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Part of the book series: Progress in Biological Control ((PIBC,volume 5))

Abstract

Bacillus thuringiensis (Bt) plants dominate today’s commercial market for insect-resistant transgenic crops. However, not all pests are susceptible to Bt Cry toxins and there are concerns that even susceptible species may evolve to become resistant to these crops. The search for alternatives is well under way, with significant progress already made towards producing transgenic crops expressing insecticidal compounds from plants, such as protease inhibitors, lectins and alpha-amylase inhibitors. New types of proteins from B. thuringiensis, such as the vegetative insecticidal proteins, are also being exploited. At an earlier stage of development but attracting much research interest are other insecticidal compounds, such as chitinases, defensins, enhancins, biotin-binding proteins, proteases and toxins, sourced from bacteria, viruses, plants and arthropods. Fusion proteins, combining the features of different insecticidal proteins, have significant potential for extending the range of insect species which could be controlled via transgenic plants. In the future, metabolic engineering of plants could allow us to alter with great precision the ways in which plants and insects interact. The compatibility of these novel insect control strategies with biological control and integrated pest management is discussed.

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References

  • Abdeen, A., Virgos, A., Olivella, E., Villanueva, J., Aviles, X., Gabarra, R., and Prat, S., 2005. Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Molecular Biology 57: 189–202.

    PubMed  CAS  Google Scholar 

  • Aharoni, A., Giri, A.P., Deuerlein, S., Griepink, F., de Kogel, W.J., Verstappen, F.W.A., Verhoeven, H.A., Jongsma, M.A., Schwab, W., and Bouwmeester, H.J., 2003. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15: 2866–2884.

    PubMed  CAS  Google Scholar 

  • Aharoni, A., Jongsma, M.A., and Bouwmeester, H.J., 2005. Volatile science? Metabolic engineering of terpenoids in plants. Trends in Plant Science 10: 594–602.

    PubMed  CAS  Google Scholar 

  • Alfonso-Rubi, J., Ortego, F., Castanera, 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 Sitophilas oryzae. Transgenic Research 12: 23–31.

    PubMed  CAS  Google Scholar 

  • Alibhai, M.F., and Rydal, T.J., 2003. Insect inhibitory lipid acyl hydrolases. United States Patent 6657046.

    Google Scholar 

  • Álvarez-Alfageme, F., Martinez, M., Pascual-Ruiz, S., Castanera, P., Diaz, I., and Ortego, F., 2007. Effects of potato plants expressing a barley cystatin on the predatory bug Podisus maculiventris via herbivorous prey feeding on the plant. Transgenic Research 16: 1–13.

    PubMed  Google Scholar 

  • Amirhusin, B., Shade, R.E., Koiwa, H., Hasegawa, P.M., Bressan, R.A., Murdock, L.L., and Zhu-Salzman, K., 2004. Soyacystatin N inhibits proteolysis of wheat alpha-amylase inhibitor and potentiates toxicity against cowpea weevil. Journal of Economic Entomology 97: 2095–2100.

    PubMed  CAS  Google Scholar 

  • Arai, S., and Abe, K., 2000. Cystatin-based control of insects, with special reference to oryzacystatin. In: Recombinant Protease Inhibitors in Plants, D. Michaud, ed., Eurekah.com, Georgetown, TX, USA, pp. 27–42.

    Google Scholar 

  • Ashouri, A., Michaud, D., and Cloutier, C., 2001a. Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes. BioControl 46: 401–418.

    Google Scholar 

  • Ashouri, A., Michaud, D., and Cloutier, C., 2001b. Unexpected effects of different potato resistance factors to the Colorado potato beetle (Coleoptera: Chrysomelidae) on the potato aphid (Homoptera: Aphididae). Environmental Entomology 30: 524–532.

    Google Scholar 

  • Azzouz, H., Campan, E.D.M., Cherqui, A., Saguez, J., Couty, A., Jouanin, L., Giordanengo, P., and Kaiser, L., 2005a. Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae). Journal of Insect Physiology 51: 941–951.

    PubMed  CAS  Google Scholar 

  • Azzouz, H., Cherqui, A., Campan, E.D.M., Rahbé, Y., Duport, G., Jouanin, L., Kaiser, L., and Giordanengo, P., 2005b. Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). Journal of Insect Physiology 51: 75–86.

    PubMed  CAS  Google Scholar 

  • Bates, S.L., Zhao, J.-Z., Roush, R.T., and Shelton, A.M., 2005. Insect resistance management in GM crops: past, present and future. Nature Biotechnology 23: 57–62.

    PubMed  CAS  Google Scholar 

  • Bell, H.A., Fitches, E.C., Down, R.E., Marris, G.C., Edwards, J.P., Gatehouse, J.A., and Gatehouse, A.M.R., 1999. The effect of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on Eulophus pennicornis (Hymenoptera: Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae). Journal of Insect Physiology 45: 983–991.

    PubMed  CAS  Google Scholar 

  • Bell, H.A., Fitches, E.C., Down, R.E., Ford, L., Marris, G.C., Edwards, J.P., Gatehouse, J.A., and Gatehouse, A.M.R., 2001a. Effect of dietary cowpea trypsin inhibitor (CpTI) on the growth and development of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and on the success of the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Pest Management Science 57: 57–65.

    PubMed  CAS  Google Scholar 

  • Bell, H.A., Fitches, E.C., Marris, G.C., Bell, J., Edwards, J.P., Gatehouse, J.A., and Gatehouse, A.M.R., 2001b. Transgenic GNA expressing potato plants augment the beneficial biocontrol of Lacanobia oleracea (Lepidoptera: Noctuidae) by the parasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Transgenic Research 10: 35–42.

    PubMed  CAS  Google Scholar 

  • Bell, H.A., Down, R.E., Fitches, E.C., Edwards, J.P., and Gatehouse, A.M.R., 2003. Impact of genetically modified potato expressing plant-derived insect resistance genes on the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae). Biocontrol Science and Technology 13: 729–741.

    Google Scholar 

  • Bell, H.A., Kirkbride-Smith, A.E., Marris, G.C., Edwards, J.P., and Gatehouse, A.M.R., 2004. Oral toxicity and impact on fecundity of three insecticidal proteins on the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Agricultural and Forest Entomology 6: 215–222.

    Google Scholar 

  • Bennett, J., Cohen, M.B., Katiyar, S.K., Ghareyazie, B., and Khush, G.S., 1997. Enhancing insect resistance in rice through biotechnology. In: Advances in Insect Control, N. Carozzi and M. Koziel, eds., Taylor & Francis, London, UK, pp. 75–93.

    Google Scholar 

  • Bernal, J.S., and Sétamou, M., 2003. Fortuitous antixenosis in transgenic sugarcane: antibiosis-expressing cultivar is refractory to ovipositing herbivore pests. Environmental Entomology 32: 886–894.

    Google Scholar 

  • Bi, R.-M., Jia, H.-Y., and Feng, D.-S., 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.

    CAS  Google Scholar 

  • Birch, N.E., Geoghegan, I.E., Majerus, M.E.N., McNicol, J.W., Hackett, C.A., Gatehouse, A.M.R., and Gatehouse, J.A., 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding 5: 75–83.

    Google Scholar 

  • Blackburn, M.B., Farrar, R.R., Novak, N.G., and Lawrence, S.D., 2006. Remarkable susceptibility of the diamondback moth (Plutella xylostella) to ingestion of Pir toxins from Photorhabdus luminescens. Entomologia Experimentalis et Applicata 121: 31–37.

    CAS  Google Scholar 

  • Boets, A., Arnaut, G., Van Rie, J., and Damme, N., 2006. Transgenic plants expressing insecticidal proteins and methods of producing the same. United States Patent 7091399.

    Google Scholar 

  • Bouchard, E., Cloutier, C., and Michaud, D., 2003a. Oryzacystatin I expressed in transgenic potato induces digestive compensation in an insect natural predator via its herbivorous prey feeding on the plant. Molecular Ecology 12: 2439–2446.

    PubMed  CAS  Google Scholar 

  • Bouchard, E., Cloutier, C., and Michaud, D., 2003b. Molecular interactions between an insect predator and its herbivore prey on transgenic potato expressing a cysteine protease inhibitor from rice. Molecular Ecology 12: 2429–2437.

