Summary
The insecticidal cry (crystal) genes from Bacillus thuringiensis (Bt) have been used for insect control both as biopesticides and in transgenic plants. Discovery of new insecticidal genes is of importance for delaying the development of resistance in target insects. The diversity of Bt strains facilitates isolation of new types of cry and vip (vegetative insecticidal protein) genes. PCR is a useful technique for quick and simultaneous screening of Bt strains for classification and prediction of insecticidal activities. PCR together with other methods of analysis such as RFLP, gene sequence determination, electrophoretic, immunological and chromatographic analysis of Cry proteins and insect bioassays for evaluation of toxicity have been employed for identification of new insecticidal proteins. Some other new approaches have also been devised. Many Bt strains with novel insecticidal genes have been found. A desired combination of Cry proteins can be assembled via site-specific recombination vectors into a recipient Bt strain to create a genetically improved biopesticide. For better pest control, the cry genes have been transferred to plants. Stacking of more than one insecticidal gene is required for resistance management in transgenic crops. Modification of Cry proteins through protein engineering for increasing the toxicity and/or the insecticidal spectrum is also a promising approach, but requires detailed understanding of the structure and function of these proteins and analysis of toxin-receptor interactions. More research into this area will provide useful insights for the design of toxins for management of insect resistance. Insecticidal genes from other bacteria and plants are also being examined for their potential for deployment in transgenic crops. Stringent implementation of resistance management is needed for maintaining the efficacy of Bt transgenic crops and deriving maximum economic and environmental benefit.
Similar content being viewed by others
References
Adamczyk J.J., Hardee D.D., Adams L.C., Sumerford D.V., 2001 Correlating differences in larval survival and development of bollworm (Lepidoptera: Noctuidae) and fall armyworm (Lepidoptera: Noctuidae) to differential expression of Cry1A(c) delta-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton Journal of Economic Entomology 94:284–290
Akhurst R.J., James W., Bird L.J., Beard C., 2003 Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) Journal of Economic Entomology 96:1290–1299
Ammons D., Rampersad J., Khan A., 2002 Usefulness of staining parasporal bodies when screening for Bacillus thuringiensis Journal of Invertebrate Pathology 79:203–204
Aronson A.I., Shai Y., 2001 Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action FEMS Microbiology Letters 195:1–8
Arora N., Ahmad T., Rajagopal R., Bhatnagar R.K., 2003. A constitutively expressed 36 kDa exochitinase from Bacillus thuringiensis HD-1 Biochemical and Biophysical Research Communications 307:620–625
Avisar D., Keller M., Gazit E., Prudovsky E. Sneh B., Zilberstein A., 2004 The role of Bacillus thuringiensis Cry1C and Cry1E separate structural domains in the interaction with Spodoptera littoralis gut epithelial cells Journal of Biological Chemistry 279:15779–15786
Ballester V., Granoro F., Tabashnik B.E., Malvar T., Ferre J., 1999 Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella) Applied and Environmental Microbiology 65:1413–1419
Bandyopadhyaya S., Roy A., Das S., 2001 Binding of garlic (Allium sativum) leaf lectin to the gut receptors of homopteran pests is correlated with its insecticidal activity Plant Science 161:1025–1033
Barboza-Corona J.E., Lopez Meza J.E., Ibarra J.E., 1998 Cloning and expression of the cry 1Ea4 gene of Bacillus thuringiensis at comparative toxicity of its gene product World Journal of Microbiology and Biotechnology 14:437–441
Barloy F., Delecluse A., Nicolas L., Lecadet M., 1996 Cloning and expression of the first anaerobic toxin gene from Clostridium bifermentas subsp. malasia, encoding a new mosquitocidal protein with homologies to Bacillus thuringiensis delta-endotoxins Journal of Bacteriology 178:3099–3105
Barloy F., Lecadet M.M., Delecluse A., 1998 Cloning and sequencing of three new putative genes from Clostridium bifermentas CH18 Gene 211:293–299
Barton K.A., Whiteley H.R., Yang N.S., 1987 Bacillus thuringiensis delta-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to lepidopteran insects Plant Physiology 85:1103–1109
Baum J.A., Kakefuda M., Gawron-Burke C., 1996 Engineering Bacillus thuringiensis bioinsecticide with an indigenous site specific recombination system Applied and Environmental Microbiology 62:4367–4373
Baxter S.W., Zhao J.-Z., Gahan L.J., Shelton A.M., Tabashnik B.E., Heckel D.G., 2005 Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella Insect Molecular Biology 14:327–334
Beard C.E. Ranasinghe C., Akhurst R.J., 2001 Screening for novel cry genes by hybridization Letters in Applied Microbiology33:241–245
Beattie S.H., Halt C., Hirst D., Williams A.G., 1998 Discrimination among Bacillus cereus, Bacillus mycoides and Bacillus thuringiensis and some other species of the genus Bacillus by Fourier transform infrared spectroscopy FEMS Microbiology Letters 164:201–206
Bell H.A., Fitches E.C., Down R.E., Ford F., Marris G.C., Edwards J.P., Gatehouse J.A., Gatehouse A.M.R., 2001. 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: Eulophydae) Pesticide Management Science 57:57–65
Ben-Dov E., Zaritsky A., Dahan E., Barak Z., Sinai R., Manasherob R., Khamraev A., Troitskaya E., Dubitsky A., Berezino N., Margalith Y., 1997 Extended screening by PCR for seven cry group genes from field collected strains of Bacillus thuringiensis Applied and Environmental Microbiology 63:2997–3002
Ben-Dov E., Manasherob R., Zaritsky A., Barak Z., Margalith Y., 2001 PCR analysis of cry7 genes in Bacillus thuringiensis by the five conserved blocks of toxins Current Microbiology 42:96–99
Benedict J.H., Ring D.R., 2004 Transgenic crops expressing Bt proteins: current status, challenges and outlook. In: Koul O., Dhaliwal D.S., eds Transgenic Crop Protection: Concepts and Strategies.Enfield, NH: Science Publishers Inc. pp. 15–84. ISBN 1-57808-302-8
Bernhard K., Jarrett P., Meadows M., Butt J., Ellis D.J., Roberts G.M., Pauli S., Rodgers P., Burges H.D., 1997 Natural isolates of Bacillus thuringiensis: worldwide distribution, characterization and activity against insect pests Journal of Invertebrate Pathology 70:59–68
Bolter C.J., LatoszekGreen M., 1997. Effect of chronic ingestion of cysteine proteinase inhibitor, E-64, on Colorado potato beetle gut proteinases Entomological Experimental Applications 83:295–303
