Inducible direct plant defense against insect herbivores: A review

Insect Science

Volumn 15, Issue 2, 2008, Pages 101-114

  Chen, Ming Shun ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Chemical defense; Defensive protease; Lectins; Protease inhibitor; Scondary metabolite

Indexed keywords

HEXAPODA;

EID: 48449103966     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2008.00190.x     Document Type: Article

References (163)

1. Agrios, G.N. (1997) Plant diseases caused by Mollicutes: phyto plasmas and spiroplasmas. Plant Pathology, 4th ed. (ed. G.N. Agrios), pp. 457-470. Academic Press, New York.
2. Ahn, J.-E., Salzman, R.A., Braunagel, S.C., Koiwa, H. and Zhu-Salzman, K. (2004) Functional roles of specific bruchid protease isoforms in adaptation to a soybean protease inhibitor. Insect Molecular Biology, 13, 649-657.
3. Akhtar, Y. and Isman, M.B. (2004) Comparative growth inhibitory and antifeedant effects of plant extracts and pure allelochemicals on four phytophagous insect species. Journal of Applied Entomology, 128, 32-38.
4. Alfonso-Rub, J., Ortego, F., Castañera, P., Carbonero, P. and Diaz, I. (2003) Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Research, 12, 23-31.
5. Altpeter, F., Diaz, I., McAuslane, H., Gaddour, K., Carbonero, P. and Vasil, I.K. (1999) Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Molecular Breeding, 5, 53-63.
6. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. and Preston, C.A. (2006) Volatile signaling in plant-plant interactions: "Talking Trees" in the genomics era. Science, 311, 812-815.
7. Bennett, R.N. and Wallsgrove, R.M. (1994) Secondary metabolites in plant defence mechanisms. New Physiologist, 127, 617-633.
8. Bentur, J.S. and Kalode, M.B. (1996) Hypersensitive reaction and induced resistance in rice against the Asian rice gall midge Orseolia oryzae. Entomologia Experimentalis et Applicata, 78, 77-81.
9. Bi, R.-M., Jia, H.-Y., Feng, D.-S. and Wang, H.-G. (2006) Production and analysis of transgenic wheat (Triticum aestivum L.) with improved insect resistance by the introduction of cowpea trypsin inhibitor gene. Euphytica, 151, 351-360.
10. Blau, P.A., Feeney, P., Contardo, L. and Tobson, D.S. (1978) Allylglucosinolate and herbivorous caterpillars: a contrast in toxicity and tolerance. Science, 200, 1296-1298.
11. Borek, V., Elberson, L.R., McCaffrey, J.P. and Morra, J.M. (1998) Toxicity of isothiocyanates produced by glucosinolates in Brassicaceae species to black vine weevil eggs. Journal of Agriculture and Food Chemistry, 46, 5318-5323.
12. Brodeur-Campbell, S.E., Vucetich, J.A., Richter, D.L., Waite, T. A., Rosemier, J.N. and Tsai, C.-J. (2006) Insect herbivory on low-lignin transgenic aspen. Environmental Entomology, 35, 1696-1701.
13. Brunelle, F., Girard, C., Cloutier, C. and Michaud, D. (2005) A haybrid, broad-spectrum inhibitor of Colorado potato beetle aspartate and cysteine digestive proteinases. Archives of Insect Biochemistry and Physiology, 60, 20-31.
14. Bu, Q.-Y., Wu, L., Yang, S.-H. and Wan, J.-M. (2006) Cloning of a potato proteinase inhibitor gene PINII-2x from diploid potato (Solanum phurejia L.) and transgenic investigation of its potential to confer insect resistance in rice. Journal of Integrative Plant Biology, 48, 732-739.
15. Chang, T., Chen, L., Chen, S., Cai, H., Liu, X., Xiao, G. and Zhu, Z. (2003) Transformation of tobacco with genes encoding Helianthus tuberosus agglutinin (HTA) confers resistance to peach-potato aphid (Myzus persicae). Transgenic Research, 12, 607-614.
16. Charity, J.A., Anderson, M.A., Bittisnich, D.J., Whitecross, M. and Higgins, T.J.V. (1999) Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Molecular Breeding, 5, 357-365.
17. Chen, H., Gonzales-Vigil, E., Wilkerson, C.G. and Howe, G.A. (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiology, 143, 1954-1967.
18. Chen, H., McCaig, B.C., Melotto, M., He, S.Y. and Howe, G.A. (2004) Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. Journal of Biological Chemistry, 279, 45998-46007.
