Plant protease inhibitors in control of phytophagous insects

Electronic Journal of Biotechnology

Volumn 5, Issue 1, 2002, Pages 93-109

  Lawrence, Paulraj K ^a   Koundal, Kripa Ram ^b  

^a TEXAS TECH UNIVERSITY   (United States)

^b NATIONAL RESEARCH CENTRE ON PLANT BIOTECHNOLOGY   (India)

Author keywords

Crop pests; Protease inhibitors; Transgenic plants

Indexed keywords

EID: 34347386663     PISSN: 07173458     EISSN: 07173458     Source Type: Journal    
DOI: 10.2225/vol5-issue1-fulltext-3     Document Type: Review

References (170)

1. ABE, M.; ABE, K.; KURODA, M. and ARAI, S. Corn kernel cysteine proteinase inhibitor as a novel cystatin superfamily memb er of plant origin. Molecular cloning and statement studies. European Journal of Biochemistry, November 1992, vol. 209, no. 3, p. 933-937.
2. ABE, K.; EMORI, Y.; KONDO, H.; SUZUKI, K. and ARAI, S. Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin). Homology with animal cystatins and transient expression in the ripening process of rice seeds. Journal of Biological Chemistry, December 1987, vol. 262, no. 35, p. 16793-16797.
3. ABE, K. and ARAI, S. Purification of a cysteine proteinase inhibitor from rice, Oryza sativa L. japonica. Agriculture Biology and Chemistry, 1985, vol. 49, p. 3349-3350.
4. ALPTETER, F.; DIAZ, I.; McAUSLANE, H.; GADDOUR, K.; CARBONERO, P. and VASIL, I.K. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Molecular Breeding, 1999, vol. 5, p. 53-63.
5. APPLEBAUM, S.W. Biochemistry of digestion. In: KERKOT, G.A. and GILBERT, L.I., eds. Comprehensive insect physiology; Biochemistry and Pharmacology. New York, Pergamon Press, 1985, vol. 4, p. 279-311.
6. ARAI, S.; WATANABE, H.; KONDO, H.; EMORI, Y. and ABE, K. Papain inhibitory activity of oryzacystatin, a rice seed cysteine proteinase inhibitor, depends on the central Gln-Val-Val-Ala-Gly region conserved among cystatin superfamily members. Journal of Biochemistry, 1991, vol. 109, p. 294-298.
7. ARGANDOÑA, V.H.; CHAMAN, M.; CARDEMIL, L.; MUÑOZ, O., ZUÑIGA, G.E. and CORCUERA, L.J. Ethylene production and peroxidase activity in aphidinfested barley. Journal of Chemical Ecology, 2001, vol. 27, p. 53-68.
8. BABIYCHUK, Elena; FUANGTHONG, Mayuree; VAN MONTAGU, Mare; INZE, Dirk and KUSHNIR, Sergei. Efficient gene tagging in Arabidopsis thaliana using a gene trap approach. Proceedings of the National Academy of Sciences United States of America, November 1997, vol. 94, p.12722-12727.
9. BAKER, J.E.; WOO, S.M. and MULLEN, M.A. Distribution of proteinases and carbohydrates in the midgut of the larvae of the sweet potato weevil Cyclas formicarius and response of proteinase to inhibitors from sweet potato. Entomologia Experimentalis et Applicata, 1984, vol. 36, p. 97-105.
10. BARRETT, A.J. Classification of peptidases. In: BARRETT, A.J, ed. Methods in Enzymology, New York, Academic Press, 1994, vol. 244, p. 1-15.
11. BARRETT, A.J. The classes of proteolytic enzymes. In: DALLING, M.J ed. Plant proteolytic enzymes, Florida, CRC Press Inc., 1986, vol. 1, p. 1-16.
12. BENT, A.F. Plant disease resistance genes: Function meets structure. Plant Cell, 1996, vol. 8, p. 1757-1771.
13. BERGEY, Daniel R.; OROZCO-CARDENAS, Martha; DE MOURA, Daniel S. and RYAN, Clarence A. A wound- and systemin-inducible polygalacturonase in tomato leaves. Proceedings of the National Academy of Sciences United States of America, February 1999, vol. 96, no. 4, p.1756-1760.
14. BIRK, Y. and APPLEBAUM, Y. Effect of soybean trypsin inhibitors on the development and midgut proteolytic activity of Tribolium castaneum larvae. Enzymologia Acta Biocatalytica, November 1960, vol. 22, no. 5, p. 318-326.
15. BIRKENMEIER, Guy F. and RYAN, Clarence A. Wound signaling in tomato plants: evidence that ABA is not a primary signal for defense gene activation. Plant Physiology, June 1998, vol. 117, no. 2, p. 687-693.
16. BLANCOLABRA, A.; MARTÍNEZ-GALLARDO, N.A.; SANDOVAL-CARDOSO, L. and DÉLANO-FRIER, J. Purification and characterization of a digestive cathepsinD proteinase isolated from Tribolium castaneum larvae (Herbst). Insect Biochemistry and Molecular Biology, 1996, vol. 26, p. 95-100.
17. BROADWAY, R.M. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. Insect Biochemistry and Molecular Biology, 1997, vol. 43, p. 855-874.
18. BROADWAY, R.M. Are insects resistant to plant proteinase inhibitors? Journal of Insect Physiology, 1995, vol. 41, p. 107-116.
19. BROADWAY, R.M. and DUFFEY, S.S. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. Journal of Insect Physiology, 1986a, vol. 32, p. 673-680.
20. BROADWAY, R.M. and DUFFEY, S.S. Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. Journal of Insect Physiology, 1986b, vol. 32, p. 827-833.
21. BROVOSKY, D. Proteolytic enzymes and blood digestion in the mosquito Culex nigripalpus. Archives of Insect Biochemistry and Physiology, 1986, vol. 3, p. 147-160.
