Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action

Pesticide Biochemistry and Physiology

Volumn 104, Issue 2, 2012, Pages 103-110

  Heckel, David G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

ABC transporter; Bacillus thuringiensis; Cry1A toxin; Insect resistance; Lepidoptera

Indexed keywords

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA; LEPIDOPTERA;

EID: 84868001840     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2012.05.007     Document Type: Article

References (82)

1. Sanchis V. From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review. Agron. Sustainable Dev. 2011, 31:217-231.
2. C. James, Global Status of Commercialized Biotech/GM Crops: 2008. ISAAA Brief No. 39, International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY, 2009.
3. Pietrantonio P.V., Gill S.S. Bacillus thuringiensis toxins: action on the insect midgut. Biology of the Insect Midgut 1996, 345-372. Chapman & Hall, London. M.J. Lehane, P.F. Billingsley (Eds.).
4. Soberón M., Gill S.S., Bravo A. Signaling versus punching hole: How do Bacillus thuringiensis toxins kill insect midgut cells?. Cell. Mol. Life Sci. 2009, 66:1337-1349.
5. Pigott C.R., Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 2007, 71:255-281.
6. Soberón M., Pardo L., Muñóz-Garay C., Sánchez J., Gómez I., Porta H., Bravo A. Pore formation by Cry toxins. Proteins: Membrane Binding and Pore Formation 2010, 127-142. Landes Bioscience, Austin, TX. G. Anderluh, J. Lakey (Eds.).
7. Knowles B.H., Ellar D.J. Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis delta-endotoxins with different insect specificity. Biochim. Biophys. Acta 1987, 924:509-518.
8. Broderick N.A., Raffa K.F., Handelsman J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. USA 2006, 103:15196-15199.
9. Griffitts J.S., Haslam S.M., Yang T.L., Garczynski S.F., Mulloy B., Morris H., Cremer P.S., Dell A., Adang M.J., Aroian R.V. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 2005, 307:922-925.
10. Kao C.-Y., Los F.C.O., Huffman D.L., Wachi S., Kloft N., Husmann M., Karabrahimi V., Schwartz J.-L., Bellier A., Ha C., Sagong Y., Fan H., Ghosh P., Hsieh M., Hsu C.-S., Chen L., Aroian R.V. Global functional analyses of cellular responses to pore-forming toxins. PLoS Path. 2011, 7:e1001314.
11. Kho M.F., Bellier A., Balasubramani V., Hu Y., Hsu W., Nielsen-LeRoux C., McGillivray S.M., Nizet V., Aroian R.V. The pore-forming protein Cry5B elicits the pathogenicity of Bacillus sp against Caenorhabditis elegans. PLoS One 2011, 6:e29122.
12. Zhang X.B., Candas M., Griko N.B., Taussig R., Bulla L.A. 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.
13. de Maagd R.A., Bravo A., Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world [Review]. Trends Genet. 2001, 17:193-199.
14. Tabashnik B.E., Van Rensburg J.B.J., Carrière Y. Field-evolved insect resistance to Bt crops: definition, theory, and data. J. Econ. Entomol. 2009, 102:2011-2025.
15. Tabashnik B.E., Cushing N.L., Finson N., Johnson M.W. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 1990, 83:1671-1676.
16. Shelton A.M., Robertson J.L., Tang J.D., Pérez C., Eigenbrode S.D., Preisler H.K., Wilsey W.T., Cooley R.J. Resistance of diamondback moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the field. J. Econ. Entomol. 1993, 86:697-705.
17. Ferré J., Van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 2002, 47:501-533.
18. Tabashnik B.E., Liu Y.B., Malvar T., Heckel D.G., Masson L., Ferré J. Insect resistance to Bacillus thuringiensis: uniform or diverse?. Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 1998, 353:1751-1756.
19. Tabashnik B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 1994, 39:47-97.
20. Oppert B., Kramer K.J., Beeman R.W., Johnson D., McGaughey W.H. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J. Biol. Chem. 1997, 272:23473-23476.
21. Ferré J., Real M.D., van Rie J., Jansens S., Peferoen M. Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. Proc. Natl. Acad. Sci. USA 1991, 88:5119-5123.
