Proteolytic digestive enzymes and peritrophic membranes during the development of Plodia interpunctella (Lepidoptera: Piralidae): Targets for the action of Soybean Trypsin Inhibitor (SBTI) and Chitin-Binding Vicilin (EvV)

Journal of Agricultural and Food Chemistry

Volumn 56, Issue 17, 2008, Pages 7738-7745

  Amorim, Ticiana M L ^a   Macedo, Leonardo L P ^a   Uchoa, Adriana F ^a   Oliveira, Adeliana S ^a   Pitanga, Joelma C M ^a   Macedo, Francisco P ^a   Santos, Elizeu A ^a   De Sales, Mauricio P ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

Chitin binding vicilina; Erythrina velutina; Peritrophic membrane; Plodia interpunctella; SBTI; Serine proteinases

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE; FLUORESCENT DYE; INSECTICIDE; PEPTIDE HYDROLASE; TRYPSIN INHIBITOR; VEGETABLE PROTEIN; VICILIN PROTEIN, PLANT;

ANIMAL; ARTICLE; CHEMISTRY; ENZYMOLOGY; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; LARVA; LEPIDOPTERA; METABOLISM; PH; SOYBEAN;

ANIMALS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GASTROINTESTINAL TRACT; HYDROGEN-ION CONCENTRATION; INSECTICIDES; LARVA; LEPIDOPTERA; PEPTIDE HYDROLASES; PLANT PROTEINS; SOYBEANS; TRYPSIN INHIBITORS;

ERYTHRINA VELUTINA; GLYCINE MAX; LEPIDOPTERA; PLODIA INTERPUNCTELLA;

EID: 52649126793     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf801224d     Document Type: Article

References (57)

