MAPK Signaling Pathway Alters Expression of Midgut ALP and ABCC Genes and Causes Resistance to Bacillus thuringiensis Cry1Ac Toxin in Diamondback Moth

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Guo, Zhaojiang ^a   Kang, Shi ^a   Chen, Defeng ^a   Wu, Qingjun ^a   Wang, Shaoli ^a   Xie, Wen ^a   Zhu, Xun ^a   Baxter, Simon W ^b   Zhou, Xuguo ^c   Jurat Fuentes, Juan Luis ^d   Zhang, Youjun ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF KENTUCKY   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER C; ALKALINE PHOSPHATASE; CRY1AC TOXIN; MITOGEN ACTIVATED PROTEIN KINASE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 3; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BIOLOGICAL CONTROL AGENT; ENDOTOXIN; HEMOLYSIN; INSECT PROTEIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; PROTEIN BINDING;

ABCC GENE; ABCC1 GENE; ABCC2 GENE; ABCC3 GENE; ALP GENE; ARTHROPOD LARVA; ARTICLE; BACILLUS THURINGIENSIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SILENCING; INSECT RESISTANCE; MAP4K4 GENE; MICROBIAL PEST CONTROL; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLUTELLA XYLOSTELLA; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; ANIMAL; BACILLUS; BIOLOGICAL CONTROL AGENT; DRUG EFFECTS; GENETICS; INSECTICIDE RESISTANCE; INTESTINE; METABOLISM; MOTH; PHARMACOLOGY; SIGNAL TRANSDUCTION; TOXICITY;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA; PLUTELLA XYLOSTELLA; PLUTELLIDAE;

ALKALINE PHOSPHATASE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACILLUS; BACTERIAL PROTEINS; BIOLOGICAL CONTROL AGENTS; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECT PROTEINS; INSECTICIDE RESISTANCE; INTESTINES; MAP KINASE SIGNALING SYSTEM; MOTHS; PROTEIN BINDING;

EID: 84929998949     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005124     Document Type: Article

References (94)

1. Sanchis V, From microbial sprays to insect-resistant transgenic plants: history of the biopesticide Bacillus thuringiensis. A review. Agron Sustain Dev. 2011;31: 217–231.
2. Crickmore N, Baum J, Bravo A, Lereclus D, Narva K, Sampson K, et al. Bacillus thuringiensis toxin nomenclature. 2014. http://wwwlifescisussexacuk/home/Neil_Crickmore/Bt/.
3. James C. Global status of commercialized biotech/GM crops: 2013. ISAAA Brief No. 46. ISAAA: Ithaca, NY. 2013.
4. Tabashnik BE, Huang F, Ghimire MN, Leonard BR, Siegfried BD, Rangasamy M, et al. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat Biotechnol. 2011;29: 1128–1131. doi: 10.1038/nbt.1988 21983521
5. Tabashnik BE, Brévault T, Carrière Y, Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013;31: 510–521. doi: 10.1038/nbt.2597 23752438
6. Adang MJ, Crickmore N, Jurat-Fuentes JL, Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Adv Insect Physiol. 2014;47: 39–87.