    PubMed  CAS  Google Scholar 

  • Boulter, D., Edwards, G.A., Gatehouse, A.M.R., Gatehouse, J.A., and Hilder, V.A., 1990. Additive protective effects of different plant-derived insect resistance genes in transgenic tobacco plants. Crop Protection 9: 351–354.

    Google Scholar 

  • Bown, D.P., Wilkinson, H.S., and Gatehouse, J.A., 1997. 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 27: 625–638.

    PubMed  CAS  Google Scholar 

  • Brookes, G., and Barfoot, P., 2006. Global impact of biotech crops: socio-economic and environmental effects in the first ten years of commercial use. AgBioForum 9: 139–151.

    Google Scholar 

  • Brown, S.E., Cao, A.T., Dobson, P., Hines, E.R., Akhurst, R.J., and East, P.D., 2006. Txp40, a ubiquitous insecticidal toxin protein from Xenorhabdus and Photorhabdus bacteria. Applied and Environmental Microbiology 72: 1653–1662.

    PubMed  CAS  Google Scholar 

  • Brunelle, F., Girard, C., Cloutier, C., and Michaud, D., 2005. A hybrid, broad-spectrum inhibitor of Colorado potato beetle aspartate and cysteine digestive proteinases. Archives of Insect Biochemistry and Physiology 60: 20–31.

    PubMed  CAS  Google Scholar 

  • Bryan, G.T., Johnson, G.T., Parker, E.J., Scott, D.B., Tanaka, A., and Voisey, C.R., 2006. Peramine biosynthesis. PCT/NZ2006/000148.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Burgess, E.P.J., Lovei, G.L., Malone, L.A., Nielson, I.W., Gatehouse, H.S., and Christeller, J.T., 2002a. Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis. Journal of Insect Physiology 48: 1093–1101.

    PubMed  CAS  Google Scholar 

  • Burgess, E.P.J., Malone, L.A., Christeller, J.T., Lester, M.T., Murray, C., Philip, B.A., Phung, M.M., and Tregidga, E.L., 2002b. Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, Helicoverpa armigera and Spodoptera litura. Transgenic Research 11: 185–198.

    PubMed  CAS  Google Scholar 

  • Burgess, E.P.J., Philip, B.A., Christeller, J.T., Page, N.E.M., Marshall, R.K., and Wohlers, M.W., 2008. Tri-trophic effects of transgenic insect-resistant tobacco expressing a protease inhibitor or biotin-binding protein on adults of the predatory carabid beetle Ctenognathus novaezelandiae. Journal of Insect Physiology 54: 518–528.

    PubMed  CAS  Google Scholar 

  • Carlini, C.R., and Grossi-de-Sa, M.F., 2002. Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40: 1515–1539.

    PubMed  CAS  Google Scholar 

  • Chrispeels, M.J., and Raikhel, N.V., 1991. Lectins, lectin genes, and their role in plant defense. Plant Cell 3: 1–9.

    PubMed  CAS  Google Scholar 

  • Christeller, J.T., and Phung, M.M., 1998. Changes in biotin levels in the leaves of two apple cultivars during the season. New Zealand Journal of Crop and Horticultural Science 26: 39–43.

    CAS  Google Scholar 

  • Christeller, J.T., Burgess, E.P.J., Mett, V., Gatehouse, H.S., Markwick, N.P., Murray, C., Malone, L.A., Wright, M.A., Philip, B.A., Watt, D., Gatehouse, L.N., Lovei, G.L., Shannon, A.L., Phung, M.M., Watson, L.M., and Laing, W.A., 2002. The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor in tobacco and its effects on Helicoverpa armigera larvae. Transgenic Research 11: 161–173.

    PubMed  CAS  Google Scholar 

  • Christeller, J.T., Malone, L.A., Todd, J.H., Marshall, R.M., Burgess, E.P.J., and Philip, B.A., 2005. Distribution and residual activity of two insecticidal proteins, avidin and aprotinin, expressed in transgenic tobacco plants, in the bodies and frass of Spodoptera litura larvae following feeding. Journal of Insect Physiology 51: 1117–1126.

    PubMed  CAS  Google Scholar 

  • Christeller, J.T., Markwick, N.P., Poulton, J., and O’Callaghan, M., 2006. Binding of an insecticidal transgene product to soil: biological activity of soil-bound avidin and the effects of time and microbial activity. Soil Biology & Biochemistry 38: 2043–2052.

    CAS  Google Scholar 

  • Christou, P., Capell, T., Kohli, A., Gatehouse, J.A., and Gatehouse, A.M.R., 2006. Recent developments and future prospects in insect pest control in transgenic crops. Trends in Plant Science 11: 302–308.

    PubMed  CAS  Google Scholar 

  • Clouthier, C., and Michaud, D., 2000. Expression of protease inhibitors in potato. In: Recombinant Protease Inhibitors in Plants, D. Michaud, ed., Eurekah.com, Georgetown, TX, USA, pp. 148–166.

    Google Scholar 

  • Collins, C.L., Eason, P.J., Dunshea, F.R., Higgins, T.J.V., and King, R.H., 2006. Starch but not protein digestibility is altered in pigs fed transgenic peas containing -amylase inhibitor. Journal of the Science of Food and Agriculture 86: 1894–1899.

    CAS  Google Scholar 

  • Cooper, S.G., Douches, D.S., and Grafius, E.J., 2004. Combining genetic engineering and traditional breeding to provide elevated resistance in potatoes to Colorado potato beetle. Entomologia Experimentalis et Applicata 112: 37–46.

    CAS  Google Scholar 

  • Cooper, S.G., Douches, D.S., and Grafius, E.J., 2006. Insecticidal activity of avidin combined with genetically engineered and traditional host plant resistance against Colorado potato beetle (Coleoptera: Chrysomelidae) larvae. Journal of Economic Entomology 99: 527–536.

    PubMed  CAS  Google Scholar 

  • Couty, A., and Poppy, G., 2001. Does host-feeding on GNA-intoxicated aphids by Aphelinus abdominalis affect their longevity and/or fecundity? Entomologia Experimentalis et Applicata 100: 331–337.

    Google Scholar 

  • Couty, A., Clark, S.J., and Poppy, G.M., 2001a. Are fecundity and longevity of female Aphelinus abdominalis affected by development in GNA-dosed Macrosiphum euphorbiae? Physiological Entomology 26: 287–293.

    CAS  Google Scholar 

  • Couty, A., Down, R.E., Gatehouse, A.M.R., Kaiser, L., Pham-Delegue, M.H., and Poppy, G.M., 2001b. Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae). Journal of Insect Physiology 47: 1357–1366.

    PubMed  CAS  Google Scholar 

  • Cowgill, S.E., Danks, C., and Atkinson, H.J., 2004. Multitrophic interactions involving genetically modified potatoes, nontarget aphids, natural enemies and hyperparasitoids. Molecular Ecology 13: 639–647.

    PubMed  CAS  Google Scholar 

  • CRCSIIB, 2006. Cooperative Research Centre for Sugar Industry Innovation through Biotechnology 2005/06 Annual Report, Brisbane, Australia, 52 pp.

    Google Scholar 

  • Dall, D., Luque, T., and O’Reilly, D., 2001. Insect-virus relationships: sifting by informatics. BioEssays 23: 184–193.

    PubMed  CAS  Google Scholar 

  • De Leo, F., Bonade-Bottino, M., Ceci, L.R., Gallerani, R., and Jouanin, L., 2001. Effects of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests. Insect Biochemistry and Molecular Biology 31: 593–602.

    PubMed  CAS  Google Scholar 

  • de Oliveira, E.J., Rabinovitch, L., Monnerat, R.G., Passos, L.K.J., and Zahner, V., 2004. Molecular characterization of Brevibacillus laterosporus and its potential use in biological control. Applied and Environmental Microbiology 70: 6657–6664.

    PubMed  Google Scholar 

  • Delledonne, M., Allegro, G., Belenghi, B., Balestrazzi, A., Picco, F., Levine, A., Zelasco, S., Calligari, P., and Confalonieri, M., 2001. Transformation of white poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine proteinase inhibitor and analysis of insect pest resistance. Molecular Breeding 7: 35–42.

