistry of Plants, A Comprehensive Treatise, Vol. 2, Metabolism and Respiration. Academic Press, New York.Google Scholar
  14. Butt, V.S., andLamb, J.C. 1981. Oxygenases and the metabolism of plant products, pp. 627– P.K. Stumpf and E.E. Conn (eds.). The Biochemistry of Plants, A Comprehensive Treatise, Vol. 7. Secondary Plant Products, Academic Press, New York.Google Scholar
  15. Chan, B.G., Waiss, A.C., Jr., Binder, R.G. andElliger, C.A. 1978. Inhibition of lepidopterous growth by cotton constituents.Entomol. Exp. Appl. 24:94–100.Google Scholar
  16. Chiang, H., Norris, D.M., Ciepela, A., Shapiro, P., andOosterwyk, A. 1987. Inducible versus constitutive PI 227687 soybean resistance to Mexican bean beetle,Epilachna varivestis.J. Chem. Ecol. 13:741–749.Google Scholar
  17. Chippendale, G.M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borerDiatraea grandiosella.J. Insect Physiol, 16:1057–1068.Google Scholar
  18. Coley, P.D., Bryant, J.P., andChapin, F.S., III. 1985. Resource availability and plant anti-herbivore defense.Science 230:895–899.Google Scholar
  19. Compton, S. J., andJones, C.G. 1985. Mechanism of dye response and interference in the Bradford protein assay.Anal. Biochem. 151:369–374.Google Scholar
  20. Davies, A.M.C., Newby, V.K., andSynge, R.L.M. 1978. Bound quinic acid as a measure of coupling of leaf and sunflower-seed proteins with chlorogenic acid and congeners: Loss of availability of lysine.J. Sci. Food Agric. 29:33–41.Google Scholar
  21. Duffey, S.S. 1986. Plant glandular trichomes: Their role in partial defence against insects, pp. 151–172,in Sir R. Southwood and B. Juniper (eds.). Insects and the Plant Surface. Edward Arnold, London.Google Scholar
  22. Duffey, S.S., andBloem, K.A. 1986. Plant defense-herbivore-parasite interactions and biological control, pp. 135–185,in M. Kogan (ed.). Ecological Theory and Integrated Pest Management. John Wiley, New York.Google Scholar
  23. Duffey, S.S., andIsman, M.B. 1981. Inhibition of insect larval growth by phenolics in glandular trichomes of tomato leaves.Experientia 37:574–576.Google Scholar
  24. Elliger, C.A., Wong, Y., Chan, B.G., andWaiss, A.C., Jr. 1981. Growth inhibitors in tomato (Lycopersicon) to tomato fruitworm(Heliothis zea).J. Chem. Ecol. 7:753–758.Google Scholar
  25. Feeny, P.P. 1976. Plant apparency and chemical defense.Recent Adv. Phytochem. 10:1–40.Google Scholar
  26. Felton, G.W., Duffey, S.S., Vail, P.V., Kaya, H.K., andManning, J. 1987. Interaction of nuclear polyhedrosis virus with catechols: Potential incompatibility for host-plant resistance against noctuid larvae.J. Chem. Ecol. 13:947–957.Google Scholar
  27. Felton, G.W.,Broadway, R.M., andDuffey, S.S. 1989. A paradox of allelochemical interaction: activation of a plant defense by insect feeding inactivates an inducible defense.J. Insect Physiol. In press.Google Scholar
  28. Felton, G.W., andDuffey, S.S. 1990. Inactivation of a baculovirus by quinones formed in insect-damaged plant tissues.J. Chem. Ecol. In press.Google Scholar
  29. Fields, R. 1972. The rapid determination of amino groups with TNBS.Methods Enzymol. 25B:464–468.Google Scholar
  30. Finlay, T.H., Dharmgromgartama, E.D., andPerlmann, G.E., 1973. Mechanism of gossypol inactivation of pesinogen.J. Biol. Chem. 248:4827–4833.Google Scholar
  31. Free, B.L., andSatterlee, L.D. 1975. Biochemical properties of alfalfa protein concentrate.J. Food Sci. 40:85–89.Google Scholar
