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In vivo and in silico comparison analyses of Cry toxin activities toward the sugarcane giant borer

Published online by Cambridge University Press:  08 March 2023

Fernando Campos de Assis Fonseca Open the ORCID record for Fernando Campos de Assis Fonseca [Opens in a new window] ,
José Dijair Antonino Open the ORCID record for José Dijair Antonino [Opens in a new window] ,
Stéfanie Menezes de Moura Open the ORCID record for Stéfanie Menezes de Moura [Opens in a new window] ,
Paolo Lucas Rodrigues-Silva Open the ORCID record for Paolo Lucas Rodrigues-Silva [Opens in a new window] ,
Leonardo Lima Pepino Macedo Open the ORCID record for Leonardo Lima Pepino Macedo [Opens in a new window] ,
José Edílson Gomes Júnior Open the ORCID record for José Edílson Gomes Júnior [Opens in a new window] ,
Isabela Tristan Lourenço-Tessuti Open the ORCID record for Isabela Tristan Lourenço-Tessuti [Opens in a new window] ,
Wagner Alexandre Lucena Open the ORCID record for Wagner Alexandre Lucena [Opens in a new window] ,
Carolina Viana Morgante Open the ORCID record for Carolina Viana Morgante [Opens in a new window]  and
Thuanne Pires Ribeiro Open the ORCID record for Thuanne Pires Ribeiro [Opens in a new window]
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Fernando Campos de Assis Fonseca*
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil Biology Cellular Department, Federal University of Brasília (UnB), Brasília, DF, Brazil Federal Institut of Goias (IFG), Águas Lindas, GO, Brazil
José Dijair Antonino
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil Biology Cellular Department, Federal University of Brasília (UnB), Brasília, DF, Brazil Federal Rural University of Pernambuco (UFRPE), Recife, PE, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Stéfanie Menezes de Moura*
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Paolo Lucas Rodrigues-Silva
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Leonardo Lima Pepino Macedo
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
José Edílson Gomes Júnior
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil Biology Cellular Department, Federal University of Brasília (UnB), Brasília, DF, Brazil
Isabela Tristan Lourenço-Tessuti
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Wagner Alexandre Lucena
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Carolina Viana Morgante
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil Embrapa Semiarid, Petrolina, PE, Brazil
Thuanne Pires Ribeiro
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Rose Gomes Monnerat
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil
Magali Aparecida Rodrigues
Affiliation:
University of São Paulo (USP-SP), São Paulo, SP, Brazil
Iolanda Midea Cuccovia
Affiliation:
University of São Paulo (USP-SP), São Paulo, SP, Brazil
Maria Cristina Mattar Silva
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil
Maria Fatima Grossi-de-Sa*
Affiliation:
Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil National Institute of Science and Technology, INCT PlantStress Biotech, Embrapa, Brazil Catholic University of Brasília, Brasília, DF, Brazil
*
Author for correspondence: Maria Fatima Grossi-de-Sa, Email: fatima.grossi@embrapa.br; Fernando Campos de Assis Fonseca, Email: fernando.fonseca@ifg.edu.br; Stéfanie Menezes de Moura, Email: stefmmoura@gmail.com