19. Chen, H., Wilkerson, C.G., Kuchar, J.A., Phinney, B.S. and Howe, G.A. (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proceedings of the National Academy of Sciences of the United States of America, 102, 18771-18772.
20. Clissold, F.J., Sanson, G.D. and Read, J. (2004) Indigestibility of plant cell wall by the Australian plague locust, Chortoicetes terminifera. Entomologia Experimentalis et Applicata, 112, 159-168.
21. Cole, R.A. (1994) Isolation of a chitin-binding lectin, with insecticidal activity in chemically-defined synthetic diets, from two wild brassica species with resistance to cabbage aphid Brevicoryne brassicae. Entomologia Experimentalis et Applicata, 72, 181-187.
22. Confalonieri, M., Allegro, G., Balestrazzi, A., Fogher, C. and Delledonne, M. (1998) Regeneration of Populus nigra transgenic plants expressing a Kunitz proteinase inhibitor (KTi3) gene. Molecular Breeding, 4, 137-145.
23. Constabel, C.P., Bergey, D.R. and Ryan, C.A. (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 92, 407-411.
24. Cornelissen, T., Negreiros, D. and Fernandes, G. (2002) Plant resistance against gall-forming insects: the role of hypersensitivity. Mechanisms and Deployment of Resistance in Trees to Insects (eds. M.R. Wagner, K.M. Clancy, F. Lieutier & T.D. Paine), pp. 137-152. Kluwel Academic Publisher, Dordrecht, the Netherlands.
25. Dangl, J.L. and McDowell, J.M. (2006) Two modes of pathogen recognition by plants. Proceedings of the National Academy of Sciences of the United States of America, 103, 8575-8576.
26. Danks, H.V. (2002) Modification of adverse conditions by insects. Oikos, 99, 10-24.
27. De Luca, V. and St Pierre, B. (2000) The cell and developmental biology of alkaloid biosynthesis. Trends in Plant Science, 5, 168-173.
28. DeMoraes, C.M., Mescher, M.C. and Tumlinson, J.H. (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature, 410, 577-580.
29. Ding, L.-C., Hu, C., Yeh, K.-W. and Wang, P.-J. (1998) Development of insect-resistant transgenic cauliflower plants expressing the trypsin inhibitor gene isolated from local sweet potato. Plant Cell Reports, 17, 854-860.
30. Down, R.E., Gatehouse, A.M.R., Hamilton, W.D.O. and Gatehouse, J.A. (1996) Snowdrop lectin inhibits development and fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. Journal of Insect Physiology, 42, 1035-1045.
31. Duan, X., Li, X., Xue, Q., Abo-El-Saad, M., Xu, D. and Wu, R. (1996) Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nature Biotechnology, 14, 494-498.
32. Duffey, S.S. and Stout, M.J. (1996) Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology, 32, 3-37.
33. Dutta, I., Saha, P., Majumder, P., Sarkar, A., Chakraborti, D., Banerjee, S. and Das, S. (2005) The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnology Journal, 3, 601-911.
34. Estruch, J.J., Carozzi, N.B., Desai, N., Duck, N.B., Warren, G.W. and Koziel, M.G. (1997) Transgenic plants: An emerging approach to pest control. Nature Biotechnology, 15, 137-141.
35. Felton, G.W. (2005) Indigestion is a plant's best defense. Proceedings of the National Academy of Sciences of the United States of America, 102, 18771-18772.
36. Felton, G., Donato, K., Broadway, R. and Duffey, S. (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. Journal Insect Physiology, 38, 277-285.
37. Felton, G.W. and Summers, C.B. (1993) Potential role of ascorbate oxidase as a plant defense protein against insect herbivory. Journal of Chemical Ecology, 19, 1553-1568.
38. Felton, G.W., Bi, J.L., Summers, C.B., Mueller, A.J. and Duffey, S.S. (1994) Potential role of lipoxygenases in defense against insect herbivory. Journal of Chemical Ecology, 20, 651-666.
39. Feng, G.H., Chen, M.S., Kramer, K.J. and Reeck, G.R. (1991) α-Amylase inhibitors from rice: fractionation and selectivity towards insects, mammalian and bacterial alpha;-Amylases. Cereal Chemistry, 68, 516-521.
40. Fernandes, G.W. and Negreiros, D. (2001) The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecology Entomology, 26, 45-55.
41. Ferry, N., Edwards, M.G., Gatehouse, J.A. and Gatehouse, A.M. R. (2004) Plant-insect interactions: Molecular approaches to insect resistance. Current Opinion in Biotechnology, 15, 155-161.