Bosch D., Schipper B., van der Kleij H., deMaagd R.A., Steikema W.J., 1994 Recombinant Bacillus thuringiensis crystal proteins with new properties: possibilities for resistance management Bio/Technology 12:915–918
Bourque S.N., Valero J.R., Mercier J., Lavoie M.C., Levesque R.C., 1993. Multiplex polymerase chain reaction for detection and differentiation of the microbial insecticide Bacillus thuringiensis Applied and Environmental Microbiology 59:523–527
Bowen D., Rocheleau T.A., Blackburn M., Andreev O., Golubeva E., Bhartia R., Ffrench-Constant R.H., 1998 Insecticidal toxins from the bacterium Photorhabdus luminescens Science 280:2129–2132
Bravo A., 1997 Phylogenetic relationship of Bacillus thuringiensis delta endotoxin family proteins and their functional domains Journal of Bacteriology 179:2793–2801
Bravo A., Jansens S., Peferoen M., 1992 Immunocytochemical characterization of Bacillus thuringiensis insecticidal crystal proteins in intoxicated insects Journal of Invertebrate Pathology 60:237–246
Bravo A., Sarabia S., Lopez L., Ontiveros H., Abarca C., Ortiz A., Ortiz M., Lina L., Villalobos F.J., Pena G., 1998. Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection Applied and Environmental Microbiology 64:4965–4972
Brito L.O., Lopes A.R., Parra J.R.P., Terra W.R., Silva M.C., 2001. Adaptation of tobacco budworm Heliothis virescens to proteinase inhibitors may be mediated by the synthesis of new proteinases Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology128:365–375
Brousseau R., Saintonge A., Prefontaine G., Masson L., Cabana J., 1993 Arbitrary primer polymerase chain reaction – a powerful method to identify Bacillus thuringiensis serovar and strains Applied and Environmental Microbiology 59:114–119
Burton S.L., Ellar D.J., Li J., Derbyshire D.J., 1999 N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognised by a site on the domain III lectin like fold of a Bacillus thuringiensis insecticidal toxin Journal of Molecular Biology 287:1011–1022
Butko P., 2003 Cytolytic toxin CytA and its mechanism of membrane damage: data and hypotheses Applied and Environmental Microbiology 69:2415–2422
Caprio M.A., 1998 Evaluating resistance management strategies for multiple toxins in the presence of external refuges Journal of Economic Entomology 91:1021–1031
Caprio M.A., Suckling D.M., 2000 Simulating the impact of cross resistance between Bt toxins in transformed clover and apples in New Zealand Journal of Economic Entomology 93:173–179
Carlson C.R., Kolsto A.B., 1993 A complete physical map of a Bacillus thuringiensis chromosome Journal of Bacteriology 175:1053–1060
Carmona A.A., Ibarra J.E., 1999 Expression and crystallization of Cry 3Aa–Cry-IAc chimerical protein of Bacillus thuringiensis World Journal of Microbiology and Biotechnology 15:455–463
Carozzi N.B., Kramer V.C., Warren G.W. Evola S., Koziel M.G., 1991 Prediction of insecticidal activity of Bacillus thuringiensis strains by polymerase chain reaction product profiles Applied and Environmental Microbiology 57:3057–3061
Ceron J., Ortiz A., Quintero R., Bravo A., 1995 Specific primers directed to identify cryI and cryIII genes in a Bacillus thuringiensis strain collection Applied and Environmental Microbiology 61:3826–3831
Chandra A., Ghosh P., Mandaokar A.D., Bera A.K., Sharma R.P., Das S., Kumar P.A., 1999 Amino acid substitution in α-helix 7 of Cry1Ac δ-endotoxin of Bacillus thuringiensis leads to enhanced toxicity to Helicoverpa armigera Hubner FEBS Letters 458:174–179
Chang L., Grant R., Aronson A., 2001 Regulation of the Packaging of Bacillus thuringiensis delta-endotoxins into inclusions Applied and Environmental Microbiology 67:5032–5036
Charity J.A., Anderson M.A., Bittisnich D.J., Whitecross M., 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
Chattopadhyaya A., Bhatnagar N.B., Bhatnagar R., 2004 Bacterial insecticidal toxins Critical Reviews in Microbiology 30:33–54
Chen F.-C., Shen L.-F., Chak K.-F., 2004 A facile analytical method for the identification of protease gene profiles from Bacillus thuringiensis strains Journal of Microbial Methods 56:125–132
Chestukhina G.C., Kostina L.I., Mikahilova S.A., Tyurin F., Klepikova S., Stepanov M., 1994 Production of multiple endotoxins by Bacillus thuringiensis: endotoxins produced by strains of the subspecies galleriae and wuhanenesis Canadian Journal of Microbiology 40:1026–1034
Chitra S., Narayanan R., Balakrishnan A., Jayaraman K., 1998 A rapid and specific method for the identification of Bacillus thuringiensis strains by indirect immunofluorescence Journal of Invertebrate Pathology 74:263–267
Choi S.K., Shin B.S., Kong E.M., Rho H.M., Park S.H., 2000 Cloning of a new cry 1I-type crystal protein gene Current Microbiology 41:65–69
Christov N.K., Imaishi H., Ohkawa H., 1999 Green-tissue-specific expression of a reconstructed cry1C gene encoding the active fragment of Bacillus thuringiensis delta-endotoxin in haploid tobacco plants conferring resistance to Spodoptera litura Biosciences Biotechnology and Biochemistry 63:1433–1444
Cody V., Luft J., Jensen E., Pangborn W., English L., 1992 Purification and crystallization of insecticidal delta endotoxin CryIII 2 from Bacillus thuringiensis proteins Structural and Functional Genetics 14:324–330
Crickmore N., Zeigler D.R., Feitelson J., Schnepf E., Van Rie J., Lereclus D., Baum J., Dean D.H., 1998. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins Microbiology and Molecular Biology Reviews 62:807–813
Damgaard P.H., 1995 Diarrhoeal enterotoxin production by strains of Bacillus thuringiensis isolated from commercial Bacillus thuringiensis based insecticides FEMS Immunology and Medical Microbiology 12:245–250
Datta K., Vasquez A., Tu J., Torrizo L., Alam M.F., Olivia N., Abrigo E., Khush, G.S., Datta S.K., 1998 Constitutive and tissue-specific differential expression of the cry1Ab gene in transgenic rice plants conferring resistance to rice insect pests Theoretical and Applied Genetics 97:20–30
De Cosa B., Moar W., Lee S.B., Miller M., Daniell H., 2001 Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals Nature Biotechnology 19:71–74
De Leo F., Bonade-Bottino M.A., Ceci L.R., Gallerani R., Jouanin L., 2001. Effect of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests Insect Biochemistry and Molecular Biology 31:593–602
De Leo F., Bonade-Bottino M.A., Ceci L.R., Gallerani R., Jouanin L., 1998. Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants Plant Physiology 118:997–1004
deMaagd R.A., Bravo A., Berry C., Crickmore N., Schnepf H.E., 2003 Structure, diversity and evolution of protein toxins from spore-forming entomopathogenic bacteria Annual Reviews in Genetics 37:409–433