Author for correspondence: Maria Fatima Grossi-de-Sa, Email: fatima.grossi@embrapa.br; Fernando Campos de Assis Fonseca, Email: fernando.fonseca@ifg.edu.br; Stéfanie Menezes de Moura, Email: stefmmoura@gmail.com
Author for correspondence: Maria Fatima Grossi-de-Sa, Email: fatima.grossi@embrapa.br; Fernando Campos de Assis Fonseca, Email: fernando.fonseca@ifg.edu.br; Stéfanie Menezes de Moura, Email: stefmmoura@gmail.com
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Abstract

The sugarcane giant borer, Telchin licus licus, is an insect pest that causes significant losses in sugarcane crops and in the sugar-alcohol sector. Chemical and manual control methods are not effective. As an alternative, in the current study, we have screened Bacillus thuringiensis (Bt) Cry toxins with high toxicity against this insect. Bioassays were conducted to determine the activity of four Cry toxins (Cry1A (a, b, and c) and Cry2Aa) against neonate T. licus licus larvae. Notably, the Cry1A family toxins had the lowest LC50 values, in which Cry1Ac presented 2.1-fold higher activity than Cry1Aa, 1.7-fold larger than Cry1Ab, and 9.7-fold larger than Cry2Aa toxins. In silico analyses were performed as a perspective to understand putative interactions between T. licus licus receptors and Cry1A toxins. The molecular dynamics and docking analyses for three putative aminopeptidase N (APN) receptors (TlAPN1, TlAPN3, and TlAPN4) revealed evidence for the amino acids that may be involved in the toxin–receptor interactions. Notably, the properties of Cry1Ac point to an interaction site that increases the toxin's affinity for the receptor and likely potentiate toxicity. The interacting amino acid residues predicted for Cry1Ac in this work are probably those shared by the other Cry1A toxins for the same region of APNs. Thus, the presented data extend the existing knowledge of the effects of Cry toxins on T. licus licus and should be considered in further development of transgenic sugarcane plants resistant to this major occurring insect pest in sugarcane fields.

Keywords

Aminopeptidase NBacillus thuringiensiscry toxinsmolecular modelingSaccharum officinarumTechin licus licus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 3 , June 2023 , pp. 335 - 346
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Copyright © The Author(s), 2023. Published by Cambridge University Press

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References

Abbott, WS (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265–267.CrossRefGoogle Scholar
Arenas, I, Bravo, A, Soberón, M and Gómez, I (2010) Role of alkaline phosphatase from Manduca sexta in the mechanism of action of Bacillus thuringiensis Cry1Ab toxin. Journal of Biological Chemistry 285, 12497–12503.CrossRefGoogle ScholarPubMed
Aronson, AI, Beckman, W and Dunn, P (1986) Bacillus thuringiensis and related insect pathogens. Microbiological Reviews 50, 1–24.CrossRefGoogle ScholarPubMed
Baranek, J, Pogodziński, B, Szipluk, N and Zielezinski, A (2020) TOXiTAXi: a web resource for toxicity of Bacillus thuringiensis protein compositions towards species of various taxonomic groups. Scientific Reports 10, 1–12.CrossRefGoogle ScholarPubMed
Berendsen, HJC, Grigera, JR and Straatsma, TP (1987) The missing term in effective pair potentials. The Journal of Physical Chemistry A 91, 6269–6271.CrossRefGoogle Scholar
