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INSECT PROTEASES, PLANT PROTEASE INHIBITORS, AND POSSIBLE PEST CONTROL

Published online by Cambridge University Press:  31 May 2012

Jon G. Houseman ,
A.M. Larocque  and
N.M.R. Thie
Jon G. Houseman
Affiliation:
Ottawa-Carleton Institute of Biology, Biology Department, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5
A.M. Larocque
Affiliation:
Ottawa-Carleton Institute of Biology, Biology Department, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5
N.M.R. Thie
Affiliation:
Ottawa-Carleton Institute of Biology, Biology Department, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5
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Abstract

Since the first observation that plants contained protease inhibitors, as identified by their ability to inhibit vertebrate enzymes, it has been postulated that the presence of these substances was related to their phytoprotective abilities. However the following assumptions (1) that phytophagous insects use trypsin, and (2) that ingested inhibitors disrupt digestive proteolysis in insects, have not been adequately tested. Identification of non-tryptic enzymes, cathepsin B, D, and H in phytophagous Coleoptera and unique trypsin-like enzymes in Lepidoptera, indicates insect proteases may differ from their vertebrate counterparts. Putative inhibitor proteins inhibited vertebrate trypsin and chymotrypsin in vitro but had no effect on the trypsin- or chymotrypsin-like activity from the insect midgut. Feeding experiments with the European corn borer, Ostrinia nubilalis (Hübner), indicate that ingestion of inhibitors may not disrupt digestive proteolysis in vivo and the vertebrate trypsin inhibitor in corn may be ineffective as a phytoprotective strategy for this insect. Limitations and implications of ingested inhibitors for future pest control may depend on the origin of the inhibitor, as well as the insect's response.

Résumé

Depuis qu'il a été remarqué pour la première fois que les plantes renferment les inhibiteurs des proteases, comme cela a été signalé par leurs capacités de perturber l'action des enzymes des vertébrés, la présence de ces substances a été posée comme principe relié à leurs capacités phytoprotectrices. Cependant, les hypothèses n'ont pas été suffisamment mises à l'épreuve en ce qui concerne ce principe, à savoir : (1) que les insectes phytophages utilisent la trypsine et (2) que les inhibiteurs ingérés perturbent la protéolyse digestive chez les insectes. L'identification d'enzymes non-tryptiques, les cathepsines B, D et H chez les Coléoptères phytophages et des enzymes exceptionnelles semblables à la trypsine chez les Lépidoptères signale que les protéases des insectes pourraient se distinguer de leurs contreparties chez les vertébrés. Des protéines inhibitrices putatives ont perturbé l'action de la trypsine et la chymotrypsine des vertébrés in vitro, mais elles n'avaient aucun effet sur l'activité des enzymes semblables à la trypsine ou la chymotrypsine de l'intestin des insectes. Les tests de nutrition en utilisant la pyrale de maïs, Ostrinia nubilalis (Hübner), ont démontré que l'ingestion d'inhibiteurs ne perturbera peut-être pas la protéolyse digestive in vivo et que l'inhibiteur de la trypsine des vertébrés dans le maïs pourrait s'avérer inefficace comme stratégie phytoprotectrice chez cet insecte. Les limitations et les implications des inhibiteurs ingérés dans la lutte contre les insectes pourrait dépendre de l'origine de l'inhibiteur, aussi bien que de la réaction de l'insecte. [Traduit par la rédaction]

Type
Research Article
Information
The Memoirs of the Entomological Society of Canada , Volume 123 , Supplement S159 , 1991 , pp. 3 - 11
Copyright
Copyright © Entomological Society of Canada 1991

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Footnotes

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Author to whom correspondence should be addressed.