22. Knight P.J.K., Crickmore N., Ellar D.J. The receptor for Bacillus thuringiensis CrylA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 1994, 11:429-436.
23. Sangadala S., Walters F.S., English L.H., Adang M.J. A mixture of Manduca sexta aminopeptidase and phosphatase enhances Bacillus thuringiensis insecticidal CryIA(c) toxin binding and (Rb+-K+)-Rb-86 efflux in vitro. J. Biol. Chem. 1994, 269:10088-10092.
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.
25. S. Herrero, T. Gechev, P.L. Bakker, W.J. Moar, and R.A. de Maagd, Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes. BMC Genomics 6 (2005) art. 96.
26. Vadlamudi R.K., Weber E., Ji I.H., Ji T.H., Bulla L.A. Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 1995, 270:5490-5494.
27. Nagamatsu Y., Koike T., Sasaki K., Yoshimoto A., Furukawa Y. The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal CryIAa toxin. FEBS Lett. 1999, 460:385-390.
28. Gahan L.J., Gould F., Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293:857-860.
29. Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellers-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carrière Y., Dennehy T.J., Brown J.K., Tabashnik B.E. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. USA 2003, 100:5004-5009.
30. Xu X.J., Yu L.Y., Wu Y.D. Disruption of a cadherin gene associated with resistance to Cry1Ac delta-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 2005, 71:948-954.
31. Sharom F.J. The P-glycoprotein multidrug transporter. Essays Biochem. 2011, 50:161-178.
32. Slot A.J., Molinski S.V., Cole S.P.C. Mammalian multidrug-resistance proteins (MRPs). Essays Biochem. 2011, 50:179-207.
33. Tamaki A., Ierano C., Szakacs G., Robey R.W., Bates S.E. The controversial role of ABC transporters in clinical oncology. Essays Biochem. 2011, 50:209-232.
34. Higgins C.F., Linton K.J. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 2004, 11:918-926.
35. Linton K.J. Structure and function of ABC transporters. Physiology 2007, 22:122-130.
36. Buss D.S., Callaghan A. Interaction of pesticides with P-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic. Biochem. Physiol. 2008, 90:141-153.
37. Leprohon P., Legare D., Ouellette M. ABC transporters involved in drug resistance in human parasites. Essays Biochem. 2011, 50:121-144.
38. Lanning C.L., Fine R.L., Corcoran J.J., Ayad H.M., Rose R.L., AbouDonia M.B. Tobacco budworm P-glycoprotein: biochemical characterization and its involvement in pesticide resistance. Biochim. Biophys. Acta 1996, 1291:155-162.
39. Labbé R., Caveney S., Donly C. Expression of multidrug resistance proteins is localized principally to the Malpighian tubules in larvae of the cabbage looper moth Trichoplusia ni. J. Exp. Biol. 2011, 214:937-944.
40. Aurade R.M., Jayalakshmi S.K., Sreeramulu K. P-glycoprotein ATPase from the resistant pest, Helicoverpa armigera: purification, characterization and effect of various insecticides on its transport function. Biochim. Biophys. Acta 2010, 1798:1135-1143.
41. Aurade R.M., Akbar S.M., Goud H., Jayalakshmi S.K., Sreeramulu K. Inhibition of P-glycoprotein ATPase and its transport function of Helicoverpa armigera by morin, quercetin and phloroglucinol. Pestic. Biochem. Physiol. 2011, 101:212-219.
42. 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.
43. S.M. Liu, S. Zhou, L. Tian, E.N. Guo, Y.X. Luan, J.Z. Zhang, S. Li, Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics 12 (2011) art. 491.
44. Lee M.K., Rajamohan F., Gould F., Dean D.H. Resistance to Bacillus thuringiensis CryIA delta-endotoxins in a laboratory-selected Heliothis virescens strain is related to receptor alteration. Appl. Environ. Microbiol. 1995, 61:3836-3842.
45. Jurat-Fuentes J.L., Gahan L.J., Gould F.L., Heckel D.G., Adang M.J. The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry 2004, 43:14299-14305.