Berendsen, HJC, van der Spoel, D and van Drunen, R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Computer Physics Communications 91, 43–56.CrossRefGoogle Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Brisceno, SHR (2008) Informações sobre: lepidopteros da família Castiniidae – Distribuição geográfica das espécies conhecidas na américa tropical e subtropical e importância econômica da Castnia licus Drury, 1773 no nordeste do Brasil. Maceió, AL: Cooperativa regional dos produtores de açúcar e álcool de Alagoas.Google Scholar
Carmona, D, Rodríguez-Almazán, C, Muñoz-Garay, C, Portugal, L, Pérez, C, de Maagd, RA, Bakker, P, Soberón, M and Bravo, A (2011) Dominant negative phenotype of Bacillus thuringiensis Cry1Ab, Cry11Aa and Cry4Ba mutants suggest hetero-oligomer formation among different Cry toxins. PLoS ONE 6(5), e19952. doi: 10.1371/journal.pone.0019952CrossRefGoogle ScholarPubMed
Carroll, J and Ellar, DJ (1993) An analysis of Bacillus thuringiensis d-endotoxin action on insect-midgut-membrane permeability using a light-scattering assay. European Journal of Biochemistry 214, 771–778. doi: 10.1111/j.1432-1033.1993.tb17979.xCrossRefGoogle Scholar
Chen, W, Liu, C, Xiao, Y, Zhang, D, Zhang, Y, Li, X, Tabashnik, BE and Wu, K (2015) A toxin-binding alkaline phosphatase fragment synergizes Bt toxin Cry1Ac against susceptible and resistant Helicoverpa armigera. PLoS ONE 10, 1–19.Google ScholarPubMed
Christou, P, Capell, T, Kohli, A, Gatehouse, JA and Gatehouse, AMR (2006) Recent developments and future prospects in insect pest control in transgenic crops. Trends in Plant Science 11, 302–308.Google ScholarPubMed
Coates, BS, Sumerford, DV, Siegfried, BD, Hellmich, RL and Abel, CA (2013) Unlinked genetic loci control the reduced transcription of aminopeptidase N 1 and 3 in the European corn borer and determine tolerance to Bacillus thuringiensis Cry1Ab toxin. Insect Biochemistry and Molecular Biology 43, 1152–1160.CrossRefGoogle ScholarPubMed
Comeau, SR, Gatchell, DW, Vajda, S and Camacho, CJ (2004) ClusPro: a fully automated algorithm for protein-protein docking. Nucleic Acids Research 32 (Web Server issue), W96–9. doi: 10.1093/nar/gkh354Google ScholarPubMed
Cooper, MA, Carroll, J, Travis, ER, Williams, DH and Ellar, DJ (1998) Bacillus thuringiensis Cry1Ac toxin interaction with Manduca sexta aminopeptidase N in a model membrane environment. Biochemical Journal 333, 677–683.CrossRefGoogle Scholar
Craveiro, KIC, Júnior, JEG, Silva, MCM, Macedo, LLP, Lucena, WA, Silva, MS, Júnior, JDAdS, Oliveira, GR, de Magalhães, MTQ, Santiago, AD and Grossi-de-Sa, MF (2010) Variant Cry1Ia toxins generated by DNA shuffling are active against sugarcane giant borer. Journal of Biotechnology 145, 215–221.CrossRefGoogle ScholarPubMed
Crickmore, N (2022) Bacillus thuringiensis. Toxin Nomenclature. In: Full list of delta-endotoxins. Available at http://www.lifesci.sussex.ac.uk/home/Neil_Crickmore/Bt (accessed 22 April 2022).Google Scholar
de Groot, BL and Grubmüller, H (2001) Water permeation across biological membranes: mechanism and dynamics of Aquaporin-1 and GlpF. Science 294, 2353–2357.CrossRefGoogle ScholarPubMed
Deist, BR, Rausch, MA, Fernandez-Luna, MT, Adang, MJ and Bonning, BC (2014) Bt toxin modification for enhanced efficacy. Toxins 6, 3005–3027.CrossRefGoogle ScholarPubMed
