Tri-trophic effects of transgenic insect-resistant tobacco expressing a protease inhibitor or a biotin-binding protein on adults of the predatory carabid beetle Ctenognathus novaezelandiae

Journal of Insect Physiology

Volumn 54, Issue 2, 2008, Pages 518-528

  Burgess, E P J ^a   Philip, B A ^a   Christeller, J T ^a   Page, N E M ^a   Marshall, R K ^a   Wohlers, M W ^a  

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

Author keywords

Aprotinin (BPTI); Avidin; Bovine spleen trypsin inhibitor (BSTI); Carabid beetle; Transgenic plant; Tri trophic non target impacts

Indexed keywords

AVIDIN; BIOTIN BINDING PROTEINS; BIOTIN-BINDING PROTEINS; CARRIER PROTEIN; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG;

ADULT; BEETLE; CATERPILLAR; ENZYME ACTIVITY; GENE EXPRESSION; INHIBITOR; MOTH; PEST CONTROL; PROTEIN; SEX-RELATED DIFFERENCE; TOBACCO; TRANSGENIC PLANT; TRITROPHIC INTERACTION;

ANIMAL; ARTICLE; BEETLE; BIOLOGICAL PEST CONTROL; DRUG EFFECT; FEMALE; GENETICS; LARVA; MALE; METABOLISM; MOTH; PARASITOLOGY; PREDATION; REPRODUCTION; TIME; TOBACCO; TRANSGENIC PLANT;

ANIMALS; AVIDIN; BEETLES; CARRIER PROTEINS; FEMALE; LARVA; MALE; MOTHS; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; PREDATORY BEHAVIOR; REPRODUCTION; TIME FACTORS; TOBACCO; TRYPSIN INHIBITORS;

BOVINAE; CARABIDAE; COLEOPTERA; HEXAPODA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; SPODOPTERA LITURA;

EID: 38749145887     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2007.12.002     Document Type: Article

References (81)