    CAS  Google Scholar 

  • Dively, G.P., 2005. Impact of transgenic VIP3A x Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community. Environmental Entomology 34: 1267–1291.

    Google Scholar 

  • Down, R.E., Gatehouse, A.M.R., Hamilton, W.D.O., and Gatehouse, J.A., 1996. Snowdrop lectin inhibits development and decreases 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.

    CAS  Google Scholar 

  • Down, R.E., Ford, L., Woodhouse, S.D., Raemaekers, R.J.M., Leitch, B., Gatehouse, J.A., and Gatehouse, A.M.R., 2000. Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.). Journal of Insect Physiology 46: 379–391.

    PubMed  CAS  Google Scholar 

  • Down, R.E., Ford, L., Woodhouse, S.D., Davison, G.M., Majerus, M.E.N., Gatehouse, J.A., and Gatehouse, A.M.R., 2003. Tritrophic interactions between transgenic potato expressing snowdrop lectin (GNA), an aphid pest (peach-potato aphid; Myzus persicae (Sulz.) and a beneficial predator (2-spot ladybird; Adalia bipunctata L.). Transgenic Research 12: 229–241.

    PubMed  CAS  Google Scholar 

  • Du, J., Foissac, X., Carss, A., Gatehouse, A.M.R., and Gatehouse, J.A., 2000. Ferritin acts as the most abundant binding protein for snowdrop lectin in the mid-guts of brown plant hopper (Nilaparvata lugens). Insect Biochemistry and Molecular Biology 30: 297–305.

    PubMed  CAS  Google Scholar 

  • Duchaud, E., Rusniok, C., Frangeul, L., Buchrieser, C., Givaudan, A., Taourit, S., Bocs, S., Boursaux-Eude, C., Chandler, M., Charles, J.F., Dassa, E., Derose, R., Derzelle, S., Freyssinet, G., Gaudriault, S., Medigue, C., Lanois, A., Powell, K., Siguier, P., Vincent, R., Wingate, V., Zouine, M., Glaser, P., Boemare, N., Danchin, A., and Kunst, F., 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nature Biotechnology 21: 1307–1313.

    PubMed  CAS  Google Scholar 

  • Dutta, I., Majumder, P., Saha, P., Ray, K., and Das, S., 2005a. Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Science 169: 996–1007.

    CAS  Google Scholar 

  • Dutta, I., Saha, P., Majumder, P., Sarkar, A., Chakraborti, D., Banerjee, S., and Das, S., 2005b. The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnology Journal 3: 601–611.

    PubMed  CAS  Google Scholar 

  • Estruch, J.J., Warren, G.W., Mullins, M.A., Nye, G.J., Craig, J.A., and Koziel, M.G., 1996. Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proceedings of the National Academy of Sciences of the USA 93: 5389–5394.

    PubMed  CAS  Google Scholar 

  • Fernandes, O.A., Faria, M., Martinelli, S., Schmidt, F., Carvalho, V.F., and Moro, G., 2007. Short-term assessment of Bt maize on non-target arthropods in Brazil. Scientia Agricola 64: 249–255.

    Google Scholar 

  • Ferry, N., Raemaekers, R.J.M., Majerus, M.E.N., Jouanin, L., Port, G., Gatehouse, J.A., and Gatehouse, A.M.R., 2003. Impact of oilseed rape expressing the insecticidal cysteine protease inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle). Molecular Ecology 12: 493–504.

    PubMed  CAS  Google Scholar 

  • Ferry, N., Jouanin, L., Ceci, L.R., Mulligan, A., Emami, K., Gatehouse, J.A., and Gatehouse, A.M.R., 2005. Impact of oilseed rape expressing the insecticidal serine protease inhibitor, mustard trypsin inhibitor-2 on the beneficial predator Pterostichus madidus. Molecular Ecology 14: 337–349.

    PubMed  CAS  Google Scholar 

  • Ferry, N., Edwards, M., Gatehouse, J., Capell, T., Christou, P., and Gatehouse, A., 2006. Transgenic plants for insect pest control: a forward looking scientific perspective. Transgenic Research 15: 13–19.

    PubMed  CAS  Google Scholar 

  • 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 tomato moth (Lacanobia oleracea) larvae in laboratory and glasshouse trials. Journal of Insect Physiology 43: 727–739.

    PubMed  CAS  Google Scholar 

  • Fitches, E., Edwards, M.G., Mee, C., Grishin, E., Gatehouse, A.M.R., Edwards, J.P., and Gatehouse, J.A., 2004. Fusion proteins containing insect-specific toxins as pest control agents: snowdrop lectin delivers fused insecticidal spider venom toxin to insect haemolymph following oral ingestion. Journal of Insect Physiology 50: 61–71.

    PubMed  CAS  Google Scholar 

  • Fitt, G.P., 2000. An Australian approach to IPM in cotton: integrating new technologies to minimise insecticide dependence. Crop Protection 19: 793–800.

    Google Scholar 

  • Flinn, P.W., Kramer, K.J., Throne, J.E., and Morgan, T.D., 2006. Protection of stored maize from insect pests using a two-component biological control method consisting of a hymenopteran parasitoid, Theocolax elegans, and transgenic avidin maize powder. Journal of Stored Products Research 42: 218–225.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Franco, O.L., Rigden, D.J., Melo, F.R., and Grossi-de-Sa, M.F., 2002. Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases - Structure, function and potential for crop protection. European Journal of Biochemistry 269: 397–412.

    PubMed  CAS  Google Scholar 

  • Gatehouse, A.M.R., Down, R.E., Powell, K.S., Sauvion, N., Rahbé, Y., Newell, C.A., Merryweather, A., and Gatehouse, J.A., 1996. Effects of GNA-expressing transgenic potato plants on peach-potato aphid, Myzus persicae. Entomologia Experimentalis et Applicata 79: 295–307.

    Google Scholar 

  • Gatehouse, A.M.R., Davison, 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.

    CAS  Google Scholar 

  • Gatehouse, A.M.R., Davison, G.M., Stewart, J.N., Galehouse, L.N., Kumar, A., Geoghegan, I.E., Birch, A.N.E., and Gatehouse, J.A., 1999. Concanavalin A inhibits development of tomato moth (Lacanobia oleracea) and peach-potato aphid (Myzus persicae) when expressed in transgenic potato plants. Molecular Breeding 5: 153–165.

    CAS  Google Scholar 

  • Gatehouse, J.A., Gatehouse, A.M.R., and Bown, D.P., 2000. Control of phytophagous insect pests using serine proteinase inhibitors. In: Recombinant Protease Inhibitors in Plants, D. Michaud, ed., Eurekah.com, Georgetown, TX, USA, pp. 9–26.

    Google Scholar 

  • Geng, J.H., Shen, Z.R., Song, K., and Zheng, L., 2006. Effect of pollen of regular cotton and transgenic Bt plus CpTI cotton on the survival and reproduction of the parasitoid wasp Trichogramma chilonis (Hymenoptera: Trichogrammatidae) in the laboratory. Environmental Entomology 35: 1661–1668.

    Google Scholar 

  • Gerard, P.J., 2000. Ryegrass endophyte infection affects Argentine stem weevil adult behaviour and susceptibility to parasitism. New Zealand Plant Protection 53: 406–409.

    Google Scholar 

  • Glare, T.R., O’Callaghan, M., Malone, L.A., Burgess, E.P.J., and Philip, B.A., 2004. Measuring environmental impacts of genetically modified crops in New Zealand. In: GM Crops–Ecological Dimensions, H.F. van Emden and A.J. Gray, eds., The Association of Applied Biologists, Warwick, UK, pp. 91–99.

    Google Scholar 

  • Gould, F., Anderson, A., Jones, A., Sumerford, D., Heckel, D.G., Lopez, J., Micinski, S., Leonard, R., and Laster, M., 1997. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Sciences of the USA 94: 3519–3523.

    PubMed  CAS  Google Scholar 

  • Graham, J., Gordon, S.C., and McNicol, J.W., 1997. The effects of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F., Coleoptera: Curculionidae). Annals of Applied Biology 131: 133–139.