22. BRYANT, J.; GREEN, T.R., GURUSADDAIAH, T. and RYAN, C.A. Proteinase inhibitor II from potatoes: isolation and characterization of its promoter components. Biochemistry, 1976, vol. 15, p. 3418-3424.
23. BOULTER, D. Insect pest control by copying nature using genetically engineered crops. Biochemistry, 1993, vol. 34, p. 1453-1466.
24. BOWN, D.P.; WILKINSON, H.S. and 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 Biochemistry and Molecular Biology, July 1997, vol. 27, no.7, p. 625-638.
25. BURGESS, E.P.J.; STEVEN, P.S.; KEEN, G.K.; LAING, W.A. and CHRISTELLER, J.T. Effects of protease inhibitors and dietary protein level on the black field cricket Teleogryllus commodus. Entomologia Experimentalis et Applicata, 1991, vol. 61, p. 123-130.
26. CAMPOS, F.A.P.; XAVIER-FILHO, J.; SILVA, C.P. and ARY, M.B. Resolution and partial characterization of proteinases and a-amylases from midgets of larvae of the bruchid beetle Callosobruchus maculatus (F.). Comparative Biochemistry and Physiology-B, 1989, vol. 92, p. 51-57.
27. CARBONERO, P.; ROYO, J.; DÍAZ, I., GARCÍAMAROTO, F.; GONZALEZ-HIDALGO, E.; GUTIERREZ, C. and CASANERA, P. Cereal inhibitors of insect hydrolases (a-amylases and trypsin): genetic control, transgenic expression and insect pests. In: Workshop on engineering plants against pests and pathogens (1st - 13rd January, 1993, Madrid, Spain). Instituto Juan March de Estudios Investigaciones, BRUENING, G.J.; GARCÍAOLMEDO, F. and PONZ, F.J. eds., 1993.
28. CHARITY, Julia A.; ANDERSON, Merilyn A.; BITTISNICH, Dennis J.; WHITECROSS, Malcom and HIGGINS, T.J.V. Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Molecular Breeding, 1999, vol. 5, no. 4, p. 357-365.
29. CHEN, M.S.; JOHNSON, B.; WEN, L.; MUTHUKRISHNAN, S.; KRAMER, K.J.; MORGAN, T. and REECK, G.R. Rice cystatin: bacterial expression, purification, cysteine proteinase inhibitory activity, and insect growth suppressing activity of a truncated form of the protein. Protein Expresssion and Purification, 1992, vol. 3, p. 41-49.
30. DELANEY, T.P.; UKNES, S.; VERNOOIJ, B.; FRIEDRICH, L.; WEYMANN, K.; NEGROTTO, D.; GAFFNEY, T.; GUT-RELLA, M.; KESSMANN, H.; WARD, E. and RYALS, J. A central role of salicylic acid in plant disease resistance. Science, 1994, vol. 266, p. 1247-1250.
31. DENNIS, M.S.; HERZKA, A. and LAZARUS, R.A. Potent and selective Kunitz domain inhibitors of plasma kallikrein designed by phage display. Journal of Biological Chemistry, October 1994, vol. 270, no. 50, p. 25411-25417.
32. DICKE, M.; BEEK, T.A.; POSTHUMUS, M.A.; BEN DOM, N.; VAN BOKHOVEN, H. and DE GROOT, A.E. Isolation and identification of volatile kairomone that affects acarine predator prey interactions. Journal of Chemical Ecology, 1990, vol. 16, p. 381-396.
33. DUAN, X.; LI, X.; XUE, Q.; ABO-EI-SAAD, M.; XU, D. and WU, R. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nature Biotechnology, April 1996, vol. 14, no. 4, p. 494-498.
34. DUNAEVSKII, Y.E.; GLADYSHEVA, I.P.; PAVLUKOVA, E.B.; BELIAKOVA, G.A.; GLADYSCHEV, D.P.; PAPISOVA A.I.; LARIONOVA N.I. and BELOZERSKY M.A. The anionic protease inhibitor BBWI - 1 from buckwheat seeds. Kinetic properties and possible biological role. Physiologia Plantarum, 1997, vol. 100, p. 483-488.
35. DUNN, B.M. Proteolytic enzymes: A practical approach. Oxford, IRL Press, 1989. 278 p. ISBN 0-19-963058-5.
36. EDMONDS, H.S.; GATEHOUSE, L.N.; HILDER, V.A. and GATEHOUSE, J.A. The inhibitory effects of the cysteine protease inhibitor, oryzacystatin, on digestive proteases and on larval survival and development of the southern corn rootworm (Diabrotica undecimpunctata howardi). Entomologia Experimentalis et Applicata, 1996, vol. 78, p. 83-94.
37. EGUCHI, M.; IWAMOTO, A. and YAMAGUHI, K. Interaction of proteases from the midgut lumen, epithelial and peritrophic membrane of the silkworm Bombyx mori L. Comparative Biochemistry and Physiology-A, 1982, vol. 72, p. 359-363.
38. EPPLE, P.; APRL, K. and BOHLMANN, H. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis related protein. Plant Physiology, 1995, vol. 109, p. 813-820.
39. FERNANDES, K.V.S.; SABELLI, P.A.; BARRATT, D.H.P.; RICHARDSON, M.; XAVIER-FILHO, J. and SHEWRY, P.R. The resistance of cowpea seeds to bruchid beetles is not related to level of cysteine proteinase inhibitors. Plant Molecular Biology, October 1993, vol. 23, no. 1, p. 215-219.
40. FRAZAO, Carlos; BENTO, Isabel; COSTA, Julia; SOARES, Claudio M.; VERISSIMO, Paula; FARO, Carlos; PIRES, Euclides; COOPER, Jon and CARRONDO, Maria A. Crystal structure of cardosin A, a glycosylated and Arg-Gly-Asp- containing aspartic proteinase from the flowers of Cyanara cardunculus L. Journal of Biological Chemistry, September 1999, vol. 274, no. 39, p. 27694-27701.