1. Ahmad A., Wilde G.E., and Zhu K.Y. Delectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environmental Entomology 34 (2005) 385-394
2. Ahmad A., Wilde G.E., Whitworth R.J., and Zolnerowich G. Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. Journal of Economic Entomology 99 (2006) 1085-1095
3. Allegro G., and Sciaky R. Assessing the potential role of ground beetles (Coleoptera: Carabidae) as bioindicators in poplar stands, with a newly proposed ecological index (FAI). Forest Ecology and Management 175 (2003) 275-284
4. Anon. Hazardous Substances and New Organisms Act 1996 (1996), New Zealand Government, Wellington
5. Barra D., Simmaco M., Bossa F., Fioretti E., Angeletti M., and Ascoli F. Primary structure of a protease inhibitor from bovine spleen. Journal of Biological Chemistry 262 (1987) 13916-13919
6. Bishop-Hurley S.L., Zabkiewicz R.J., Grace L., Gardner R.C., Wagner A., and Walter C. Conifer genetic engineering: transgenic Pinus radiata (D. Don) and Picea abies (Karst) plants are resistant to the herbicide Buster. Plant Cell Reports 20 (2001) 235-243
7. Boscaini A., Franceschini A., and Maiolini B. River ecotones: carabid beetles as a tool for quality assessment. Hydrobiologia 422 (2000) 173-181
8. Bown D.P., Wilkinson H.S., and Gatehouse J.A. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochemistry and Molecular Biology 27 (1997) 625-638
9. Burgess E.P.J., Malone L.A., Christeller J.T., Lester M.T., Murray C., Philip B.A., Phung M.M., and Tregidga E.L. Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, Helicoverpa armigera and Spodoptera litura. Transgenic Research 11 (2002) 185-198
10. Burgess E.P.J., Lovei G.L., Malone L.A., Nielsen I.W., Gatehouse H.S., and Christeller J.T. Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis. Journal of Insect Physiology 48 (2002) 1093-1101
11. Burgio G., Ramilli F., Fiore M.C., and Cellini F. Impact of transgenic oilseed rape on soil arthropod assemblages. Bulletin OILB/SROP 27 (2004) 31-35
12. Castro M.J.M., and Anderson S. Alanine point-mutations in the reactive region of bovine pancreatic trypsin inhibitor: effects on the kinetics and thermodynamics of binding to beta-trypsin and alpha-chymotrypsin. Biochemistry 35 (1996) 11435-11446
13. Cheung A.C., and Gooding R.H. A study of trypsin in Calosoma calidum (FAB.) and Carabus taedatus FAB. Comparative Biochemistry and Physiology B-Biochemistry and Molecular Biology 37 (1970) 331-338
14. Christeller J.T. Evolutionary mechanisms acting on proteinase inhibitor variability. FEBS Journal 272 (2005) 5710-5722
15. Christeller J.T., and Shaw B.D. The interactions of a range of serine proteinase inhibitors with bovine trypsin and Costelytra zealandica trypsin. Insect Biochemistry 19 (1989) 233-241
16. Christeller J.T., Laing W.A., Markwick N.P., and Burgess E.P.J. Midgut protease activities in 12 phytophagous lepidopteran larvae: dietary and protease inhibitor interactions. Insect Biochemistry and Molecular Biology 22 (1992) 735-746
17. Christeller J.T., Burgess E.P.J., Mett V., Gatehouse H.S., Markwick N.P., Murray C., Malone L.A., Wright M.A., Philip B.A., Watt D., Gatehouse L.N., Lovei G.L., Shannon A.L., Phung M.M., Watson L.M., and Laing W.A. The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor in tobacco and its effects on Helicoverpa armigera larvae. Transgenic Research 11 (2002) 161-173
18. Christeller J.T., Malone L.A., Todd J.H., Marshall R.M., Burgess E.P.J., and Philip B.A. Distribution and residual activity of two insecticidal proteins, avidin and aprotinin, expressed in transgenic tobacco plants, in the bodies and frass of Spodoptera litura larvae following feeding. Journal of Insect Physiology 51 (2005) 1117-1126
19. Cooper S.G., Douches D.S., and Grafius E.J. Insecticidal activity of avidin combined with genetically engineered and traditional host plant resistance against Colorado potato beetle (Coleoptera: Chrysomelidae) larvae. Journal of Economic Entomology 99 (2006) 527-536
20. Cui J., and Xia J. Effects of transgenic Bt cotton R93-6 on the insect community. Acta Entomologica Sinica 43 (2000) 43-51
21. de la Poza M., Pons X., Farinos G.P., Lopez C., Ortego F., Eizaguirre M., Castanera P., and Albajes R. Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Protection 24 (2005) 677-684
22. Ditta G., Stanfield S., Corbin D., and Helsinki D.R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proceedings of the National Academy of Sciences of the United States of America 77 (1980) 7347-7351
23. Duan J.J., Head G., Jensen A., and Reed G. Effects of transgenic Bacillus thuringiensis potato and conventional insecticides for Colorado potato beetle (Coleoptera: Chrysomelidae) management on the abundance of ground-dwelling arthropods in Oregon potato ecosystems. Environmental Entomology 33 (2004) 275-281
24. Dymock J.J., Laing W.A., Shaw B.D., Gatehouse A.M.R., and Christeller J.T. Behavioral and physiological responses of grass grub larvae (Costelytra zealandica) feeding on protease inhibitors. New Zealand Journal of Zoology 19 (1992) 123-131
25. Edwards, C.A., Subler, S., Chen, S.K., Bogomolov, D.M., 1996. Essential criteria for selecting bioindicator species, processes, or systems to assess the environmental impact of chemicals on soil ecosystems. Bioindicator systems for soil pollution. In: Proceedings of the NATO Advanced Research Workshop on New Approaches to the Development of Bioindicator Systems for Soil Pollution, Moscow, Russia, 24-28 April 1995. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 67-84.
26. Ferris R., and Humphrey J.W. A review of potential biodiversity indicators for application in British forests. Forestry 72 (1999) 313-328
27. Ferry N., Jouanin L., Ceci L.R., Mulligan A., Emami K., Gatehouse J.A., and Gatehouse A.M.R. Impact of oilseed rape expressing the insecticidal serine protease inhibitor, mustard trypsin inhibitor-2 on the beneficial predator Pterostichus madidus. Molecular Ecology 14 (2005) 337-349