deMaagd R.A., Bravo A., Crickmore N., 2001 How Bacillus thuringiensis has evolved specific toxins to colonize the insect world Trends in Genetics 17:193–199
deMaagd R.A., Wemen-Hendriks M., Steikema W., Bosch. D., 2000 Bacillus thuringiensis Delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different but not all Cry1–Cry1C hybrids Applied and Environmental Microbiology 66:1559–1563
deMaagd R.A., Bakker P.L., Masson L., Adang M.J., Sangadala S., Steikema W., Bosch D., 1999 Domain III of Bacillus thuringiensis delta endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and its purified amino peptidase N Molecular Microbiology 31:463–471
Dichn S.H., Chiu E.L., De Rocher E.J., Green P.J., 1998. Premature adenylation at multiple sites within a Bacillus thuringiensis toxin gene coding region Plant Physiology 117:143–1443
Donovan W.P., Donovan J.C., Engleman J.T., 2001 Gene knockout demonstrates that vip3A contributes to the pathogenesis of Bacillus thuringiensis toward Agrotis ipsilon and Spodoptera exigua Journal of Invertebrate Pathology 78:45–51
Doss V.A., Kumar A., Jayakumar R., Sekar V., 2002 Cloning and expression of vegetative insecticidal protein (vip3V) gene of Bacillus thuringiensis in Escherichia coli Protein Expression and Purification 26:82–88
Du J., Knowles B.H., Li J., Ellar D.J., 1999 Biochemical characterization of Bacillus thuringiensis cytolytic toxins in association with phospholipid bilayer Biochemical Journal 338:185–193
Duan X., Li X., Xue Q., Abo-El-saad M., Xu D., Wu R., 1996. Transgenic rice plants harbouring an introduced potato proteinase inhibitor II gene are insect-resistant Nature Biotechnology 14:494–496
Duan X., Gopalakrishnan B., Johnson L.B., White F.F., Wang X., Morgan T.D., Kramer K.J., Muthukrishnan S., 1998. Insect resistance of transgenic tobacco expressing an insect chitinase gene Transgenic Research 7:77–84
Dubois N.R., Dean D.H., 1995. Synergism between Cry1A insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae Environmental Entomology 24:1741–1747
Ebinuma H., Sugita K., Matsunaga E., Yamakado M., 1997. Selection of marker-free transgenic plants using the isopentenyl transferase gene Proceedings of the National Academy Sciences USA 94:2117–2121
Edmonds H.S., Gatehouse L.N., Hilder V.A., Gatehouse J.A., 1996. The antimetabolic effects of oryzacystatin on larvae of the Southern corn rootworm (Diabrotica undecimpunctata howardi): use of a bacterial expression system for oryzacystatin Entomological Experimental Applications 78:83–94
Estela A., Escriche B., Ferre J., 2004 Interaction of Bacillus thuringiensis toxins with larval midgut binding sites of Helicoverpa armigera (Lepidoptera: Noctuidae) Applied and Environmental Microbiology 70:1378–1384
Estruch J.J., Warren G.W., Mullins M.A., Nye G.J., Craig J.A., Koziel M.A., 1996 Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects Proceedings of the National Academy Sciences USA 93:5389–5394
Feitelson J.S., Payne J., Kim L., 1992. Bacillus thuringiensis insects and beyond Bio/Technology 10:271–275
Ffrench-Constant R.H., Bowen D.J., 2000 Novel insecticidal toxins from nematode-symbiotic bacteria Cellular and Molecular Life Sciences 57:828–833
Flexner J.L., Belnavis D.L., 1999 Microbial insecticides. In Rechcigl J.E., Rechcigl N.A., eds. Biological and Biotechnological Control of Insect Pests, Boca Raton: Lewis Publishers. pp., 35–62. ISBN 1-56670-479-0
Flores H., Soberon X., Sanchez J., Bravo A., 1997. Isolated domain II and III from the Bacillus thuringiensis Cry1Ab delta endotoxin binds to lepidopteran midgut membranes FEBS Letters 414:313–318
Foissac X., Loc N.T., Christou P., Gatehouse A.M.R., Gatehouse J.A., 2000. Resistance to green leaf hopper (Nephotettix virescens) and brown plant hoper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivaslis agglutinin, GNA) Journal of Insect Physiology 46:573–583
Forsyth G., Logan N.A., 2000 Isolation of Bacillus thuringiensis from northern Victoria land, Antarctica Letters in Applied Microbiology 30:263–266
Franco O.L., Rigden D.J., Melo M.R., Grossi-De-Sa M.F., 2002. Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases European Journal of Biochemistry 269:397–412
Fujimoto H., Itoh K., Yamamoto M., Kayozuka J., Shimamoto K., 1993. Insect resistant rice generated by a modified delta-endotoxin gene of Bacillus thuringiensis Bio/Technology 11:1151–1155
Garcia-Robles I., Sanchez J., Gruppe A., Martinez-Ramirez A.C., Rausell C., Real M.D., Bravo A., 2001 Mode of action of Bacillus thuringiensis PS86Q3 strain in hymenopteran forest pests Insect Biochemistry and Molecular Biology 31:849–856
Gatehouse A.M.R., Norton E., Davison G.M., Babbe S.M., Newell C.A., Gatehouse J.A., 1999. Digestive proteolytic activity in the larvae of tomato moth, Lacanobia oleracea: effect of plant protease inhibitors in vitro and in vivo Journal of Insect Physiology 45:545–558
Gatehouse J.A., Gatehouse A.M.R., 1999. Genetic engineering of plants for insect resistance. In Rechcigl J.E., Rechcigl N.A., eds. Biological and Biotechnological Control of Insect Pests, Boca Raton: Lewis Publishers. pp.211–241. ISBN 1-56670-479-0
Gaviria-Rivera A.M., Priest F.G., 2003 Molecular typing of Bacillus thuringiensis serovars by RAPD-PCR Systemic and Applied Microbiology 26:254–261
Gill M., Ellar D., 2002 Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1 Insect Molecular Biology 11:619–625
Gill S.S., Cowles E.A., Pietrantonio P.V., 1992 The mode of action of Bacillus thuringiensis endotoxins Annual Review of Entomology 37:615–636
Girard C., Le Metayer M., Zaccomer B., Barlet E., Williams L., Bonade-Bottino M., Pham-Delegue M.H., Jouanin L., 1998. Growth stimulation of beetle larvae reared on a transgenic oilseed rape expressing a cysteine proteinase inhibitor Journal of Insect Physiology 44:263–270
Gleave A.P., Mitra D.S., Markwick N.P., Morris B.A.M., Bouning L.L., 1998 Enhanced expression of the Bacillus thuringiensis cry9Aa2 gene in transgenic plants by nucleotide sequence modification confers resistance to potato tubermoth Molecular Breeding 4:459–472
Gomez I., Dean D.H., Bravo A., Soboren M., 2003 Cadherin-like receptor binding facilitates proteolytic cleavage of helix alph-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin Biochemistry 42:10482–10489
Gould F., 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology Annual Review of Entomology 43:701–726
Griffitts J.S., Whitacre J.L., Stevens D.E., Aroian R.V., 2001 Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme Science 293:860–864
Griffitts J.S., Huffman D.L., Whitacre J.L., Barrows B.D., Marroquin L.D., Muller R., Brown J.R., Hennet T., Esko J.D., Aroian R.V., 2003 Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin–host interactions Journal of Biological Chemistry 278:45594–45602