41. GARCIAOLMEDO SALCEDO, F.; SANCHEZ MONGE, G.; GOMEZ, R.L.; ROYO, J. and CARBONERO, P. Plant proteinaceous inhibitors of proteinases and a-amylases. Oxford Survey Plant Molecular and Cell Biology, 1987, vol. 4, p. 275-334.
42. GATEHOUSE, A.M.R.; DAVIDSON, G.M.; NEWELL, C.A.; MERRYWEATHER, A.; HAMILTON, W.D.O.; BURGESS, E.P.J.; GILBERT, R.J.C. and GATEHOUSE, J.A. Trangenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Molecular Breeding, 1997, vol. 3, p. 49-63.
43. GATEHOUSE, A.M.R. and 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. Journal of the Science of Food and Agriculture, 1983, vol. 34, p. 345-350.
44. GIRARD, C.; LE MÉTAYER, M.; BONADÉ-BOTTINO, M.; PHAM-DELÈGUE M.H. and JOUANIN, L. High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochemistry and Molecular Biology. 1998, vol. 28, p. 229-237.
45. GOURINATH, S.; ALAM, N.; SRINIVASAN, A.; BETZEL, C. and SINGH, T.P. Structure of the bifunctional inhibitor of trypsin and alpha-amylase from ragi seeds at 2.2 A resolution. Acta Crystallography D Biology Crystallography, March 2000, vol. 56, no. 3, p. 287-293.
46. GRAHAM J.; GORDON, S.C. and MCNICOL, R.J. The effect of the CpTI gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae). Annals of Applied Biology, 1997, vol. 131, p. 133-139.
47. GRAHAM, J.S. and RYAN, C.A. Accumulation of metallocarboxy -peptidase inhibitor in leaves of wounded potato plants. Biochemical and Biophysics Research Communication, 1997, vol. 101, p. 1164-1170.
48. GREENBLATT, H.M.; RYAN, C.A. and JAMES, M.N.G. Strucuture of the complex Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-I at 2.1 A resolution. Journal of Molecular Biology, 1989, vol. 205, p. 201-228.
49. GRUDEN, K.; STRUKELJ, B.; POPOVIC, T.; LENARCIC, B.; BEVEC, T.; BRZIN, J.; KREGAR, I.; HERZOG-VELIKONJA, J.; STIEKEMA, W.J.; BOSCH, D. and JONGSMA M.A. The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type1 domain inhibitors. Insect Biochemistry and Molecular Biology, 1998, vol. 28, p. 549-560.
50. HABU, Y.; PEYACHOKNAGUL, S.; SAKATA, Y.; FUKASAWA, K. and OHNO, T. Evolution of a multigene family that encodes the Kunitz chymotrypsin inhibitor in winged bean: a possible intermediate in the generation of a new gene with a distinct pattern of expression. Molecular General Genetics, 1997, vol. 254, no. 1, p. 73-80.
51. HAVKIOJA, E. and NEUVONEN, L. Induced long-term resistance to birch foliage against defoliators : defense or incidental. Ecology, 1985, vol. 66, p. 1303-1308.
52. HEATH, R.G.; MCDONALD, J.T.; CHRISTELLER, M.; LEE, K.; BATEMAN, J.; WEST, R.; VAN HEESWIJCK and ANDERSON, M.A. Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. Journal of Insect Physiology, 1997, vol. 9, p. 833-842.
53. HILDER, V.A.; BARKER, R.F.; SAMOUR, R.A.; GATEHOUSE, A.M.R.; GATEHOUSE, J.A. and BOULTER, D. Protein and cDNA sequences of Bowman-Birk protease inhibitors from the cowpea (Vigna unguiculata Walp.). Plant Molecular Biology, December 1989, vol. 13, no. 6, p. 701-710.
54. HILDER, V.A.; GATEHOUSE, A.M.R.; SHEERMAN, S.E.; BARKER, R.F. and BOULTER, D. A novel mechanism of insect resistance engineered into tobacco. Nature, 1987, vol. 300, p. 160-163.
55. HOBDAY, S.M.; THURMAeN, D.A. and BARBER, D.J. Proteolytic and trypsin inhibitory activities in extracts of germinating Pisum sativum seeds. Phytochemistry, 1973, vol. 12, p. 1041-1046.
56. HOLLANDER-CZYTKO, H.; ANDERSEN, J.L. and RYAN, C.A. Vacuolar localization of wound-induced carboxy peptidase inhibitor in potato leaves. Plant Physiology, 1985, vol. 78, p. 76-79.
57. HOUSEMAN, J.G.; DOWNE, A.E.R. and PHILOGENE, B.J.R. Partial characterization of proteinase activityin the larval midgut of the European corn borer Ostrinia nubilalis Hubner (Lepidoptera: Pyralidae). Canadian Journal of Zoology, 1989, vol. 67, p. 864-868.
58. HOUSEMAN, J.G.; CAMPBELL, F.C. and MORRISON, P.E. A preliminary characterization of digestive proteases in the posterior midgut of the stable fly Stomoxys calcitrans (L.) (Diptera: Muscidae). Insect Biochemistry, 1987, vol. 17, p. 213-218.
59. HOUSEMAN, J.G. and DOWNE, A.E.R. Cathepsin D-like activity in the posterior midgut of Hemipteran insects. Comparative Biochemistry and Physiology-B, 1983, vol. 75, p. 509-512.
60. HUBER, R. and CARRELL, R.W. Implications of the three-dimensional structure of alpha I -antitrypsin for structure and function of serpins. Biochemistry, 1989, vol. 28, p. 8951-8966.