    Google Scholar 

  • Graham, J., Gordon, S.C., Smith, K., McNicol, R.J., and McNicol, J.W., 2002. The effect of the cowpea trypspin inhibitor in strawberry on damage by vine weevil under field conditions. Journal of Horticultural Science & Biotechnology 77: 33–40.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Guo, H.N., Jia, Y.T., Zhou, Y.G., Zhang, Z.S., Ouyang, Q., Jiang, Y., and Tian, Y.C., 2004. Effects of transgenic tobacco plants expressing ACA gene from Amaranthus caudatus on the population development of Myzus persicae. Acta Botanica Sinica 46: 1100–1105.

    CAS  Google Scholar 

  • Guo, H.N., Wu, J.-H., Chen, X.-Y., Luo, X.-L., Lu, R., Shi, Y.-J., Qin, H.-M., Xiao, J.-L., and Tian, Y.-C., 2003. Cotton plants transformed with the activated chimeric Cry1Ac and API-B genes. Acta Botanica Sinica 45: 108–113.

    CAS  Google Scholar 

  • Guo, S.D., Cui, H.Z., Xia, L.Q., and Wu, D., 1999. Effects of CpTI-Bt transgenic cotton and Bt transgenic cotton on survival, growth and nutrition utilization of Helicoverpa armigera (Hübner). Scientia Agricultura Sinica 32: 1–7.

    Google Scholar 

  • Hajaij-Ellouze, M., Fedhila, S., Lereclus, D., and Nielsen-LeRoux, C., 2006. The enhancin-like metalloprotease from the Bacillus cereus group is regulated by the pleiotropic transcriptional activator PlcR but is not essential for larvicidal activity. FEMS Microbiology Letters 260: 9–16.

    PubMed  CAS  Google Scholar 

  • Han, L.Z., Wu, K.M., Peng, Y.F., Wang, F., and Guo, Y.Y., 2006. Evaluation of transgenic rice expressing Cry1Ac and CpTI against Chilo suppressalis and intrapopulation variation in susceptibility to Cry1Ac. Environmental Entomology 35: 1453–1459.

    Google Scholar 

  • Hao, C., Chai, B., Wang, W., Sun, Y., and Liang, A., 2005. Polyclonal antibody against Manduca sexta chitinase and detection of chitinase expressed in transgenic cotton. Biotechnology Letters 27: 97–102.

    PubMed  CAS  Google Scholar 

  • Harrison, R.L., and Bonning, B.C., 2001. Use of proteases to improve the insecticidal activity of baculoviruses. Biological Control 20: 199–209.

    CAS  Google Scholar 

  • Hayakawa, T., Hashimoto, Y., Mori, M., Kaido, M., Shimojo, E., Furusawa, I., and Granados, R.R., 2004. Transgenic tobacco transformed with the Trichopusia ni granulovirus enhancin gene affects insect development. Biocontrol Science and Technology 14: 211–214.

    Google Scholar 

  • He, H., Wang, Z., and Zhang, Y., 2008. Monitoring Bt resistance in the field; China as a case study. In: Environmental Impact of Genetically Modified/Novel Crops, N. Ferry and A.M.R. Gatehouse, eds., CAB International, Wallingford, UK, in press.

    Google Scholar 

  • Hilder, V.A., and Boulter, D., 1999. Genetic engineering of crop plants for insect resistance - a critical review. Crop Protection 18: 177–191.

    Google Scholar 

  • Hilder, V.A., Gatehouse, A.M.R., Sheerman, S., Barker, R.F., and Boulter, D., 1987. A novel mechanism of insect resistance engineered into tobacco. Nature 330: 160–163.

    CAS  Google Scholar 

  • Hogervorst, P.A.M., Ferry, N., Gatehouse, A.M.R., Wäckers, F.L., and Romeis, J., 2006. Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion. Journal of Insect Physiology 52: 614–624.

    PubMed  CAS  Google Scholar 

  • Hoover, K., Schultz, C.M., Lane, S.S., Bonning, B.C., Duffey, S.S., McCutchen, B.F., and Hammock, B.D., 1995. Reduction in damage to cotton plants by a recombinant baculovirus that knocks moribund larvae of Heliothis virescens off the plant. Biological Control 5: 419–426.

    Google Scholar 

  • Huang, J.K., Hu, R.F., Rozelle, S., and Pray, C., 2005. Insect-resistant GM rice in farmers’ fields: assessing productivity and health effects in China. Science 308(5722): 688–690.

    PubMed  CAS  Google Scholar 

  • Hukuhara, T., Hayakawa, T., and Wijonarko, A., 1999. Increased baculovirus susceptibility of armyworm larvae feeding on transgenic rice plants expressing an entomopoxvirus gene. Nature Biotechnology 17: 1122–1124.

    PubMed  CAS  Google Scholar 

  • ICAC, 2003. VIP cotton: a new type of transgenic cotton. The ICAC Recorder 21(2): 3–6.

    Google Scholar 

  • ICAC, 2004. Cotton: Review of the World Situation. Volume 58, Number 2. November–December 2004. International Cotton Advisory Committee, Washington, DC, USA. http://www.icac.org/cotton_info/publications/samples/reviews/erev_november_04.pdf (accessed 15 January 2008).

  • Ignacimuthu, S., and Prakash, S., 2006. Agrobacterium-mediated transformation of chickpea with alpha-amylase inhibitor gene for insect resistance. Journal of Biosciences 31: 339–345.

    PubMed  CAS  Google Scholar 

  • Ishimoto, M., Sato, T., Chrispeels, M.J., and Kitamura, K., 1996. Bruchid resistance of transgenic azuki bean expressing seed alpha-amylase inhibitor of common bean. Entomologia Experimentalis et Applicata 79: 309–315.

    CAS  Google Scholar 

  • Jackson, R.E., Marcus, M.A., Gould, F., Bradley, J.R., Jr., and Van Duyn, J.W., 2007. Cross-resistance responses of Cry1Ac-selected Heliothis virescens (Lepidoptera: Noctuidae) to the Bacillus thuringiensis protein Vip3A. Journal of Economic Entomology 100: 180–186.

    PubMed  CAS  Google Scholar 

  • James, C., 2005. Global Status of Commercialized Transgenic Crops: 2005. ISAAA Brief No. 34, International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY, USA.

    Google Scholar 

  • James, C., 2007. Global Status of Commercialized Biotech/GM Crops: 2007. ISAAA Brief No. 37, International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY, USA.

    Google Scholar 

  • Jongsma, M.A., and Bolter, C., 1997. The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology 43: 885–895.

    PubMed  CAS  Google Scholar 

  • Jorgensen, H.B., and Lovei, G.L., 1999. Tri-trophic effect on predator feeding: consumption by the carabid Harpalus affinis of Heliothis armigera caterpillars fed on proteinase inhibitor-containing diet. Entomologia Experimentalis et Applicata 93: 113–116.

    Google Scholar 

  • Jouanin, L., Bonade-Bottino, M., Girard, C., Morrot, G., and Giband, M., 1998. Transgenic plants for insect resistance. Plant Science 131: 1–11.

    CAS  Google Scholar 

  • Khan, S.A., Zafar, Y., Briddon, R.W., Malik, K.A., and Mukhtar, Z., 2006. Spider venom toxin protects plants from insect attack. Transgenic Research 15: 349–357.

    PubMed  CAS  Google Scholar 

  • Knowles, J.R., 1989. The mechanism of biotin-dependent enzymes. Annual Review of Biochemistry 58: 195–221.

    PubMed  CAS  Google Scholar 

  • Kondrak, M., Kutas, J., Szenthe, B., Patthy, A., Banfalvi, Z., Nadasy, M., Graf, L., and Asboth, B., 2005. Inhibition of Colorado potato beetle larvae by a locust proteinase inhibitor peptide expressed in potato. Biotechnology Letters 27: 829–834.

    PubMed  CAS  Google Scholar 

  • 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. Plant Journal 37: 370–378.

    PubMed  CAS  Google Scholar 

  • Kramer, K.J., Morgan, T.D., Thorne, J.E., Dowell, F.E., Bailey, M., and Howard, J.A., 2000. Transgenic avidin maize is resistant to storage insect pests. Nature Biotechnology 18: 670–674.