de Maagd, RA, Bakker, PL, Masson, L, Adang, MJ, Sangadala, S, Stiekema, W and Bosch, D (1999) Domain III of the Bacillus thuringiensis delta-endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified aminopeptidase N. Molecular Microbiology 31, 463–471.CrossRefGoogle ScholarPubMed
Essmann, U, Perera, L, Berkowitz, ML, Darden, T, Lee, H and Pedersen, LG (1995) A smooth particle mesh Ewald method. The Journal of Chemical Physics 103, 8577–8593.CrossRefGoogle Scholar
Fiser, AS and Sali, AS (2003) Modeller: generation and refinement of homology-based protein structure models. Methods in Enzymology 374, 461–491.CrossRefGoogle ScholarPubMed
Florez, AM, Suarez-Barrera, MO, Morales, GM, Rivera, KV, Orduz, S, Ochoa, R, Guerra, D and Muskus, C (2018) Toxic activity, molecular modeling and docking simulations of Bacillus thuringiensis Cry11 toxin variants obtained via DNA shuffling. Frontiers in Microbiology 9, 2461.CrossRefGoogle ScholarPubMed
Fonseca, FCdA, Firmino, AAP, de Macedo, LLP, Coelho, RR, de Sousa Júnior, JDA, Silva-Junior, OB, Togawa, RC, Pappas, GJ, de Góis, LAB, da Silva, MCM and Grossi-de-Sá, MF (2015) Sugarcane giant borer transcriptome analysis and identification of genes related to digestion. PLoS ONE 10, e0123836.Google ScholarPubMed
Fortier, M, Vachon, V, Kirouac, M, Schwartz, JL and Laprade, R (2005) Differential effects of ionic strength, divalent cations and pH on the pore-forming activity of Bacillus thuringiensis insecticidal toxins. Journal of Membrane Biology 208, 77–87.CrossRefGoogle ScholarPubMed
Gómez, I, Oltean, DI, Gill, SS, Bravo, A and Soberón, M (2001) Mapping the epitope in cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. Journal of Biological Chemistry 276, 28906–28912.CrossRefGoogle ScholarPubMed
Gómez, I, Sánchez, J, Miranda, R, Bravo, A and Soberón, M (2002) Cadherin-like receptor binding facilitates proteolytic cleavage of helix alpha-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Letters 513, 242–246.CrossRefGoogle Scholar
Gómez, I, Arenas, I, Benitez, I, Miranda-Ríos, J, Becerril, B, Grande, R, Almagro, JC, Bravo, A and Soberón, M (2006) Specific epitopes of domains II and III of Bacillus thuringiensis Cry1Ab toxin involved in the sequential interaction with cadherin and aminopeptidase-N receptors in Manduca sexta. Journal of Biological Chemistry 281, 34032–34039.CrossRefGoogle ScholarPubMed
Gong, L, Kang, S, Zhou, J, Sun, D, Guo, L, Qin, J, Zhu, L, Bai, Y, Ye, F, Akami, M, Wu, Q, Wang, S, Xu, B, Yang, Z, Bravo, A, Soberón, M, Guo, Z, Wen, L and Zhang, Y (2020) Reduced expression of a novel midgut trypsin gene involved in protoxin activation correlates with Cry1ac resistance in a laboratory-selected strain of Plutella xylostella (L.). Toxins 12, 1–15.CrossRefGoogle Scholar
Grossi-de-Sa, MF, Silva, MCM, Fonseca, FCDA, Macedo, LLP, Lourenço, IT and Freire, ÉVSA (2013) Aparato e método de criação de larvas de insetos em laboratório. INPI BR10201303033112–0 patent.Google Scholar
Groulx, N, McGuire, H, Laprade, R, Schwartz, JL and Blunck, R (2011) Single molecule fluorescence study of the Bacillus thuringiensis toxin Cry1Aa reveals tetramerization. Journal of Biological Chemistry 286, 42274–42282.CrossRefGoogle ScholarPubMed
Herrero, S, González-Cabrera, J, Tabashnik, BE and Ferré, J (2001) Shared binding sites in Lepidoptera for Bacillus thuringiensis Cry1Ja and Cry1A toxins. Applied and Environmental Microbiology 67, 5729–5734.CrossRefGoogle ScholarPubMed