References

Akov, S. 1972. Protein digestion in haematophagous insects, pp. 531–540in Rodriguez, J.G. (Ed.), Insect and Mite Nutrition. North-Holland Biomedical Press, Amsterdam.Google Scholar
Ahmad, Z., Saleemuddin, M., and Siddiqi, M.. 1976. Alkaline protease in the larvae of the army worm, Spodoptera litura. Insect Biochem. 6: 501–505.Google Scholar
Applebaum, S.W. 1985. pp. 279–311in Kerkut, G.A., and Gilbert, L.I. (Eds.), Biochemistry of Digestion in Comparative Physiology, Biochemistry and Pharmacology of Insects. Vol. 4. Pergamon Press, London.Google Scholar
Baker, J.E. 1981 a. Resolution and partial characterization of the digestive proteinases from larvae of the black carpet beetle, pp. 283–315in Bhaskaran, G., Friedman, S., and Rodriguez, J.G. (Eds.), Current Topics in Insect Endocrinology and Nutrition. Plenum Press, New York, NY.Google Scholar
Baker, J.E. 1981 b. Isolation and properties of digestive carboxypeptidases from midgut of larvae of the Black carpet beetle Attagenus megatoma. Insect Biochem. 11: 583–591.Google Scholar
Baker, J.E. 1982. Digestive proteases of Sitophilus weevils (Coleoptera: Curculionidae) and their response to inhibitors from wheat and corn flour. Can. J. Zool. 60: 3206–3214.Google Scholar
Baker, J.E., and Woo, S.M. 1981. Properties and specificities of a digestive aminopeptidase from larvae of Attagenus megatoma (Coleoptera: Dermestidae). Comp. Biochem. Physiol. 69B: 189–193.Google Scholar
Baker, J.E., Woo, S.M., and Mullen, M.A. 1984. Distribution of proteases and carbohydrases in the midgut of larvae of the sweetpotato weevil Cyclas formicarius elegantus and response of proteinases to inhibitors from sweet potato. Entomologia exp. appl. 36: 97–105.Google Scholar
Barrett, A.J., and McDonald, J.K. 1980. Mammalian Proteases. A Glossary and Bibliography. Vol. I. Endo-proteinases. Academic Press, New York, NY.Google Scholar
Berenbaum, M. 1980. Adaptive significance of midgut pH in larval Lepidoptera. Am. nat. 115: 138–146.Google Scholar
Bramhall, S.N., Noack, N., Wu, M., and Loewenberg, J.R. 1969. A simple colormetric method for determining protein. Anal. Biochem. 31: 146–148.Google Scholar
Broadway, R.M., and Duffey, S.S. 1986. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 32: 673–680.Google Scholar
Bryant, J., Green, T.R., Gurusaddaiah, T., and Ryan, C.A. 1976. Proteinase inhibitor II from potatoes: Isolation and characterization of its protomer components. Biochemistry 154: 3418–3424.Google Scholar
Chen, I., and Mitchell, H.L. 1973. Trypsin inhibitors in plants. Phytochemistry 12: 327–330.Google Scholar
Christeller, J.T., Shaw, B.D., Gardiner, S.E., and Dymock, J.. 1989. Partial purification and characterization of the major midgut proteases of grass grub larvae (Costelytra zealandica, Coleoptera: Scarabaeidae). Insect Biochem. 19: 221–231.Google Scholar
Colepicolo-Neto, P., Bechara, E.J.H., Ferreira, C., and Terra, W.R. 1987. Digestive enzymes in close and distant genera of a same family: Properties of midgut hydrolases from luminescent Pyrophorus divergens (Coleoptera: Elateridae) larvae. Comp. Biochem. Physiol. 87B: 755–759.Google Scholar
Dow, J.A.T. 1986. Insect midgut structure. Adv. Insect Physiol. 19: 187–328.Google Scholar
Eguchi, M., and Iwamoto, A.. 1976. Alkaline proteases in the midgut tissue and digestive fluid of the silkworm, Bombyx mori. Insect Biochem. 6: 491–496.Google Scholar
Gatehouse, A.M.R., Butler, K.J., Fenton, K.A., and Gatehouse, J.A. 1985. Presence and partial characterisation of a major proteolytic enzyme in the larval gut of Callosobruchus maculatus. Entomologia exp. appl. 39: 279–286.Google Scholar