    PubMed  CAS  Google Scholar 

  • Lawo, N.C., and Romeis, J., 2008. Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea. Biological Control 44: 389–398.

    CAS  Google Scholar 

  • Lawrence, P.K., and Koundal, K.P., 2002. Plant protease inhibitors in control of phytophagous insects. Electronic Journal of Biotechnology [online]. 15 April 2002, 5(1). Available from: http://www.ejbiotechnology.info/content/vol5/issue1/full/3/index.html.

  • Lay, F.T., and Anderson, M.A., 2005. Defensins–components of the innate immune system in plants. Current Protein & Peptide Science 6: 85–101.

    CAS  Google Scholar 

  • Lay, F.T., Schirra, H.J., Scanlon, M.J., Anderson, M.A., and Craik, D.J., 2003. The three-dimensional solution structure of NaD1, a new floral defensin from Nicotiana alata and its application to a homology model of the crop defense protein alfAFP. Journal of Molecular Biology 325: 175–188.

    PubMed  CAS  Google Scholar 

  • Lecardonnel, A., Chauvin, L., Jouanin, L., Beaujean, A., Prevost, G., and Sangwan-Norreel, B., 1999. Effects of rice cystatin I expression in transgenic potato on Colorado potato beetle larvae. Plant Science 140: 71–79.

    CAS  Google Scholar 

  • Lee, M.K., Walters, F.S., Hart, H., Palekar, N., and Chen, J.S., 2003. Mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab delta-endotoxin. Applied and Environmental Microbiology 69: 4648–4657.

    PubMed  CAS  Google Scholar 

  • Lee, P.J., Ahn, J.Y., Kim, Y.H., Kim, S.W., Kim, J.Y., Park, J.S., and Lee, J., 2004. Cloning and heterologous expression of a novel insecticidal gene (tccC1) from Xenorhabdus nematophilus strain. Biochemical and Biophysical Research Communications 319: 1110–1116.

    PubMed  CAS  Google Scholar 

  • Lee, M.K., Miles, P., and Chen, J.S., 2006. Brush border membrane binding properties of Bacillus thuringiensis Vip3A toxin to Heliothis virescens and Helicoverpa zea midguts. Biochemical and Biophysical Research Communications 339: 1043–1047.

    PubMed  CAS  Google Scholar 

  • Legaspi, J.C., Legaspi, B.C., Jr., and Sétamou, M., 2004. Insect-resistant transgenic crops expressing plant lectins. In: Transgenic Crop Protection: Concepts and Strategies, O. Koul and D.S. Dhaliwal, eds., Science Publishers, Inc., Enfield, USA, pp. 85–116.

    Google Scholar 

  • Lei, J.J., Yang, W.J., Yuan, S.H., Ying, F.Y., and Qiong, L.C., 2006. Study on transformation of cysteine proteinase inhibitor gene into cabbage (Brassica oleracea var. capitata L.). In: Proceedings of the Joint Meeting of the Fourteenth Crucifer Genetics Workshop and Fourth I.S.H.S. Symposium on Brassicas, Y.P. Lim, ed., International Society Horticultural Science, Leuven 1, pp. 231–238.

    Google Scholar 

  • Leple, J.C., Bonade-Bottino, M., Augustin, S., Pilate, G., le Tan, 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.

    CAS  Google Scholar 

  • Lepore, L.S., Roelvink, P.R., and Granados, R.R., 1996. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. Journal of Invertebrate Pathology 68: 131–140.

    PubMed  CAS  Google Scholar 

  • Li, G.Y., Xu, X.P., Xing, H.T., Zhu, H.C., and Fan, Q., 2005. Insect resistance to Nilaparvata lugens and Cnaphalocrocis medinalis in transgenic indica rice and the inheritance of gna plus sbti transgenes. Pest Management Science 61: 390–396.

    PubMed  CAS  Google Scholar 

  • Li, X., Higgins, T.J.V., and Bryden, W.L., 2006. Biological response of broiler chickens fed peas (Pisum sativum L.) expressing the bean (Phaseolus vulgaris L.) -amylase inhibitor transgene. Journal of the Science of Food and Agriculture 86: 1900–1907.

    CAS  Google Scholar 

  • Lingling, L.V., Jianjun, L., Ming, S., Liyun, L., and Bihao, C., 2005. Study on transformation of cowpea trypsin inhibitor gene into cauliflower (Brassica oleracea L. var. botrytis). African Journal of Biotechnology 4: 45–49.

    Google Scholar 

  • Liu, D., Burton, S., Glancy, T., Li, Z.S., Hampton, R., Meade, T., and Merlo, D.J., 2003. Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nature Biotechnology 21: 1222–1228.

    PubMed  CAS  Google Scholar 

  • Liu, X.X., Zhang, Q.W., Zhao, J.Z., Li, H.C., Xu, B.L., and Ma, X.M., 2005. Effects of Bt transgenic cotton lines on the cotton bollworm parasitoid Microplitis mediator in the laboratory. Biological Control 35: 134–141.

    CAS  Google Scholar 

  • Liu, S.J., Li, H.R., Sivakumar, S., and Bonning, B.C., 2006a. Virus-derived genes for insect-resistant transgenic plants. In: Insect Viruses: Biotechnological Applications, B.C. Bonning, ed., Elsevier, San Diego, CA, USA, pp. 427–457.

    Google Scholar 

  • Liu, Y.J., Cheng, C.S., Lai, S.M., Hsu, M.P., Chen, C.S., and Lyu, P.C., 2006b. Solution structure of the plant defensin VrD1 from mung bean and its possible role in insecticidal activity against bruchids. Proteins-Structure Function and Bioinformatics 63: 777–786.

    CAS  Google Scholar 

  • Loc, N.T., Tinjuangjun, P., Gatehouse, A.M.R., Christou, P., and Gatehouse, J.A., 2002. Linear transgene constructs lacking vector backbone sequences generate transgenic rice plants which accumulate higher levels of proteins conferring insect resistance. Molecular Breeding 9: 231–244.

    CAS  Google Scholar 

  • Ma, X.M., Liu, X.X., Zhang, Q.W., Zhao, J.Z., Cai, Q.N., Ma, Y.A., and Chen, D.M., 2006. Assessment of cotton aphids, Aphis gossypii, and their natural enemies on aphid-resistant and aphid-susceptible wheat varieties in a wheat-cotton relay intercropping system. Entomologia Experimentalis et Applicata 121: 235–241.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Malone, L.A., Burgess, E.P.J., Mercer, C.F., Christeller, J.T., Murray, C., Phung, M.M., Philip, B.A., Tregidga, E.L., and Todd, J.H., 2002a. Effects of biotin-binding proteins on eight species of pasture invertebrates. New Zealand Plant Protection 55: 411–420.

    Google Scholar 

  • Malone, L.A., Tregidga, E.L., Todd, J.H., Burgess, E.P.J., Philip, B.A., Markwick, N.P., Poulton, J., Christeller, J.T., Lester, M.T., and Gatehouse, H.S., 2002b. Effects of ingestion of a biotin-binding protein on adult and larval honey bees. Apidologie 33: 447–458.

    CAS  Google Scholar 

  • Malone, L.A., Todd, J.H., Burgess, E.P.J., Philip, B.A., and Christeller, J.T., 2005. Effects of kiwifruit (Actinidia deliciosa) cysteine protease on growth and survival of Spodoptera litura larvae (Lepidoptera: Noctuidae) fed with control or transgenic avidin-expressing tobacco. New Zealand Journal of Crop and Horticultural Science 33: 99–105.

    CAS  Google Scholar 

  • Manyangarirwa, W., Turnbull, M., McCutcheon, G.S., and Smith, J., 2006. Gene pyramiding as a Bt resistance management strategy: how sustainable is this strategy? African Journal of Biotechnology 5: 781–785.

    CAS  Google Scholar 

  • Maqbool, S.B., Riazuddin, S., Loc, N.T., Gatehouse, A.M.R., Gatehouse, J.A., and Christou, P., 2001. Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Molecular Breeding 7: 85–93.

