Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor

Apidologie

Volumn 35, Issue 6, 2004, Pages 655-664

  Malone, Louise A ^a   Todd, Jacqui H ^a   Burgess, Elisabeth P J ^a   Christeller, John T ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

Apis mellifera; Hypopharyngeal gland; Insecticidal transgenic plant protein; Laboratory assay

Indexed keywords

HONEYBEE; INSECTICIDE; LARVAL DEVELOPMENT; PROTEIN; TRANSGENIC PLANT;

APINAE; APIS; APIS MELLIFERA; APOIDEA;

EID: 12444347508     PISSN: 00448435     EISSN: None     Source Type: Journal    
DOI: 10.1051/apido:2004063     Document Type: Article

References (48)

1. Ambrose J.T. (1992) Management for honey production, in: Graham J.M. (Ed.), The Hive and the Honey Bee, Hamilton, Illinois, pp. 601-655.
2. Anon (2000) Bt Plant-Pesticides Biopesticides Registration Action Document, United States Environmental Protection Agency, http://www.epa.gov/ scipoly/sap/2000/october/brad2_scienceassessment.pdf (accessed on 19 October 2004).
3. Arpaia S. (1996) Ecological impact of Bt-transgenic plants: 1. Assessing possible effects of CryIIIB toxin on honey bee (Apis mellifera L.) colonies, J. Genet. Breed. 50, 315-319.
4. Babendreier D., Kalberer N., Romeis J., Fluri P., Bigler F. (2004) Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants, Apidologie 35, 293-300.
5. Billingsley P.F., Lehane M.J. (1996) Structure and ultrastructure of the insect midgut: in: Lehane M.J., Billingsley P.F. (Eds.), Biology of the Insect Midgut, Chapman & Hall, London, UK, pp. 3-30.
6. Bonadé Bottino M., Girard C., Le Métayer M., Picard-Nizou A.L., Sandoz G., Lerin J., Pham-Delègue M.H., Jouanin L. (1998) Effects of transgenic oilseed rape expressing proteinase inhibitors on pest and beneficial insects, Proc. Int. Symp. Brassicas, Acta Hort. 459, 235-239.
7. Brødsgaard H.F., Brødsgaard C.J., Hansen H., Lövei G.L. (2003) Environmental risk assessment of transgene products using honey bee (Apis mellifera) larvae, Apidologie 34, 139-145.
8. Bruins B.G., Scharloo W., Thorig G.E.W. (1991) The harmful effect of light on Drosophila is diet-dependent, Insect Biochem. 21, 535-539.
9. Burgess E.P.J., Malone L.A., Christeller J.T. (1996) Effects of two proteinase inhibitors on the digestive enzymes and survival of honey bees (Apis mellifera). J. Insect Physiol. 42, 823-828.
10. Burgess E.P.J., Malone L.A., Christeller J.T., Lester M.T., Murray C., Philip B.A., Phung M.M., Tregidga E.L. (2002a) Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, Helicoverpa armigera and Spodoptera litura, Transgenic Res. 11, 185-198.
11. Burgess E.P.J., Lövei G.L., Malone L.A., Nielsen I.W., Gatehouse H.S., Christeller J.T. (2002b) Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis, J. Insect Physiol. 48, 1093-1101.
12. Colebatch G.M. (1999) Organisation of digestion and digestive proteinases in the green mirid, Creotiades dilutus, Ph.D Thesis, Australian National University, Canberra, 184 p.
13. Christeller J.T., Burgess E.P.J., Mett V., Gatehouse H.S., Markwick N.P., Murray C., Malone L.A., Wright M., Philip B.A., Watt D., Gatehouse L.N., Lovei G.L., Shannon A.L., Phung M.M., Watson L., Laing W.A. (2002) The expression of a mammalian protease inhibitor, bovine spleen trypsin inhibitor (SI), in tobacco and effects on Helicoverpa armigera larvae, Transgenic Res. 11, 161-173.
14. Crailsheim K., Stolberg E. (1989) Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L.), J. Insect Physiol. 35, 595-602.