  32. Gregory, P., andTingey, W.M. 1981. Chemical mechanisms of potato resistance to the leafhop-per. pp. 95–99,in Breeding for Resistance to Insects and Mites, Proc. 2nd Eucarpia/IOBC Meeting of the Working Group Breeding for Resistance to Insects and Mites. Canterbury, England.Google Scholar
  33. Gregory, P., Ave, D.A., Bouthyette, P.Y., andTingey, W.M. 1986. Insect-defensive chemistry of potato glandular trichomes, pp. 173–183,in Sir R. Southwood and B. Juniper (eds.). Insects and the Plant Surface. Edward Arnold, London.Google Scholar
  34. Hagerman, A.E. andButler, L.G. 1981. The specificity of proanthocyanidin-protein interactions.J. Biol. Chem. 256:4494–4497.Google Scholar
  35. Haider, K., Frederick, L.R., andFlaig, W. 1965. Reactions between amino acid compounds and phenols during oxidation.Plant Soil 22:49–64.Google Scholar
  36. Harborne, J.B. 1982. Phytochemical Methods. Chapman and Hall, London. 292 pp.Google Scholar
  37. Haukioja, E., andNiemela, P. 1977. Retarded growth of a geometrid larva after mechanical damage to leaves of its host tree.Ann. Zool. Fenn. 14:48–52.Google Scholar
  38. Hedin, P.A., Jenkins, J.N., Collum, D.H., White, W.H., andParott, W.L. 1983. Mutliple factors in cotton contributing to resistance to the tobacco budworm,Heliothis virescens F., pp. 347–365,in P.A. Hedin (ed.). Plant Resistance to Insects. American Chemical Society, Washington, D.C.Google Scholar
  39. Horigome, T., andKandatsu, T. 1968. Biological value of proteins allowed to react with phenolic compounds in presence of o-diphenol oxidase.Agric. Biol. Chem. 32:1093–1102.Google Scholar
  40. Hurrell, R.F., Finot, P.A., andCuq, J.L. 1982. Protein-polyphenol reactions. 1. Nutritional and metabolic consequences of the reaction between oxidized caffeic acid and the lysine residues of casein.J. Nutr. 47:191–211.Google Scholar
  41. Igarashi, K., andYasui, T. 1985. Oxidation of free methionine and methionine residues in protein involved in the browning reaction of phenolic compounds.Agric. Biol. Chem. 49:2309–2315.Google Scholar
  42. Isman, M.B., andDuffey, S.S. 1982a. Toxicity of tomato phenolic compounds to the fruitworm,Heliothis zea.Entomol. Exp. Appl. 31:370–376.Google Scholar
  43. Isman, M.B., andDuffey, S.S. 1982b. Phenolic compounds in the foliage of commercial tomato cultivars as growth inhibitors to the fruitworm,Heliothis zea.J. Am. Hortic. Sci. 107:167–170.Google Scholar
  44. Isman, M.B., andDuffey, S.S. 1983. Pharmacokinetics of chlorogenic acid and rutin in larvae ofHeliothis zea.J. Insect Physiol. 29:295–300.Google Scholar
  45. Jones, D. 1984. Use, misuse, and role of multiple-comparison procedures in ecological and agricultural entomology.Environ. Entomol. 13:635–649.Google Scholar
  46. Kawakishi, S., andKaneko, T. 1987. Interaction of proteins with allyl isothiocyanate.J. Agric. Food Chem. 35:85–88.Google Scholar
  47. Klun, J.A., Tipton, C.L., andBrindley, T.A. 1967. 2,4-Dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), an active agent in the resistance of maize to the European corn borer.J. Econ. Entomol. 60:1529–1533.Google Scholar
  48. Kreisfeld, K. 1987. Impact of plant protein and oxidative enzymes on antibiosis against larvalSpodoptera exigua (Hubner) (Lepidoptera: Noctuidae). University of California, Davis. MS thesis, 113 pp.Google Scholar
  49. Lange, W.H., andBronson, L. 1981. Insect pests of tomatoes.Annu.Rev. Entomol. 26:345–371.Google Scholar