    CAS  Google Scholar 

  • Markwick, N.P., Christeller, J.T., Docherty, L.C., and Lilley, C.M., 2001. Insecticidal activity of avidin and streptavidin against four species of pest Lepidoptera. Entomologia Experimentalis et Applicata 98: 59–66.

    CAS  Google Scholar 

  • Markwick, N.P., Docherty, L.C., Phung, M.M., Lester, M.T., Murray, C., Yao, J.L., Mitra, D.S., Cohen, D., Beuning, L.L., Kutty-Amma, S., and Christeller, J.T., 2003. Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth and lightbrown apple moth, respectively. Transgenic Research 12: 671–681.

    PubMed  CAS  Google Scholar 

  • McCafferty, H.R.K., Moore, P.H., and Zhu, Y.J., 2006. Improved Carica papaya tolerance to carmine spider mite by the expression of Manduca sexta chitinase transgene. Transgenic Research 15: 337–347.

    PubMed  CAS  Google Scholar 

  • Mehlo, L., Gahakwa, D., Nghia, P.T., Loc, N.T., Capell, T., Gatehouse, J.A., Gatehouse, A.M.R., and Christou, P., 2005. An alternative strategy for sustainable pest resistance in genetically enhanced crops. Proceedings of the National Academy of Sciences of the USA 102: 7812–7816.

    PubMed  CAS  Google Scholar 

  • Meiyalaghan, S., Takla, M.F.G., Jaimess, O.O., Shang, Y.J., Davidson, M.M., Cooper, P.A., Barrell, P.J., Jacobs, J.M.E., Wratten, S.D., and Conner, A.J., 2005. Evaluation of transgenic approaches for controlling tuber moth in potatoes. Communications in Agricultural and Applied Biological Sciences (Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Ghent, Belgium) 70: 641–650.

    PubMed  CAS  Google Scholar 

  • Melander, M., Ahman, I., Kamnert, I., and Stromdahl, A.C., 2003. Pea lectin expressed transgenically in oilseed rape reduces growth rate of pollen beetle larvae. Transgenic Research 12: 555–567.

    PubMed  CAS  Google Scholar 

  • Morgan, T.D., Oppert, B., Czapla, T.H., and Kramer, K.J., 1993. Avidin and streptavidin as insecticidal and growth-inhibiting dietary proteins. Entomologia Experimentalis et Applicata 69: 97–108.

    CAS  Google Scholar 

  • Morton, R.L., Schroeder, H.E., Bateman, K.S., Chrispeels, M.J., Armstrong, E., and Higgins, T.J.V., 2000. Bean alpha-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 USA 97: 3820–3825.

    PubMed  CAS  Google Scholar 

  • Mulligan, E.A., Ferry, N., Jouanin, L., Walters, K.F.A., Port, G.R., and Gatehouse, A.M.R., 2006. Comparing the impact of conventional pesticide and use of a transgenic pest-resistant crop on the beneficial carabid beetle Pterostichus melanarius. Pest Management Science 62: 999–1012.

    PubMed  CAS  Google Scholar 

  • Murray, C., Sutherland, P.W., Phung, M.M., Lester, M.T., Marshall, R.K., and Christeller, J.T., 2002. Expression of biotin-binding proteins, avidin and streptavidin, in plant tissues using plant vacuolar targeting sequences. Transgenic Research 11: 199–214.

    PubMed  CAS  Google Scholar 

  • Nagadhara, D., Ramesh, S., Pasalu, I.C., Rao, Y.K., Krishnaiah, N.V., Sarma, N.P., Bown, D.P., Gatehouse, J.A., Reddy, V.D., and Rao, K.V., 2003. Transgenic indica rice resistant to sap-sucking insects. Plant Biotechnology Journal 1: 231–240.

    PubMed  CAS  Google Scholar 

  • Nagadhara, D., Ramesh, S., Pasalu, I.C., Rao, Y.K., Sarma, N.P., Reddy, V.D., and Rao, K.V., 2004. Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high level resistance to the whitebacked planthopper (Sogatella furcifera). Theoretical and Applied Genetics 109: 1399–1405.

    PubMed  CAS  Google Scholar 

  • Naimov, S., Dukiandjiev, S., and de Maagd, R.A., 2003. A hybrid Bacillus thuringiensis delta-endotoxin gives resistance against a coleopteran and a lepidopteran pest in transgenic potato. Plant Biotechnology Journal 1: 51–57.

    PubMed  CAS  Google Scholar 

  • Narva, K.E., Schnepf, H.E., Feitelson, J.S., Stockhoff, B.A., Schmeits, J., Loewer, D., Dullum, C.J., Muller-Cohn, J., Stamp, L., Morrill, G., and Finstad-Lee, S., 2003. Plants and cells transformed with a nucleic acid from Bacillus thuringiensis strain KB59A4–6 encoding a novel SUP toxin. United States Patent 6603063.

    Google Scholar 

  • O’Callaghan, M., Glare, T.R., Burgess, E.P.J., and Malone, L.A., 2005. Effects of plants genetically modified for insect resistance on nontarget organisms. Annual Review of Entomology 50: 271–292.

    PubMed  Google Scholar 

  • OGTR (Office of the Gene Technology Regulator), 2004. Risk Assessment and Risk Management Plan. Application for licence for dealings involving an intentional release of GMOs into the environment. DIR 048/2003. Title: Field trial to assess transgenic insecticidal cotton expressing natural plant genes. Applicant: Hexima Limited. July 2004. Office of the Gene Technology Regulator, Australian Government, Woden, Australia. http://www.ogtr.gov.au/pdf/ir/dir048finalrarmp.pdf (accessed 15 January 2008).

  • OGTR (Office of the Gene Technology Regulator), 2005. Risk Assessment and Risk Management Plan for DIR 058/2005. Limited and controlled release of insect resistant (VIP) GM cotton. Applicant: Deltapine Australia Pty Ltd. October 2005. Office of the Gene Technology Regulator, Australian Government, Woden, Australia. http://www.ogtr.gov.au/pdf/ir/dir058finalrarmp1.pdf (accessed 15 January 2008).

  • Outchkourov, N.S., de Kogel, W.J., Schuurman-de Bruin, A., Abrahamson, M., and Jongsma, M.A., 2004a. Specific cysteine protease inhibitors act as deterrents of western flower thrips, Frankliniella occidentalis (Pergande), in transgenic potato. Plant Biotechnology Journal 2: 439–448.

    PubMed  CAS  Google Scholar 

  • Outchkourov, N.S., de Kogel, W.J., Wiegers, G.L., Abrahamson, M., and Jongsma, M.A., 2004b. Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Frankliniella occidentalis) in greenhouse trials. Plant Biotechnology Journal 2: 449–458.

    PubMed  CAS  Google Scholar 

  • Pang, Y., Shen, G., Qi, H., Tan, E., Sun, X., and Tang, K., 2004. Transgenic tobacco expressing Zephyranthes candida agglutinin showing enhanced resistance to aphids. Engineering in Life Sciences 4: 155–159.

    CAS  Google Scholar 

  • Pechan, T., Ye, L.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.

    PubMed  CAS  Google Scholar 

  • Petell, J.K., Merlo, D.J., Herman, R.A., Roberts, J.L., Guo, L., Schafer, B.W., Sukhapinda, K., and Merlo, A.O., 2004. Transgenic plants expressing photorhabdus toxin. United States Patent 6717035.

    Google Scholar 

  • Peumans, W.J., and Van Damme, E.J.M., 1995. Lectins as plant defense proteins. Plant Physiology 109: 347–352.

    PubMed  CAS  Google Scholar 

  • 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 (Stal). Journal of Insect Physiology 44: 529–539.

    PubMed  CAS  Google Scholar 

  • Prescott, V.E., Campbell, P.M., Moore, A., Mattes, J., Rothenberg, M.E., Foster, P.S., Higgins, T.J.V., and Hogan, S.P., 2005. Transgenic expression of bean P-amylase inhibitor in peas results in altered structure and immunogenicity. Journal of Agricultural and Food Chemistry 53: 9023–9030.