Griko N., Candas M., Zhang X., Junker M., Bulla L.A. Jr., 2004 Selective antaginism to the cadherin BT-R1 interferes with the calcium-induced adhesion of epithelial membrane vesicles Biochemistry 43:1393–1400
Grochulski P., Masson L., Borisova S., Pusztai-Carry M., Schwartz R. Brousseau R., Cygler M., 1995 Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation Journal of Molecular Biology 254:447–464
Gruden K., Strukelj B., Popovic T., Lenarcic B., Bevec T., Brzin J., Kregar I., Herzog-Velikonja J., Steikema W.J., Bosch D., Jongsma M.A., 1998. The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type-1 domain inhibitors Insect Biochemistry and Molecular Biology 28:549–560
Guerchicoff A., Delecluse A., Rubinstein C.P., 2001 The Bacillus thuringiensis cyt genes for hemolytic endotoxins constitute a gene family Applied and Environmental Microbiology 67:1090–1096
Guihard G., Laprade R., Schwartz J.L., 2001 Unfolding affects insect cell permeabilization by Bacillus thuringiensis Cry1C toxin Biochimica et Biophysica Acta 1515:110–119
Hansen B.M., Damgaard P.H., Eilenberg J., Pederson J.C., 1998. Characterization of Bacillus thuringiensis isolated from leaves and insects Journal of Invertebrate Pathology 71:106–114
Harsulkar A.M., Giri A.P., Patankar A.G., Gupta V.S., Sainani M.N., Ranjekar P.K., Deshpande V.V., 1999 Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth Plant Physiology 121:497–506
Haq S.K., Atif S.M., Khan R.H., 2004 Protein proteinase inhibitor genes in combat against insects, pests and pathogens: natural and engineered phytoprotection Archives of Biochemistry and Biophysics 431:145–189
Herrero S., Ferre J., Escriche B., 2001 Mannose phosphate isomerase isoenzymes in Plutella xylostella support common genetic bases of resistance to Bacillus thuringiensis toxins in Lepidopteran species Applied and Environmental Microbiology 67:979–981
Hilder V.A., Gatehouse A.M.R., Sheerman M.E., Baker R.F., Boulter, D. 1987. A novel mechanism of insect resistance engineered into tobacco Nature 330:160–163
Hofte H., Whiteley H.R., 1989 Insecticidal crystal proteins of Bacillus thuringiensis Microbiological Reviews 53:242–255
Honee G., Convents D., Van Rie J. Jansens S., Peferoen M., Visser B., 1991. The carboxyl terminal domain of the toxic fragment of a Bacillus thuringiensis crystal protein determines receptor binding Molecular Microbiology 5:2799–2806
Houseman J.G., Larocque A.M., Thie N.M.R., 1991. Insect proteases, plant protease inhibitors and possible pest control Memoirs of the Entomological Society of Canada 159:3–11
Hua G., Masson L., Jurat-Fuentes J.L., Schwab G., Adang M.J., 2001 Binding analyses of Bacillus thuringiensis Cry delta-endotoxins using brush border membrane vesicles of Ostrinia nubilalis Applied and Environmental Microbiology 67:872–879
Hua G., Jurat-Fuentes J.L., Adang M.J., 2004 Flourescent-based assays establish Manduca sexta BtR1a Cadherin as a receptor for multiple Bt Cry1A toxin in Drosophila S2 cells Insect Biochemistry and Molecular Biology 34:193–202
Huang J., Hu R., Rozelle S., Pray C., 2005 Insect-resistant GM rice in farmers’ fields: assessing productivity and health effects in China Science 308:688–690
Hwang S.H., Saitoh H., Mizuki E., Higuch K., Ohba M., 1998. A novel class of mosquitocidal delta endotoxin Cry19B encoded by a Bacillus thuringiensis serovar higo gene Systematic and Applied Microbiology 21:179–184
Ingle S.S., Trivedi N., Prasad R., Kuruvila J., Rao K.K., Chatpar H.S., 2001 Aminopeptidase-N from the Helicoverpa armigera (Hubner) brush border membrane vesicles as a receptor of Bacillus thuringiensis Cry1Ac δ-endotoxin Current Microbiology 43:255–259
Ishimoto M., Sato J., Chrispeels M.J., Kitamura K., 1996. Bruchid resistance of transgenic azuki bean expressing seed α-amylase inhibitor in the common bean Entomological Experimental Applications 79:309–315
Itoua-Apoyolo C., Drif L., Vassal J.M., De Barjac H., Bossy J.P., Leclant F., Frutos R., 1996 Isolation of multiple species of Bacillus thuringiensis from a population of the European Sunflower moth, Homoeosoma nebulella Applied and Environmental Microbiology 61:4343–4347
Jalali S.K., Mohan K.S., Singh S.P., Manjunath T.M., Lalitha Y., 2004 Baseline-susceptibility of the old-world bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) populations from India to Bacillus thuringiensis Cry1Ac insecticidal protein Crop Protection 23: 53–59
James, C. 2004 Global view of commercialized transgenic crops: 2004. ISAAA (International Service for Acquisition of Agri-biotech Applications), Brief no., 32 Preview, Ithaca, New York, ISBN 1-892456-36-2. http://www.isaaa.org/publications/briefs/Brief_32.htm
Jermutus L., Honeger A., Schwesinger F., Hanes J., Pluckthun A., 2001. Tailoring in vitro evolution for protein affinity or stability Proceedings of the National Academy Sciences USA 98:75–80
Johnson C., Bishop A.H., Turner C.L., 1998 Isolation and activity of strains of Bacillus thuringiensis toxic to larvae of the housefly (Diptera: Muscidae) and tropical blowflies (Diptera: Calliphoridae) Journal of Invertebrate Pathology 71:138–144
Johnson R., Narvaez J., An G., Ryan C., 1989. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects of natural defence against Manduca sexta larvae Proceedings of the National Academy Sciences USA 86:9871–9875
Jongsma M.A., Bakker P.L., Peters J., Bosch D., Steikema W.J., 1995. Adaptation of Spodoptera exigua larvae to the plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition Proceedings of the National Academy Sciences USA 92:8041–8045
Joshi B.N., Sainani M.N., Bastawade K.B., Deshpande V.V., Gupta V.S., Ranjekar P.K., 1999. Pearl millet cysteine proteinase inhibitor – evidence for the presence of two distinct sites responsible for antifungal and antifeedant activities European Journal of Biochemistry 265:556–563
Joung K.B., Cote J.C., 2001 Phylogenetic analysis of Bacillus thuringiensis serovars based on 16S rRNA gene restriction fragment length polymorphisms Journal of Applied Microbiology 90:115–122
Juarez-Perez V.M., Ferrandis M.D., Frutos R., 1997 PCR based approach for detection of novel Bacillus thuringiensis cry genes Applied and Environmental Microbiology 63:2997–3002
Jung Y.C., Kim S.U., Cote J.C., Lecadet M.M., Chung Y.S., Bok S.H., 1998. Characterization of a new Bacillus thuringiensis subsp. Rigo strain isolated from rice bran in Korea Journal of Invertebrate Pathology 71:95–96
Jurat-Fuentes J.L., Adang M.J., 2001 Importance of Cry1 delta-endotoxin domain II loops for binding specificity in Heliothis virescens (L.) Applied and Environmental Microbiology 67:323–329
Kalman S., Kiehne K.L., Libs J.L., Yamamoto T., 1993. Cloning of a novel cryIC-type gene from a strain of Bacillus thuringiensis subsp. galleriae Applied and Environmental Microbiology 59:1131–1137