Hess, B, Bekker, H, Berendsen, HJC and Fraaije, JGEM (1997) LINCS: a linear constraint solver for molecular simulations. Journal of Computational Chemistry 18, 14631472.3.0.CO;2-H>CrossRefGoogle Scholar
ISAAA (2020) Global status of commercialized biotech/GM crops in 2019: biotech crops drive socio-economic development and sustainable environment in the new frontier. In ISAAA Brief No. 55 (ISAAA Brie). Ithaca, NY: ISAAA. Available at http://www.isaaa.org/resources/publications/briefs/54/executivesummary/pdf/B54-ExecSum-English.pdf (accessed 19 March 2022).Google Scholar
Javaid, S, Naz, S, Amin, I, Jander, G, Ul-Haq, Z and Mansoor, S (2018) Computational and biological characterization of fusion proteins of two insecticidal proteins for control of insect pests. Scientific Reports 8, 1–11.CrossRefGoogle ScholarPubMed
Kirouac, M, Vachon, V, Quievy, D, Schwartz, JL and Laprade, R (2006) Protease inhibitors fail to prevent pore formation by the activated Bacillus thuringiensis toxin Cry1Aa in insect brush border membrane vesicles. Applied and Environmental Microbiology 72, 506–515.CrossRefGoogle ScholarPubMed
Laskowski, R, Hutchinson, E, Michie, A, Wallace, A, Jones, M and Thornton, J (1997) PDBsum: a web-based database of summaries and analyzes of all PDB structures. Trends in Biochemical Sciences 22, 488–490.CrossRefGoogle Scholar
Lucena, WA, Pelegrini, PB, Martins-de-Sa, D, Fonseca, FCA, Gomes, JE, de Macedo, LLP, da Silva, MCM, Sampaio, R and Grossi-de-Sa, MF (2014) Molecular approaches to improve the insecticidal activity of Bacillus thuringiensis cry toxins. Toxins 6, 2393–2423.CrossRefGoogle ScholarPubMed
Masson, L, Lu, Y-J, Masza, A, Brousseauj, R and Adan, MJ (1995) The CryIA(c) receptor purified from Manduca sexta displays multiple specificities. Journal of Biological Chemistry 270, 20309–20315.CrossRefGoogle ScholarPubMed
Mendonça, AF, Viveiros, AJA and Sampaio, FF (1996) A broca gigante da cana-de-açúcar, Castnia licus Drury, 1770 (Lep.: Castniidae). In Mendonça, AF (ed.), Pragas da cana-de-Açúcar. Maceió: Insetos & Cia, pp. 133–167.Google Scholar
Monnerat, RG, Batista, AC, de Medeiros, PT, Martins, ÉS, Melatti, VM, Praça, LB, Dumas, VF, Morinaga, C, Demo, C, Gomes, ACM, Falcão, R, Siqueira, CB, Silva-Werneck, JO and Berry, C (2007) Screening of Brazilian Bacillus thuringiensis isolates active against Spodoptera frugiperda, Plutella xylostella and Anticarsia gemmatalis. Biological Control 41, 291–295.CrossRefGoogle Scholar
Muñoz-Garay, C, Sánchez, J, Darszon, A, de Maagd, RA, Bakker, P, Soberón, M and Bravo, A (2006) Permeability changes of Manduca sexta midgut brush border membranes induced by oligomeric structures of different Cry toxins. Journal of Membrane Biology 212, 61–68.CrossRefGoogle ScholarPubMed
Nair, MS and Dean, DH (2008) All domains of Cry1A toxins insert into insect brush border membranes. Journal of Biological Chemistry 283, 26324–26331.CrossRefGoogle ScholarPubMed
Nakanishi, K, Yaoi, K, Nagino, Y, Hara, H, Kitami, M, Atsumi, S, Miura, N and Sato, R (2002) Aminopeptidase N isoforms from the midgut of Bombyx mori and Plutella xylostella – their classification and the factors that determine their binding specificity to Bacillus thuringiensis Cry1A toxin. FEBS Letters 519, 215–220.CrossRefGoogle ScholarPubMed