61. HUNT, M.D.; NEUENSCHWANDER, U.H.; DELANEY, T.P.; WEYMANN, K.B.; FRIEDRICH, L.B.; LAWTON, K.A.; STEINER, H.Y. and RYALS, J.A. Recent advances in systemic acquired resistance research-a review. Gene, November 1996, vol. 179, no. 1, p. 89-95
62. ISHIKAWA, A.; OHTA, S.; MATSUOKA, K.; HATTORI, T. and NAKAMURA, K. A family of potato genes that encode Kunitz-type proteinase inhibitors: structural comparisons and differential expression. Plant and Cell Physiology, 1994, vol. 35, p. 303-312.
63. ISHIKAWA, C.; WATANABE, K.; SAKATA, N.; NAKAGSAKI, C.; NAKAMURA, S. and TAKAHASHI, K. Azuki bean (Vigna angularis) protease inhibitors: isolation and amino acid sequences. Journal of Biochemistry, 1985, vol. 97, p. 55-70.
64. JOHNSON, R.; NARRAEZ, J.; AN, G. and RYAN, C.A. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proceedings of the National Academy of Sciences United States of America, 1989, vol. 86, p. 9871-9875.
65. JOHNSTON, K.A.; GATEHOUSE, J.A. ANSTEE, J.H. Effects of soybean protease inhibitors on the growth and development of larval Helicoverpa armigera. Journal of Insect Physiology, 1993, vol. 39, p. 657-664.
66. JONGSMA, M.A. and BOLTER, C. The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 1997, vol. 43, p. 885-895.
67. JONGSMA, M.A.; STIEKEMA, W.J. and BOSCH, D. Combatting inhibitor insensitive proteases of insect pests. Trends in Biotechnology, 1996, vol. 14, p. 331-333.
68. JONGSMA, M.A.; BAKKER, P.L.; STIEKEMA, W.J. and BOSCH, D. Phage display of a double-headed proteinase inhibitor: analysis of the binding domains of potato proteinase inhibitor II. Molecular Breeding, 1995, vol. 1, p. 181-191.
69. JOSHI, B.; SAINANI, M.; BASTAWADE, K.; GUPTA, V.S. and RANJEKAR, P.K. Cysteine protease inhibitor from pearl millet: a new class of antifungal protein. Biochemical and Biophysical Research Communications, 1998, vol. 246, p. 382-387.
70. KEILOVA, H. and TOMASEK, V. Isolation and properties of cathespin D inhibitor from potatoes. Collection of Czechoslovak Chemical Communication, 1976, vol. 41, p. 489-497.
71. KERIN, J. Opening address. In: Proceedings of the International Working Conference on Stored-product Protection. (6, 17th-23rd April, 1994, Canberra, Australia). Volume 1, p. xix-xx.
72. KERVINEN, J.; TOBIN, G.J.; COSTA, J.; WAUGH, D.S.; WLODAWER, A. and ZDANOV, A. Crystal structure of plant aspartic proteinase prophytepsin: inactivation and vacuolar targeting. Journal of European Molecular Biology Organization, July 1999, vol. 18, no. 14, p. 3947-3955.
73. KIMURA, M.; IKEDA, T.; FUKUMOTO, D.; YAMASAKI, N. and YONEKURA, M. Primary structure of a cysteine proteinase inhibitor from the fruit of avocado (Persea americana Mill). Bioscience Biotechnology and Biochemistry, December 1995, vol. 59, no. 1, p. 2328-2329.
74. KISHIMOTO, N.; HIGO, H.; ABE, K.; ARAI, S.; SAITO, A. and HIGO, K. Identification of the duplicated segments in rice chromosomes 1 and 5 by linkage analysis of cDNA markers of known functions. Theoretical and Applied Genetics, 1994, vol. 88, p. 722-726.
75. KITCH, L.W. and MURDOCK, L.L. Partial characterization of a major gut thiol proteinase from larvae of Callosobruchus maculatus (F.). Archives of Insect Biochemistry and Physiology, 1986, vol. 3, p. 561-575.
76. KRATTIGER, Anatole F. Insect resistance in crops: a case study of Bacillus thuringiensis (Bt) and its transfer to developing countries. ISAAA Briefs, 1997, no. 2, p. 42.
77. KONDO, H.; ABE, K.; EMORI, Y. and ARAI, S. Gene organization of oryzacystatinII, a new cystatin superfamily member of plant origin, is closely related to that of oryzacystatinI but different from those of animal cystatins. FEBS Letters, 1991, vol. 278, p. 87-90.
78. KOIWA, K.; SHADE, R.E.; ZHU-SALZMAN, K.; SUBRAMANIAN, L.; MURDOCK, L.L.; NIELSEN, S.S.; BRESSAN, R.A. and HASEGAWA, P.M. Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant Journal, 1998, vol. 14, p. 371-379.
79. KOIWA, H.; BRESSAN, R.A. and HASEGAWA, P.M. Regulation of protease inhibitors and plant defense. Trends in Plant Science, 1997, vol. 2, p. 379-384.
80. KORTH, K.L. and DIXON, R.A. Evidence for chewing insect specific molecular events distinct from a general wound response in leaves. Plant Physiology, 1997, vol. 115, p. 1299-1305.
81. KUNITZ, M. Crystallization of a trypsin inhibitor from soybean. Science, 1945, vol. 101, p. 668-669.
82. LASKOWSKI, M. JR. and KATO, I. Protein inhibitors of proteinases. Annual Review of Biochemistry, 1980, vol. 49, p. 685-693.
83. LAWRENCE, Paulraj K. and KOUNDAL, Kripa Ram. Agrobacterium tumefaciens mediated transformation of pigeonpea (Cajanus cajan (L.) Millsp) and molecular analysis of regenerated plants. Current Science, June 2001, vol. 80, no. 11, p. 1428-1432.