  50. Lincoln, D.E. 1985. Host-plant protein and phenolic resin effects on larval growth and survival of a butterfly.J. Chem. Ecol. 11:1459–1467.Google Scholar
  51. Lindroth, R.L., andPeterson, S.S. 1988. Effects of plant phenols on performance of southern armyworm larvae.Oecolgia 75:185–189.Google Scholar
  52. Loper, G.M. 1968. Effect of aphid infestation on the coumestrol content of alfalfa varieties differing in aphid resistance.Crop Sci. 8:104–106.Google Scholar
  53. Martin, J.S., Martin, M.M., andBernays, E.A. 1987. Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: Implications for theories of plant defense.J. Chem. Ecol. 13:605–620.Google Scholar
  54. Martin, M.M., andMartin, J.S. 1984. Surfactants: their role in preventing the precipitation of proteins by tannins in insect guts.Oecologia 61:342–345.Google Scholar
  55. Matheis, G., andWhitaker, J.R. 1984. Modification of proteins by polyphenol oxidase and peroxidase and their products.J. Food Biochem. 8:137–162.Google Scholar
  56. Mattoo, R.L., Ishaq, M., andSaleemuddin, M. 1987. Protein assay by coomassie brilliant blue G-250-binding method is unsuitable for plant tissues rich in phenols and phenolases.Anal. Biochem. 163:376–384.Google Scholar
  57. Mattson, W.J. 1980. Herbivory in relation to plant nitrogen content.Annu. Rev. Ecol. Syst. 11:119–161.Google Scholar
  58. Mayer, A.M. 1987. Polyphenol oxidases in plants-recent progress.Phytochemistry 26:11–20.Google Scholar
  59. Mayer, A.M., andHarel, E. 1979. Polyphenol oxidases in plants.Phytochemistry 18:193–215.Google Scholar
  60. McNamus, J., Lilley, T.H., andHaslam, E. 1983. Plant polyphenols and their associations with proteins, pp. 123–137,in P.A. Hedin (ed.). Plant Resistance to Insects. American Chemical Society, Washington, D.C.Google Scholar
  61. Miles, P.W. 1978. Redox reactions of hemipterous saliva in plant tissues.Entomol. Exp. Appl. 24:334–339.Google Scholar
  62. Moore, R.F. 1983. Effect of dietary gossypol on the boll weevil (Coleoptera: Curculionidae).J. Econ. Entomol. 76:696–699.Google Scholar
  63. Motoda, S. 1979. Formation of aldehydes from amino acids by polyphenol oxidase.J. Ferment. Technol. 57:395–399.Google Scholar
  64. Pierpoint, W.S. 1966. The enzymic oxidation of chlorogenic acid and some reactions of the qui-none produced.Biochem. J. 98:567–580.Google Scholar
  65. Pierpoint, W.S. 1969.o-Quinones formed in plant extracts: Their reactions with amino acids and peptides.Biochem. J. 112:609–617.Google Scholar
  66. Pierpoint, W.S. 1983. Reactions of phenolic compounds with proteins, and their relevance to the production of leaf protein, pp. 235–267,in L. Telek and H.D. Graham (eds.). Leaf Protein Concentrates. Avi Publishing, Westport, Connecticut.Google Scholar
  67. Pierpoint, W.S., Ireland, R.J., andCarpenter, J.M. 1977. Modification of proteins during the oxidation of leaf phenols: Reaction of potato virus X with chlorogenoquinone.Phytochemistry 16:29–34.Google Scholar
  68. Raupp, M.J., andDenno, R.F. 1983. Leaf age as a predictor of herbivore distribution and abundance, pp. 91–124,in R.F. Denno and M.S. McClure (eds.). Variable Plants and Herbivores in. Natural and Managed Systems. Academic Press, New York.Google Scholar
  69. Rhoades, D.F. 1977. The antiherbivore chemistry ofLarrea, pp. 135– T.J. Mabry, J.H. Hunziker, and D.R. DiFeo, Jr. (eds.). Cresote Bush. Dowden, Hutchinson and Ross, New York.Google Scholar