Noriega, DD, Arraes, FBM, Antonino, JD, Macedo, LLP, Fonseca, FCA, Togawa, RC, Grynberg, P, Silva, MCM, Negrisoli, AS and Grossi-de-Sa, MF (2020) Transcriptome analysis and knockdown of the juvenile hormone esterase gene reveal abnormal feeding behavior in the sugarcane giant borer. Frontiers in Physiology 11, 588450.Google ScholarPubMed
Oliveira, GR, Silva, MC, Lucena, WA, Nakasu, EY, Firmino, AA, Beneventi, MA, Souza, DS, Gomes, JE, da De Souza, J, Rigden, DJ, Ramos, HB, Soccol, CR and Grossi-De-Sa, MF (2011) Improving Cry8Ka toxin activity towards the cotton boll weevil (Anthonomus grandis). BMC Biotechnology 11, 85. doi: 10.1186/1472-6750-11-85CrossRefGoogle ScholarPubMed
Oliveira, RS, Oliveira-Neto, OB, Moura, HFN, de Macedo, LLP, Arraes, FBM, Lucena, WA, Lourenço-Tessutti, IT, Barbosa, AAD, da Silva, MCM and Grossi-de-Sa, MF (2016) Transgenic cotton plants expressing cry1Ia12 toxin confer resistance to fall armyworm (Spodoptera frugiperda) and cotton boll weevil (Anthonomus grandis). Frontiers in Plant Science 7, 1–11.CrossRefGoogle ScholarPubMed
Pacheco, S, Gómez, I, Arenas, I, Saab-Rincon, G, Rodríguez-Almazán, C, Gill, SS, Bravo, A and Soberón, M (2009) Domain II loop 3 of Bacillus thuringiensis Cry1Ab toxin is involved in a ‘Ping Pong’ binding mechanism with Manduca sexta aminopeptidase-N and cadherin receptors. Journal of Biological Chemistry 284, 32750–32757.CrossRefGoogle Scholar
Pardo-López, L, Soberón, M and Bravo, A (2013) Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiology Reviews 37, 3–22.CrossRefGoogle ScholarPubMed
Peña, G, Miranda-Rios, J, de La Riva, G, Pardo-López, L, Soberón, M and Bravo, A (2006) A Bacillus thurigiensis S-layer protein involved in toxicity against Epilachna varivestis (Coleoptera: Coccinellidae). Applied and Environmental Microbiology 72, 353–360.Google Scholar
Pinto, ADS, Garcia, JF and Oliveira, HND (2006) Manejo das principais pragas da cana-de-açúcar. In Segato, SV (ed.), Atualização em Produção de cana-de-Açúcar. Piracicaba, SP: CP2, pp. 257–280.Google Scholar
Qiu, L, Zhang, B, Liu, L, Ma, W, Wang, X, Lei, C and Chen, L (2017) Proteomic analysis of Cry2Aa-binding proteins and their receptor function in Spodoptera exigua. Scientific Reports 7, 1–10.Google ScholarPubMed
Rajagopal, R, Agrawal, N, Selvapandiyan, A, Sivakumar, S, Ahmad, S and Bhatnagar, RK (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.CrossRefGoogle ScholarPubMed
Ribeiro, TP, Arraes, FBM, Lourenço-Tessutti, IT, Silva, MS, Lisei-de-Sá, ME, Lucena, WA, Macedo, LLP, Lima, JN, Santos Amorim, RM, Artico, S, Alves-Ferreira, M, Mattar Silva, MC and Grossi-de-Sa, MF (2017) Transgenic cotton expressing Cry10Aa toxin confers high resistance to the cotton boll weevil. Plant Biotechnology Journal 15, 997–1009.CrossRefGoogle Scholar
Ribeiro, TP, Basso, MF, de Carvalho, MH, de Macedo, LLP, da Silva, DML, Lourenço-Tessutti, IT, de Oliveira-Neto, OB, de Campos-Pinto, ER, Lucena, WA, da Silva, MCM, Tripode, BMD, Abreu-Jardim, TPF, Miranda, JE, Alves-Ferreira, M, Morgante, CV and Grossi-de-Sa, MF (2019) Stability and tissue-specific Cry10Aa overexpression improves cotton resistance to the cotton boll weevil. Biotechnology Research and Innovation 3, 27–41.CrossRefGoogle Scholar
Rodrigo-Simón, A, Caccia, S and Ferré, J (2008) Bacillus thuringiensis Cry1Ac toxin-binding and pore-forming activity in brush border membrane vesicles prepared from anterior and posterior midgut regions of lepidopteran larvae. Applied and Environmental Microbiology 74, 1710–1716.CrossRefGoogle ScholarPubMed