42. Fischer, D.C., Kogan, M. and Paxton, J.D. (1990) Effect of glyceollin, asoybean phytoalexin, on feeding by three phytophagous beetles (Coleoptera: Coccinellidae): dose versus response. Environmental Entomology, 19, 1278-1282.
43. Fitches, E. and Gatehouse, J.A. (1998) A comparison of the short and long term effects of insecticidal lectins on the activities of soluble and brush border enzymes of tomato moth larvae (Lacanobia oleracea). Journal of Insect Physiology, 44, 1213-1224.
44. Fitches, E., Gatehouse, A.M.R. and Gatehouse, J.A. (1997) Effects of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on the development of the tomato moth (Lacanobia oleracea) larvae in laboratory and glasshouse trials. Journal of Insect Physiology, 43, 727-739.
45. Foissac, X., Loc, N.T., Christou, P., Gatehouse, A.M.R. and Gatehouse, J.A. (2000) Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). Journal of Insect Physiology, 46, 573-583.
46. Forkner, R.E., Marquis, R.J. and Lill, J.T. (2004) Feeny revisited: condensed tannins as anti-herbivore defenses in leaf-chewing herbivore communities of Quercus. Ecological Entomology, 29, 174-187.
47. Garza, R., Vera, J., Cardona, C., Barcenas, N. and Singh, S.P. (2001) Hypersensitive response of beans to Apion godmani (Coleoptera: Curculionidae). Journal of Economical Entomology, 94, 958-962.
48. 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. (1997) Transgenic potato plants with enhanced resistance to the tomato moth Lacanobia oleracea: growth room trials. Molecular Breeding, 3, 49-63.
49. Gatehouse, A.M.R., Down, R.E., Powell, K.S., Sauvion, N., Rahbe, Y., Newell, C.A., Merryweather, A., Hamilton, W.D. O. and Gatehouse, J.A. (1996) Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomologia Experimentalis et Applicata, 79, 295-307.
50. Gatehouse, A.M.R., Powell, K.S., Van Damme, E.J.M. and Gatehouse, J.A. (1995) Insecticidal properties of plant lectins: Their potential in plant protection. Lectins: Biomedical Perspectives (eds. A.J. Pusztai & S. Bardocz), pp. 35-58. Taylor and Francis, London, UK.
51. Giamoustaris, A. and Mithen, R. (1995) The effect of modifying the glucosinolate content of leaves on oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Annals of Applied Biology, 126, 347-363.
52. Gianoli, E., Rios, J.M. and Niemeyer, H.M. (1999) Within-plant allocation of a chemical defense in Secale cereale. Is concentration the appropriate currency of allocation? Chemoecology, 9, 113-117.
53. Goethals, K., Vereecke, D., Jaziri, M., Van Montagu, M. and Holsters, M. (2001) Leafy gall formation by Rhodococcus fascians. Annual Review of Phytopathology, 39, 27-52.
54. Goggin, F.L. (2007) Plant-aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology, 10, 399-408.
55. Goodman, R.N. and Novacky, A.J. (1994) The Hypersensitive Reaction in Plants to Pathogens. APS Press, St Paul. 256 pp.
56. Goussain, M.M., Prado, E. and Moraes, J.C. (2005) Effect of silicon applied to wheat plants on the biology and probing behaviour of the greenbug Schizaphis graminum (Rond.) (Hemiptera: Aphididae). Neotropical Entomology, 34, 807-813.
57. Graham, J., Gordon, S.C. and McNicol, R.J. (1997) The effect of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae). Annals of Applied Biology, 131, 133-139.
58. Green, T.R. and Ryan, C.A. (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science, 175, 776-777.
59. Grover, P.B. (1995) Hypersensitive response of wheat to the Hessian fly. Entomologia Experimentalis et Applicata, 74, 283-294.
60. Hahlbrock, K., Bednarek, P., Ciolkowski, I., Hamberger, B., Heise, A., Liedgens, H., Logemann, E., Nürnberger, T., Schmelzer, E., Somssich, I.E. and Tan, J. (2003) Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proceedings of the National Academy of Sciences of the United States of America, 100, 14569-14576.
61. Haruta, M., Major, I.T., Christopher, M.E., Patton, J.J. and Constabel, C.P. (2001) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Molecular Biology, 46, 347-359.
62. Harris, M.O., Freeman, T.P., Rohfritsch, O., Anderson, K.G., Payne, S.A. and Moore, J.A. (2006) Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Annals of the Entomological Society of America, 99, 305-316.
