Abstract
Previously it was reported that significant amounts of the tomato phenolic, chlorogenic acid, were oxidized in the digestive system of generalist feedersSpodoplera exigua andHelicoverpa zea. The covalent binding of the oxidized phenolic (i.e., quinone) to dietary protein exerts a strong antinutritive effect against larvae. In this study, we examined the fate of ingested chlorogenic acid in larvalManduca sexta, a leaf-feeding specialist of solanaceous plants. Significant amounts of chlorogenic acid were bound to excreted protein byM. sexta when larvae fed on tomato foliage. However, in the case ofM. sexta we suggest that the strong alkalinity and detergency of the midgut may minimize the antinutritive effects of oxidized phenolics. The solubility of tomato leaf protein is significantly greater at pH 9.7, representative of the midgut ofM. sexta, than at pH 8.0, representative of the midguts ofH. zea and S. exigua. We suggest that this increase in solubility would compensate for any loss in bioavailability of essential amino acids caused by the covalent binding of chlorogenic acid to amino acids. Furthermore, lysolecithin, a surfactant likely to contribute to the detergent properties of the midgut fluid, was shown to enhance protein solubility as well as inhibit polyphenol oxidase activity. The adaptive significance of gut alkalinity and detergency is discussed.
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References
Appel, H.M. andMartin, M.M. 1990. Gut redox conditions in herbivorous lepidopteran larvae.J. Chem. Ecol. 16:3277–3290.
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.
Barbeau, W.E., andKinsella, J.E. 1985. Effects of free and bound chlorogenic acid on the in vitro digestibility of ribulose bisphosphate carboxylase from spinach.J. Food Sci. 50:1083–1100.
Berenbaum, M. 1980. Adaptive significance of midgut pH in larval lepidoptera.Am. Nat. 115:138–146.
Betschart, A., andKinsella, J.E. 1973. Extractability and solubility of leaf protein.J. Agric. Food Chem. 21:60–64.
Blytt, H.J., Guscar, T.K., andButler, L.G. 1988. Antinutritional effects and ecological significance of dietary condensed tannins may not be due to binding and inhibiting digestive enzymes.J. Chem. Ecol. 14:1455–1465.
Broadway, R.M., Duffey, S.S., Pearce, G., andRyan, C.A. 1986. Plant proteinase inhibitors: A defence against herbivorous insects?Entomol. Exp. Appl. 24:94–100.
Brodbeck, B.V., andStrong, D.R. 1987. Amino acid nutrition of herbivorous insects and stress to host plants, pp. 347–364,in P. Barbosa and J.C. Schultz (eds.). Insect Outbreaks. Academic Press, New York.
Chippendale, G.M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borerDiatraea grandiosella.J. Insect Physiol. 16:1057–1068.
Ciliers, J.J.L., andSingleton, V.L. 1989. Nonenzymic autoxidative phenolic browning reactions in a caffeic acid model system.J. Agric. Food Chem. 37:890–896.
Dow, J.A.T. 1984. Extremely high pH in biological systems: a model for carbonate transport.Am. J. Physiol. 246R:633–635.
Duffey, S.S., andFelton, G.W. 1989. Role of plant enzymes in resistance to insects, pp. 289–313,in J. Whitaker and P. Sonnet (eds.). Biocatalysis in Agricultural Biotechnology. American Chemical Society, Washington, D.C.
Feeny, P.P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:561–581.
Felton, G.W., andDuffey, S.S. 1990. Inactivation of a baculovirus by quinones formed in insectdamaged plant tissues.J. Chem. Ecol. 16:1221–1236.
Felton, G.W., Donato, K., Del Vecchio, R.J., andDuffey, S.S. 1989a. Activation of plant foliar oxidases by insect feeding reduces the nutritive quality of foliage for noctuid herbivores.J. Chem. Ecol. 15:2667–2694.
Felton, G.W., Broadway, R.M., andDuffey, S.S. 1989b. Inactivation of protease inhibitors by plant-derived quinones: Complications for host-plant resistance against noctuid herbivores.J. Insect Physiol. 35:981–990.
Finot, P.A. 1983. Influence of processing on the nutritional value of proteins.Qual. Plant Foods Hum. Nutr. 32:439–453.
Friedman, M. 1982. Lysinoalanine formation in soybean proteins: Kinetics and mechanisms, pp. 231–273,in Food Protein Deterioration. Mechanisms and Functionality. J.P. Cherry (ed.). American Chemical Society, Washington, D.C.
Fujita, S., andTono, T. 1988. Purification and some properties of polyphenol oxidase in eggplant (Solanum melongela).J. Sci. Food Agric. 46:115–123.
Gentile, I.A., Ferraris, L., andMatta, A. 1988. Variations of polyphenoloxidase activities as a consequence of stresses that induce resistance toFusarium wilt of tomato.J. Phytopathol. 122:45–53.