7. Ferré J, Van Rie J, Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol. 2002;47: 501–533. 11729083
8. Pigott CR, Ellar DJ, Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev. 2007;71: 255–281. 17554045
9. Gahan LJ, Pauchet Y, Vogel H, Heckel DG, An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet. 2010;6: e1001248. doi: 10.1371/journal.pgen.1001248 21187898
10. Baxter SW, Badenes-Pérez FR, Morrison A, Vogel H, Crickmore N, Kain W, et al. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics. 2011;189: 675–679. doi: 10.1534/genetics.111.130971 21840855
11. Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, Sezutsu H, et al. Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc Natl Acad Sci USA. 2012;109: E1591–E1598. doi: 10.1073/pnas.1120698109 22635270
12. Park Y, Gonzalez-Martinez RM, Navarro-Cerrillo G, Chakroun M, Kim Y, Ziarsolo P, et al. ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biol. 2014;12: 46. doi: 10.1186/1741-7007-12-46 24912445
13. Xiao Y, Zhang T, Liu C, Heckel DG, Li X, Tabashnik BE, et al. Mis-splicing of the ABCC2 gene linked with Bt toxin resistance in Helicoverpa armigera. Sci Rep. 2014;4: 6184. doi: 10.1038/srep06184 25154974
14. Tanaka S, Miyamoto K, Noda H, Jurat-Fuentes JL, Yoshizawa Y, Endo H, et al. The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J. 2013;280: 1782–1794. doi: 10.1111/febs.12200 23432933
15. Dermauw W, Van Leeuwen T, The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol. 2014;45: 89–110. doi: 10.1016/j.ibmb.2013.11.001 24291285
16. Merzendorfer H, ABC transporters and their role in protecting insects from pesticides and their metabolites. Adv Insect Physiol. 2014;46: 1–72.
17. Jurat-Fuentes JL, Karumbaiah L, Jakka SR, Ning C, Liu C, Wu K, et al. Reduced levels of membrane-bound alkaline phosphatase are common to lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLoS ONE. 2011;6: e17606. doi: 10.1371/journal.pone.0017606 21390253
18. Caccia S, Moar WJ, Chandrashekhar J, Oppert C, Anilkumar KJ, Jurat-Fuentes JL, et al. Association of Cry1Ac toxin resistance in Helicoverpa zea (Boddie) with increased alkaline phosphatase levels in the midgut lumen. Appl Environ Microbiol. 2012;78: 5690–5698. doi: 10.1128/AEM.00523-12 22685140
19. Furlong MJ, Wright DJ, Dosdall LM, Diamondback moth ecology and management: problems, progress and prospects. Annu Rev Entomol. 2013;58: 517–541. doi: 10.1146/annurev-ento-120811-153605 23020617
20. Tabashnik BE, Cushing NL, Finson N, Johnson MW, Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol. 1990;83: 1671–1676.
21. Janmaat AF, Myers J, Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc R Soc Lond B. 2003;270: 2263–2270. 14613613
22. Tabashnik BE, Liu YB, Malvar T, Heckel DG, Masson L, Ballester V, et al. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proc Natl Acad Sci USA. 1997;94: 12780–12785. 9371752
23. Wang P, Zhao JZ, Rodrigo-Simón A, Kain W, Janmaat AF, Shelton AM, et al. Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of the cabbage looper, Trichoplusia ni. Appl Environ Microbiol. 2007;73: 1199–1207. 17189446
24. Tiewsiri K, Wang P, Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proc Natl Acad Sci USA. 2011;108: 14037–14042. doi: 10.1073/pnas.1102555108 21844358
25. Baxter SW, Zhao JZ, Gahan LJ, Shelton AM, Tabashnik BE, Heckel DG, Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol Biol. 2005;14: 327–334. 15926902
26. Baxter SW, Zhao JZ, Shelton AM, Vogel H, Heckel DG, Genetic mapping of Bt-toxin binding proteins in a Cry1A-toxin resistant strain of diamondback moth Plutella xylostella. Insect Biochem Mol Biol. 2008;38: 125–135. doi: 10.1016/j.ibmb.2007.09.014 18207074
27. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, Aroian RV, Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci USA. 2004;101: 10995–11000. 15256590
28. Kao CY, Los FCO, Huffman DL, Wachi S, Kloft N, Husmann M, et al. Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog. 2011;7: e1001314. doi: 10.1371/journal.ppat.1001314 21408619
29. Cancino-Rodezno A, Alexander C, Villaseñor R, Pacheco S, Porta H, Pauchet Y, et al. The mitogen-activated protein kinase p38 is involved in insect defense against Cry toxins from Bacillus thuringiensis. Insect Biochem Mol Biol. 2010;40: 58–63. doi: 10.1016/j.ibmb.2009.12.010 20040372
30. Porta H, Cancino-Rodezno A, Soberón M, Bravo A, Role of MAPK p38 in the cellular responses to pore-forming toxins. Peptides. 2011;32: 601–606. doi: 10.1016/j.peptides.2010.06.012 20599578
31. Krishna M, Narang H, The complexity of mitogen-activated protein kinases (MAPKs) made simple. Cell Mol Life Sci. 2008;65: 3525–3344. doi: 10.1007/s00018-008-8170-7 18668205
32. Horton A, Wang B, Camp L, Price M, Arshi A, Nagy M, et al. The mitogen-activated protein kinome from Anopheles gambiae: identification, phylogeny and functional characterization of the ERK, JNK and p38 MAP kinases. BMC Genomics. 2011;12: 574. doi: 10.1186/1471-2164-12-574 22111877
33. Guo Z, Kang S, Zhu X, Wu Q, Wang S, Xie W, et al. The midgut cadherin-like gene is not associated with resistance to Bacillus thuringiensis toxin Cry1Ac in Plutella xylostella (L.). J Invertebr Pathol. 2015;126: 21–30. doi: 10.1016/j.jip.2015.01.004 25595643
34. Perera OP, Willis JD, Adang MJ, Jurat-Fuentes JL, Cloning and characterization of the Cry1Ac-binding alkaline phosphatase (HvALP) from Heliothis virescens. Insect Biochem Mol Biol. 2009;39: 294–302. doi: 10.1016/j.ibmb.2009.01.006 19552892
35. Ning C, Wu K, Liu C, Gao Y, Jurat-Fuentes JL, Gao X, Characterization of a Cry1Ac toxin-binding alkaline phosphatase in the midgut from Helicoverpa armigera (Hübner) larvae. J Insect Physiol. 2010;56: 666–672. doi: 10.1016/j.jinsphys.2010.02.003 20170658
36. Lei Y, Zhu X, Xie W, Wu Q, Wang S, Guo Z, et al. Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene. 2014;533: 180–187. doi: 10.1016/j.gene.2013.09.091 24120626
37. Kulkarni MM, Booker M, Silver SJ, Friedman A, Hong P, Perrimon N, et al. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat Methods. 2006;3: 833–838. 16964256
38. Gong Y, Wang C, Yang Y, Wu S, Wu Y, Characterization of resistance to Bacillus thuringiensis toxin Cry1Ac in Plutella xylostella from China. J Invertebr Pathol. 2010;104: 90–96. doi: 10.1016/j.jip.2010.02.003 20167218
39. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, et al. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science. 2004;306: 1937–1940. 15591204
40. You M, Yue Z, He W, Yang X, Yang G, Xie M, et al. A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet. 2013;45: 220–225. doi: 10.1038/ng.2524 23313953
41. Tabashnik BE, Mota-Sanchez D, Whalon ME, Hollingworth RM, Carrière Y, Defining terms for proactive management of resistance to Bt crops and pesticides. J Econ Entomol. 2014;107: 496–507. 24772527
42. Tang JD, Shelton AM, Van Rie J, de Roeck S, Moar WJ, Roush RT, et al. Toxicity of Bacillus thuringiensis spore and crystal protein to resistant diamondback moth (Plutella xylostella). Appl Environ Microbiol. 1996;62: 564–569. 16535241
43. Zhu X, Lei Y, Yang Y, Baxter SW, Li J, Wu Q, et al. Construction and characterisation of near-isogenic Plutella xylostella (Lepidoptera: Plutellidae) strains resistant to Cry1Ac toxin. Pest Manag Sci. 2015;71: 225–233. doi: 10.1002/ps.3785 24687616
44. Tabashnik BE, Liu Y-B, Malvar T, Heckel DG, Masson L, Ferré J, Insect resistance to Bacillus thuringiensis: uniform or diverse? Phil Trans R Soc Lond B. 1998;353: 1751–1756.