63. Heath, M.C. (2000) Hypersensitive response-related death. Plant Molecular Biology, 44, 321-334.
64. Herbert, R.B. (1989) The Biosynthesis of Secondary Metabolites. 2nd edn., Chapman and Hall, London. 232 pp.
65. Hertiani, T. (2007) Isolation and Structure Elucidation of Bioactive Secondary Metabolites from Indonesian Marine Sponges. Cuvillier Verlag, Düsseldorf. 344 pp.
66. Henzell, R.F. and Hall, W.T. (1974) Substituted phenols as repellents for male Costelytra zealandica (Goleoptera: Scarabaeidae) in mating flights. New Zealand Journal of Zoology, 1, 509-513.
67. Hilder, V.A., Powell, K.S., Gatehouse, A.M.R., Gatehouse, J.A., Gatehouse, L.N., Shi, Y., Hamilton, W.D.O., Merryweather, A., Newell, C., Timans, J.C., Peumans, W.J., Van Damme, E. J.M. and Boulter, D. (1995) Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgen Research, 4, 18-25.
68. Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, R.F. and Boulter, D. (1987) A novel mechanism of insect resistance engineered in to tobacco. Nature, 330, 160-163.
69. Hildmann, T., Ebneth, M., Penacortes, H., Sanchezserrano, J.J., Willmitzer, L. and Prat, S. (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell, 4, 1157-1170.
70. Hoglund, S., Larrson, S. and Wingsle, G. (2005) Both hypersensitive and non-hypersensitive responses are associated with resistance in Salix viminalis against the gall midge Dasineura marginemtorquens. Journal of Experimental Botany, 56, 3215-3222.
71. Horiguchi, T. and Kitagishik, K. (1971) Studies on rice seed protease V. Protease inhibitor in rice seed. Plant Cell Physiology, 12, 907-915.
72. Hostettmann, K.A. and Marston, A. (1995) Saponins (Chemistry and Pharmacology of Natural Products). Cambridge University Press, Cambridge, UK. 560 pp.
73. Huber, D.P.W. and Bohlmann, J. (2006) The role of terpene synthases in the direct and indirect defense of conifers against insect herbivory and fungal pathogens. Multigenic and Induced Systemic Resistance in Plants (eds. S. Tuzun & E. Bent), pp. 296-313. Springer-Verlag, New York.
74. Irvine, J.E. and Mirkov, T.E. (1997) The development of genetic transformation of sugarcane in Texas. International Sugar Journal, 60, 25-29.
75. Ishimoto, M., Sato, T., Chrispeels, M.J. and Kitamura, K. (1996) Bruchid resistance of transgenic azuki bean expressing seed α- amylase inhibitor of common bean. Entomologia Experimentalis et Applicata, 79, 309-315.
76. James, D.J., Passey, A.J., Webster, A.D., Barbara, D.J., Dandekar, A.M., Uratsu, S.L. and Viss, P. (1993) Transgenic apples and strawberries: advances in transformation, introduction of genes for insect resistance and field studies of tissue cultured plants. Acta Horticulturae, 336, 179-184.
77. Janzen, D.H., Juster, H.B. and Liener, I.E. (1976) Insecticidal action of the phytohemagglutinin in black beans on Bruchid beetle. Science, 192, 795-796.
78. Johnson, R., Narvaez, J., An, G. and Ryan, C.A. (1989) 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 of the United States of America, 86, 9871-9875.
79. Jongsma, M.A., Bakker, P.L., Peters, J., Bosch, D. and Stiekema, W.J. (1995) Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of the National Academy of Sciences of the United States of America, 92, 8041-8045.
80. Jongsma, M.A. and Bolter, C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 43, 885-895.
81. Kaloshian, I. (2004) Gene-for-gene disease resistance: Bridging insect pest and pathogen defense. Journal of Chemical Ecology, 30, 2419-2438.
82. Kang, J.-H., Wang, L., Giri, A. and Baldwin, I.T. (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuate impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell, 18, 3303-3320.
83. Kawano, T. (2003) Role of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports, 21, 829-837.
84. Kessler, A. and Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291, 2141-2144.
85. Kessler, A. and Baldwin, I.T. (2002) Plant responses to insect herbivory. Annual Review of Plant Biology, 53, 299-328.
86. Kessler, A., Halitschke, R. and Baldwin, I.T. (2004) Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science, 305, 665-668.