15. Crailsheim K., Hrassnigg N., Lorenz W., Lass A. (1993) Protein consumption and distribution in a honeybee colony (Apis mellifera carnica Pollm.), Apidologie 24, 509-511.
16. Fishman L., Zlotkin E. (1984) A diffusional route of transport of horseradish peroxidase through the midgut of the fleshfly, J. Exp. Zool. 229, 189-195.
17. Graham J., Gordon S.C., McNicol R.J. (1997) The effect of the CpTI gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae), Ann. Appl. Biol. 131, 133-139.
18. Greenplate J. (1997) Response to reports of early damage in 1996 commercial Bt transgenic cotton (Bollgard™) plantings, Soc. Invertebr. Pathol. Newsletter 29, 15-18.
19. Hanley A.V., Huang Z.Y., Pett W.L. (2003) Effects of dietary transgenic Bt corn pollen on larvae of Apis mellifera and Galleria mellonella, J. Apicult. Res. 42, 77-81.
20. Hatfield P.R. (1988) Detection and localisation of antibody ingested with a mosquito blood meal, Med. Vet. Entomol. 2, 339-345.
21. Heath R.L., McDonald G., Christeller J.T., Lee M., Bateman K., West J., van Heeswijck R., Anderson M.A. (1997) Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests, J. Insect Physiol. 43, 833-842.
22. Hood E.E., Witcher D.R., Maddock S., Meyer T., Baszczynski C., Bailey M., Flynn P., Register J., Marshall L, Bond D., Kulisek E., Kusnadi A., Evangelista R., Nikolov Z., Wooge C., Mehigh R.J., Hernan R., Kappel W.K., Ritland D., Li C.P., Howard J.A. (1997) Commercial production of avidin from transgenic maize: characterization of transformant, production, processing, extraction and purification, Mol. Breed. 3, 291-306.
23. Huang Z.Y., Otis G.W. (1989) Factors determining hypopharyngeal gland activity of worker honey bees (Apis mellifera L.), Insectes Soc. 36, 264-276.
24. Jouanin L., Girard C., Bonadé-Bottino M., Le Métayer M., Picard Nizou A.L., Lerin J., Pham-Delègue M.H. (1998) Impact de colzas transgéniques exprimant des inhibiteurs de protéases sur coléoptères phytophages et sur abeilles, Cah. Agric. 7, 531-536.
25. Koziel M.G., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., Dawson J., Desai N., Hill M., Kadwell S., Launis K., Lewis K., Maddox D., McPherson K., Meghji M.R., Merlin E., Rhodes R., Warren G., Wright M., Evola S.V. (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis, Bio/Technology 11, 194-200.
26. Kramer K.J., Morgan T.D., Throne J.E., Dowell F.E., Bailey M., Howard J.A. (2000) Transgenic avidin maize is resistant to storage insect pests, Nat. Biotechnol. 18, 670-674.
27. Lass A., Crailsheim K. (1996) Influence of age and caging upon protein metabolism, hypopharyngeal glands and trophallactic behavior in the honey bee (Apis mellifera L.), Insectes Soc. 43, 347-358.
28. Leplé J.C., Bonadé-Bottino M., Augustin S., Pilate G., le Tan V.D., Delplanque A., Cornu D., Jouanin L. (1995) Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor, Mol. Breed. 1, 319-328.
29. Levinson H.Z., Levinson A.R., Offenberger M. (1992) Effect of dietary antagonists and corresponding nutrients on growth and reproduction of the flour mite (Acarus siro L), Experientia 48, 721-729.
30. Malone L.A., Giacon H.A., Burgess E.P.J., Maxwell J.Z., Christeller J.T., Laing W.A. (1995) Toxicity of trypsin endopeptidase inhibitors to honey bees (Hymenoptera: Apidae), J. Econ. Entomol. 88. 46-50.
31. Malone L.A., Burgess E.P.J., Christeller J.T., Gatehouse H.S. (1998) In vivo responses of honey bee mid-gut proteases to two protease inhibitors from potato, J. Insect Physiol. 44, 141-147.
32. Malone L.A., Burgess E.P.J., Stefanovic D. (1999) Effects of a Bacillus thuringiensis toxin, two Bacillus thuringiensis biopesticide formulations, and a soybean trypsin inhibitor on honey bee (Apis mellifera L.) survival and food consumption, Apidologie 30, 465-473.