1. Mohandass, S.; Arthur, F. H.; Zhu, K. Y.; Throne, J. E. Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. J. Stored Prod. Res. 2007, 43, 302-311.
2. Rees, D. Insects of Stored Products; CSIRO Publishing: Collingwood, Victoria, 2004.
3. Sales, M. P.; Gerhardt, I. R.; Grossi-de-Sa, M. F.; Xavier, J. Do legume storage proteins play a role in defending seeds against bruchids? Plant Physiol. 2000, 124 (2), 515-522.
4. Botella, M. A.; Xu, Y.; Prabha, T. N.; Zhao, Y.; Narasimhan, M. L.; Wilson, K. A.; Nielsen, S. S.; Bressan, R. A.; Hasegawa, P. M. Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant physiol. 1996, 112 (3), 1201-10.
5. Koiwa, H.; Bressan, R. A.; Hasegawa, P. M. Regulation of protease inhibitors and plant defense. Trends Plant Sci. 1997, 2 (10), 379384(6).
6. Ryan, C. A. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Ann. Rev. Phytol. 1991, 28, 425-449.
7. Sales, M. P.; Pimenta, P. P.; Paes, N. S.; Grossi-de-Sa, M. F.; Xavier, J. Vicilins (7S storage globulins) of cowpea (Vigna unguiculata) seeds bind to chitinous structures of the midgut of Callosobruchus maculatus (Coleoptera: Bruchidae) larvae. Braz. J. Med. Biol. Res. 2001, 34 (1), 27-34.
8. Haq, S. K.; Atif, S. M.; Khan, R. H. Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Arch. Biochem. Biophys. 2004, 431 (1), 145-59.
9. Falco, M. C.; Silva-Filho, M. C. Expression of soybean proteinase inhibitors in transgenic sugarcane plants: effects on natural defense against Diatraea saccharalis. Plant Physiol. Biochem. 2003, 41 (8), 761-766.
10. Pompermayer, P.; Lopes, A. R.; Terra, W. R.; Parra, J. R. P.; Falco, M. C.; Silva, M. C. Effects of soybean proteinase inhibitor on development, survival and reproductive potential of the sugarcane borer, Diatraea saccharalis. Entomol. Exp. Appl. 2001, 99 (1), 79-85.
11. Terra, W. R.; Ferreira, C. Insect digestive enzymes - Properties, compartmentalization and function. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 1994, 109 (1), 1-62.
12. Xavier-Filho, J. Sementes e suas defesas contra insetos. In Projeto Multinacional de Biotecnologia e Alimentos; Organizacão dos Estados Americanos (OEA), 1993; pp 1-31.
13. Tellam, R. L.; Wijffels, G.; Willadsen, P. Peritrophic matrix proteins. Insect Biochem. Mol. Biol. 1999, 29 (2), 87-101.
14. Macedo, L. L. P.; Amorim, T. M. L.; Uchoa, A. F.; Oliveira, A. S.; Ribeiro, J. K. C.; De Macedo, F. P.; Santos, E. A.; De Sales, N. P. Larvicidal effects of a chitin-binding vicilin from Erythrina velutina seeds on the mediterranean fruit fly Ceratitis capitata. J. Agric. Food Chem. 2008, 56 (3), 802-808.
15. Bradford, M. M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72 (1-2), 248-254.
16. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 1951, 193 (1), 265-275.
17. Beynon, R. J.; Bond, J. S. Proteolytic Enzymes: A Practical Approach; IRL Press: Oxford, 1996; p 259.
18. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227 (5259), 680-685.
19. Thorpe, R. Producing Antibodies. In Immunochemistry - Labfax, 1st ed.; Kerr, M. A., Thorpe, R., Eds. BIOS Scientific Publishers Limited: Oxford, U.K., 1994; pp 63-81.
20. Roger, H. J.; Perkins, H. R. Cell Walls of Filamentous Fungi. In Spon: London, 1968; Vol. 23, pp 153-160.
21. Towbin, H.; Staehelin, T.; Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 1979, 76 (9), 4350-4354.
22. Johnston, L. A.; Pearson, R. D.; Leatch, G. Evaluation of an indirect fluorescent-antibody test for detecting babesia-argentina infection in cattle. Aust. Vet. J. 1973, 49 (8), 373-377.
23. Girard, C.; Le Metayer, M.; Bonade-Bottino, M.; Pham-Delegue, M. H.; Jouanin, L. High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochem. Mol. Biol. 1998, 28 (4), 229-237.