87. Koiwa, H., Bressan, R.A. and Hasegawa, P.M. (1997) Regulation of protease inhibitors and plant defense. Trends in Plant Science, 2, 379-384.
88. Komath, S.S., Kavitha, M. and Swamy, M.J. (2006) Beyond carbohydrate binding: new directions in plant lectin research. Organic and Biomolecular Chemistry, 4, 973-988.
89. Konno, K., Hirayama, C., Nakamura, M., Tateishi, K., Tamura, Y., Hattori, M. and Kohno, K. (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. The Plant Journal, 37, 370-378.
90. Kost, C. and Heil, M. (2006) Herbivore-induced plant volatiles induce an indirect defense in neighbouring plants. Journal of Ecology, 94, 619-628.
91. Larsson, H.S.S. and Wingsle, G. (2005) Both hypersensitive and non-hypersensitive responses are associated with resistance in Salix viminalis against the gall midge Dasineura marginemtorquens. Journal of Experimental Botany, 56, 3215-3222.
92. Lee, E.A., Byrne, P.F., McMullen, M.D., Snook, M.E., Wiseman, B.R., Widstrom, N.W. and Coe, E.H. (1998) Genetic mechanisms underlying apimaysin and maysin synthesis and corn earworm antibiosis in maize (Zea mays L.). Genetics, 149, 1997-2006.
93. 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. (1999) Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stål) in transgenic rice. Molecular Breeding, 5, 1-9.
94. Legaspi, J.C., Legaspi, Jr. B.C., King, E.G. and Saldan, R. (1997) Mexican rice borer, Eoreuma loftini (Lepidoptera: Pyralidae) in the lower Rio Grande valley of Texas: its history and control. Subtropical Plant Science, 49, 53-59.
95. Leplé, J.-C., Bonadebottino, M., Augustin, S., Pilate, G., Letan, V.D., Delplanque, A., Cornu, D. and Jouanin, L. (1995) Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Molecular Breeding, 1, 319-328.
96. Li, Y.E., Chen, Z.X., Wu, X., Li, S.J., Jiao, G.L., Wu, J.H., Fan, X. P., Meng, J.H., Zhu, Z., Wang, W., Zhu, Y., Xu, H.L., Xiao, G.F. and Li, X.H. (1998) Obtaining transgenic cotton plants with cowpea trypsin inhibitor gene. Acta Gossypii Sinica, 10, 237-243.
97. Li, L. and Steffens, J.C. (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta, 215, 239-247.
98. Liu, X.-M., Bai, J., Huang, L., Zhu, L., Liu, X., Weng, N., Reese, J.C., Harris, M., Stuart, J.J. and Chen, M.S. (2007) Gene expression of different wheat genotypes during attack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae. Journal of Chemical Ecology, 33, 2171-2194.
99. Lu, L., Lei, J., Ming, S., Li, L. and Cao, B. (2005) Study on transformation of cowpea trypsin inhibitor gene into cauliflower (Brassica oleracea L. var. botrytis). African Journal of Biotechnology, 4, 45-49.
100. Macedo, M.L.R., de Castro, M.M. and das Graças Machado Freire, M. (2004) Mechanisms of the insecticidal action of TEL (Talisia esculenta Lectin) against Callosobruchus maculates (Coleoptera: Bruchidae). Archives of Insect Biochemistry and Physiology, 56, 84-96.
101. Maheswaran, G., Pridmore, L., Franz, P. and Anderson, M.A. (2007) A proteinase inhibitor from Nicotiana alata inhibits the normal development of light-brown apple moth, Epiphyas postvittana in transgenic apple plants. Plant Cell Reports, 26, 773-782.
102. Mao, J., Burt, A.J., Ramputh, A.-L., Simmons, J., Cass, L., Hubbard, K., Miller, S., Altosaar, I. and Arnason, J.T. (2007) Diverted secondary metabolism and improved resistance to European corn borer (Ostrinia nubilalis) in maize (Zea mays L.) transformed with wheat oxalate oxidase. Journal of Agriculture and Food Chemistry, 55, 2582-2589.
103. Marchetti, S., Delledonne, M., Fogher, C., Chiabá, C., Chiesa, F., Savazzini, F., Giordano, A. (2000) Soybean Kunitz, C-II and PI-IV inhibitor genes confer different levels of insect resistance to tobacco and potato transgenic plants. Theoretical and Applied Genetics, 101, 519-526.