45. Ballester V, Granero F, Tabashnik BE, Malvar T, Ferré J, Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella). Appl Environ Microbiol. 1999;65: 1413–1419. 10103230
46. Yang ZX, Wu QJ, Wang SL, Chang XL, Wang JH, Guo ZJ, et al. Expression of cadherin, aminopeptidase N and alkaline phosphatase genes in Cry1Ac-susceptible and Cry1Ac-resistant strains of Plutella xylostella (L.). J Appl Entomol. 2012;136: 539–548.
47. Arenas I, Bravo A, Soberón M, Gómez I, Role of alkaline phosphatase from Manduca sexta in the mechanism of action of Bacillus thuringiensis Cry1Ab toxin. J Biol Chem. 2010;285: 12497–12503. doi: 10.1074/jbc.M109.085266 20177063
48. Flores-Escobar B, Rodríguez-Magadan H, Bravo A, Soberón M, Gómez I, Differential role of Manduca sexta aminopeptidase-N and alkaline phosphatase in the mode of action of Cry1Aa, Cry1Ab, and Cry1Ac toxins from Bacillus thuringiensis. Appl Environ Microbiol. 2013;79: 4543–4550. doi: 10.1128/AEM.01062-13 23686267
49. Gahan LJ, Gould F, Heckel DG, Identification of a gene associated with Bt resistance in Heliothis virescens. Science. 2001;293: 857–860. 11486086
50. Herrero S, Gechev T, Bakker PL, Moar WJ, de Maagd RA, Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes. BMC Genomics. 2005;6: 96. 15978131
51. Grailles M, Brey PT, Roth CW, The Drosophila melanogaster multidrug-resistance protein 1 (MRP1) homolog has a novel gene structure containing two variable internal exons. Gene. 2003;307: 41–50. 12706887
52. Roth CW, Holm I, Graille M, Dehoux P, Rzhetsky A, Wincker P, et al. Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. Mol Cells. 2003;15: 150–158. 12803476
53. Labbé R, Caveney S, Donly C, Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol Biol. 2011;20: 243–256. doi: 10.1111/j.1365-2583.2010.01064.x 21199020
54. Chen Y, Li M, Islam I, You L, Wang Y, Li Z, et al. Allelic-specific expression in relation to Bombyx mori resistance to Bt toxin. Insect Biochem Mol Biol. 2014;54: 53–60. doi: 10.1016/j.ibmb.2014.07.007 25123097
55. Coates BS, Sumerford DV, Siegfried BD, Hellmich RL, Abel CA, 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 Biochem Mol Biol. 2013;43: 1152–1160. doi: 10.1016/j.ibmb.2013.09.003 24121099
56. Suzuki A, Guicheux J, Palmer G, Miura Y, Oiso Y, Bonjour JP, et al. Evidence for a role of p38 MAP kinase in expression of alkaline phosphatase during osteoblastic cell differentiation. Bone. 2002;30: 91–98. 11792570
57. Sowa H, Kaji H, Yamaguchi T, Sugimoto T, Chihara K, Activations of ERK1/2 and JNK by transforming growth factor β negatively regulate Smad3-induced alkaline phosphatase activity and mineralization in mouse osteoblastic cells. J Biol Chem. 2002;277: 36024–36031. 12130649
58. Hager S, Lampert FM, Orimo H, Stark GB, Finkenzeller G, Up-regulation of alkaline phosphatase expression in human primary osteoblasts by cocultivation with primary endothelial cells is mediated by p38 mitogen-activated protein kinase-dependent mRNA stabilization. Tissue Eng Part A. 2009;15: 3437–3447. doi: 10.1089/ten.TEA.2009.0133 19409035
59. Sukhai M, Piquette-Miller M, Regulation of the multidrug resistance genes by stress signals. J Pharm Pharm Sci. 2000;3: 268–280. 10994039
60. Kim SH, Bark H, Choi CH, Mercury induces multidrug resistance-associated protein gene through p38 mitogen-activated protein kinase. Toxicol Lett. 2005;155: 143–150. 15585369
61. Tan KPH, Ito S, Coordinate induction of ATP-binding cassette (ABC) proteins by bile acids via Nrf2 is mediated by mitogen activated protein kinases (MAPK). FASEB J. 2008;22: 921.919.