24. Koiwa, H.; Shade, R. E.; Zhu-Salzman, K.; D'Urzo, M. P.; Murdock, L. L.; Bressan, R. A.; Hasegawa, P. M. A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett. 2000, 471 (1), 67-70.
25. Lemos, F. J. A.; Campos, F. A. P.; Silva, C. P.; Xavierfilho, J. Proteinases and amylases of larval midgut of Zabrotes subfasciatus reared on cowpea (Vigna unguiculata) seeds. Entomol. Exp. Appl. 1990, 56 (3), 219-227.
26. Silva, C. P.; Xavier-Filho, J. Comparison between the levels of aspartic and cysteine proteinases of the larval midguts of Callosobruchus maculatus (F) and Zabrotes subfasciatus (Boh) (Coleoptera, Bruchidae). Comp. Biochem. Physiol. B 1991, 99 (3), 529-533.
27. Silva, C. P.; Terra, W. R.; Lima, R. M. Differences in midgut serine proteinases from larvae cf the bruchid beetles Callosobruchus maculatus and Zabrotes subfasciatus. Arch. Insect Biochem. Physiol. 2001, 47 (1), 18-28.
28. Johnson, R.; Narvaez, J.; An, G. H.; Ryan, C. Expression of proteinase inhibitor-I and inhibitor-II in transgenic tobacco plants - Effects on natural defense against Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 1989, 86 (24), 9871-9875.
29. Broadway, R. M.; Duffey, S. S. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 1986, 32, 673-680.
30. Mcmanus, M. T.; Burgess, E. P. J. Effects of the soybean (Kunitz) trypsin inhibitor on growth and digestive proteases of larvae of Spodoptera litura. J. Insect Physiol. 1995, 41 (9), 731-738.
31. Purcell, J. P.; Greenplate, J. T.; Sammons, R. D. Examination of midgut luminal proteinase activities in 6 economically important insects. Insect Biochem. Mol. Biol. 1992, 22 (1), 41-47.
32. Casu, R. E.; Jarmey, J. M.; Elvin, C. M.; Eisemann, C. H. Isolation of a trypsin-like serine protease gene family from the sheep blowfly Lucilia cuprina. Insect Mol. Biol. 1994, 3 (3), 159-70.
33. Franco, O. L.; Dias, S. C.; Magalhaes, C. P.; Monteiro, A. C.; Bloch, C., Jr.; Melo, F. R.; Oliveira-Neto, O. B.; Monnerat, R. G.; Grossi-de-Sa, M. F. Effects of soybean Kunitz trypsin inhibitor on the cotton boll weevil (Anthonomus grandis). Phytochemistry 2004, 65 (1), 81-9.
34. Franco, O. L.; dos Santo, R. C.; Batista, J. A. N.; Mendes, A. C. M.; de Araujo, M. A. M.; Monnerat, R. G.; Grossi-de-Sa, M. F.; de Freitas, S. M. Effects of black-eyed pea trypsin/chymotrypsin inhibitor on proteolytic activity and on development of Anthonomus grandis. Phytochemistry 2003, 63 (3), 343-349.
35. Gatehouse, A. M. R.; Boulter, D. Assessment of the antimetabolic effects of trypsin-inhibitors from cowpea (Vigna unguiculata) and other legumes on development of the bruchid beetle Callosobruchus maculatus. J. Sci. Food Agric. 1983, 34 (4), 345-350.
36. Leple, J. C.; Bonadebottino, M.; Augustin, S.; Pilate, G.; Letan, V. D.; Delplanque, A.; Cornu, D.; Jouanin, L. Toxicity to chrysomela tremulae (coleoptera, chrysomelidae) of transgenic poplars expressing a cysteine proteinase-inhibitor. Mol. Breed. 1995, 1 (4), 319-328.
37. Richardson, M. Seed Storage Proteins: The Enzyme Inhibitors. In Methods in Plant Biochemistry; Elsevier: New York, 1991; Vol. 5, pp 259-305.
38. Oliveira-Neto, O. B.; Batista, J. A. N.; Rigden, D. J. F., R. R.; Silva, R. O.; Gomes, E. A.; Franco, O. L.; Dias, S. C.; Cordeiro, C. M. T.; Monnerat, R. G.; Grossi-de-Sa, M. F. A diverse family of serine protease genes expressed in cotton boll weevil (Anthonomus grandis): implications for the design of pest-resistant transgenic cotton plants. Insect Biochem. Mol. Biol. 2004, 34 (9), 903-918.
39. Broadway, R. M. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J. Insect Physiol. 1997, 43 (9), 855-874.
40. Jongsma, M. A.; Bakker, P. L.; Peters, J.; Bosch, D.; Stiekma, W. J. Adaptation of Spodoptera exigua to plant proteinase inhibitors by induction of proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 8041-8045.
