Impact of cysteine proteinase inhibition in midgut fluid and oral secretion on fecundity and pollen consumption of western corn rootworm (Diabrotica virgifera virgifera)

Archives of Insect Biochemistry and Physiology

Volumn 52, Issue 3, 2003, Pages 139-154

  Kim, Jae Hak ^a,b   Mullin, Christopher A ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Corn pollen feeding; Cysteine PLS; Diabrotica virgifera virgifera; E 64; Fecundity; Midgut fluid; Oral secretion; Weight

Indexed keywords

COLEOPTERA; DIABROTICA; DIABROTICA VIRGIFERA VIRGIFERA; ZEA MAYS;

CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; DRUG DERIVATIVE; LEUCINE; LEUPEPTIN; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; N ACETYLLEUCYL LEUCYL METHIONINAL; N-ACETYLLEUCYL-LEUCYL-METHIONINAL; OLIGOPEPTIDE;

ANIMAL; ARTICLE; BEETLE; DIGESTIVE SYSTEM; DRUG EFFECT; EATING; ENZYMOLOGY; FEMALE; FERTILITY; MAIZE; MALE; METABOLISM; PHYSIOLOGY; POLLEN;

ANIMALS; BEETLES; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; DIGESTIVE SYSTEM; EATING; FEMALE; FERTILITY; LEUCINE; LEUPEPTINS; MALE; OLIGOPEPTIDES; POLLEN; ZEA MAYS;

EID: 0037365970     PISSN: 07394462     EISSN: None     Source Type: Journal    
DOI: 10.1002/arch.10074     Document Type: Article

References (45)