Kasman L.M., Lukowiak A.A., Garczynski S.F., McNall R.J. Youngman P., Adang M.J., 1998. Phage display of a biologically active Bacillus thuringiensis toxin Applied and Environmental Microbiology 64:2995–3003
Kaur, S. 2002 Potential for development of novel Bacillus thuringiensis strains and transgenic crops and their implications for Indian agriculture AgBiotechNet 4: ABN 088, pp. 1–10. http://www.agbiotechnet.com CAB International
Kaur S., Singh A., 2000a Distribution of Bacillus thuringiensis isolates in different soil types from North India Indian Journal of Ecology 27: 52–60
Kaur S., Singh A., 2000b Natural occurrence of Bacillus thuringiensis in leguminous phylloplanes in the New Delhi region of India World Journal of Microbiology and Biotechnology 16:679–682
Kaur S., 2000 Molecular approaches towards development of novel Bacillus thuringiensis biopesticides World Journal of Microbiology and Biotechnology 16:781–793
Kaur S., 2004 Ecological, economic and social perspectives on transgenic crop protection: path for the developing world. In Koul O., Dhaliwal D.S., eds. Transgenic Crop Protection: Concepts and strategies. Enfield, NH: Science Publishers Inc. pp. 373–405. ISBN 1-57808-302-8
Kaur S., Gujar G.T., 2004 Contemporary approaches for genetically engineered insect resistant transgenic crops. In Dhaliwal G.S., Singh R., eds. Host Plant Resistance to Insects: Concepts and Applications. New Delhi: Panima Publishing Corporation. pp. 492–516. ISBN 81-86535-49-7
Kaur S., Rai R., Singh A., 2004 Role of transgenic microbes and endophytes in crop protection. In Koul O., Dhaliwal D.S., eds. Transgenic Crop Protection: Concepts and Strategies. Enfield, New Hampshire: Science Publishers Inc. pp. 289–306. ISBN 1-57808-302-8
Khanna H.K., Raina S.K., 2002. Elite indica transgenic plants expressing modified Cry 1Ac endotoxin of Bacillus thuringiensis show enhanced resistance to yellow stem borer (Scirpophaga incertulas) Transgenic Research 11:411–423
Kim H.S., Li M.S., 2001 Molecular cloning of a new crystal protein gene cry1Af1 of Bacillus thuringiensis NT0423 from Korean Sericultural Farms Current Microbiology 43:408–413
Kim H.S., Saitoh H., Yamashita S., Akao T., Park Y.S., Maeda M., Tanaka R., Mizuki E., Ohba M., 2003 Cloning and characterization of two novel crystal protein genes from a Bacillus thuringiensis serovar Dakota strain Current Microbiology 46:33–46
Koiwa H., Bressan R.A., Hasegawa P.M., 1997. Regulation of protease inhibitors and plant defense Trends in Plant Sciences 2:379–384
Kota M., Daniell H., Varma S., Garczynski S.F., Gould F., Moar W.J., 1999 Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects Proceedings of the National Academy of Sciences USA 96:1840–1845
Koziel M.G., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., Dawson J., Desai N., Hill M., Kadwell S., Launis K., Maddox D., McPherson K., Meghji M.R., Merlin E., Rhodes R., Warren G.W., Wright M., Evola S.V., 1993. Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis BioTechnology 11:194–200
Kronstad J.W., Whiteley H.R., 1986 Three classes of homologous Bacillus thuringiensis crystal protein genes Gene 43:29–40
Kumar A.S.M., Aronson A.I., 1999 Analysis of mutations in the pore-forming region essential for insecticidal activity of a Bacillus thuringiensis δ-endotoxin Journal of Bacteriology 181:6103–6107
Kumar P.A., Mandaokar A., Sreenivasu K., Chakrabarti S.K., Bisaria S., Sharma S.R., Kaur S., Sharma R.P., 1998 Insect resistant transgenic brinjal plants Molecular Breeding 4:33–37
Kumar S., Udaisuriyan V., Sangeetha P., Bharathi M., 2004 Analysis of Cry2A proteins encoded by genes cloned from indigenous isolates of Bacillus thuringiensis for toxicity against Helicoverpa armigera Current Science 86:566–570
Kumar H., Kumar V., 2004 Tomato expressing Cry1Ab insecticidal proteins from Bacillus thuringiensis protected against tomato fruit borer Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) damage in laboratory, greenhouse and field Crop Protection 23:135–139
Kuo W.S., Chak K.F., 1996. Identification of novel cry type genes from Bacillus thuringiensis strains on the basis of restriction fragment length polymorphism of the PCR amplified DNA Applied and Environmental Microbiology 62:1369–1377
Lecadet M.M., Franchon E., Dumanoir V.C., Ripoteau H., Hamon S., Laurent P., Thiery I., 1999 Updating the H-antigen classification of Bacillus thuringiensis Journal of Applied Microbiology 86:660–672
Lee M.K., Aguda R.M., Cohen M.B., Gould F.L., Dean D.H., 1997 Determination of binding of Bacillus thuringiensis endotoxin receptors to rice stem borer midguts Applied and Environmental Microbiology 63:583–586
Lee M.K., Walters F.S., Hart H., Palekar N., Chen J.-S., 2003 The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab δ-endotoxin Applied and Environmental Microbiology 69:4648–4657
Lereclus D., Mahillon J., Menou G., Lecadet M.M., 1986. Identification of Tn 4430, a transposon of Bacillus thuringiensis functional in Escherichia coli Molecular and General Genetics 204:52–57
Letourneau D.K., Hagen VII J.A., Robinson G.S., 2002 Bt crops: evaluating benefits under cultivation and risks from escaped transgenes in the wild. In Letourneau D.K., Burrows B.E., Eds. Genetically Engineered Organisms. Boca Raton: CRC Press, pp 33–98. ISBN 0-8493-0439-3
Li H., Gonzalez-Cabrera J., Opert B., Ferre J., Higgins R.A., Suschman L.L., Radke G.A., Zhu K.Y., Huang F., 2004 Binding analysis of Cry1Ab and Cry1Ac with membrane vesicles from Bt resistant and susceptible Ostrinia nubilalis Biochemical and Biophysical Research Communications 323:52–57
Li J., Caroll J., Ellar D.J., 1991. Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution Nature 353:815–821
Li J., Koni P.A., Ellar D.J., 1996 Structure of the mosquitocidal δ-endotoxin cytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation Journal of Molecular Biology 257:129–152
Lovgren A., Carlson C.R., Eskils K., Kolsto A.B., 1998. Localization of putative virulence genes on a physical map of the Bacillus thuringiensis subsp. gelechiae chromosome Current Microbiology 37:245–250
Malone L.A., Pham-Delegue M.H., 2001. Effects of transgene products on honey bees (Apis mellifera) and Bumble bees (Bombus sp.) Apidologie 32:287–304
Martin P., Travers R., 1989. Worldwide abundance and distribution of Bacillus thuringiensis isolates Applied and Environmental Microbiology 55:2437–2442
Masson L., Erlandson M., Puzstai-Carey M., Brousseau R., Juarez-Perez V., Frutos R., 1998. A holistic approach for determining the entomopatho potential of Bacillus thuringiensis strains Applied and Environmental Microbiology 64:4782–4788
