Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of the pea aphid, Acyrthosiphon pisum (Harris)

Journal of Invertebrate Pathology

Volumn 107, Issue 1, 2011, Pages 69-78

  Li, Huarong ^a,b   Chougule, Nanasaheb P ^a   Bonning, Bryony C ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b DOW AGROSCIENCES LLC   (United States)

Author keywords

Bacillus thuringiensis; Cysteine protease; Delta endotoxin; Gut proteases; Pea aphid; Toxin stability

Indexed keywords

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

ANIMAL; APHID; ARTICLE; BACILLUS THURINGIENSIS; CHEMISTRY; GASTROINTESTINAL TRACT; INSECTICIDE RESISTANCE; METABOLISM; PHYSIOLOGY;

ANIMALS; APHIDS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; GASTROINTESTINAL TRACT; HEMOLYSIN PROTEINS; INSECTICIDE RESISTANCE;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); PISUM SATIVUM;

EID: 79953767331     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2011.02.001     Document Type: Article

References (48)

1. Abdul-Rauf M., Ellar D.J. Isolation and Characterization of brush border membrane vesicles from whole Aedes aegypti larvae. J. Invertebr. Pathol. 1999, 73:45-51.
2. Ali M.I., Luttrell R.G., Young S.Y. Suscepibilities of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) populations to Cry1Ac insecticidal protein. J. Econ. Entomol. 2006, 99:164-175.
3. Ashouri A. Seasonal occurrence and relative abundance of aphids on potato plants with classical and transgenic characters of resistance to Colorado potato beetle Leptinotarsa decemlineata (Say). Commun. Agric. Appl. Biol. Sci. 2004, 69:273-280.
4. Ashouri A. Transgenic-Bt potato plant resistance to the colorado potato beetle affect the aphid parasitoid Aphidius nigripes. Commun. Agric. Appl. Biol. Sci. 2004, 69:185-189.
5. Ashouri A., Michaud D., Cloutier C. Unexpected effects of different potato resistance factors to the Colorado potato beetle (Coleoptera: Chrysolmelidae) on the potato aphid (Homoptera: Aphididae). Environ. Entomol. 2001, 30:524-532.
6. Blanco C.A., Gould F., Vega-Aquino P., Jurat-Fuentes J.L., Perera O.P., Abel C.A. Response of Heliothis virescens (Lepidoptera: Noctuidae) strains to Bacillus thuringiensis Cry1Ac incorporated into different insect artificial diets. J. Econ. Entomol. 2009, 102:1599-1606.
7. Bolin P.C., Hutchinson W.D., Andow D.A. Long-term selection for resistance to Bacillus thuringiensis Cry1Ac endotoxin in a Minnesota population of European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 1999, 92:1021-1030.
8. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., Soberon M. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta 2004, 1667:38-46.
9. Brisson J.A., Stern D.L. The pea aphid, Acyrthosiphon pisum: an emerging genomic model system for ecological, developmental and evolutionary studies. Bioessays 2006, 28:747-755.
10. Burgio G., Lanzoni A., Accinelli G., Dinelli G., Bonetti A., Marotti I., Ramilli F. Evaluation of Bt-toxin uptake by the non-target herbivore, Myzus persicae (Hemiptera: Aphididae), feeding on transgenic oilseed rape. Bull. Entomol. Res. 2007, 97:211-215.
11. Burton S.L., Ellar D.J., Li J., Derbyshire D.J. 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. J. Mol. Biol. 1999, 287:1011-1022.
12. Cristofoletti P.T., Ribeiro A.F., Deraison C., Rahbe Y., Terra W.R. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J. Insect Physiol. 2003, 49:11-24.
13. Deraison C., Darboux I., Duportets L., Gorojankina T., Rahbe Y., Jouanin L. Cloning and characterization of a gut-specific cathepsin L from the aphid Aphis gossypii. Insect Mol. Biol. 2004, 13:165-177.
14. Faria C.A., Wackers F.L., Pritchard J., Barrett D.A., Turlings T.C. High susceptibility of bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS One 2007, 2:e600.
15. Febvay G., Delobel B., Rahbe Y. Influence of the amino acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera: Aphididae). Can. J. Zool. 1987, 66:2449-2453.
16. Garczynski S.F., Crim J.W., Adang M.J. Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis delta-endotoxin by protein blot analysis. Appl. Environ. Microbiol. 1991, 57:2816-2820.
17. Ge A.Z., Pfister R.M., Dean D.H. Hyperexpression of a Bacillus thuringiensis delta-endotoxin-encoding gene in Escherichia coli: properties of the product. Gene 1990, 93:49-54.
18. Gomez I., Sanchez J., Miranda R., Bravo A., Soberon M. 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 Lett. 2002, 513:242-246.
19. Greene J.K., Turnipseed S.G., Sullivan M.J., Herzog G.A. Boll damage by southern green stink bug (Hemiptera: Pentatomidae) and tarnished plant bug (Hemiptera: Miridae) caged on transgenic Bacillus thuringiensis cotton. J. Econ. Entomol. 1999, 92:941-944.