84. LAWRENCE, Paulraj, K.; NIRMALA, Jayaveeramuthu and KOUNDAL Kripa Ram. Nucleotide sequence of a genomic clone encoding a cowpea (Vigna unguiculata L.) trypsin inhibitor. EJB Electronic Journal of Biotechnology [online]. 15 April 2001, vol. 4, no. 1 [cited 16 April 2001]. Available from Internet: http://www.ejb.org/content/vol4/issue1/full/4/index.html. ISSN 0717-3458.
85. LEE, S.I.; LEE, S.H.; KOO, J.C.; CHUN, H.J.; LIM, C.O.; MUN, J.H.; SONG, Y.H. and CHO, M.J. Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Molecular Breeding, 1999, vol. 5, p. 1-9.
86. LEE, M.J. and ANSTEE, J.H. Endoproteases from the midgut of larval Spodoptera littoralis include a chymotrypsinlike enzyme with an extended binding site. Insect Biochemistry and Molecular Biology, 1995, vol. 25, p. 49-61.
87. LEMOS, F.J.A.; XAVIER-FILNO, J. and CAMPOS, F.A.P. Proteinases of the midgut of Savrotes subfasciatos larvae. Agricultural Biology Tecnoi, 1987, vol. 80, p. 46.
88. LEÓN, José.; ROJO, Enrique and SANCHEZ-SERRANO, José J. Wound signalling in plants. Journal of Experimental Botany, January 2001, vol. 52, no. 354, p. 1-9.
89. LEPLE, J.C.; BONADE-BOTTINO, M.; AUGUSTIN, S.; PILATE, G.; LE TÂN, V.D.; DELPLANQUE, A.; CORNU, D. and JOUANIN, L. Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Molecular Breeding, 1995, vol. 1, p. 319-328.
90. LI, Y.E.; ZHU, Z.; CHEN, Z.X.; WU, X.; WANG, W. and LI, S.J. Obtaining transgenic cotton plants with cowpea trypsin inhibitor. Acta Gossypii Sinica, 1998, vol. 10, p. 237-243.
91. LIPKE, H.; FRAENKEL, G.S. and LIENER, I.E. Effects of soybean inhibitors on growth of Tribolium confusum. Journal of the Science of Food and Agriculture, 1954, vol. 2, p. 410-415.
92. MACINTOSH, S.C.; KISHORE, G.M.; PERLAK, F.J.; MARRONE, P.G.; STONE, T.B.; SIMS, S.R. and FUCHS, R.L. Potentiation of Bacillus thuringiensis insecticidal activity by serine protease inhibitors. Journal of Agriculture and Food Chemistry, 1990, vol. 38, p. 50-58.
93. MACPHALEN, C.N. and JAMES, M.N.G. Crystal and molecular structure of the serine proteinase inhibitor CI-2 from barley seeds. Biochemistry, 1987, vol. 26, p. 261-269.
94. MALONE, M. and ALARCON, J.J. Only xylem-borne factors can account for systemic wound signalling in the tomato plant. Planta, 1995, vol. 196, p. 740-746.
95. MARES, M.; MELOUN, B.; PAVLIK, M.; KOSTKA, V. and BAUDYS, M. Primary structure of Cathepsin-D inhibitor from potatoes and its structural relationship to trypsin inhibitor family. FEBS Letters, 1989, vol. 251, p. 94-98.
96. MCGURL, B.; OROZCO-CARDENAS, M.; PEARCE, G. and RYAN, Clarence A. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proceedings of the National Academy of Sciences United States of America, 1994, vol. 91, p. 9799-9802.
97. MCMANUS, M.T. and BURGESS, E.P.J. Effects of the soybean (Kunitz) trypsin inhibitor on growth and digestive proteases of larvae of Spodoptera litura. Transgenic Research, 1995, vol. 8, p. 383-395.
98. MCMANUS, M.T., WHITE, D.W.R. AND MCGREGOR, P.G. Accumulation of chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Research, 1994, vol. 3, p. 50-58.
99. MEIGE, M.; MASCHERPA, J.; ROYER-SPIERER, A.; GRANG, A. and MEIGE, J. Analyse des crops proteiques isoles de Lablab Pupureus (L.) Sweet: localisation intracellulaire des globulines proteases et inhibiteurs de la trypsire. Planta, 1976, vol. 131, p. 181-86.
100. MEINERS, J.P. and ELDEN, T.C. Resistance to insects and diseases in Phaseolus. In: Advances in legume science. International Legume Conference, (1978, Kew Surrey, UK). SUMMERFIELD, R.S and BUNTING, A.H. eds., 1978. p. 359-364.
101. MELVILLE, J.C. and RYAN, C.A. Chymotrypsin inhibitor I from potato: large scale preparation and the characterization of its subunit components. Journal of Biological Chemistry, 1973, vol. 247, p. 3415-3453.
102. METCALF, R.L. The ecology of insecticides and the chemical control of insects. In: KOGAN, M. ed. Ecological theory and integrated pest management. New York, John Wiley and Sons, 1986, p. 251-297.
103. MICHAUD, D. Avoiding protease mediated resistance in herbivorous pests. Trends in Biotechnology, 1997, vol. 15, p. 4-6.
104. MICHAUD, D.; NGUYEN-QUOC, B.; VRAIN, T.C.; FONG, D. and YELLE, S. 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. Archieves of Insect Biochemistry and Physiology, 1996, vol. 31, p. 451-64.
105. MICHAUD, D.; CANTIN, L. and VRAIN T.C. Carboxy terminal truncation of oryzacystatin II by oryzacystatin insensitive insect digestive proteinases. Archives of Biochemistry and Biophysics, October 1995a, vol. 322, no. 2, p. 469-474.
