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. 1997 May;63(5):1814–1819. doi: 10.1128/aem.63.5.1814-1819.1997

A Change in a Single Midgut Receptor in the Diamondback Moth (Plutella xylostella) Is Only in Part Responsible for Field Resistance to Bacillus thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai

D J Wright, M Iqbal, F Granero, J Ferre
PMCID: PMC1389152  PMID: 16535597

Abstract

A population (SERD3) of the diamondback moth (Plutella xylostella L.) with field-evolved resistance to Bacillus thuringiensis subsp. kurstaki HD-1 (Dipel) and B. thuringiensis subsp. aizawai (Florbac) was collected. Laboratory-based selection of two subpopulations of SERD3 with B. thuringiensis subsp. kurstaki (Btk-Sel) or B. thuringiensis subsp. aizawai (Bta-Sel) increased resistance to the selecting agent with little apparent cross-resistance. This result suggested the presence of independent resistance mechanisms. Reversal of resistance to B. thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai was observed in the unselected SERD3 subpopulation. Binding to midgut brush border membrane vesicles was examined for insecticidal crystal proteins specific to B. thuringiensis subsp. kurstaki (Cry1Ac), B. thuringiensis subsp. aizawai (Cry1Ca), or both (Cry1Aa and Cry1Ab). In the unselected SERD3 subpopulation (ca. 50- and 30-fold resistance to B. thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai), specific binding of Cry1Aa, Cry1Ac, and Cry1Ca was similar to that for a susceptible population (ROTH), but binding of Cry1Ab was minimal. The Btk-Sel (ca. 600-and 60-fold resistance to B. thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai) and Bta-Sel (ca. 80-and 300-fold resistance to B. thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai) subpopulations also showed reduced binding to Cry1Ab. Binding of Cry1Ca was not affected in the Bta-Sel subpopulation. The results suggest that reduced binding of Cry1Ab can partly explain resistance to B. thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai. However, the binding of Cry1Aa, Cry1Ac, and Cry1Ca and the lack of cross-resistance between the Btk-Sel and Bta-Sel subpopulations also suggest that additional resistance mechanisms are present.