33. Malone L.A., Burgess E.P.J., Gatehouse H.S., Voisey C.R., Tregidga E.L., Philip B.A. (2001) Effects of ingestion of a Bacillus thuringiensis toxin and a trypsin inhibitor on honey bee flight activity and longevity, Apidologie 32, 57-68.
34. Malone L.A., Pham-Delègue M.H. (2001) Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.), Apidologie 32, 287-304.
35. Malone L.A., Burgess E.P.J., Mercer C.F., Christeller J.T., Lester M.T., Murray C., Phung M.M., Philip B.A., Tregidga E.L., Todd, J.H. (2002a) Effects of biotin-binding proteins on eight species of pasture invertebrates, N.Z. Plant Prot. 55, 411-415.
36. Malone L.A., Tregidga E.L., Todd J.H., Burgess E.P.J., Philip B.A., Markwick N.P., Poulton J., Christeller J.T., Lester M.T. Gatehouse H.S. (2002b) Effects of ingestion of a biotin-binding protein on adult and larval honey bees, Apidologie 33, 447-458.
37. Markwick N.P., Docherty L.C., Phung M.M., Lester M.T., Murray C., Yao J.-L., Mitra D.S., Cohen D., Beuning L.L., Kutty-Amma S., Christeller J.T. (2003) Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth and lightbrown apple moth, respectively. Transgenic Res. 12, 671-681
38. Murray C., Sutherland P.W., Phung M.M., Lester M.T., Marshall R.K., Christeller J.T. (2002) Expression of biotin-binding proteins, avidin and streptavidin, in plant tissues using plant vacuolar targeting sequences, Transgenic Res. 11, 199-214.
39. Naiem E.S., Hrassnigg N., Crailsheim K. (1999) Nurse bees support the physiological development of young bees (Apis mellifera L.), J. Comp. Physiol. B 169, 271-279.
40. Pham-Delègue M.H., Girard C., Le Métayer M., Picard-Nizou A.L., Hennequet C., Pons O., Jouanin L. (2000) Long-term effects of soybean protease inhibitors on digestive enzymes, survival and learning abilities of honeybees, Entomol. Exp. Appl. 95, 21-29.
41. Picard-Nizou A.L., Grison R., Olsen L., Pioche C., Arnold G., Pham-Delègue M.H. (1997) Impact on proteins used in plant genetic engineering toxicity and behavioral study in the honeybee, J. Econ. Entomol. 90, 1710-1716.
42. Sandoz G. (1996) Étude des effets d'inhibiteurs de protéases sur un insecte pollinisateur, l'abeille domestique Apis mellifera L., Institut National Agronomique Paris-Grignon, Diplôme d'Agronomie Approfondie thesis, 1996.
43. Schur A., Tornier I., Neumann C. (2000) Bt-Mais und non Bt-Mais: vergleichende Untersuchungen an Honigbienen (Tunnelzeltversuch), Apidologie 31, 616-617.
44. Simpson R.M., Burgess E.P.J., Markwick N.P. (1997) Bacillus thuringiensis d-endotoxin binding sites in two Lepidoptera. Wiseana spp. and Epiphyas postvittana, J. Invertebr. Pathol. 70. 136-42.
45. Sims S.R. (1995) Bacillus thuringiensis var. kurstaki (CryIA(c)) protein expressed in transgenic cotton: Effects on beneficial and other non-target insects. Southwest. Entomol. 20, 493-500.
46. Stanley-Horn D.E., Dively G.P., Hellmich R.L., Mattila H.R., Sears M.K., Rose R., Jesse L.C.H., Losey J.E., Obrycki J.J., Lewis L. (2001) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies, Proc. Natl. Acad. Sci. (USA) 98, 11931-11936.
47. Suzuki K. (1988) The development of hypopharyngeal glands in honey bee workers. Bull. Fac. Education. Chiba University 36, pp. 93-101.
48. Vaughan J.A., Wirtz R.A., do Rosario V.E., Azad A.F. (1990) Quantitation of antisporozoite immunoglobulins in the hemolymph of Anopheles stephensi after bloodfeeding, Am. J. Trop. Med. Hyg. 42, 10-16.