Shen, M and Sali, A (2006) Statistical potential for assessment and prediction of protein structures. Protein Science 15, 2507–2524.CrossRefGoogle ScholarPubMed
Silva-Brandão, KL, Almeida, LC, Moraes, SS and Cônsoli, FL (2013) Using population genetic methods to identify the origin of an invasive population and to diagnose cryptic subspecies of Telchin licus (Lepidoptera: Castniidae). Bulletin of Entomological Research 103, 89–97.CrossRefGoogle ScholarPubMed
Soberón, M, Pérez, RV, Nuñez-Valdéz, ME, Lorence, A, Gómez, I, Sánchez, J and 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.CrossRefGoogle ScholarPubMed
Stephens, E, Sugars, J, Maslen, SL, Williams, DH, Packman, LC and Ellar, DJ (2004) The N-linked oligosaccharides of aminopeptidase N from Manduca sexta: site localization and identification of novel N-glycan structures. European Journal of Biochemistry 271, 4241–4258.CrossRefGoogle ScholarPubMed
Tajne, S, Sanam, R, Gundla, R, Gandhi, NS, Mancera, RL, Boddupally, D, Vudem, DR and Khareedu, VR (2012) Molecular modeling of Bt Cry1Ac (DI-DII)-ASAL (Allium sativum lectin)-fusion protein and its interaction with aminopeptidase N (APN) receptor of Manduca sexta. Journal of Molecular Graphics and Modelling 33, 61–76.CrossRefGoogle ScholarPubMed
Tajne, S, Boddupally, D, Sadumpati, V, Vudem, DR and Khareedu, VR (2013) Synthetic fusion-protein containing domains of Bt Cry1Ac and Allium sativum lectin (ASAL) conferred enhanced insecticidal activity against major lepidopteran pests. Journal of Biotechnology 171, 71–75.CrossRefGoogle ScholarPubMed
Talaei-Hassanloui, R, Bakhshaei, R, Hosseininaveh, V and Khorramnezhad, A (2014) Effect of midgut proteolytic activity on susceptibility of lepidopteran larvae to Bacillus thuringiensis subsp. Kurstaki. Frontiers in Physiology 4, 1–6.CrossRefGoogle ScholarPubMed
Tiewsiri, K and Wang, P (2011) Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proceedings of the National Academy of Sciences of the USA 108, 14037–14042.CrossRefGoogle ScholarPubMed
Vachon, V, Laprade, R and Schwartz, JL (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. Journal of Invertebrate Pathology 111, 1–12.CrossRefGoogle ScholarPubMed
van Gunsteren, WF (1996) Biomolecular Simulation: GROMOS 96 Manual and User Guide. Zürich: Biomos.Google Scholar
Wolfersberger, M, Luethy, P, Maurer, A, Parenti, P, Sacchi, FV, Giordana B, and Hanozett, GM (1987) Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comparative Biochemistry and Physiology 86, 301–308.CrossRefGoogle Scholar
Yang, Y, Zhu, YC, Ottea, J, Husseneder, C, Rogers Leonard, B, Abel, C and Huang, F (2010) Molecular characterization and RNA interference of three midgut aminopeptidase N isozymes from Bacillus thuringiensis-susceptible and -resistant strains of sugarcane borer, Diatraea saccharalis. Insect Biochemistry and Molecular Biology 40, 592–603.CrossRefGoogle ScholarPubMed
Yaoi, K, Nakanishi, K, Kadotani, T, Imamura, M, Koizumi, N, Iwahana, H and Sato, R (1999) Bacillus thuringiensis Cry1Aa toxin-binding region of Bombyx mori aminopeptidase N. FEBBS Letter 463, 221–224.CrossRefGoogle ScholarPubMed
Zhang, S, Cheng, H, Gao, Y, Wang, G, Liang, G and Wu, K (2009) Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochemistry and Molecular Biology 39, 421–429.CrossRefGoogle ScholarPubMed
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