20. Greene J.K., Turnipseed S.G., Sullivan M.J., May O.L. Treatment thresholds for stink bugs (Hemiptera: Pentatomidae) in cotton. J. Econ. Entomol. 2001, 94:403-409.
21. 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, 173:85-91.
22. Hofmann C., Vanderbruggen H., Heofte H., Van Rie J., Jansens S., Van Mellaert H. Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc. Natl. Acad. Sci. USA 1988, 85:7844-7848.
23. International Aphid Genomics Consortium Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 2010, 8:e1000313.
24. Jurat-Fuentes J.L., Adang M.J. Cry toxin mode of action in susceptible and resistant Heliothis virescens larvae. J. Invertebr. Pathol. 2006, 92:166-171.
25. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
26. Lawo N.C., Wackers F.L., Romeis J. Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS One 2009, 4:e4804.
27. Li H., Buschman L.L., Huang F., Zhu K.Y., Bonning B., Oppert B. DiPel-selected Ostrinia nubilalis larvae are not resistant to transgenic corn expressing Bacillus thuringiensis Cry1Ab. J. Econ. Entomol. 2007, 100:1862-1870.
28. MacIntosh S.C., Lidster B.D., Kirkham C.L. Isolation of brush border membrane vesicles from whole diamondback moths (Lepidoptera: Pluttellidae) larvae. J. Invertebr. Pathol. 1994, 63:97-98.
29. Mellet M.A., Shoeman A.S. Effect of Bt cotton on chrysopids, ladybird beetles and their prey: aphids and whiteflies. Indian J. Exp. Biol. 2007, 45:554-562.
30. Ochoa-Campuzano C., Real M.D., Martinez-Ramirez A.C., Bravo A., Rausell C. An ADAM metalloprotease is a Cry3Aa Bacillus thuringiensis toxin receptor. Biochem. Biophys. Res. Commun. 2007, 362:437-442.
31. Pardo-Lopez L., Gomez I., Rausell C., Sanchez J., Soberon M., Bravo A. Structural changes of the Cry1Ac oligomeric pre-pore from Bacillus thuringiensis induced by N-acetylgalactosamine facilitates toxin membrane insertion. Biochemistry 2006, 45:10329-10336.
32. Park Y., Abdullah M.A., 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.
33. Payne, J.R., Cannon, R.J.C., 1993. Use of Bacillus thuringiensis Isolates for Controlling Pests in the Family Aphididae. US Patent No. 5,262,159.
34. Pérez C., Fernandez L.E., Sun J., Folch J.L., Gill S.S., Soberón M. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. USA 2005, 102(51):18303-18308.
35. Philip J.M., Fitches E., Harrison R.L., Bonning B., Gatehouse J.A. Characterisation of functional and insecticidal properties of a recombinant cathepsin L-like proteinase from flesh fly (Sarcophaga peregrina), which plays a role in differentiation of imaginal discs. Insect Biochem. Mol. Biol. 2007, 37:589-600.
36. Porcar M., Grenier A.M., Federici B., Rahbe Y. Effects of Bacillus thuringiensis delta-endotoxins on the pea aphid (Acyrthosiphon pisum). Appl. Environ. Microbiol. 2009, 75:4897-4900.
37. Raps A., Kehr J., Gugerli P., Moar W.J., Bigler F., Hilbeck A. Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol. Ecol. 2001, 10:525-533.
38. Rausell C., Garcia-Robles I., Sanchez J., Munoz-Garay C., Martinez-Ramirez A.C., Real M.D., Bravo A. Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say). Biochim. Biophys. Acta 2004, 1660:99-105.
39. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998, 62:775-806.
40. Shelton A.M., Zhao J.Z., Roush R.T. Economic, ecological, food safety, and social consequences of the deployment of bt transgenic plants. Annu. Rev. Entomol. 2002, 47:845-881.
41. Sivasupramaniam S., Moar W.J., Ruschke L.G., Osborn J.A., Jiang C., Sebaugh J.L., Brown G.R., Shappley Z.W., Oppenhuizen M.E., Mullins J.W., Greenplate J.T. Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of lepidopteran pests. J. Econ. Entomol. 2008, 101:546-554.
42. Slaney A.C., Robbins H.L., English L. Mode of action of Bacillus thuringiensis toxin CryIIIA: an analysis of toxicity in Leptinotarsa decemlineata (Say) and Diabrotica undecimpunctata howardi Barber. Insect Biochem. Mol. Biol. 1992, 22:9-18.
43. 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, 56(5):1378-1385.
44. Walters F.S., English L.H. Toxicity of Bacillus thuringiensis delta-endotoxins toward the potato aphid in an artificial diet bioassay. Entomol. Exp. Appl. 1995, 77:211-216.
45. Walters F.S., Kulesza C.A., Phillips A.T., English L.H. A stable oligomer of Bacillus thuringiensis delta-endotoxin, CryIIIA. Insect Biochem. Mol. Biol. 1994, 24:963-968.
46. Wolfersberger M.G., Luthy P., Maurer A., Parenti P., Sacchi V.F., Giordana B., Hanozet G.M. 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.
47. Zhang X., 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.
48. Zhuang M., Oltean D.I., Gomez I., Pullikuth A.K., Soberon M., Bravo A., Gill S.S. Heliothis virescens and manduca sexta lipd rafts are invovled in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J. Biol. Chem. 2002, 277:13863-13872.