41. Giri, A. P.; Harsulkar, A. M.; Deshpande, V. V.; Sainani, M. N.; Gupta, V. S.; Ranjekar, P. K. Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiol. 1998, 116 (1), 393-401.
42. Michaud, D. Avoiding protease-mediated resistance in herbivorous pests. Trends Biotech. 1997, 15 (1), 4-6.
43. Reeck, G.; Oppert, B.; Denton, M.; Kanost, M.; Baker, J.; Kramer, K. Insect Proteinases. In Proteases, New Perspectives; Turk, V., Ed.; Birkhauser: Basel, Switzerland, 1999; pp125-148.
44. Bown, D. P.; Wilkinson, H. S.; Gatehouse, J. A. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem. Mol. Biol. 1997, 27 (7), 625-38.
45. Dennis, M. S.; Herzka, A.; Lazarus, R. A. Potent and selective Kunitz domain inhibitors of plasma kallikrein designed by phage display. J. Biol. Chem. 1995, 270 (43), 25411-7.
46. Jongsma, M. A.; Peters, J.; Stiekema, W. J.; Bosch, D. Characterization and partial purification of gut proteinases of Spodoptera exigua Hübner (Lepidoptera:Noctuidae). Insect Biochem. Mol. Biol. 1996, 26, 623-632.
47. Agrawal, A. A. Ecology - Phenotypic plasticity in the interactions and evolution of species. Science 2001, 294 (5541), 321-326.
48. Macedo, M. L. R.; Fernandes, K. V. S.; Sales, M. P.; Xavier, J. Purification and properties of storage proteins (vicilins) from cowpea (Vigna unguiculata) seeds which are susceptible or resistant to the bruchid beetle Callosobruchus maculatus. Braz. J. Med. Biol. Res. 1995, 28 (2), 183-190.
49. Yunes, A. N. A.; de Andrade, M. T.; Sales, M. P.; Morais, R. A.; Fernandes, K. V. S.; Gomes, V. M.; Xavier-Filho, J. Legume seed vicilins (7S storage proteins) interfere with the development of the cowpea weevil (Callosobruchus maculatus (F)). J. Sci. Food Agric. 1998, 76 (1), 111-116.
50. Sales, M. P.; Gomes, V. M.; Fernandes, K. V. S.; Xavier, J. Chitin-binding proteins from cowpea (Vigna unguiculata) seeds. Braz. J. Med. Biol. Res. 1996, 29 (3), 319-326.
51. Huesing, J. E.; Murdock, L. L.; Shade, R. E. Rice and stinging nettle lectins - insecticidal activity similar to wheat germ agglutinin. Phytochemistry 1991, 30 (11), 3565-3568.
52. Macedo, M. L. R.; Mello, G. C.; Freire, M. D. G. M.; Novello, J. C.; Marangoni, S.; de Matos, D. G. G. Effect of a trypsin inhibitor from Dimorphandra mollis seeds on the development of Callosobruchus maculatus. Plant Physiol. Biochem. 2002, 40 (10), 891-898.
53. Moura, F. T.; Oliveira, A. S.; Macedo, L. L. P.; Vianna, A. L. B. R.; Andrade, L. B. S.; Martins-Miranda, A. S.; Oliveira, J. T. A.; Santos, E. A.; de Sales, M. P. Effects of a chitin-binding vicilin from Enterolobium contortisiliquum seeds on bean bruchid pests (Callosobruchus maculatus and Zabrotes subfasciatus) and phytopathogenic fungi (Fusarium solani and Colletrichum lindemuntianum). J. Agric. Food Chem. 2007, 55 (2), 260-266.
54. Johnson, D. E. Cellular toxicities and membrane binding characteristics of insecticidal crystal proteins from Bacillus thuringiensis toward cultured insect cells. J. Invertebr. Pathol. 1994, 63 (2), 123-129.
55. Higgins, T. J. V.; Chrispeels, M. J.; de Sa, M. F. G. Genetic engineering with alpha-amylase inhibitors makes seeds resistant to bruchids. Seed Sci. Res 1998, 8 (2), 257-263.
56. Czapla, T. H.; Lang, B. A. of plant-lectins on the larval development of european corn-borer (lepidoptera, pyralidae) and southern corn-rootworm (coleoptera, chrysomelidae). J. Econ. Entomol. 1990, 83 (6), 2480-2485.
57. Eisemann, C. H.; Donaldson, R. A.; Pearson, R. D.; Cadogan, L. C.; Vuocolo, T.; Tellam, R. L. Larvicidal activity of lectins on Lucilia cuprina - mechanism of action. Entomol. Exp. Appl. 1994, 72 (1), 1-10.