Hare, J.D. 1983. Manipulation of host suitability for herbivore pest management, pp. 655–680,in R.F. Denno and M.S. McClure (eds.). Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.
Haslam, E. 1988. Plant polyphenols (syn. vegetable tannins) and chemical defense—a reappraisal.J. Chem. Ecol. 14:1789–1805.
Hurrell, R.F., andFinot, P.A. 1985. Effects of food processing on protein digestibility and amino acid availability, pp. 233–246,in J.W. Finley and D.T. Hopkins (eds.). Digestibility and Amino Acid Availability in Cereals and Oilseeds. American Association of Cereal Chemists, St. Paul, Minnesota.
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.
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.
Isman, M.B., andDuffey, S.S. 1983. Pharmacokinetics of chlorogenic acid and rutin in larvae ofHeliothis zea.J. Insect Physiol. 29:295–300.
Jones, C.G., Hare, J.D., andCompton, S.J. 1989. Measuring plant protein with the Bradford assay. 1. Evaluation and standard method.J. Chem. Ecol. 15:979–992.
Kalyanaraman, B., Premovic, P.I., andSealy, R.C. 1987. Semiquinone anion radicals from the addition of amino acids, peptides, and proteins to quinones derived from the oxidation of catechols and catecholamines.J. Biol. Chem. 262:11080–11087.
Kang, K., Choo, Y., andKim, K. 1983. Enzymatic discoloration of raw potato tubers: With special reference to the formation and inhibition of dopachrome.Am. Potato J. 60:451–460.
Lange, W.H., andBronson, L. 1981. Insect pests of tomato.Annu. Rev. Entomol. 26:345–371.
Martin, J.S., andMartin, M.M. 1983. Tannin assays in ecological studies: Precipitation of ribulose-1,5-bisphosphate carboxylase/oxygenase by tannic acid, quebracho, and oak foliage extracts.J. Chem. Ecol. 9:285–294.
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.J. Chem. Ecol. 13:605–621.
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.
Mattson, W.J. 1980. Herbivory in relation to nitrogen content.Annu. Rev. Ecol. Syst. 11:119–161.
Mayer, A.M. 1987. Polyphenol oxidases in plants-recent progress.Phytochemistry 26:11–20.
Mayer, A.M., andHarel, E. 1979. Polyphenol oxidases in plants.Phytochemistry 8:193–215.
Meyer, H.-U., andBiehl, B. 1981. Activation of latent phenolase during spinach leaf senescence.Phytochemistry 20:955–959.
Mole, S., andWaterman, P.G. 1985. Stimulatory effects of tannins and cholic acid on tryptic hydrolysis of proteins: Ecological implications.J. Chem. Ecol. 11:1323–1332.
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 Publ. Westport, Connecticut.
Rock, G.C., andHodgson, E. 1971. Dietary amino acid requirements forHeliothis zea determined by dietary deletion and radiometric techniques.J. Insect Physiol. 17:1087–1097.
Ryan, J.D., Gregory, P., andTingey, W.M. 1982. Phenolic oxidase activities in glandular trichomes ofSolanum berthaultii.Phytochemistry 21:1885–1887.
Sandstrom, R.P., andCleland, R.E. 1989. Selective delipidation of plasma membrane by surfactants.Plant Physiol. 90:1524–1531.
Sharma, R.C., andAli, R. 1980. Isolation and characterization of catechol oxidase fromSolanum melongena.Phytochemistry 19:1597–1600.
Singer, S.J., Eggman, L., Campbell, J.M., andWildman, S.G. 1952. The proteins of green leaves. IV. A high molecular weight protein comprising a large part of the cytoplasmic proteins.J. Biol. Chem. 197:233–239.
Terra, W.R. 1988. Physiology and biochemistry of insect digestion: An evolutionary perspective.Braz. J. Med. Biol. Res. 21:675–734.
Whitaker, J.R., andFeeney, R.E. 1983. Chemical and physical modification of proteins by the hydroxide ion.CRC Crit. Rev. Food Sci. Nutr. 19:173–212.
White, T.C.R. 1978. The importance of a relative shortage of food in animal ecology.Oecologia 33:71–86.
Woodham, A.A. 1983. The nutritional evaluation of leaf protein concentrates, pp. 415–433,in L. Telek and H.D. Graham (eds.). Leaf Protein Concentrates. Avi Publ., Westport, Connecticut.
Zucker, W.V. 1983. Tannins: does structure determine function? An ecological perspective.Am. Nat. 121:335–365.
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Felton, G.W., Duffey, S.S. Reassessment of the role of gut alkalinity and detergency in insect herbivory. J Chem Ecol 17, 1821–1836 (1991). https://doi.org/10.1007/BF00993731
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DOI: https://doi.org/10.1007/BF00993731