46. Jurat-Fuentes J.L., Gould F.L., Adang M.J. Altered glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl. Environ. Microbiol. 2002, 68:5711-5717.
47. Gahan L.J., Gould F., López J.D., Micinski S., Heckel D.G. A polymerase chain reaction screen of field populations of Heliothis virescens for a retrotransposon insertion conferring resistance to Bacillus thuringiensis toxin. J. Econ. Entomol. 2007, 100:187-194.
48. Gahan L.J., Pauchet Y., Vogel H., Heckel D.G. An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet. 2010, 6:e1001248.
49. Tabashnik B.T., Liu Y.-B., Finson N., Masson L., Heckel D.G. One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proc. Natl. Acad. Sci. USA 1997, 94:1640-1644.
50. Tabashnik B.E., Liu Y.B., Malvar T., Heckel D.G., Masson L., Ballester V., Granero F., Mensua J.L., Ferré J. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 1997, 94:12780-12785.
51. Tabashnik B.E., Finson N., Groeters F.R., Moar W.J., Johnson M.W., Luo K., Adang M.J. Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. Proc. Natl. Acad. Sci. USA 1994, 91:4120-4124.
52. Heckel D.G., Gahan L.J., Liu Y.B., Tabashnik B.E. Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphasic linkage analysis. Proc. Natl. Acad. Sci. USA 1999, 96:8373-8377.
53. Baxter S.W., Zhao J.Z., Gahan L.J., Shelton A.M., Tabashnik B.E., Heckel D.G. Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol. Biol. 2005, 14:327-334.
54. Baxter S.W., Zhao J.Z., Shelton A.M., Vogel H., Heckel D.G. 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.
55. Baxter S.W., Badenes-Pérez F.R., Morrison A., Vogel H., Crickmore N., Kain W., Wang P., Heckel D.G., Jiggins C.D. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 2011, 189:U675-U814.
56. Janmaat A.F., Wang P., Kain W., Zhao J.Z., Myers J. Inheritance of resistance to Bacillus thuringiensis subsp kurstaki in Trichoplusia ni. Appl. Environ. Microbiol. 2004, 70:5859-5867.
57. S. Atsumi, K. Miyamoto, K. Yamamoto, J. Narukawa, S. Kawai, H. Sezutsu, I. Kobayashi, K. Uchino, T. Tamura, K. Mita, K. Kadono-Okuda, S. Wada, K. Kanda, M.R. Goldsmith, H. Noda, A single amino acid mutation in an ABC transporter causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. PNAS Plus (2012) doi:10.1073/pnas.1120698109.
58. Heckel D.G. Molecular genetics of insecticide resistance in Lepidoptera. Molecular Biology and Genetics of the Lepidoptera 2010, 239-269. CRC Press, Boca Raton. M.R. Goldsmith, F. Marec (Eds.).
59. Bravo A., Gill S.S., Soberón M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49:423-435.
60. Aller S.G., Yu J., Ward A., Weng Y., Chittaboina S., Zhuo R., Harrell P.M., Trinh Y.T., Zhang Q.H., Urbatsch I.L., Chang G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323:1718-1722.
61. Wang P., Zhao J.Z., Rodrigo-Simón A., Kain W., Janmaat A.F., Shelton A.M., Ferré J., Myers J. 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.
62. Vadlamudi R.K., Ji T.H., Bulla L.A. A specific binding protein from Manduca sexta for the insecticidal toxin of Bacillus thuringiensis subsp Berliner. J. Biol. Chem. 1993, 268:12334-12340.
63. Nagamatsu Y., Toda S., Yamaguchi F., Ogo M., Kogure M., Nakamura M., Shibata Y., Katsumoto T. Identification of Bombyx mori midgut receptor for Bacillus thuringiensis insecticidal CryIA(a) toxin. Biosci. Biotechnol. Biochem. 1998, 62:718-726.
64. Hossain D.M., Shitomi Y., Moriyama K., Higuchi M., Hayakawa T., Mitsui T., Sato R., Hori H. Characterization of a novel plasma membrane protein, expressed in the midgut epithelia of Bombyx mori, that binds to Cry1A toxins. Appl. Environ. Microbiol. 2004, 70:4604-4612.
65. Valaitis A.P., Jenkins J.L., Lee M.K., Dean D.H., Garner K.J. Isolation and partial characterization of gypsy moth BTR-270, an anionic brush border membrane glycoconjugate that binds Bacillus thuringiensis Cry1A toxins with high affinity. Arch. Insect Biochem. Physiol. 2001, 46:186-200.