106. MICHAUD, D.; BERNIERVADNAIS, N.; OVERNEY, S. and YELLE, S. Constitutive expression of digestive cysteine proteinase forms during development of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Insect Biochemistry and Molecular Biology, 1995b, vol. 25, p. 1041-1048.
107. MICKEL, C.E. and STANDISH, J. Susceptibility of processed soy flour and soy grits in storage to attack by Tribolium castaneum. University of Minnesota Agricultural Experimental Station Technical Bulletin, 1947, vol. 178, p. 1-20.
108. MOURA, Daniel S. and RYAN, Clarence A. Woundinducible proteinase inhibitors in pepper. Differential regulation upon wounding, systemin, and methyl jasmonate. Plant Physiology, May 2001, vol. 126, p. 289-298.
109. MUKHOPADHYAY, D. The molecular evolutionary history of an winged bean alpha-chymotrypsin inhibitor and modeling of its mutations through structural analysis. Journal of Molecular Evolution, 2000, vol. 50, p. 214-223.
110. MURDOCK, L.L.; SHADE, R.E. and POMEROY, M.A. Effects of E. 64 a cysteine proteinase inhibitor on cowpea weevil growth development and fecundity. Environmental Entomology, 1988, vol. 17, p. 467-469.
111. MURDOCK, L.L.; BROOKHART, G.; DUNN, P.E.; FOARD, D.E. and KELLEY, S. Cysteine digestive proteinases in Coleoptera. Comparative Biochemistry and Physiology-B, 1987, vol. 87, p. 783-787.
112. NAGATA, K.; KUDO, N.; ABE, K.; ARAI, S. and TANOKURA, M. Three dimensional solution structure of oryzacystatin-I, a cysteine proteinase inhibitor of the rice, Oryza sativa L. japonica. Biochemistry, 2000, vol. 39, p. 14753-14760.
113. NEWELL, C.A.; LOWE, J.M.; MERRYWEATHER, A.; ROOKE, L.M. and HAMILTON, W.D.O. Transformation of sweet potato (Ipomea batatas (L.). Lam) with Agrobacterium tumefaciens and regeneration of plants expressing cowpea trypsin inhibitor and Snowdrop lectin. Plant Science, 1995, vol. 107, p. 215-227.
114. NOVILLO, C.; CASTAÑERA, P. and ORTEGO, F. Inhibition of digestive trypsin like proteases from larvae of several lepidopteran species by the diagnostic cysteine protease inhibitor E64. Insect Biochemistry and Molecular Biology, 1997, vol. 27, p. 247-254.
115. ODANI, S.; KOIDE, T. and ONO, T. The complete amino acid sequence of barley trypsin inhibitor. Journal of Biological Chemistry, July 1983, vol. 258, no. 13, p. 7998-8003.
116. ODANI, S. and IKENAKA, T. The amino acid sequences of two soybean double-headed proteinase inhibitors and evolutionary considerations on the legume proteinase inhibition. Journal of Biochemistry, September 1976, vol. 80, no. 3, p. 641-643.
117. OPPERMAN, C.H.; TAYLOR, C.G. and CONKLING, M.A. Rootknot nematode directed expression of a plant root specific gene. Science, 1994, vol. 263, p. 221-223.
118. OPPERT, B.; MORGAN, T.D.; CULBERTSON, C. and KRAMER, K.J. Dietary mixtures of cysteine and serine proteinase inhibitors exhibit synergistic toxicity toward the red flour beetle, Tribolium castaneum. Comparative Biochemistry and Physiology, 1993, vol. 105C, p. 379-385.
119. ORR, G.L.; STRICKLAND, J.A. and WALSH, T.A. Inhibition of Diabrotica larval growth by a multicystatin from potato tubers. Journal of Insect Physiology, 1994, vol. 40, p. 893-900.
120. PANNEKOEK, H.; VAN MEIJER, M.; SCHLEEF, R.R.; LOSKUTOFF, D.J. and BARBAS, III. Functional display of human plasminogen activator inhibitor 1 (PAI-1) on phages: Novel perspectives for structure-function analysis by error-prone DNA synthesis. Gene, June 1993, vol. 128, no. 1, p. 135-140.
121. PANNETIER, C.; GIBAND, M.; COUZI, P.; LETAN, V.; MAZIER, M.; TOURNEUR, J. and HAU, B. Introduction of new traits into cotton through genetic engineering: insect resistance as example. Euphytica, 1997, vol. 96, p. 163-166.
122. PARK, H.; YAMANAKA, N.; MIKKONEN, A.; KUSAKABE, I. and KOBAYASHI, H. Purification and characterization of aspartic proteinase from sunflower seeds. Bioscience Biotechnology and Biochemistry, 2000, vol. 64, p. 931-939.
123. PERLER, F.; EFSTRATIADIS, A.; LOMEDICO, P.; GILBERT, N.; KOLODNER, R. and OODGSON, J. The evolution of genes: the chicken preproinsulin gene. Cell, June 1980, vol. 20, no. 2, p. 555-556.
124. RAKWAK, R.; AGARWAL, K.G. and JHA, N.S. Characterization of a rice (Oryza sativa L.) Bowman-Birk proteinase inhibitor: tightly light regulated induction in response to cut, jasmonic acid, ethylene and protein phosphatase 2A inhibitors. Gene, January 2001, vol. 263, no. 1-2, p. 189-198.
125. RANCOUR, J.M. and RYAN, C.A. Isolation of a carboxypeptidase B inhibitor from potatoes. Archives of Biochemistry and Biophysics, 1968, vol. 125, p. 380-382.
126. RAVICHANDARAN, S.; SEN, U.; CHAKRABARTI, C. and DATTAGUPTA, J.K. Cryocrystallography of a Kunitz type serine protease inhibitor: 90 K structure of winged bean chymotrypsin WCI) at 2.13 A resolution. Acta Crystallography D Biology Crystallography, 1999, vol. 55, p. 1814-1821.