Gooding, R.H. 1975. Digestive enzymes and their control in haematophagous arthropods. Ada trop. 32: 96–111.Google Scholar
Gooding, R.H. 1977. Digestive processes in haematophagous insects: Secretion of trypsin and carboxypeptidase B by Glossina morsitans morsitans Westwood. Can. J. Zool. 55: 215–222.Google Scholar
Gooding, R.H., and Huang, C.T. 1969. Trypsin and chymotrypsin from the beetle Pterostichus melanarius. J. Insect Physiol. 15: 325–339.Google Scholar
Green, T.R., and Ryan, C.A. 1972. Wound induced proteinase inhibitors in plant leaves: A possible defense mechanism against insects. Science 175: 776–777.Google Scholar
Hamed, M.B.B., and Attias, J.. 1987. Isolation and partial characterization of two alkaline proteases of the greater wax moth Galleria mellonella (L.). Insect Biochem. 17: 653–658.Google Scholar
Heimburger, N. 1975. Proteinase inhibitors of human plasma — Their properties and control functions, pp. 367–386 in Reich, E., Rifkin, D.B., and Shaw, E. (Eds.), Proteases and Biological Control. Cold Spring Harbor Laboratory, Cold Spring Harbor.Google Scholar
Hochstrasser, K., Muss, M., and Werle, E.. 1967. Reindarstellung und charakterisierung des trypsin-inhibitors aus mais. Hoppe-Seyer's Z. Physiol. Chem. 348: 1337–1340.Google Scholar
House, H.L. 1974. Digestion, pp. 63–117in Rockstein, M. (Ed.), The Physiology of Insecta. Vol. 5. Academic Press, New York, NY.Google Scholar
Houseman, J.G. 1978. A thiol activated digestive proteinase from adults of Rhodnius prolixus Stal. Can. J. Zool. 56: 1140–1143.Google Scholar
Houseman, J.G., Aresta, F., Mark, W.A., and Morrison, P.E. 1988. Effect of fractionated blood components on trypsin activity in the stable fly, Stomoxys calcitrans (L.) (Diptera: Muscidae). Can. J. Zool. 66: 1180–1190.Google Scholar
Houseman, J.G., Campbell, F.C., and Morrison, P.E. 1987. A preliminary characterization of digestive proteases in the posterior midgut of the stable fly Stomoxys calcitrans (L.) (Diptera: Muscidae). Insect Biochem. 17: 213–218.Google Scholar
Houseman, J.G., and Downe, A.E.R. 1980. Endoproteinase activity in the posterior midgut of Rhodnius prolixus Stal (Hemiptera: Reduviidae). Insect Biochem. 10: 363–366.Google Scholar
Houseman, J.G., and Downe, A.E.R. 1981. Identification and partial characterization of digestive proteinases from Triatoma phyllosoma pallidipennis Stal (Hemiptera: Reduviidae). Insect Biochem. 10: 363–366.Google Scholar
Houseman, J.G., and Downe, A.E.R. 1982. Identification and partial characterization of digestive proteinases from two species of bedbug (Hemiptera: Cimicidae). Can. J. Zool. 60: 1837–1840.Google Scholar
Houseman, J.G., and Downe, A.E.R. 1983. Cathepsin D-like activity in the posterior midgut of Hemipteran insects. Comp. Biochem. Physiol. 75B: 509–512.Google Scholar
Houseman, J.G., Downe, A.E.R., and Morrison, P.E. 1985. Similarities in digestive proteinase production in Rhodnius prolixus (Hemiptera: Reduviidae) and Stomoxys calcitrans (Diptera: Muscidae). Insect Biochem. 15: 471–474.Google Scholar
Houseman, J.G., MacNaughton, W.K., and A.Downe, E.R. 1985. Cathepsin B and aminopeptidase activity in the posterior midgut of Euschistus euschistoides (Vollenhoven) (Hemiptera: Pentatomidae). Can. Ent. 116: 1393–1396.Google Scholar
Houseman, J.G., Morrison, P.E., and Downe, A.E.R. 1985. Cathepsin B and aminopeptidase in the posterior midgut of Phymata wolffi Stal (Hemiptera: Phymatidae). Can. J. Zool. 63: 1288–1291.Google Scholar
Houseman, J.G., Philogène, B.J.R., and Downe, A.E.R. 1989. Partial characterization of proteinase activity in the larval midgut of the European corn borer, Ostrinia nubilalis Hubner (Lepidoptera: Pyralidae). Can. J. Zool. 67: 864–868.Google Scholar