62. El Azreq MA, Naci D, Aoudjit F, Collagen/β1 integrin signaling up-regulates the ABCC1/MRP-1 transporter in an ERK/MAPK-dependent manner. Mol Biol Cell. 2012;23: 3473–3484. doi: 10.1091/mbc.E12-02-0132 22787275
63. Su YC, Treisman JE, Skolnik EY, The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev. 1998;12: 2371–2380. 9694801
64. Chapman JO, Li H, Lundquist EA, The MIG-15 NIK kinase acts cell-autonomously in neuroblast polarization and migration in C. elegans. Dev Biol. 2008;324: 245–257. doi: 10.1016/j.ydbio.2008.09.014 18840424
65. Collins CS, Hong J, Sapinoso L, Zhou Y, Liu Z, Micklash K, et al. A small interfering RNA screen for modulators of tumor cell motility identifies MAP4K4 as a promigratory kinase. Proc Natl Acad Sci USA. 2006;103: 3775–3780. 16537454
66. Pece S, Gutkind JS, Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J Biol Chem. 2000;275: 41227–41233. 10969083
67. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA, Jr.A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci USA. 2006;103: 9897–9902. 16788061
68. Yang Y, Zhu YC, Ottea J, Husseneder C, Leonard BR, Abel C, et al. Down regulation of a gene for cadherin, but not alkaline phosphatase, associated with Cry1Ab resistance in the sugarcane borer Diatraea saccharalis. PLoS ONE. 2011;6: e25783. doi: 10.1371/journal.pone.0025783 21991350
69. Jin T, Chang X, Gatehouse AM, Wang Z, Edwards MG, He K, Downregulation and mutation of a cadherin gene associated with Cry1Ac resistance in the Asian corn borer, Ostrinia furnacalis (Guenée). Toxins. 2014;6: 2676–2693. doi: 10.3390/toxins6092676 25216082
70. Sorrell JM, Brinon L, Baber MA, Caplan AI, Cytokines and glucocorticoids differentially regulate APN/CD13 and DPPIV/CD26 enzyme activities in cultured human dermal fibroblasts. Arch Dermatol Res. 2003;295: 160–168. 12861419
71. Kehlen A, Geisler M, Olsen JV, Sablotzki A, Langner J, Riemann D, IL-10 and TGF-β differ in their regulation of aminopeptidase N/CD13 expression in monocytes. Int J Mol Med. 2004;13: 877–882. 15138629
72. Yang Y, Zhu YC, Ottea J, Husseneder C, Leonard BR, Abel C, et al. Molecular characterization and RNA interference of three midgut aminopeptidase N isozymes from Bacillus thuringiensis-susceptible and-resistant strains of sugarcane borer, Diatraea saccharalis. Insect Biochem Mol Biol. 2010;40: 592–603. doi: 10.1016/j.ibmb.2010.05.006 20685334
73. Guo Z, Kang S, Zhu X, Xia J, Wu Q, Wang S, et al. Down-regulation of a novel ABC transporter gene (Pxwhite) is associated with Cry1Ac resistance in the diamondback moth, Plutella xylostella (L.). Insect Biochem Mol Biol. 2015;59: 30–40. doi: 10.1016/j.ibmb.2015.01.009 25636859
74. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV, Selection in the evolution of gene duplications. Genome Biol. 2002;3: research0008.0001–0008.0009.