127. RAWLINGS, N.D. and BARRETT, A.J. Evolutionary families of metallopeptidases. In: BARRETT, A.J., ed. Methods in Enzymology. New York, Academic Press, 1995, vol. 248, p. 183-228.
128. REECK, G.R.; KRAMER, K.J.; BAKER, J.E.; KANOST, M.R.; FABRICK J.A. and BEHNKE, C.A. Proteinase inhibitors and resistance of transgenic plants to insects. In: CAROZZI, N. and KOZIEL, M., eds. Advances in insect control: the role of transgenic plants. London, Taylor and Francis, 1997, p. 157-183.
129. RICHARDSON, M.J. Seed storage proteins: The enzyme inhibitors. In: RICHARDSON, M.J, ed. Methods in Plant Biochemistry, New York, Academic Press, 1991, p. 259-305.
130. ROGERS, B.L.; POLLOCK, J.; KLAPPER, D.G. and GRIFFITH, I.J. Sequence of the proteinase inhibitor cystatin homolog from the pollen of Ambrosia artemisiifolia (short ragweed). Gene, 1993, vol. 133, p. 219-221.
131. ROTTGEN, P. and COLLINS, J. A human pancreatic secretory trypsin inhibitor presenting a hypervariable highly constrained epitope via monovalent phagemid display. Gene, October 1995, vol. 194, no. 2, p. 243-250.
132. ROUSH, R.T. and MCKENZIE, J.A. Ecological and genetics of insecticide and araricide resistance. Annual Review of Entomology, 1987, vol. 32, p. 361-381.
133. RYAN, Clarence A. The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta, March 2000, vol. 1477, no. 1-2, p. 112-121.
134. RYAN, Clarence A. Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 1990, vol. 28, p. 425-449.
135. RYAN, Clarence A. Insect-induced chemical signals regulating natural plant protection responses. In: DENNO, R.F. and MCCLURE M.S., eds. Variable plants and herbivores in natural and managed systems. New York, Academic Press, 1989, p. 43-60.
136. SANE, V.A.; NATH, P.; AMINUDDIN and SANE, P.V. Development of insect-resistant transgenic plants using plant genes: expression of cowpea trypsin inhibitor in transgenic tobacco plants. Current Science, 1997, vol. 72, p. 741-747.
137. SARDANA, R.K.; GANZ, P.R.; DUDANI, A.K.; TACKABERRY, E.S.; CHENG, X. and ALTOSAAR, I. Synthesis of recombinant human cytokine GMCSF in the seeds of transgenic tobacco plants. In: CUNNINGHAM, C. and PORTER A.J.R., eds. Recombinant proteins from plants. Production and isolation of clinically useful compounds. Totowa NJ, Humana Press, 1998, p. 77-87.
138. SHULKE, R.H. and MURDOCK, L.L. Lipoxygenase trypsin inhibitor and lectin from soybeans: effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae). Environmental Entomology, 1983, vol. 12, p. 787-791.
139. SONG, I.; TAYLOR, M. and BAKER, K. Inhibition of cysteine proteinases by Carica papaya cystatin produced in Escherichia coli. Gene, September 1995, vol. 162, no. 2, p. 221-224.
140. SPARBER, S.B. Insect resistance to biological insecticide Bacillus thuringiensis. Science, 1985, vol. 229, p. 193-195.
141. STEVENS, F.C.; WOERY, S. and KRAHU, J. Structurefunction relationship in lima bean proteinase inhibitor. In: FRITZ, H., TSCHESCHE, H., GREENE, L.J and TRUSCHEIT, E., eds. Proteinase inhibitors, 1974, Berlin, Springer-Verlag, p. 344-354.
142. STRATMANN, Johannes W.; SCHEER, Justin and RYAN, Clarence A. Suramin inhibits initiation of defense signaling by systemin, chitosan, and a beta-glucan elicitor in suspension-cultured Lycopersicon peruvianum cells. Proceedings of the National Academy of Sciences United States of America, August 2000a, vol. 97, no. 16, p. 8862-8867.
143. STRATMANN, Johannes W.; STELMACH, B.A.; WEILER, E.W. and RYAN, Clarence A. UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochemistry and Photobiology, February 2000b, vol. 71, no. 2, p. 116-23.
144. STINTZI, Annick; WEBER, Hans.; REYMOND, Philippe; BROWSE, John and FARMER, Edward E. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proceedings of the National Academy of Sciences United States of America, October 2001, vol. 98, no. 22, p. 12837-12842.
145. SUZUKI, A.; TSONOGA, Y.; TANAKA, I.; YAMANE, T.; ASHIDA, T.; NORIOKA, S.; HARA, S. and IKENAKA, T. The structure of Bowman-Birk type protease inhibitor A-II from peanut (Arachis hypogaea) at 3.3A resolution. Journal of Biochemistry, 1987, vol. 101, p. 267-274.
146. TANAKA, A.S.; SAMPAIO, C.A; FRITZ H. and AUERSWALD, E.A. Functional display and expression of chicken cystatin using a phagemid system. Biochemical and Biophysical Research Communications, 1995, vol. 214, p. 389-395.
147. TAYLOR, M.A.J.; BAKER, K.C.; BRIGGS, G.S.; CONNERTON, I.F.; CUMMINGS, N.J.; PRATT, K.A.; REVELL, D.F.; FREEDMAN, R.B. and GOODENOUGH, P.W. Recombinant proregions from papain and papaya proteinase IV are selective high affinity
148. TERRA , W.R.; FERREIRA, C. and JORDAO, B.P. Digestive enzymes. In: LEHANE M. J., ed. Billin London, Chapman and Hall, 1996, p.153-194.