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Selected References

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  1. Alstad D. N., Andow D. A. Managing the evolution of insect resistance to transgenic plants. Science. 1995 Jun 30;268(5219):1894–1896. doi: 10.1126/science.268.5219.1894. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Denolf P., Jansens S., Peferoen M., Degheele D., Van Rie J. Two Different Bacillus thuringiensis Delta-Endotoxin Receptors in the Midgut Brush Border Membrane of the European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae). Appl Environ Microbiol. 1993 Jun;59(6):1828–1837. doi: 10.1128/aem.59.6.1828-1837.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Estada U., Ferre J. Binding of Insecticidal Crystal Proteins of Bacillus thuringiensis to the Midgut Brush Border of the Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), and Selection for Resistance to One of the Crystal Proteins. Appl Environ Microbiol. 1994 Oct;60(10):3840–3846. doi: 10.1128/aem.60.10.3840-3846.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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 U S A. 1991 Jun 15;88(12):5119–5123. doi: 10.1073/pnas.88.12.5119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fiuza L., Nielsen-Leroux C., Goze E., Frutos R., Charles J. Binding of Bacillus thuringiensis Cry1 Toxins to the Midgut Brush Border Membrane Vesicles of Chilo suppressalis (Lepidoptera: Pyralidae): Evidence of Shared Binding Sites. Appl Environ Microbiol. 1996 May;62(5):1544–1549. doi: 10.1128/aem.62.5.1544-1549.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gill S. S., Cowles E. A., Pietrantonio P. V. The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol. 1992;37:615–636. doi: 10.1146/annurev.en.37.010192.003151. [DOI] [PubMed] [Google Scholar]
  8. Gould F., Martinez-Ramirez A., Anderson A., Ferre J., Silva F. J., Moar W. J. Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):7986–7990. doi: 10.1073/pnas.89.17.7986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hofmann C., Lüthy P., Hütter R., Pliska V. Binding of the delta endotoxin from Bacillus thuringiensis to brush-border membrane vesicles of the cabbage butterfly (Pieris brassicae). Eur J Biochem. 1988 Apr 5;173(1):85–91. doi: 10.1111/j.1432-1033.1988.tb13970.x. [DOI] [PubMed] [Google Scholar]
  10. Höfte H., Whiteley H. R. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev. 1989 Jun;53(2):242–255. doi: 10.1128/mr.53.2.242-255.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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 Nov;61(11):3836–3842. doi: 10.1128/aem.61.11.3836-3842.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. MacIntosh S. C., Stone T. B., Jokerst R. S., Fuchs R. L. Binding of Bacillus thuringiensis proteins to a laboratory-selected line of Heliothis virescens. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8930–8933. doi: 10.1073/pnas.88.20.8930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Masson L., Préfontaine G., Péloquin L., Lau P. C., Brousseau R. Comparative analysis of the individual protoxin components in P1 crystals of Bacillus thuringiensis subsp. kurstaki isolates NRD-12 and HD-1. Biochem J. 1990 Jul 15;269(2):507–512. doi: 10.1042/bj2690507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McGaughey W. H., Whalon M. E. Managing Insect Resistance to Bacillus thuringiensis Toxins. Science. 1992 Nov 27;258(5087):1451–1455. doi: 10.1126/science.258.5087.1451. [DOI] [PubMed] [Google Scholar]
  15. Moar W. J., Pusztai-Carey M., Van Faassen H., Bosch D., Frutos R., Rang C., Luo K., Adang M. J. Development of Bacillus thuringiensis CryIC Resistance by Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). Appl Environ Microbiol. 1995 Jun;61(6):2086–2092. doi: 10.1128/aem.61.6.2086-2092.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Munson P. J., Rodbard D. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem. 1980 Sep 1;107(1):220–239. doi: 10.1016/0003-2697(80)90515-1. [DOI] [PubMed] [Google Scholar]
  17. Oppert B., Kramer K. J., Johnson D. E., MacIntosh S. C., McGaughey W. H. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella. Biochem Biophys Res Commun. 1994 Feb 15;198(3):940–947. doi: 10.1006/bbrc.1994.1134. [DOI] [PubMed] [Google Scholar]
  18. Tabashnik B. E. Evaluation of synergism among Bacillus thuringiensis toxins. Appl Environ Microbiol. 1992 Oct;58(10):3343–3346. doi: 10.1128/aem.58.10.3343-3346.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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 U S A. 1994 May 10;91(10):4120–4124. doi: 10.1073/pnas.91.10.4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tabashnik B. E., Finson N., Johnson M. W., Moar W. J. Resistance to Toxins from Bacillus thuringiensis subsp. kurstaki Causes Minimal Cross-Resistance to B. thuringiensis subsp. aizawai in the Diamondback Moth (Lepidoptera: Plutellidae). Appl Environ Microbiol. 1993 May;59(5):1332–1335. doi: 10.1128/aem.59.5.1332-1335.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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 Aug;62(8):2839–2844. doi: 10.1128/aem.62.8.2839-2844.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tang J. D., Shelton A. M., Van Rie J., De Roeck S., Moar W. J., Roush R. T., Peferoen M. Toxicity of Bacillus thuringiensis Spore and Crystal Protein to Resistant Diamondback Moth (Plutella xylostella). Appl Environ Microbiol. 1996 Feb;62(2):564–569. doi: 10.1128/aem.62.2.564-569.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Thompson M. A., Schnepf H. E., Feitelson J. S. Structure, function and engineering of Bacillus thuringiensis toxins. Genet Eng (N Y) 1995;17:99–117. [PubMed] [Google Scholar]
  24. Van Rie J., Jansens S., Höfte H., Degheele D., Van Mellaert H. Receptors on the brush border membrane of the insect midgut as determinants of the specificity of Bacillus thuringiensis delta-endotoxins. Appl Environ Microbiol. 1990 May;56(5):1378–1385. doi: 10.1128/aem.56.5.1378-1385.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Van Rie J., Jansens S., Höfte H., Degheele D., Van Mellaert H. Specificity of Bacillus thuringiensis delta-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur J Biochem. 1989 Dec 8;186(1-2):239–247. doi: 10.1111/j.1432-1033.1989.tb15201.x. [DOI] [PubMed] [Google Scholar]
  26. Van Rie J., McGaughey W. H., Johnson D. E., Barnett B. D., Van Mellaert H. Mechanism of insect resistance to the microbial insecticide Bacillus thuringiensis. Science. 1990 Jan 5;247(4938):72–74. doi: 10.1126/science.2294593. [DOI] [PubMed] [Google Scholar]
  27. Wolfersberger M. G. The toxicity of two Bacillus thuringiensis delta-endotoxins to gypsy moth larvae is inversely related to the affinity of binding sites on midgut brush border membranes for the toxins. Experientia. 1990 May 15;46(5):475–477. doi: 10.1007/BF01954236. [DOI] [PubMed] [Google Scholar]

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