104. McManus, M.T., Burgess, E.P.J., Philip, B., Watson, L.M., Laing, W.A., Voisey, C.R. and White, D.W.R. (1999) Expression o the soybean (Kunitz) trypsin inhibitor in transgenic tobacco: effects on larval development of Spodoptera litura. Transgenic Research, 8, 383-395.
105. McManus, M.T., White, D.W.R. and McGregor, P.G. (1994) Accumulation of the chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Research, 3, 50-58.
106. Mochizuki, A., Nishizawa, Y., Onodera, H., Tabei, Y., Toki, S., Habu, Y., Ugaki, M. and Ohashi, Y. (1999) Transgenic rice plants expressing a trypsin inhibitor are resistant against rice stem borers, Chilo suppressalis. Entomologia Experimentalis et Applicata, 93, 173-178.
107. Morton, R.L., Schroeder, H.E., Bateman, K.S., Chrispeels, M.J., Armstrong, E. and Higgins, T.J.V. (2000) Bean α-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proceedings of the National Academy of Sciences of the United States of America, 97, 3820-3825.
108. Murdock, L.L., Huesing, J.E., Nielsen, S.S., Pratt, R.C. and Shade, R.E. (1990) Biological effects of plant lectins on the cowpea weevil. Phytochem, 29, 85-89.
109. Niemeyer, H.M. (1988) Hydroxamic acids (4-hydroxy-1,4- benzoxazin-3-ones), defence chemicals in Gramineae. Phytochem, 27, 3349-3358.
110. Nutt, K.A., Allsopp, P.G., McGhie, T.K., Shepherd, K.M., Joyce, P.A., Taylor, G.O., McQualter, R.B. and Smith, G.R. (1999) Transgenic sugarcane with increased resistance to canegrubs. Proceedings of Australian Society of Sugar Cane Technologists, 21, 171-176.
111. Pautot, V., Holzer, F.M., Reischt, B. and Walling, L.L. (1993) Leucine aminopeptidase: An inducible component of the defense response in Lycopersicon esculentum (tomato). Proceedings of the National Academy of Sciences of the United States of America, 90, 9906-9910.
112. Pechan, T., Cohen, A., Williams, W.P. and Luthe, D.S. (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proceedings of the National Academy of Sciences of the United States of America, 99, 13319-13323.
113. Pechan, T., Ye, J., Chang, Y.M., Mitra, A., Lin, L., Davis, F.M., Williams, W.P. and Luthe, D.S. (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell, 12, 1031-1040.
114. Peumans, W.J. and Van Damme, E.J.M. (1995) The role of lectins in plant defense. Histochemical Journal, 27, 253-271.
115. Powell, K.S. (2001) Antimetabolic effects of plant lectins towards nymphal stages of the planthoppers Tarophagous proserpina and Nilaparvata lugens. Entomologia Experimentalis et Applicata, 99, 71-77.
116. Powell, K.S., Gatehouse, A.M.R., Hilder, V.A. and Gatehouse, J. A. (1993) Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cinciteps. Entomologia Experimentalis et Applicata, 66, 119-126.
117. Powell, K.S., Gatehouse, A.M.R., Hilder, V.A. and Gatehouse, J. A. (1995) Antifeedant effects of plant-lectins and an enzyme on the adult stage of the rice brown planthopper, Nilaparvata lugens. Entomologia Experimentalis et Applicata, 75, 51-59.
118. Powell, K.S., Spence, J., Bharathi, M., Gatehouse, J.A. and Gatehouse, A.M.R. (1998) Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens. Journal Insect Physiology, 44, 529-539.
119. Ralph, J., Bunzel, M., Marita, J.M., Hatfield, R.D., Lu, F., Kim, H., Schatz, P.F., Grabber, J.H. and Steinhart, H. (2004) Peroxidase- dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochemistry Reviews, 3, 79-96.
120. Rawlings, N.D., Tolle, D.P. and Barrett, A.J. (2005) Evolutionary families of peptidase inhibitors. Biochemical Journal, 378, 705-716.
121. Rahbé, Y., Sauvion, N., Febvay, G., Peumans, W.J. and Gatehouse, A.M.R. (1995) Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Entomologia Experimentalis et Applicata, 76, 143-155.
122. Rao, K.V., Rathore, K.S., Hodges, T.K., Fu, X., Stoger, E., Sudhakar, D., Williams, S., Christou, P., Bharathi, M., Bown, D.P., Powell, K.S., Spence, J., Gatehouse, A.M.R. and Gatehouse, J.A. (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant Journal, 15, 469-477.
123. Rohfritsch, O. (2005) Gall making. Encyclopedia of Plant and Crop Science (ed. R. M. Goodman), pp. 1021-1022. Marcel Dekker, New York.