1. Ashouri A, Overney S, Michaus D, Cloutier C. 1998. Fitness and feeding are affected in the two-spotted stinkbug, Perillus bioculatus, by the cysteine proteinase inhibitor, oryzacystatin I. Arch Insect Biochem Physiol 38:74-83.
2. Bolter CJ, Latoszek-Green M. 1997. Effect of chronic ingestion of the cysteine proteinase inhibitor, E-64, on Colorado potato beetle gut proteinases. Entomol Exp Appl 83:295-303.
3. Bradford MM. 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.
4. Broadway RM, Duffey SS. 1986. Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J Insect Physiol 32:827-833.
5. Broadway RM, Duffey, SS. 1988. The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. J Insect Physiol 34:1111-1117.
6. Cloutier C, Fournier M, Jean C, Yelle S, Michaud D. 1999. Growth compensation and faster development of Colorado potato beetle (Coleoptera: Chrysomelidae) feeding on potato foliage expressing oryzacystatin I. Arch Insect Biochem Physiol. 40:69-79.
7. Cloutier C, Jean C, Fournier M, Yelle S, Michaud D. 2000. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch Insect Biochem Physiol 44:69-81.
8. Eiden TC. 1995. Selected proteinase inhibitor effects on alfalfa weevil (Coleoptera:Curculionidae) growth and development. J Econ Entomol 88:1586-1590.
9. Elden TC. 2000. Effects of proteinase inhibitors and plant lectins on the adult alfalfa weevil (Coleoptera: Curculionidae). J Entomol Sci 35:62-69.
10. Fabrick J, Behnke C, Cazpla T, Bala K, Rao AG, Kramer KJ, Reeck GR. 2002. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera:Chrysomelidae). Insect Biochem Mol Biol 32:405-415.
11. Gillikin JW, Bevilacqua S, Graham JS. 1992. Partial characterization of digestive tract proteinases from western corn rootworm larvae, Diabrotica virgifera. Arch Insect Biochem Physiol 19:285-298.
12. Girard C, Le Metayer M, Monade-Bottino M, Pham-Delegue M, Jouanin L. 1998a. High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochem Mol Biol 28: 229-237.
13. Girard C, Le Metayer M, Zaccomer B, Bartlet E, Williams I, Bonade-Bottino M, Pham-Delegue M, Jouanin L. 1998b. Growth stimulation of beetle larvae reared on a transgenic oilseed rape expressing a cysteine proteinase inhibitor. J Insect Physiol 44:263-270.
14. Girard C, Bonade-Bottino M, Pham-Delegue M, Jouanin L. 1998c. Two strains of cabbage seed weevil (Coleoptera: Curculionidae) exhibit differential susceptibility to a transgenic oilseed rape expressing oryzacystatin 1. J Insect Physiol 44:569-577.
15. Green TR, Ryan CA. 1971. Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175:776-777.
16. Hines ME, Nielsen SS, Shade RE, Pomeroy MA. 1990. The effect of two proteinase inhibitors, E-64 and the Bowman-Birk inhibitor, on the developmental time and mortality of Acanthoscelides obtectus. Entomol Exp Appl 57: 201-207.
17. Hollister B, Mullin CA. 1999. Isolation and identification of primary metabolite feeding stimulants for adult western corn rootworm, Diabrotica virgifera virgifera LeConte, from host pollens. J Chem Ecol 25:1263-1280.
18. Jongsma MA, Bolter C. 1997. The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885-895.
19. Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ. 1995. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Natl Acad Sci USA 92: 8041-8045.
20. Jouanin L, Bonade-Bottino M, Girard C, Morrot G, Giband M. 1998. Transgenic plants for insect resistance. Plant Sci 131:1-11.
21. Kim JH. 2002. Effects of corn pollen chemistry, dietary proteinase inhibitors and beetle oral secretions on feeding behaviors and fecundity of adult western corn rootworm. Ph.D Thesis. The Pennsylvania State University.
22. Koiwa H, Bressan RA, Hasegawa PM. 1997. Regulation of protease inhibitors and plant defense. Trends Plant Sci 2:379-384.
23. Koiwa H, Shade RE, Zhu-Salzman K, D'Urzo MP, Murdock LL, Bressan RA, Hasegawa PM. 2000. 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 471:67-70.
24. Lecardonnel A, Chauvin L, Jouanin L, Beaujean A, Prevost G, Sangwan-Norreel B. 1999. Effects of rice cystatin I expression in transgenic potato on Colorado potato beetle larvae. Plant Sci 140:87-98.
25. Mazumdar-Leighton S, Broadway RM. 2001a. Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochem Mol Biol 31:633-644.
26. Mazumdar-Leighton S, Broadway RM. 2001b. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem Mol Biol 31:645-657.
27. Michaud D, Nguyen-Quoc B, Vrain TC, Fong D, Yelle S. 1996. Response of digestive cysteine proteinases from the Colorado potato beetle (Leptinotarsa decemlineata) and the black vine weevil (Otiorynchus sulcatus) to a recombinant form of human stefin A. Arch Insect Biochem Physiol 31:451-464.
28. Murdock LL, Brookhart G, Dunn PE, Foard DE, Kelley S, Kitch L, Shade RE, Shukle RH, Wolfson JL. 1987. Cysteine digestive proteinases in Coleoptera. Comp Biochem Physiol 87B:783-787.
29. Novillo C, Castanera P, Ortego F. 1997. Characterization and distribution of chymotrypsin-like and other digestive proteases in Colorado potato beetle larvae. Arch Insect Biochem Physiol 36:181-201.
30. Oppert B, Kramer KJ, Beeman RW, Johnson D, McGaughey W. 1997. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J Biol Chem 272:23473-23476.
31. Orr GL, Strickland JA, Walsh TA. 1994. Inhibition of Diabrotica larval growth by a multicystatin from potato tubers. J Insect Physiol 40:893-900.
32. Otto H-H, Schirmeister T. 1997. Cysteine proteases and their inhibitors. Chem Rev 97:133-171.
33. Pradhan S. 1939. Glands in the head capsule of Coccinellid beetles with a discussion on some aspects of gnathal glands. J Morphol 64:47-66.
34. Purcell JP, Greenplate JT, Sammons RD. 1992. Examination of midgut luminal proteinase activities in six economically important insects. Insect Biochem Mol Biol 22:41-47.
35. Radlowski M, Kalinowski A, Adamczyk J, Krolikowski Z, Bartkowiak S. 1996. Proteolytic activity in the maize pollen wall. Physiol Planta 98:172-178.
36. Sarath G, Motte RSDJ, Wagner RW. 1989. Protease assay methods. In: Beynon RJ, editor. Proteolytic enzymes: a practical approach, New York: IRL Press. p 25-55.
37. Sasaki T, Kishi M, Saito M, Tanaka T, Higuchi N, Kominami E, Katunuma N, Murachi T. 1990. Inhibitory effect of diand tripeptidyl aldehydes on calpains and cathepsins. J Enz Inhibit 3:195-201.
38. Schuler TH, Poppy GM, Kerry BR, Denholm I. 1998. Insect-resistant transgenic plants. Trends Biotech 16:168-175.
39. Sreedharan SK, Verma C, Caves LSD, Brocklehurst SM, Gharbia SE, Shah HN, Brocklehurst K. 1996. Demonstration that 1-trans-epoxysuccinyl-L-leucylamido-(4- guanidino) butane (E-64) is one of the most effective low Mr inhibitors of trypsin-catalysed hydrolysis. Characterization by kinetic analysis and by energy minimization and molecular dynamics simulation of the E-64-beta-trypsin complex. Biochem J 316:777-786.
40. Srivastava US. 1959. The maxillary glands of some Coleoptera. Proc R Ent Soc Lond (A) 34:57-62.
41. Terra WR, Ferreira C. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109B:1-62.
42. Wang KKW, Yuen P-W. 1999. Calpain substrates, assay methods, regulation, and its inhibitory agents. In: Wang KKW, Yeun P-W, editors. Calpain: pharmacology and toxicology of calcium-dependent protease. Philadelphia: Taylor & Francis. p 77-101.
43. Wang RY, Gergerich RC, Kim KS. 1994. Entry of ingested plant viruses into the hemocoel of the beetle vector Diabrotica undecimpunctata howardi. Phytopathology 84:147-153.
44. Wolfson JL, Murdock LL. 1990. Diversity in digestive proteinase activity among insects. J Chem Ecol 16:1089-1102.
45. Zhao Y, Botella MA, Subramanian L, Niu X, Neilsen SS, Bressan RA, Hasegawa PM. 1996. Two wound-inducible soybean cysteine proteinase inhibitors have greater insect digestive proteinase inhibitory activities than a constitutive homolog. Plant Physiol 111:1299-1306.