149. THOMAS, J.C.; ADAMS, D.G.; KEPPENNE, V.D.; WASMANN, C.C.; BROWN, J.K.; KANOSH, M.R. and BOHNERT, H.J. Proteinase inhibitors of Manduca sexta expressed in transgenic cotton. Plant Cell Reports, 1995, vol. 14, p. 758-762.
150. THOMAS, J.C.; WASMANN, C.C.; ECHT, C.; DUNN, R.L.; BOHNERT, H.J. and MCCOY, T.J. Introduction and expression of an insect proteinase inhibitor in alfalfa (Medicago sativa L.). Plant Cell Reports, 1994, vol. 14, p. 31-36.
151. TIFFIN, Peter and GAUT, Brandon S. Molecular evolution of the wound- induced serine protease inhibitor wip1 In Zea and related genera. Molecular Biology and Evolution, 2001, vol. 18, p. 2092-20101.
152. TITARENKO, E.; ROJO, E.; LEON, J.; SANCHEZSERRANO, J.J. Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiology, 1997, vol. 115, p. 817-826.
153. TURK, V. and BODE, W. The cystatins: protein inhibitors of cysteine proteinases. FEBS Letters, 1991, vol. 285, p. 213-219.
154. URWIN, P.E.; LILLEY, C.J.; MCPHERSON, M.J. and ATKINSON, H.J. Resistance to both cyst and rootnot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant Journal, August 1997, vol. 12, no. 2, p. 455-461.
155. URWIN, P.E.; ATKINSON, H.J.; WALLER, D.A. and MCPHERSON, M.J. Engineered oryzacystatinI expressed in hairy roots confers resistance to Globodera pallida. Plant Journal, July 1995, vol. 8, no. 1, p. 121-131.
156. VAIN, P.; WORLAND, B.; CLARKE, M.C.; RICHARD, G.; BEAVIS, M.; LIU, H.; KOHLI, A.; LEECH, M.; SNAPE, J. and CHRISTOU, P. Expression of an engineered cysteine proteinase inhibitor (Oryzacystatin-I delta D86) for nematode resistance in transgenic rice plants. Theoretical and Applied Genetics, 1998, vol. 96, p. 266-271.
157. VISAL, S.; TAYLOR, M.A.J. and MICHAUD, D. The proregion of papaya IV inhibits Colorado potato beetle digestive cysteine proteinases. FEBS Letters, September 1998, vol. 434, no. 3, p. 401-405.
158. WALDRON, C.; WEGRICH, L.M.; OWENS METRO, P.A. and WALSH, T.A. Characterization of a genomic sequence coding for potato multicystatin, of eight-domain cysteine proteinase inhibitor. Plant Molecular Biology, 1993, vol. 23, p. 801-812.
159. WALKER, A.J.; FORD, L.; MAJERUS, M.E.N.; GEOGHEGAN, I.E.; BIRCH, A.N.E.; GATEHOUSE, J.A. and GATEHOUSE, A.M.R. Characterisation of the midgut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata L.) and its sensitivity to proteinase inhibitors. Insect Biochemistry and Molecular Biology, 1998, vol. 28, p. 173-180.
160. WANG, C.I.; YANG, Q. and CRAIK, C.S. Isolation of a high affinity inhibitor of urokinase-type plasminogen activator by phage display of ecotin. Journal of Biological Chemistry, May 1995, vol. 270, no. 20, p. 12250-12256.
161. WASTERNACK, C. and PARTHIER, B. Jasmonatesignalled plant gene expression. Trends in Plant Science, 1997, vol. 2, p. 302-307.
162. WIEMAN, K.F. and NIELSEN, S.S. Isolation and partial characterization of a major gut proteinase from larval Acanthoscelides obtectus Say (Coleoptera: bruchidae). Comparative Biochemistry and Physiology-B, 1988, vol. 89, p. 419-426.
163. WILLIAMSON, V.M. and HUSSEY, R.S. Nematode pathogenesis and resistance in plants. Plant Cell, October 1996, vol. 8, p. 1735-1745.
164. WOLFSON, J.L. and MURDOCK, L.L. Diversity in digestive proteinase activity among insects. Journal of Chemical Ecology, 1990, vol. 16, p. 1089-1102.
165. WOLFSON, J.L. and MURDOCK, L.L. Suppression of larval Colorado beetle growth and development by digestive proteinase inhibitors. Entomologia Experimentalis et Applicata, 1987, vol. 44, p. 235-240.
166. XU, D.P.; XUE, Q.Z.; MCELROY, D.; MAWAL, Y.; HILDER, V.A. and WU, R. Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests. Molecular Breeding, 1996, vol. 2, p. 167-173.
167. YEH, K.W.; LIN, M.L.; TUAN, S.J.; CHEN, Y.M.; LIN, C.Y. and KAO, S.S. Sweet potato (Ipomea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Reporter, 1997, vol. 16, p. 696-699.
168. ZHANG, Y.S.; LOS, S.; TAN, F.L.; CHI, C.W.; XU, L.X. and ZHANG A.L. Complete amino acid sequence of mung bean trypsin inhibitor. Science Sinica, March 1982, vol. 25, no. 3, p. 268-277.
169. ZHAO, Y.; BOTELLA, M.A.; SUBRAMANIAN, L.; NIU, X.; NIELSEN, S.S.; BRESSAN, R.A. and HASEGAWA, P.M. Two wound inducible soybean cysteine proteinase inhibitors have greater insect digestive proteinase inhibitory activities than a constitutive homolog. Plant Physiology, August 1996, vol. 111, no. 4, p. 1299-1306.
170. ZHU-SALZMAN, K.; SALZMAN, R.A.; KOIWA, H.; MURDOCK, L.L.; BRESSAN, R.A. and HASEGAWA, P.M. Ethylene negatively regulates local expression of plant defense lectin genes. Physiologia Plantarum, 1998, vol. 104, p. 365-372.