124. Ryan, C.A. (1990) Proteinase inhibitors in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 28, 425-449.
125. Salunke, B.K., Kotkar, H.M., Mendki, P.S., Upasani, S.M. and Maheshwari, V.L. (2005) Efficacy of flavonoids in controlling Callosobruchus chinensis (L.) (Coleoptera: Brachidae), a postharvest pest of grain legumes. Crop Protection, 24, 888-893.
126. Sane, V.A., Nath, P., Aminuddin, N. and Sane, P.V. (1997) Development of insect-resistant transgenic plants using plant genes: Expression of cowpea trypsin inhibitor in transgenic tobacco plants. Current Science, 72, 741-747.
127. Sarmah, B.K., Moore, A., Tate, W., Molvig, L., Morton, R.L., Rees, D.P., Chiaese, P., Chrispeels, M.J., Tabe, L.M. and Higgins, T.J. V. (2004) Transgenic chickpea seeds expressing high levels of a bean α-amylase inhibitor. Molecular Breeding, 14, 73-82.
128. Sauge, M.H., Kervella, J. and Pascal, T. (1998) Settling behaviour and reproductive potential of the green peach aphid Myzus persicae on peach varieties and a related wild Prunus. Entomologia Experimentalis et Applicata, 89, 233-242.
129. Sauvion, N., Charles, H., Febvay, G. and Rahbé, Y. (2004) Effects of jackbean lectin (ConA) on the feeding behaviour and kinetics of intoxication of the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata, 110, 31-44.
130. Sauvion, N., Rahbé, Y., Peumans, W.J., Van Damme, E.J.M., Gatehouse, J.A. and Gatehouse, A.M.R. (1996) Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae. Entomologia Experimentalis et Applicata, 79, 285-293.
131. Schmetz, E.A., Carroll, M.J., LeClere, S., Phipps, S.M., Meredith, J., Chourey, P.S., Alborn, H.T. and Teal, P.E.A. (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proceedings of the National Academy of Sciences of the United States of America, 103, 8894-8899.
132. Schroeder, F.C., del Campo, M.L., Grant, J.B., Weibel, D.B., Smedley, S.R., Bolton, K.L., Meinwald, J. and Eisner, T. (2006) Pinoresinol: A lignol of plant origin serving for defense in a caterpillar. Proceedings of the National Academy of Sciences of the United States of America, 103, 15497-15501.
133. Setamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E. and Legaspi, Jr. B.C. (2002) Evaluation of lectin-expressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): Effects on life history parameters. Journal of Economic Entomology, 95, 469-477.
134. Setamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E. and Legaspi, Jr. B.C. (2003) Effects of snowdrop lectin (GNA) on Mexican rice borer (Lepidoptera: Pyralidae) life history parameters. Journal of Economic Entomology, 96, 950-956.
135. Shade, R.E., Schroeder, H.E., Pueyo, J.J., Tabe, L.M., Murdock, L.L., Higgins, T.J.V. and Chrispeels, M.J. (1994) Transgenic pea seeds expressing the α-Amylase inhibitor of the common bean are resistant to bruchid beetles. Bio/Tech, 12, 793-796.
136. Shukle, R.H. and Murdock, L.L. (1983) Lipoxygenase, tryspsin inhibitor, and lectin from soybeans: effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae). Environmental Entomology, 12, 787-791.
137. Smith, C.M. and Boyka, E. (2006) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata, 122, 1-16.
138. Stoger, E., Williams, S., Christou, P., Down, R.E. and Gatehouse, J.A. (1999) Expression of the insecticidal lectin from snow drop (Galanthus nivalis agglutinin; GNA) in transgenic wheat plants: effects on predation by the grain aphid Sitobion avenae. Molecular Breeding, 5, 65-73.
139. Stone, G.N. and Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18, 512-522.
140. Sun, X., Wu, A. and Tang, K. (2002) Transgenic rice lines with enhanced resistance to the small brown planthopper. Crop Protection, 21, 511-514.
141. Tattersall, D.B., Bak, S., Jones, P.R., Olsen, C.E., Nielsen, J.K., Hansen, M.L., Høj, P.B., and Møller, B.L. (2001) Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science, 293, 1826-1828.
142. Terra, W.R., Ferreira, C., Jordao, B.P. and Dillon, R.J. (1996) Digestive enzymes. Biology of the Insect Midgut (eds. M. Lehane & P. Billingsley), pp. 153-186. Chapman and Hall, London.