    PubMed  CAS  Google Scholar 

  • Rahbé, Y., Deraison, C., Bonade-Bottino, M., Girard, C., Nardon, C., and Jouanin, L., 2003. Effects of the cysteine protease inhibitor oryzacystatin (OC-I) on different aphids and reduced performance of Myzus persicae on OC-I expressing transgenic oilseed rape. Plant Science 164: 441–450.

    Google Scholar 

  • Rao, K.V., Rathore, K.S., Hodges, T.K., Fu, X., E., S., 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.

    PubMed  CAS  Google Scholar 

  • Ribeiro, A.P.O., Pereira, E.J.G., Galvan, T.L., Picanco, M.C., Picoli, E.A.T., da Silva, D.J.H., Fari, M.G., and Otoni, W.C., 2006. Effect of eggplant transformed with oryzacystatin gene on Myzus persicae and Macrosiphum euphorbiae. Journal of Applied Entomology 130: 84–90.

    CAS  Google Scholar 

  • Romeis, J., Babendreier, D., and Wäckers, F.L., 2003. Consumption of snowdrop lectin (Galanthus nivalis agglutinin) causes direct effects on adult parasitic wasps. Oecologia 134: 528–536.

    PubMed  Google Scholar 

  • Romeis, J., Meissle M., and Bigler, F., 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24: 63–71.

    PubMed  CAS  Google Scholar 

  • Rowan, D.D., Dymock, J.J., and Brimble, M.A., 1990. Effect of fungal metabolite peramine and analogs on feeding and development of Argentine stem weevil (Listronotus bonariensis). Journal of Chemical Ecology 16: 1683–1695.

    CAS  Google Scholar 

  • Sadasivam, S., and Thayumanavan, B., 2003. Molecular Host Plant Resistance to Pests. Marcel Dekker, New York, USA.

    Google Scholar 

  • Sadeghi, A., Smagghe, G., Broeders, S., Hernalsteens, J.-P., De Greve, H., Peumans, W.J., and Van Damme, E.J.M., 2008. Ectopically expressed leaf and bulb lectins from garlic (Allium sativum L.) protect transgenic tobacco plants against cotton leafworm (Spodoptera littoralis). Transgenic Research 17: 9–18.

    PubMed  CAS  Google Scholar 

  • Saha, P., Majumder, P., Dutta, I., Ray, T., Roy, S.C., and Das, S., 2006. Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests. Planta 223: 1329–1343.

    PubMed  CAS  Google Scholar 

  • Sarmah, B.K., Moore, A., Tate, W., Molvig, L., Morton, R.L., Rees, D.P., Chiaiese, P., Chrispeels, M.J., Tabe, L.M., and Higgins, T.J.V., 2004. Transgenic chickpea seeds expressing high levels of a bean alpha-amylase inhibitor. Molecular Breeding 14: 73–82.

    CAS  Google Scholar 

  • Schroeder, H.E., Gollasch, S., Moore, A., Tabe, L.M., Craig, S., Hardie, D.C., Chrispeels, M.J., Spencer, D., and Higgins, T.J.V., 1995. Bean alpha-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L). Plant Physiology 107: 1233–1239.

    PubMed  CAS  Google Scholar 

  • Schuler, T.H., Denholm, I., Jouanin, L., Clark, S.J., Clark, A.J., and Poppy, G.M., 2001. Population-scale laboratory studies of the effect of transgenic plants on nontarget insects. Molecular Ecology 10: 1845–1853.

    PubMed  CAS  Google Scholar 

  • Sétamou, M., Bernal, J.S., Legaspi, J.C., and Mirkov, T.E., 2002a. Effects of snowdrop lectin (Galanthus nivalis agglutinin) expressed in transgenic sugarcane on fitness of Cotesia flavipes (Hymenoptera: Braconidae), a parasitoid of the nontarget pest Diatraea saccharalis (Lepidoptera: Crambidae). Annals of the Entomological Society of America 95: 75–83.

    Google Scholar 

  • Sétamou, M., Bernal, J.S., Legaspi, J.C., and Mirkov, T.E., 2002b. Parasitism and location of sugarcane borer (Lepidoptera: Pyralidae) by Cotesia flavipes (Hymenoptera: Braconidae) on transgenic and conventional sugarcane. Environmental Entomology 31: 1219–1225.

    Google Scholar 

  • Sétamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E., and Legaspi, B.C., Jr., 2002c. Evaluation of lectin-expressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history parameters and damage. Journal of Economic Entomology 95: 469–477.

    PubMed  Google Scholar 

  • 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 alpha-amylase inhibitor of the common bean are resistant to bruchid beetles. BioTechnology 12: 793–796.

    CAS  Google Scholar 

  • Shah, P.A., Gatehouse, A.M.R., Clark, S.J., and Pell, J.K., 2005. Wheat containing snowdrop lectin (GNA) does not affect infection of the cereal aphid Metopolophium dirhodum by the fungal natural enemy Pandora neoaphidis. Transgenic Research 14: 473–476.

    PubMed  CAS  Google Scholar 

  • Singh, P.K., Kumar, M., Chaturvedi, C.P., Yadav, D., and Tuli, R., 2004. Development of a hybrid delta-endotoxin and its expression in tobacco and cotton for control of a polyphagous pest Spodoptera litura. Transgenic Research 13: 397–410.

    PubMed  CAS  Google Scholar 

  • Song, X.X., and Wang, S.M., 2001. Status and evaluation on the expression of cotton varieties in the production in China in the past 20 years. Cotton Science 13: 315–320.

    Google Scholar 

  • Strickland, J.A., Orr, G.L., and Walsh, T.A., 1995. Inhibition of Diabrotica larval growth by patatin, the lipid acyl hydrolase from potato tubers. Plant Physiology 109: 667–674.

    PubMed  CAS  Google Scholar 

  • Sun, X., Wu, A., and Tang, K., 2002. Transgenic rice lines with enhanced resistance to the small brown planthopper. Crop Protection 21: 511–514.

    Google Scholar 

  • Syed, S.H., 2002. Genetic transformation of cotton with Galanthus nivalis agglutinin (GNA) gene and Cry1Ac + GNA. Ph.D. thesis, University of Punjab, Lahore, Pakistan.

    Google Scholar 

  • Syngenta, 2003. Syngenta Plans to Introduce a New Choice for Transgenic Control of Worms in Cotton. http://www.syngentacropprotection-us.com/media/article.asp?article_id=303 (accessed 15 January 2008).

  • Syngenta, 2007. About Syngenta: Biotechnology. http://www.syngenta.com/en/about_syngenta/biotech_pipeline.aspx (accessed 15 January 2008).

  • Tabashnik, B.E., Roush, R.T., Earle, E.D., and Shelton, A.M., 2002. Resistance to Bt toxins. Science 287(5450): 41.

    Google Scholar 

  • Tabashnik, B.E., Carriere, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M., and Zhao, J.Z., 2003. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology 96: 1031–1038.

    PubMed  CAS  Google Scholar 

  • Tinjuangjun, P., Loc, N.T., Gatehouse, A.M.R., Gatehouse, J.A., and Christou, P., 2000. Enhanced insect resistance in Thai rice varieties generated by particle bombardment. Molecular Breeding 6: 391–399.

    CAS  Google Scholar 

  • Tomov, B.W., Bernal, J.S., and Vinson, S.B., 2003. Impacts of transgenic sugarcane expressing GNA lectin on parasitism of Mexican rice borer by Parallorhogas pyralophagus (Marsh) (Hymenoptera: Braconidae). Environmental Entomology 32: 866–872.

    Google Scholar 

  • Treacy, M.F., Rensner, P.E., and All, J.N., 2000. Comparative insecticidal properties of two nucleopolyhedrovirus vectors encoding a similar toxin gene chimer. Journal of Economic Entomology 93: 1096–1104.

    PubMed  CAS  Google Scholar 

  • Trung, N.P., Fitches, E., and Gatehouse, J.A., 2006. A fusion protein containing a lepidopteran-specific toxin from the South Indian red scorpion (Mesobuthus tamulus) and snowdrop lectin shows oral toxicity to target insects. Biomed Central Biotechnology [online]. 16 March 2006, 6(18). Available from: http://www.biomedcentral.com/1472–6750/6/18.