Marroquin L.D., Elyssnia D., Griffitts J.S., Feitelson J.S., Aroian R.V., 2000 Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Ceanorhabditis elegans Genetics 155:1693–1699
McClintock J.T., VanBeek N.A.M., Kough J.L., Mendelsohn M.L., Hutton P.O., 1999 Regulatory aspects of biological control agents and products derived by biotechnology. In: Rechcigl J.E., Rechcigl N.A., eds. Biological and Biotechnological Control of Insect Pests Boca Raton: Lewis Publishers. pp. 305–357. ISBN 1-56670-479-0
McNall R.J., Adang M.J., 2003 Identification of novel Cry1Ac binding proteins in Manduca sexta midgut through proteomic analysis Insect Biochemistry and Molecular Biology 33:999–1010
Meadows M.P., Ellis D.J., Butt J., Jarrett P., Burges H.D., 1992 Distribution, frequency and diversity of Bacillus thuringiensis in an animal feed mill Applied and Environmental Microbiology 58:1344–1350
Mehlo L., Gahakwa D., Nghia P.T., Loc N.T., Capell T., Gatehouse J.A., Gatehouse A.M., Christou P., 2005 An alternative strategy for sustainable pest resistance in genetically enhanced crops Proceedings of the National Academy of Sciences USA 102:7812–7816
Michaud D., Nguyenquoc B., Yelle S., 1993 Selective inhibition of Colorado potato beetle cathepsin-H by oryzacystatin I and oryzacystatin II FEBS Letters 331:173–176
Miranda R., Zamudio F.Z., Bravo A., 2001 Processing of Cry1Ab delta-endotoxin from Bacillus thuringiensis by Manduca sexta and Spodoptera frugiperda midgut proteases: role in protoxin activation and toxin inactivation Insect Biochemistry and Molecular Biology 31:1155–1163
Moellenbeck D.J., Peters M.L., Bing J.W., Rouse J.R., Higgins L.S., Sims L., Nevshemal T., Marshall L., Ellis R.T., Bystrak P.G., Lang B.A., Stewart J.L., Kouba K., Sondag B., Gustafson B., Nour K., Xu D., Swenson J., Zhang J., Czapla T., Schwab G., Jayne S., Stockhoff B.A., Narva K., Schnepf H.E., Stelman S.J., Poutre C., Koziel M., Duck N., 2001 Insecticidal proteins from Bacillus thuringiensis protected corn from corn rootworms Nature Biotechnology 19:668–672
Monsanto Company, 2002 Insect efficacy testing with Bollgard®II cotton. Public interest document submitted to EPA. Monsanto Co., Saint Louis, MO, USA
Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellere-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carriere Y., Dennehy T.J., Brown J.K., Tabashnik B.E., 2003 Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm Proceedings of the National Academy of Sciences USA 100:5004–5009
Morris-Coole C., 1995 Bacillus thuringiensis: ecology, the significance of natural genetic modification and regulation World Journal of Microbiology and Biotechnology 11:471–477
Naimov S., Weemen-Hendriks M., Dukiandjiev S., de Maagd R.A., 2001 Bacillus thuringiensis delta-endotoxin Cry1 hybrid proteins with increased activity against the Colorado potato beetle Applied and Environmental Microbiology 67:5328–5330
Naimov S., Dukiandjiev S., 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
Okumura S., Akao T., Mizuki E., Ohba M., Inouye K., 2001 Screening of the Bacillus thuringiensis Cry1Ac delta-endotoxin on the artificial phospholipid monolayer incorporated with brush border membrane vesicles of Plutella xylostella by optical biosensor technology Journal of Biochemical and Biophysical Methods 47:177–188
Orr G.L., Strickland J.A., Walsh T.A., 1994. Inhibition of diabrotica larval growth by a multicystatin from potato tubers Journal of Insect Physiology 40:893–900
Park H.W., Frederici B.A., 2004 Effect of specific mutations in helix alpha7 of domain I on the stability and crystallization of Cry3A in Bacillus thuringiensis Molecular Biotechnology 27:89–100
Perlak F.J., Deaton R.W., Armstrong T.A., Fuchs R.L., Sims S.R., Greenplate J.T., Fischoff D.A., 1990. Insect resistant cotton plants Bio/Technology 8:939–943
Perlak F.J., Stone T.B., Muskopf Y.N., Petersen L.J., Parker G.B., Mcpherson S.A., Wyman J., Love S., Reed. G., Biever D., Fischoff D.A., 1993. Genetically improved potatoes: protection from damage by Colorado potato beetles Plant Molecular Biology 22:313–321
Peyronnet O., Nieman B., Genereux F., Vachon V., Laprade R., Schwartz J.L., 2004 Estimation of the radius of the pores formed by the Bacillus thuringiensis Cry1C δ-endotoxin in planar lipid bilayers Biochimica et Biophysica Acta 1567:113–122
Powell K.S., Spence J., Bharathi M., Gatehouse J.A., Gatehouse A.M.R., 1998. Immunohistochemical and developmental studies to elucidate the mechanism of action of the snow drop lectin on the rice brown planthopper, Nilaparvata lugens (Stal.) Journal of Insect Physiology 44:529–539
Pueyo J.J., Morgan T.D., Ameenuddin N., Liang C., Reeck G.R., Chrispeels M.J., Kramer K.J., 1995. Effects of bean and wheat alpha-amylase inhibitors on alpha amylase activity and growth of stored-product insect pests Entomological Experimental Applications 75:237–244
Rajagopal R., Agrawal N., Selvapandiyan A., Sivakumar S., Ahmad S., Bhatnagar R.K., 2003 Recombinantly expressed isoenzymic aminopeptidases from Helicoverpa armigera (American cotton bollworm) midgut display differential interaction with closely related Bacillus thuringiensis insecticidal proteins Biochemical Journal 370:971–978
Rajamohan F., Alzate O., Cotrill J.A., Curtiss A., Dean D.H., 1996. Protein engineering of Bacillus thuringiensis δ-endotoxin mutations at domain II of CryIAb enhance receptor affinity and toxicity towards gypsy moth larvae Proceedings of the National Academy Sciences of the USA 93:14338–14343
Ramachandran S., Buntin G.D., All J.N., Tabashnik B.E., Reymer P.L., Adang M.J., Pulliam D.A., Steward C.N. Jr., 1998 Survival, development and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola toxin Journal of Economic Entomology 91:1239–1244
Ramesh S., Nagadhara D., Reddy V.D., Rao K.V., 2004 Production of transgenic indica rice resistant to yellow stem borer and sap-sucking insects using super-binary vectors of Agrobacterium Plant Science 166:1077–1085
Ranasinghe C., Akhurst R.J., 2002 Matrix associated laser desorption ionization time of flight mass spectrometry (MALDi-TOF MS) for detecting novel Bt toxins Journal of Invertebrate Pathology 79:51–58
Rang C., Vacon V., Maagd R.A., Villon M., Schwartz J.-L., Bosch D., Frutos R., Laprade R., 1999 Interaction between functional domains of Bacillus thuringiensis insecticidal crystal proteins Applied and Environmental Microbiology 65:2918–2925
Rang C., Vachon V., Coux F., Carret C., Moar W.J., Brousseau R., Schwartz J.L., Laprade R., Frutos R., 2001 Exchange of domain I from Bacillus thuringiensis Cry1 toxins influences protoxin stability and crystal formation Current Microbiology 43:1–6