Kitch, L.W., and Murdock, L.L. 1986. Partial characterization of a major gut thiol proteinase from larvae of Callosobruchus maculatus F. Arch. Insect Biochem. Physiol. 3: 561–575.Google Scholar
Klocke, J.A., and Chan, B.G. 1982. Effects of cotton condensed tannin on feeding and digestion in the cotton pest Heliothis zea. J. Insect Physiol. 28: 911–915.Google Scholar
Langley, P.A. 1966. The control of digestion in the tsetse fly, Glossina morsitans. Enzyme activity in relation to the size and nature of the meal. J. Insect Physiol. 12: 439–448.Google Scholar
Larocque, A.M. 1989. Interaction between protease inhibitors and proteases of European corn borer larvae Ostrinia nubilalis Hubner (Lepidoptera: Pyralidae). M.Sc. thesis, University of Ottawa, Ottawa, Ont., Canada.Google Scholar
Larocque, A.M., and Houseman, J.G. 1990. The effect of ingested soybean, ovomucoid and corn trypsin inhibitor on digestive processes of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). J. Insect Physiol. 36: 691–697.Google Scholar
Law, J.H., Dunn, P.E., and Kramer, K.J. 1977. Insect proteases and peptidases. Adv. Enzymol. 45: 389–425.Google Scholar
Leiner, I.E., and Kakade, M.L. 1980. Protease inhibitors, pp. 7–71in Leiner, I.E. (Ed.), Toxic Constituents of Plant Foodstuffs.Google Scholar
Levinsky, H., Birk, Y., and Applebaum, S.W. 1977. Isolation and characterization of a new trypsin-like enzyme from Tribolium molitor L. larvae. Int. J. Peptide Protein Res. 10: 252–264.Google Scholar
McDonald, J.K., and Barrett, A.J. 1980. Mammalian Proteases. A Glossary and Bibliography. Vol. I. Exoproteinases. Academic Press, New York, NY.Google Scholar
McFarlane, J.E. 1985. Nutrition and digestive organs, pp. 59–89in Blum, M.S. (Ed.), Fundamentals of Insect Physiology. John Wiley and Sons, New York, NY.Google Scholar
Melville, C.J., and Ryan, C.A. 1971. Chymotrypsin inhibitor I from potatoes. J. Biol. Chem. 247: 3445–3453.Google Scholar
Murdock, L.L., Brookhart, G., Dunn, P.E., Foard, D.E., Kelley, S., Kitch, L., Shade, R.E., Shukle, R.H., and Wolfson, J.L. 1987. Cysteine digestive proteinases in Coleoptera. Comp. Biochem. Physiol. 87B: 783–787.Google Scholar
Pritchett, D.W., Young, S.Y., and Geren, C.R. 1981. Proteolytic activity in the digestive fluid of larvae of Tricholpusia ni. Insect Biochem. 11: 523–526.Google Scholar
Ryan, C.A. 1989. Proteinase inhibitor gene families: Strategies for transformation to improve plant defenses against herbivores. BioEssays 10: 20–24.Google Scholar
Sasaki, T., Morishita, M., and Ise, M.. 1985. Cleavage site specificities of silkworm alkaline proteases. Agric. Biol. Chem. 49: 2707–2710.Google Scholar
Shambaugh, G.F. 1954. Protease stimulation by foods in adult Aedes aegypti (L.) Ohio. Science 54: 151–160.Google Scholar
Storey, R.D., and Wagner, F.W. 1986. Plant proteases: A need for uniformity. Phytochemistry 25: 2701–2709.Google Scholar
Swartz, M.J., Mitchell, H.L., Cox, D.J., and Reek, G.R. 1977. Isolation and characterization of trypsin inhibitor from opaque-2 corn seeds. J. Biol. Chem. 252: 8105–8107.Google Scholar
Thie, N.M.R., and Houseman, J.G. 1990. Identification of cathepsin B, D and H in the larval midgut of Colorado potato beetle, Leptinotarsa decemlineata SAY (Coleoptera: Chrysomelidae). Insect Biochem. 20: 313–318.Google Scholar
Zwilling, R. 1968. Zur Evolution der Endopeptidasen — IV. α-und β-Protease aus Tenebrio molitor. Z. Physiol. Chem. 349: 326–332.Google Scholar
Zwilling, R., Medugorac, I., and Mella, K.. 1972. The evolution of endopeptidases — XIV. Nontryptic cleavage specificity of a BAEE-hydrolyzing enzyme (β-protease) from Tenebrio molitor. Comp. Biochem. Physiol. 43B: 419–424.Google Scholar