  • USDA (United States Department of Agriculture), undated. National Information System for the Regional IPM Centers.United States Department of Agriculture. http://www.ipmcenters.org/newsletters.cfm?USDARegion=National%20Site&site (accessed 15 January 2008).

  • USEPA (United States Environmental Protection Agency), 2006a. Experimental use permit: receipt of application. Federal Register: May 26, 2006 (Volume 71, Number 102). United States Environmental Protection Agency. http://www.epa.gov/fedrgstr/EPA-PEST/2006/May/Day-26/p8042.htm (accessed 15 January 2008).

  • USEPA (United States Environmental Protection Agency), 2006b. Bacillus thuringiensis Vip3A Protein and the Genetic Material Necessary for its Production in Corn; Notice of Filing of a Pesticide. Petition to Establish a Temporary Tolerance. Federal Register: November 1, 2006 (Volume 71, Number 211). United States Environmental Protection Agency. http://www.epa.gov/EPA-PEST/2006/November/Day-01/p18425.htm (accessed 21 January 2008).

  • USEPA (United States Environmental Protection Agency), 2007. Biopesticides Registration Action Document Bacillus thuringiensis Cry3Bb1 corn. United States Environmental Protection Agency. http://www.epa.gov/pesticides/biopesticides/ingredients/tech_docs/cry3bb1/2_c_cry3bb1_environl.pdf (accessed 15 January 2008).

  • van Frankenhuyzen, K., and Nystrom, C., 2002. The Bacillus thuringiensis Toxin Specificity Database. http://www.glfc.cfs.nrcan.gc.ca/bacillus (accessed 15 January 2008).

  • Vila, L., Quilis, J., Meynard, D., Breitler, J.C., Marfa, V., Murillo, I., Vassal, J.M., Messeguer, J., Guiderdoni, E., and San Segundo, B., 2005. Expression of the maize proteinase inhibitor (mpi) gene in rice plants enhances resistance against the striped stem borer (Chilo suppressalis): effects on larval growth and insect gut proteinases. Plant Biotechnology Journal 3: 187–202.

    PubMed  CAS  Google Scholar 

  • Wakefield, M.E., Bell, H.A., Fitches, E.C., Edwards, J.P., and Gatehouse, A.M.R., 2006. Effects of Galanthus nivalis agglutinin (GNA) expressed in tomato leaves on larvae of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and the effect of GNA on the development of the endoparasitoid Meteorus gyrator (Hymenoptera: Braconidae). Bulletin of Entomological Research 96: 43–52.

    PubMed  CAS  Google Scholar 

  • Wang, E., Wang, R., DeParasis, J., Loughrin, J.H., Gan, S., and Wagner, G.J., 2001. Suppression of a P450 hydroxlase gene in plant trichome glands enhances natural-product-based aphid resistance. Nature Biotechnology 19: 371–374.

    PubMed  CAS  Google Scholar 

  • Wang, J.X., Chen, Z.L., Du, J.Z., Sun, Y., and Liang, A.H., 2005a. Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Reports 24: 549–555.

    PubMed  CAS  Google Scholar 

  • Wang, Z., Zhang, K., Sun, X., Tang, K., and Zhang, J., 2005b. Enhancement of resistance to aphids by introducing the snowdrop lectin gene gna into maize plants. Journal of Biosciences 30: 627–638.

    PubMed  CAS  Google Scholar 

  • Waterfield, N.R., Bowen, D.J., Fetherston, J.D., Perry, R.D., and ffrench-Constant, R.H., 2001. The tc genes of Photorhabdus: a growing family. Trends in Microbiology 9: 185–191.

    PubMed  CAS  Google Scholar 

  • Waterfield, N., Hares, M., Yang, G., Dowling, A., and ffrench-Constant, R., 2005. Potentiation and cellular phenotypes of the insecticidal toxin complexes of Photorhabdus bacteria. Cellular Microbiology 7: 373–382.

    PubMed  CAS  Google Scholar 

  • Whitehouse, M.E.A., Wilson, L.J., and Constable, G.A., 2007. Target and non-target effects on the invertebrate community of Vip cotton, a new insecticidal transgenic. Australian Journal of Agricultural Research 58: 273–285.

    CAS  Google Scholar 

  • Wood, H.G., and Barden, R.E., 1977. Biotin enzymes. Annual Review of Biochemistry 46: 385–413.

    PubMed  CAS  Google Scholar 

  • Wu, K.M., and Guo, Y.Y., 2005. The evolution of cotton pest management practices in China. Annual Review of Entomology 50: 31–52.

    PubMed  CAS  Google Scholar 

  • Wu, A., Sun, X., Pang, Y., and Tang, K., 2002. Homozygous transgenic rice lines expressing GNA with enhanced resistance to the rice sap-sucking pest Laodelphax striatellus. Plant Breeding 121: 93–95.

    Google Scholar 

  • Wu, J., Zhang, Z., Nie, Y., and Luo, X., 2005. High efficiency transformation of Gossypium hirsutum embryonic calli mediated by Agrobacterium tumefaciens and regeneration of insect-reistant plants. Plant Breeding 124: 142.

    CAS  Google Scholar 

  • Wu, J., Luo, X., Guo, H., Xiao, J., and Tian, Y., 2006. Transgenic cotton, expressing Amaranthus caudatus agglutinin, confers enhanced resistance to aphids. Plant Breeding 125: 390–394.

    CAS  Google Scholar 

  • Yao, J., Pang, Y., Qi, H., Wan, B., Zhao, X., Kong, W., Sun, X., and Tang, K., 2003. Transgenic tobacco expressing Pinellia ternata agglutinin confers enhanced resistance to aphids. Transgenic Research 12: 715–722.

    PubMed  CAS  Google Scholar 

  • Yao, J., Zhao, X., Qi, H., Wan, B., Chen, F., Sun, X., Yu, S., and Tang, K., 2004. Transgenic tobacco expressing an Arisaema heterophyllum agglutinin gene displays enhanced resistance to aphids. Canadian Journal of Plant Science 84: 785–790.

    CAS  Google Scholar 

  • Yoza, K., Imamura, T., Kramer, K.J., Morgan, T.D., Nakamura, S., Akiyama, K., Kawasaki, S., Takaiwa, F., and Ohtsubo, K., 2005. Avidin expressed in transgenic rice confers resistance to the stored-product insect pests Tribolium confusum and Sitotroga cerealella. Bioscience, Biotechnology and Biochemistry 69: 966–971.

    CAS  Google Scholar 

  • Yuan, Z.Q., Zhao, C.Y., Zhou, Y., and Tian, Y.C., 2001. Aphid-resistant transgenic tobacco plants expressing modified gna gene. Acta Botanica Sinica 43: 592–597.

    CAS  Google Scholar 

  • Zhang, B.-H., Liu, F., Yao, C.-B., and Wang, K.-B., 2000. Recent progress in cotton biotechnology and genetic engineering in China. Current Science 79: 37–44.

    CAS  Google Scholar 

  • Zhang, J.-H., Wang, C.-Z., Qin, J.-D., and Guo, S.-D., 2004. Feeding behaviour of Helicoverpa armigera on insect-resistant transgenic cotton and non-transgenic cotton. Journal Applied Entomology 128: 218–225.

    Google Scholar 

  • Zhu-Salzman, K., Ahn, J.E., Salzman, R.A., Koiwa, H., Shade, R.E., and Balfe, S., 2003. Fusion of a soybean cysteine protease inhibitor and a legume lectin enhances anti-insect activity synergistically. Agricultural and Forest Entomology 5: 317–323.

    Google Scholar 

  • Zhu, Y.C., Adamczyk, J.J., and West, S., 2005. Avidin, a potential biopesticide and synergist to Bacillus thuringiensis toxins against field crop insects. Journal of Economic Entomology 98: 1566–1571.

    PubMed  CAS  Google Scholar 

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Malone, L.A., Gatehouse, A.M.R., Barratt, B.I.P. (2008). Beyond Bt: Alternative Strategies for Insect-Resistant Genetically Modified Crops. In: Romeis, J., Shelton, A.M., Kennedy, G.G. (eds) Integration of Insect-Resistant Genetically Modified Crops within IPM Programs. Progress in Biological Control, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8373-0_13

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