143. Theis, N. and Lerdau, M. (2003) The evolution of function in plant secondary metabolites. International Journal of Plant Science, 164, S93-S102.
144. Thipyapong, P., Michelle, A.E., Hunt, D. and Steffens, J.C. (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta, 220, 105-117.
145. Thipyapong, P. and Steffens, J.C. (1997) Tomato polyphenol oxidase: Differential response of the polyphenol oxidase F promoter to injuries and wound signals. Plant Physiology, 115, 409-418.
146. Thipyapong, P., Stout, M.J. and Attajarusit, J. (2007) Functional analysis of polyphenol oxidases by antisense/sense technology. Molecules, 12, 1569-1595.
147. Thomas, J.C., Adams, D.G., Keppenne, V.D., Wasmann, C.C., Brown, J.K., Kanost, M.R. and Bohnert, H.J. (1995) Protease inhibitors of Manduca sexta expressed in transgenic cotton. Plant Cell Report, 14, 758-762.
148. Truitt, C.L., Wei, H.-X. and Pare, P.W. (2004) A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell, 16, 523-532.
149. Ussuf, K.K., Laxmi, N.H. and Mitra, R. (2001) Proteinase inhibitors: Plant-derived genes of insecticidal protein for developing insect-resistant transgenic plants. Current Science, 80, 847-853.
150. Vilaine, D.F., Thibivilliers, S., Kusiak, C., Sauge, M.H. and Dinant, S. (2007) Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environment, 30, 187-201.
151. van der Hoorn, R.A.L. and Jones, J.D.G. (2004) The plant proteolytic machinery and its role in defence. Current Opinion in Plant Biology, 7, 400-407.
152. Walling, L.L. (2000) The myriad plant responses to herbivores. Journal
153. Wan, J., Duning, F.M. and Bent, A.F. (2002) Probing plantpathogen interactions and downstream defense signaling using DNA microarrays. Functional and Integrative Genomics, 2, 259-273.
154. Wang, Z.-Y., Sun, X.-F., Wang, F., Tang, K.-X. and Zhang, J.-R. (2005) Enhanced resistance of snowdrop lectin (Galanthus nivalis L. agglutinin)-expressing maize to Asian corn borer (Ostrinia furnacalis Guenée) Journal of Integrative of Plant Biology, 47, 873-880.
155. Widstrom, N.W. and Snook, M.E. (1998) A gene controlling biosynthesis of isoorientin, a compound in corn silks antibiotic to the corn earworm. Entomologia Experimentalis et Applicata, 89, 119-124.
156. Williams, C.E., Collier, C.C., Nemacheck, J.A., Liang, C. and Cambron, S.E. (2002) A lectin-like wheat gene responds systemically to attempted feeding by avirulent first-instar Hessian fly larvae. Journal of Chemical Ecology, 28, 1411-1428.
157. Wink, M. (1999) Functions of plant secondary metabolites and their exploitation in biotechnology. Annual Plant Reviews, Vol. 3 (ed. M. Wink), Sheffield Academic Press, Sheffield, UK. 304 pp.
158. Xu, D., Xue, Q., McElroy, D., Mawal, Y., Hilder, V.A. and Wu, R. (1996) Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests. Molecular Breeding, 2, 167-173.
159. Yuan, Z., Zhao, C., Zhou, Y. and Tian, Y.C. (2001) Aphidresistant transgenic tobacco plants expressing modified gna gene. Acta Botanic Sinica, 43, 592-597.
160. Yeh, K.-W., Lin, M.-I., Tuan, S.-J., Chen, Y.-M., Lin, C.-J. and Kao, S.-S. (1997) Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Reports, 16, 696-699.
161. Zavala, J.A., Patankar, A.G., Gase, K., Hui, D. and Baldwin, I.T. (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiology, 134, 1181-1190.
162. Zhu, Y.C., Liu, X., Maddur, M., Oppert, B., Chen, M.S. (2005) Cloning and characterization of chymotrypsin- and trypsinlike cDNAs from the gut of the Hessian fly [Mayetiola destructor (Say)]. Insect Biochemistry and Molecular Biology, 35, 23-32.
163. Zhu, L., Liu, X.M., Liu, X., Jeannotte, R., Reese, J.C., Harris, M., Stuart, J.J. and Chen, M.S. (2008) Hessian fly (Mayetiola destructor) attack causes dramatic shift in carbon/nitrogen metabolism in wheat. Molecular Plant-Microbe Interaction, 21, 70-78.