Rao K.V., Rathore K.S., Hodges T.K., Fu X., Stoger E.F., Sudhakar D., Williams S., Christou P., Bharathi M., Bown D.P., Powell K.S., Spence J., Gatehouse A.M.R., Gatehouse J.A., 1998. Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown plant hopper Plant Journal 15:469–477
Rausell C., Garcia-Robles I., Munoz-Garay C., Martinez-Raminez A.C., Real M.D., Bravo A., 2004 Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say) Biochimica et Biophysica Acta 1660:99–105
Roush R., 1997 Managing resistance to transgenic crops. In Carozzi N., Koziel M.G., eds. Advances in Insect Control: The Role of Transgenic Plants, London: Taylor and Francis. pp. 271–294. ISBN 0748404171
Sampson M.N., Gooday G.W., 1998. Involvement of chitinases of Bacillus thuringiensis during pathogenesis in insects Microbiology 144:2189–2194
Sanchis V., Agaisse H., Chaufaux J., Lereclus D., 1997 A recombinase mediated system for elimination of antibiotic resistance gene markers from genetically engineered Bacillus thuringiensis strains Applied and Environmental Microbiology 63:779–784
Sanchis V., Gohar M., Chaufaux J., Arantes O., Meier A., Agaisse H., Cayley J., Lereclus D., 1999 Development and field performance of a broad-spectrum nonviable asporogenic recombinant strain of Bacillus thuringiensis with greater potency and UV resistance Applied and Environmental Microbiology 65:4032–4039
Saxena D., Stewart C.N., Altosaar I., Shu Q., Stotzky G., 2004 Larvicidal Cry proteins from Bacillus thuringiensis are released in root exudates of transgenic Bacillus thuringiensis canola, cotton and tobacco Plant Physiology and Biochemistry 42:383–387
Sayyed A.H., Crickmore N., Wright D.J., 2001 Cyt1Aa from Bacillus thuringiensis subsp. israelensis is toxic to the diamondback moth, Plutella xylostella, and synergizes the activity of Cry1Ac towards a resistant strain Applied and Environmental Microbiology 67:5859–5861
Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H., 1998 Bacillus thuringiensis and its pesticidal crystal proteins Microbiology and Molecular Biology Reviews 62:775–806
Schroeder H.E., Gollasch S., Moore A., Tabe L.M., Craig S., Hardie D.C., Chrispeels M.J., Spencer D., Higgins T.J.V., 1995. Bean alpha-amylase inhibitor confers resistance to pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L.) Plant Physiology 107:1233–1239
Selvapandiyan A., Arora N., Rajagopal R., Jalali S.K., Venkatesan T., Singh S.P., Bhatnagar R.K., 2001 Toxicity analysis of N- and C-terminus-deleted vegetative insecticidal protein from Bacillus thuringiensis Applied and Environmental Microbiology 67:5855–5858
Shade R.E., Schroeder H.E., Pueto J.J., Tabe L.M., Murdock L.L., Higgins T.J.V., Chrispeels M.J., 1994. Transgenic pea seeds expressing the alpha amylase inhibitor of the common bean are resistant to the bruchid beetles Bio/Technology 12:793–796
Shao Z., Cui Y., Liu X., Yi H., Ji J., Yu Z., 1998 Processing of delta endotoxin of Bacillus thuringiensis subsp. kurstaki HD01 in Heliothis armigera midgut juice and the effect of protease inhibitors Journal of Invertebrate Pathology 72:73–81
Sharma H.C., Sharma K.K., Seetharama N., Ortiz R., 2000. Prospects for using transgenic resistance to insects in crop improvement Electronic Journal of Biotechnology 3:1–27
Shelton A.M., Tang J.D., Roush R.T., Metz T.D., Earle E.D., 2000 Field tests on managing resistance to Bt-engineered plants Nature Biotechnology 18:339–342
Shelton A.M., Zhao J.Z., Roush R.T., 2002 Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants Annual Review of Entomology 47:845–881
Shinkawa A., Yaoi K., Kadotani T., Imamura M., Koizumi N., Iwahana. H., Sato R., 1999 Binding of phylogenetically distant Bacillus thuringiensis Cry toxins to a Bombyx mori aminopeptidase N suggests importance of Cry toxin’s conserved structure in receptor binding Current Microbiology 39:14–20
Siegel J.P., 2001 The mammalian safety of Bacillus thuringiensis-based insecticides Journal of Invertebrate Pathology 77:13–21
Smedley D.P., Ellar D.J., 1996 Mutagenesis of three surface exposed loops of a Bacillus thuringiensis insecticidal toxin reveals residues important for toxicity, receptor recognition and possibly membrane insertion Microbiology 142:1617–1624
Smith R., Couche G., 1991. The phylloplane as a source of Bacillus thuringiensis variants Applied and Environmental Microbiology 57:311–315
Smith R.A., Barry J.W. 1998 Environmental persistence of Bacillus thuringiensis spores following aerial application Journal of Invertebrate Pathology 71:263–267
Soberon M., Perez R.V., Nunez-Valdez M.E., Lorence A., Gomez I., Sanchez J., Bravo A., 2000 Evidence for intermolecular interaction as a necessary step for pore-formation activity and toxicity of Bacillus thuringiensis Cry1Ab toxin FEMS Microbiology Letters 191:221–225
Song F., Zhang J., Gu A., Wu Y., Han L., He K., Chen Z., Yao J., Hu Y., Li G., Huang D., 2003 Identification of cry1I-type genes from Bacillus thuringiensis strains and characterization of a novel cry1I-type gene Applied and Environmental Microbiology 69:5207–5211
Stewart C.N. Jr., Richards IV H.A., Halfhill M.D., 2000 Transgenic plants and biosafety: science, misconceptions and public perceptions Biotechniques 29:832–836 838–843
Stobdan T., Kaur S., Singh A., 2004 Cloning and nucleotide sequence of a novel cry gene from Bacillus thuringiensis Biotechnology Letters 26:1153–1156
Stotzky G., 2002 Release, persistence and biological activity in soil of insecticidal proteins from Bacillus thuringiensis. In Letourneau D.K., Burrows B.E., eds. Genetically Engineered Organisms, Boca Raton: CRC Press. pp. 187–222. ISBN 0-8493-0439-3
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
Tabashnik B.E., Carriere Y., Dennchy T.J., Morin S., Sisterson M.S., Roush R.E., Shelton A.M., Zhao J.Z., 2003 Insect resistance to transgenic Bt crops: lessons from the laboratory and the field Journal of Economic Entomology 96:1031–1038
Tabashnik B.E., Biggs R.W., Higginson D.M., Henderson S., Unnithan D.C., Unnithan G.C., Elers-Kirk C., Sisterson M.S., Dennehy T.J., Carriere Y., Shai M., 2005 Association between resistance to Bt cotton and cadherin genotype in pink bollworm Journal of Economic Entomology 98:635–644
Theunis W., Aguda R.M., Cruz W.T., Decock C., Peferoen M., Lambert B., Bottrell D.G., Gould T., Lalsinger J.A., Cohen M.B., 1998 Bacillus thuringiensis isolates from the Philippines. Habitat distribution, δ-endotoxin diversity and toxicity to rice stem borers (Lepidoptera: Pyralidae) Bulletin of Entomology Research 88:335–342
Thomas J.C., Adams D.G., Keppene V.D., Wasmann C.C., Brown J.K., Kanost M.R., Bohnert H.J., 1995. Manduca sexta encoded protease inhibitors expressed in Nicotiana tabacum provide protection against insects Plant Physiology and Biochemistry 33:611–614