  70. Rhoades, D.F. 1983. Responses of alder and willow to attack by tent caterpillars and webworms: Evidence for pheromonal sensitivity of willows.Am. Chem. Soc. Symp. Ser. 208:55–68.Google Scholar
  71. Rhoades, D.F. 1985. Offensive-defensive interactions between herbivores and plants: Their relevance in herbivore population dynamics and ecological theory.Am. Nat. 125:205–238.Google Scholar
  72. Rhoades, D.F., andCates, R.G. 1976. Toward a general theory of plant antiherbivore chemistry.Recent Adv. Phytochem. 10:168–213.Google Scholar
  73. Rhoades, M.J.C., andWooltorton, L.S.C. 1977. Changes in the activity of enzymes of phen-ylpropanoid metabolism in tomatoes stored at low temperatures.Phytochemistry 16:655–659.Google Scholar
  74. Ryan, J.D., Gregory, P., andTingey, W.M. 1982. Phenolic oxidase activities in glandular tri-chomes ofSolatium berthaultii.Phytochemistry 8:1185–1187.Google Scholar
  75. Schultz, J.C., andBaldwin, I.T. 1982. Oak leaf quality declines in response to defoliation by gypsy moth larvae.Science 217:149–151.Google Scholar
  76. Scriber, J.M. 1984. Host-plant suitability, pp. 159–204,in W.J. Bell and R.T. Cardé (eds.). Chemical Ecology of Insects. Sinauer Associates, Inc., Sunderland, Massachusetts.Google Scholar
  77. Scriber, J.M., andSlansky, F., Jr. 1981. The nutritional ecology of immature insects.Annu. Rev. Entomol 26:183–211.Google Scholar
  78. Singleton, V.L. 1981. Naturally occurring food toxicants: Phenolic substances of plant origin common in foods.Adv. Food Res. 27:149–242.Google Scholar
  79. Snyder, J.D., andDesborough, S.L. 1978. Rapid estimation of pototo tuber total protein content with Coomassie brilliant blue G-250.Theor. Appl. Genet. 52:135–139.Google Scholar
  80. Thielges, B.A. 1968. Altered polyphenol metabolism in the foliage ofPinus sylvestris associated with European sawfly attack.Can. J. Bot. 46:724–726.Google Scholar
  81. Waiss, A.C., Chan, B.G., Elliger, C.A., Wiseman, B.R., Mcmillan, W.W., Widstrom, N.W., Zuber, M.S., andKeaster, A.J. 1979. Maysin, a flavone glycoside from com silks with antibiotic activity toward corn earworm.J. Econ. Entomol. 72:256–258.Google Scholar
  82. Waldbauer, G.P. 1968. The consumption and utilization of food by insects.Adv. Insect Physiol. 5:229–288.Google Scholar
  83. Wardel, D.A. 1973. Effect of phenolic compounds inLycopersicon esculentum on the synthesis of ethylene.Phytochemistry 12:1523–1530.Google Scholar
  84. White, T.C.R. 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants.Oecologia 63:90–105.Google Scholar
  85. Widstrom, N.W., Waiss, A.C., Jr., McMillian, W.W., Wiseman, B.R., Elliger, C.A., Zuber, M.S., Straub, R.W., Brewbaker, J.L., Darrah, L.L., Henson, A.R., Arnold, J.M., andOverman, J.L. 1982. Maysin content of silks of nine maize genotypes grown in diverse environments.Crop Sci. 22:953–955.Google Scholar
  86. Zucker, W.V. 1982. How aphids choose leaves: The role of phenolics in host selection by a galling aphid.Ecology 63:972–981.Google Scholar
  87. Zucker, W.V. 1983. Tannins: does structure determine function? An ecological perspective.Am. Nat. 121:335–365.Google Scholar

Copyright information

© Plenum Publishing Corporation 1989

Authors and Affiliations

  • G. W. Felton
    • 1
  • K. Donato
    • 1
  • R. J. Del Vecchio
    • 1
  • S. S. Duffey
    • 1
  1. 1.Department of EntomologyUniversity of California at DavisDavis

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