Abstract
Trypsin and chymotrypsin inhibitors are proteins that are developmentally regulated in foliage of cabbage plants, appearing at high concentrations in young foliage on mature plants. This temporal and spacial regulation of foliar proteinase inhibitors is synchronized with the appearance and distribution of foliar feeding Lepidoptera. When insects were allowed to select their feeding sites, larvalPieris rapae fed on the young foliage of cabbage plants, while larvalTrichoplusia ni fed on the mature foliage on cabbage plants. LarvalP. rapae that fed on mature plants were significantly smaller than larvae feeding on young plants, while there was no significant difference between larvalT. ni feeding on mature plants and those feeding on young plants. Thus, there was a significant inverse correlation between the level of proteinase inhibitory activity in cabbage foliage and larval growth. WhenP. rapae andT. ni were provided with an artificial diet containing total protein (including significant levels of proteinase inhibitors) that was extracted from cabbage foliage, there was a significant reduction in growth and development of both species of Lepidoptera.
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References
Andaloro, J.T., Shelton, A.M., andEckenrode, C.J. 1982. Seasonal abundance of lepidopterous larvae in commercial cabbage fields.Environ. Entomol. 11:144–146.
Andaloro, J.T.,Rose, K.B.,Shelton, A.M.,Hoy, C.W., andBecker, R.F. 1983. Cabbage growth stages.New York's Food and Life Sciences Bulletin 101.
Birk, Y., andApplebaum, S.W. 1960. Effect of soybean trypsin inhibitors on the development and midgut proteolytic activity ofTribolium castaneum larvae.Enzymologia 22:318–326.
Blau, P.A., Feeny, P., Contardo, L., andRobson, D.S. 1978. Allylglucosinolate and herbivorous caterpillars: A contrast in toxicity and tolerance.Science 200:1296–1298.
Boodley, J.W., andSheldrake, R., Jr. 1977. Cornell peat-lite mixes for commercial plant growing.Cornell Inform. Bull. 43:1–8.
Broadway, R.M. 1989a. Characterization and ecological implications of midgut proteolytic activity in larvalPieris rapae andTrichoplusia ni.J. Chem. Ecol. 15:2101–2113.
Broadway, R.M. 1989b. Tryptic inhibitory activity in wild and cultivated crucifers.Phytochemistry 28:755–758.
Broadway, R.M., andDuffey, S.S. 1986. 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.
Broadway, R.M., andMissurelli, D.L. 1990. Regulatory mechanisms of tryptic inhibitory activity in cabbage plants.Phytochemistry 29:3721–3725.
Broadway, R.M., Duffey, S.S., Pearce, G., andRyan, C.A. 1986. Plant proteinase inhibitors: A defense against herbivorous insects?Entomol. Exp. Appl. 41:33–38.
Christeller, J.T., andShaw, B.D. 1989. The interaction of a range of serine proteinase inhibitors with bovine trypsin andCostelytra zealandica trypsin.Insect Biochem. 19:233–241.
Erickson, J.M., andFeeny, P. 1974. Sinigrin: A chemical barrier to the black swallowtail butterfly,Papilio polyxenes. Ecology 55:103–111.
Feeny, P. 1977. Defensive ecology of the Cruciferae.Ann. Mo. Bot. Gard. 64:221–234.
Gatehouse, A.M.R., Butler, K.J., Fenton, K.A., andGatehouse, J.A. 1985. Presence and partial characterisation of a major proteolytic enzyme in the larval gut ofCallosobruchus maculatus.Entomol. Exp. Appl. 39:279–286.
Green, T.R., andRyan, C.A. 1972. Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects.Science 175:776–777.
Heaney, R.K., andFenwick, G.R. 1981. A micro-column method for the rapid determination of total glucosinolate content of cruciferous material.Z. Pflanzenzuchtg. 87:89–95.
Hines, M.E., Osuala, C.I., andNielsen, S.S. 1991. Isolation and partial characterization of a soybean cystatin cysteine proteinase inhibitor of coleopteran digestive proteolytic activity.J. Agr. Food Chem. 39:1515–1520.
Hoy, C.W., andShelton, A.M. 1987. Feeding response ofArtogeia rapae (Lepidoptera: Pieridae) andTrichoplusia ni (Lepidoptera: Noctuidae) to cabbage leaf age.Environ. Entomol. 16:680–682.
Johnson, R., Narvaez, J., An, G., andRyan, C. 1989. Expression of proteinase inhibitors I and II in transgenic tobacco plants: Effects on natural defense againstManduca sexta larvae.Proc. Natl. Acad. Sci. USA 86:9871–9875.
Laskowski, M., andKato, I. 1980. Protein inhibitors of proteinases.Annu. Rev. Biochem. 49:593–626.
Oleszek, W. 1987. Allelopathic effects of volatiles from some Cruciferae species on lettuce, barnyard grass and wheat growth.Plant Soil 102:271–273.
Pearce, G., Strydom, D., Johnson, S., andRyan, C.A. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins.Science 253:895–898.
Ryan, C.A. 1978. Proteinase inhibitors in plant leaves: A biochemical model for pest-induced natural plant protection.TIBS 3:148–150.
Ryan, C.A. 1989. Proteinase inhibitor gene families: Strategies for transformation to improve plant defenses against herbivores.BioEssays 10:20–24.
Ryan, C.A., andWalker-Simmons, M. 1981. Plant Proteinases, pp. 321–350,in P.K. Stumpf and E.E. Conn (eds.). The Biochemistry of Plants. Academic Press, New York.
Shukle, R.H., andMurdock, L.L. 1983. Lipoxygenase, trypsin inhibitor, and lectin from soybeans: Effects on larval growth ofManduca sexta (Lepidoptera: Sphingidae).Environ. Entomol. 12:787–791.
Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J., andKlenk, D.C. 1985. Measurement of protein using bicinchoninic acid.Anal. Biochem. 150:76–85.
Steffens, R., Fox, F.R., andKassell, B. 1978. Effect of trypsin inhibitors on growth and metamorphosis of corn borer larvaeOstrinia nubilalis (Hubner).J. Agr. Food Chem. 26:170–174.
Walsh, K.A. 1970. Trypsinogens and trypsin of various species, Chap. 4,in G.E. Perlmann, and L. Lorand (eds.). Methods in Enzymology. Academic Press, New York.
Walsh, K.A., andWilcox, P.E. 1970. Serine proteases, pp. 31–34,in G.E. Perlmann and L. Lorand (eds.). Methods in Enzymology. Academic Press, New York.
Whitaker, J.R. 1981. Naturally occurring peptides and protein inhibitors of enzymes, pp. 57–104,in J.C. Ayres and J.C. Kirschman (eds.). Impact of Toxicology on Food Processing. AVI, Westport, CT.
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Broadway, R.M., Colvin, A.A. Influence of cabbage proteinase inhibitorsin situ on the growth of larvalTrichoplusia ni andPieris rapae . J Chem Ecol 18, 1009–1024 (1992). https://doi.org/10.1007/BF00980059
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DOI: https://doi.org/10.1007/BF00980059