Thompson M.A., Schnepf H.E., Feitelson J.S., 1995 Structure, function and engineering of Bacillus thuringiensis toxins. In Setlow J.K., ed. Genetic Engineering: Principles and Methods 17 New York: Plenum Press. pp. 99–117. ISBN 0-30645071-2
Ticknor L.O., Kolsto A.B., Hill K.K., Keim P., Laker M.T., Tonks M., Jackson P.J., 2001 Fluorescent amplified fragment length polymorphism analysis of Norwegian Bacillus cereus and Bacillus thuringiensis soil isolates Applied and Environmental Microbiology 67:4863–4873
Tigue N.J., Jacoby J., Ellar D.J., 2001 The alpha-helix 4 residue, Asn135, is involved in the oligomerization of Cry1Ac1 and Cry1Ab5 Bacillus thuringiensis toxins Applied and Environmental Microbiology 67:5715–5720
Tinjuangjun, P. 2002 Snow drop lectin in transgenic plants: its potential for Asian agriculture. http://www.agbiotechnet.com ABN 091, CAB International, Wallingford, UK
Tounsi S., Zouari N., Jaoua S., 2003 Cloning and study of the expression of a novel cry1Ia-type gene from Bacillus thuringiensis subsp. kurstakiJournal of Applied Microbiology 95:23–28
Tu J., Zhang G., Datta K., Xu C., He Y., Zhang Q., Khush G.S., Datta S.K., 2000 Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis δ-endotoxin Nature Biotechnology 18:1101–1104
Tuli R., Bhatia C.R., Singh P.K., Chaturvedi R., 2000 Release of insecticidal transgenic crops and gap area in developing approaches for more durable resistance Current Science 79:163–169
Uemura T., Ihara H., Wadana A., Himeno M., 1992 Fluorimetric of assay potential change of Bombyx mori midgut brush border membrane induced by δ-endotoxin from Bacillus thuringiensis Biosciences Biotechnology and Biochemistry 56:1976–1979
Uribe D., Martinez W., Cerón J., 2003. Distribution and diversity of cry genes in native strains of Bacillus thuringiensis obtained from different ecosystems from Colombia Journal of Invertebrate Pathology 82:119–127
van der Salm T., Bosch D., Honee G., Feng L., Munsteman E., Bakker P., Steikema W.J., Visser B., 1994 Insect resistance of transgenic plants that express modified Bacillus thuringiensis cry1A(b) and cryIC genes: a resistance management strategy Plant Molecular Biology 26:51–59
van Frankenhuyzen K., Gringorten L., Gauthier D., 1997 Cry9Ca1 toxin, a Bacillus thuringiensis insecticidal crystal protein with high activity against the spruce budworm (Choristoneura fumiferana) Applied and Environmental Microbiology 63:4132–4234
Vazquez-Padron R.I., de la Riva G., Aguero G., Silva Y., Pham, Si.M., Soboren M., Bravo A., Abdelouahab A., 2004 Cryptic endotoxic nature of Bacillus thuringiensis Cry1Ab insecticidal crystal protein FEBS Letters 570:30–36
Vie V., Van Mau N., Pomarede P., Dance C., Schwartz J.L., Laprade R., Frutos R., Rang C., Masson L., Heitz F., Le Grimellec C., 2001 Lipid-induced pore formation of the Bacillus thuringiensis Cry1Aa insecticidal toxin Journal of Membrane Biology 180:195–203
Vilas Boas G.F.L.T., Vilas Boas L.A., Lereclus D., Arantes O.M.N., 1998 Bacillus thuringiensis conjugation under environmental conditions FEMS Microbiology Ecology 25:369–374
Vilas-Boas L.A., Vilas-Boas G.F.L.T., Saridakis H.O., Lemos M.V.F., Lereclus D., Arantes O.M.N., 2000 Survival and conjugation of Bacillus thuringiensis in a soil microcosm FEMS Microbiology Ecology 31:255–255
Wang J., Boets A., Rie J.V., Ren G., 2003. Characterization of cry1, cry2, and cry9 genes in Bacillus thuringiensis isolates from China Journal of Invertebrate Pathology 82:63–71
Wasano N., Ohba M., 1999 Assignment of delta endotoxin genes of the four lepidoptera specific Bacillus thuringiensis strains that produce spherical parasporal inclusions Current Microbiology 37:408–411
Wasano N., Ohba M., Miyamoto K., 2001 Two delta-endotoxin genes, cry9Da and a novel related gene, commonly occurring in Lepidoptera-specific Bacillus thuringiensis Japanese isolates that produce spherical parasporal inclusions Current Microbiology 42:129–133
Waterfield N.R., Bowen D.J., Fetherston J.D., Perry R.D., Ffrench-Constant R.H., 2001 The tc genes of Photorhabdus: a growing family Trends in Microbiology 9:185–191
Wilcks A., Jayaswal N., Lereclus D., Andrup L., 1998. Characterization of plasmid pAW63, a second self transmissible plasmid in Bacillus thuringiensis subsp. kurstaki HD 73 Microbiology 144:1263–1270
Winterer, J. 2002 The mixed success of protease inhibitors to combat insect pests in transgenic crops. http://www.agbiotechnet.com ABN 082, CAB International, Wellingford, UK
Winterer J., Bergelson J., 2001. Diamondback moth compensatory consumption of protease inhibitor transformed plants Molecular Ecology 10:1069–1074
Wiwat C., Thaithanun S., Pantuwatana S., Bhumiratana A., 2000 Toxicity of chitinase-producing Bacillus thuringiensis sp. kurstaki HD-1 (G) toward Plutella xylostella Journal of Invertebrate Pathology 76:270–277
Wu D., Aronson A.I., 1992 Localized mutagenesis defines regions of the Bacillus thuringiensis δ-endotoxin involved in toxicity and specificity Journal of Biological Chemistry 267:2311–2317
Wu K., Guo Y., Lv N., Greenplate J.T., Deaton R., 2003 Efficacy of transgenic cotton containing a Cry1Ac gene from Bacillus thuringiensis against Helicoverpa armigera (Lepidoptera: Noctuidae) in north China Journal of Economic Entomology 96:1322–1328
Wu S.J., Dean D.H., 1996. Functional significance of loops in the receptor binding domain of Bacillus thuringiensis CryIIIA δ-endotoxin Journal of Molecular Biology 255:628–640
Xu D., Xue Q., Mc Elory D., Manwal Y., Hilder V.A., Wu R., 1996 Constitutive expression of a cowpea trypsin inhibitor gene CpTi in transgenic rice plants cofers resistance to two major rice insect pests Molecular Breeding 2:186–193
Yamamoto T., Powell G.K., 1993. Bacillus thuringiensis crystal proteins: recent advances in understanding its insecticidal activity. In Kim L., ed. Advanced Engineered Pesticides. New York: Marcel Dekker Inc. pp. 3–42 ISBN 0-8247-8990-3
Zhao J.Z., Cao J., Li Y., Collins H.L., Roush R.T., Earle E.D., Shelton A.M., 2003 Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution Nature Biotechnology 21:1493–1497
Zouari N., Jaoua S., 1997. Purification and immunological characterization of particular delta endotoxins from three strains of Bacillus thuringiensis Biotechnology Letters 19:825–829
Acknowledgement
Author wishes to thank Dr. Aqbal Singh and Dr. K.R. Koundal, National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, India, for research facilities.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kaur, S. Molecular approaches for identification and construction of novel insecticidal genes for crop protection. World J Microbiol Biotechnol 22, 233–253 (2006). https://doi.org/10.1007/s11274-005-9027-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-005-9027-y