66. McNall R.J., Adang M.J. Identification of novel Bacillus thuringiensis Cry1Ac binding proteins in Manduca sexta midgut through proteomic analysis. Insect Biochem. Mol. Biol. 2003, 33:999-1010.
67. Candas M., Loseva O., Oppert B., Kosaraju P., Bulla L.A. Insect resistance to Bacillus thuringiensis - alterations in the indianmeal moth larval gut proteome. Mol. Cell. Proteomics 2003, 2:19-28.
68. Krishnamoorthy M., Jurat-Fuentes J.L., McNall R.J., Andacht T., Adang M.J. Identification of novel CrylAc binding proteins in midgut membranes from Heliothis virescens using proteomic analyses. Insect Biochem. Mol. Biol. 2007, 37:189-201.
69. Chen L.Z., Liang G.M., Zhang J., Wu K.M., Guo Y.Y., Rector B.G. Proteomic analysis of novel Cry1Ac binding proteins in Helicoverpa armigera (Hübner). Arch. Insect Biochem. Physiol. 2010, 73:61-73.
70. M. Soberón, C. Rodriguez-Almazán, C. Muñóz-Garay, L. Pardo-López, H. Porta, A. Bravo, Bacillus thuringiensis Cry and Cyt mutants useful to counter toxin action in specific environments and to overcome insect resistance in the field. Pestic. Biochem. Physiol. 102 (this issue) (2012).
71. Tabashnik B.E., Huang F., Ghimire M.N., Leonard B.R., Siegfried B.D., Rangasamy M., Yang Y., Wu Y., Gahan L.J., Heckel D.G., Bravo A., Soberón M. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat. Biotechnol. 2011, 29. 1128-U98.
72. Anilkumar K.J., Sivasupramaniam S., Head G., Orth R., Van Santen E., Moar W.J. Synergistic interactions between Cry1Ac and natural cotton defenses limit survival of Cry1Ac-resistant Helicoverpa zea (Lepidoptera: Noctuidae) on Bt cotton. J. Chem. Ecol. 2009, 35:785-795.
73. Carrière Y., Ellers-Kirk C., Biggs R., Higginson D.M., Dennehy T.J., Tabashnik B.E. Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. J. Econ. Entomol. 2004, 97:1710-1718.
74. Chen J., Hua G., Jurat-Fuentes J.L., Abdullah M.A., Adang M.J. Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin. Proc. Natl. Acad. Sci. USA 2007, 104:13901-13906.
75. Park Y., Hua G., Abdullah M.A.F., Rahman K., Adang M.J. Cadherin fragments from Anopheles gambiae synergize Bacillus thuringiensis Cry4Ba's toxicity against Aedes aegypti larvae. Appl. Environ. Microbiol. 2009, 75:7280-7282.
76. Park Y., Abdullah M.A.F., Taylor M.D., Rahman K., Adang M.J. Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to coleopteran larvae by a toxin-binding fragment of an insect cadherin. Appl. Environ. Microbiol. 2009, 75:3086-3092.
77. Hernández-Rodríguez C.S., Van Vliet A., Bautsoens N., Van Rie J., Ferré J. Specific binding of Bacillus thuringiensis Cry2A insecticidal proteins to a common site in the midgut of Helicoverpa species. Appl. Environ. Microbiol. 2008, 74:7654-7659.
78. Caccia S., Hernández-Rodríguez C.S., Mahon R.J., Downes S., James W., Bautsoens N., Van Rie J., Ferré J. Binding site alteration is responsible for field-isolated resistance to Bacillus thuringiensis Cry2A insecticidal proteins in two Helicoverpa species. PLoS One 2010, 5:e9975.
79. Gould F., Martínez-Ramírez A., Anderson A., Ferré J., Silva F.J., Moar W.J. Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. Proc. Natl. Acad. Sci. USA 1992, 89:7986-7988.
80. Gahan L.J., Ma Y.T., Coble M.L.M., Gould F., Moar W.J., Heckel D.G. Genetic basis of resistance to Cry1Ac and Cry2Aa in Heliothis virescens (Lepidoptera: Noctuidae). J. Econ. Entomol. 2005, 98:1357-1368.
81. Tabashnik B.E., Malvar T., Liu Y.B., Finson N., Borthakur D., Shin B.S., Park S.H., Masson L., de Maagd R.A., Bosch D. Cross-resistance of the diamondback moth indicates altered interactions with domain II of Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 1996, 62:2839-2844.
82. Ito K., Kidokoro K., Sezutsu H., Nohata J., Yamamoto K., Kobayashi I., Uchino K., Kalyebi A., Eguchi R., Hara W., Tamura T., Katsuma S., Shimada T., Mita K., Kadono-Okuda K. Deletion of a gene encoding an amino acid transporter in the midgut membrane causes resistance to a Bombyx parvo-like virus. Proc. Natl. Acad. Sci. USA 2008, 105:7523-7527.