75. Li X, Schuler MA, Berenbaum MR, Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007;52: 231–253. 16925478
76. Bass C, Field LM, Gene amplification and insecticide resistance. Pest Manag Sci. 2011;67: 886–890. doi: 10.1002/ps.2189 21538802
77. Tang JD, Gilboa S, Roush RT, Shelton AM, Inheritance, stability, and lack-of-fitness costs of field-selected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. J Econ Entomol. 1997;90: 732–741.
78. Shelton AM, Robertson JL, Tang JD, Perez C, Eigenbrode SD, Preisler HK, et al. Resistance of diamondback moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the field. J Econ Entomol. 1993;86: 697–705.
79. Metz TD, Roush RT, Tang JD, Shelton AM, Earle ED, Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein: implications for pest resistance management strategies. Mol Breeding. 1995;1: 309–317.
80. Luo K, Banks D, Adang MJ, Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1 δ-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Appl Environ Microbiol. 1999;65: 457–464. 9925568
81. Crespo ALB, Spencer TA, Nekl E, Pusztai-Carey M, Moar WJ, Siegfried BD, Comparison and validation of methods to quantify Cry1Ab toxin from Bacillus thuringiensis for standardization of insect bioassays. Appl Environ Microbiol. 2008;74: 130–135. 17981939
82. Abbott WS, A method of computing the effectiveness of an insecticide. J Econ Entomol. 1925;18: 265–267.
83. Finney DJ, Probit Analysis. 3rd ed. London: Cambridge University Press; 1971.
84. Wolfersberger M, Luethy P, Maurer A, Parenti P, Sacchi FV, Giordana B, et al. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp Biochem Physiol. 1987;86A: 301–308.
85. Bradford MM, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72: 248–254. 942051
86. Jurat-Fuentes JL, Adang MJ, Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur J Biochem. 2004;271: 3127–3135. 15265032
87. Bel Y, Siqueira HAA, Siegfried BD, Ferré J, Escriche B, Variability in the cadherin gene in an Ostrinia nubilalis strain selected for Cry1Ab resistance. Insect Biochem Mol Biol. 2009;39: 218–223. doi: 10.1016/j.ibmb.2008.11.005 19114103
88. Xie W, Lei Y, Fu W, Yang Z, Zhu X, Guo Z, et al. Tissue-specific transcriptome profiling of Plutella xylostella third instar larval midgut. Int J Biol Sci. 2012;8: 1142–1155. doi: 10.7150/ijbs.4588 23091412
89. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28: 2731–2739. doi: 10.1093/molbev/msr121 21546353
90. Livak KJ, Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25: 402–408. 11846609
91. Bautista MA, Miyata T, Miura K, Tanaka T, RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochem Mol Biol. 2009;39: 38–46. doi: 10.1016/j.ibmb.2008.09.005 18957322
92. Jurat-Fuentes JL, Gould FL, Adang MJ, Dual resistance to Bacillus thuringiensis Cry1Ac and Cry2Aa toxins in Heliothis virescens suggests multiple mechanisms of resistance. Appl Environ Microbiol. 2003;69: 5898–5906. 14532042
93. Dechklar M, Tiewsiri K, Angsuthanasombat C, Pootanakit K, Functional expression in insect cells of glycosylphosphatidylinositol-linked alkaline phosphatase from Aedes aegypti larval midgut: a Bacillus thuringiensis Cry4Ba toxin receptor. Insect Biochem Mol Biol. 2011;41: 159–166. doi: 10.1016/j.ibmb.2010.11.006 21146607
94. Jiménez AI, Reyes EZ, Cancino-Rodezno A, Bedoya-Pérez LP, Caballero-Flores GG, Muriel-Millan LF, et al. Aedes aegypti alkaline phosphatase ALP1 is a functional receptor of Bacillus thuringiensis Cry4Ba and Cry11Aa toxins. Insect Biochem Mol Biol. 2012;42: 683–689. doi: 10.1016/j.ibmb.2012.06.001 22728570