28. Fioretti E., Binotti I., Barra D., Citro G., Ascoli F., and Antonini E. Heterogeneity of the basic pancreatic inhibitor (Kunitz) in various bovine organs. European Journal of Biochemistry 130 (1983) 13-18
29. Fioretti E., Iacopino G., Angeletti M., Barra D., Bossa F., and Ascoli F. Primary structure and antiproteolytic activity of a kunitz-type inhibitor from bovine spleen. Journal of Biological Chemistry 260 (1985) 11451-11455
30. Flinn P.W., Kramer K.J., Throne J.E., and Morgan T.D. Protection of stored maize from insect pests using a two-component biological control method consisting of a hymenopteran parasitoid, Theocolax elegans, and transgenic avidin maize powder. Journal of Stored Products Research 42 (2006) 218-225
31. Freier B., Schorling M., Traugott M., Juen A., and Volkmar C. Results of a 4-year plant survey and pitfall trapping in Bt maize and conventional maize fields regarding the occurrence of selected arthropod taxa. Bulletin OILB/SROP 27 (2004) 79-84
32. Gatehouse L.N., Shannon A.L., Burgess E.P.J., and Christeller J.T. Characterization of major midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochemistry and Molecular Biology 27 (1997) 929-944
33. Gooding R.H., and Huang C.T. Trypsin and chymotrypsin from the beetle Pterostichus melanarius. Journal of Insect Physiology 15 (1969) 325-339
34. Grace L.J., Charity J.A., Gresham B., Kay N., and Walter C. Insect-resistant transgenic Pinus radiata. Plant Cell Reports 24 (2005) 103-111
35. Graham J., Gordon S.C., Smith K., McNicol R.J., and McNicol J.W. The effect of the Cowpea trypsin inhibitor in strawberry on damage by vine weevil under field conditions. Journal of Horticultural Science & Biotechnology 77 (2002) 33-40
36. Guido M. Monitoring in forest environments: the use of arthropods. Dendronatura 21 (2000) 38-49
37. Hofig K.P., Moller R., Donaldson L., Putterill J., and Walter C. Towards male sterility in Pinus radiata-a stilbene synthase approach to genetically engineer nuclear male sterility. Plant Biotechnology Journal 4 (2006) 333-343
38. Horsch R.B., Fry J.E., Hoffmann N.L., Wallroth M., Eichholtz D., Rogers S.G., and Fraley R.T. A simple and general method for transferring genes into plants. Science 227 (1985) 1229-1231
39. Ito K., Furukawa K., and Okubo T. Conservation biological control of aphids in potato fields with reduced use of insecticides in Hokkaido, Japan. Japanese Journal of Applied Entomology and Zoology 49 (2005) 11-22
40. James, C., 2006. Global status of commercialized biotech/GM crops: 2006. The international service for the acquisition of agri-biotech applications. ISAAA Brief No. 35. ISAAA, Ithaca, NY.
41. Jongsma M.A., Bakker P.L., Peters J., Bosch D., and Stiekema W.J. Adaptation of Spodoptera exigua larvae to plant proteinase-inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of the National Academy of Sciences of the United States of America 92 (1995) 8041-8045
42. Jorgensen H.B., and Lovei G.L. Tri-trophic effect on predator feeding: consumption by the carabid Harpalus affinis of Heliothis armigera caterpillars fed on proteinase inhibitor-containing diet. Entomologia Experimentalis et Applicata 93 (1999) 113-116
43. Kalbfleisch J.D., and Prentice R.L. Statistical Analysis of Failure Time Data (1980), Wiley, New York
44. Kramer K.J., Morgan T.D., Throne J.E., Dowell F.E., Bailey M., and Howard J.A. Transgenic avidin maize is resistant to storage insect pests. Nature Biotechnology 18 (2000) 670-674
45. Laskowski M.J., and Kato I. Protein inhibitors of proteinases. Annual Review of Biochemistry 49 (1980) 593-626
46. Lawes Agricultural Trust. Genstat release 8.1 (PC/Windows XP) (2003), Rothamsted Experimental Station
47. Lopez M.D., Prasifka J.R., Bruck D.J., and Lewis L.C. Utility of ground beetle species in field tests of potential nontarget effects of Bt crops. Environmental Entomology 34 (2005) 1317-1324
48. Lovei G.L., and Sunderland K.D. Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41 (1996) 231-256
49. Lozzia G.C. Biodiversity and structure of ground beetle assemblages (Coleoptera: Carabidae) in Bt corn and its effects on non-target insects. Bollettino di Zoologia Agraria e di Bachicoltura 31 (1999) 37-50
50. Luff M.L. Biology of polyphagous ground beetles in agriculture. Agricultural Zoology Reviews 2 (1987) 237-278
51. 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., and Todd J.H. Effects of biotin-binding proteins on eight species of pasture invertebrates. New Zealand Plant Protection 55 (2002) 411-415
52. 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., and Gatehouse H. Effects of ingestion of a biotin-binding protein on adult and larval honey bees. Apidologie 33 (2002) 447-458
53. Manachini B. Ground beetle assemblages (Coleoptera: Carabidae) and plant dwelling non-target arthropods in isogenic and transgenic corn crops. Bollettino di Zoologia Agraria e di Bachicoltura 32 (2000) 261-267
54. Manachini, B., Agosti, M., Rigamonti, I., 1999. Environmental impact of Bt-corn on non target entomofauna: synthesis of field and laboratory studies. Human and environmental exposure to xenobiotics. Proceedings of the XIth Symposium on Pesticide Chemistry. Cremona, Italy. La Goliardica Pavese, 27100 Pavia, pp. 873-882.
55. Markwick N.P., Laing W.A., Christeller J.T., McHenry J.Z., and Newton M.R. Overproduction of digestive enzymes compensates for inhibitory effects of protease and alpha-amylase inhibitors fed to three species of leafrollers (Lepidoptera: Tortricidae). Journal of Economic Entomology 91 (1998) 1265-1276
56. Markwick N.P., Christeller J.T., Dochterty L.C., and Lilley C.M. Insecticidal activity of avidin and streptavidin against four species of pest Lepidoptera. Entomologia Experimentalis et Applicata 98 (2001) 59-66
57. Markwick N.P., Docherty L.C., Phung M.M., Lester M., Murray C.M., Yao J.-L., Mitra D., Cohen D., Beuning L.L., and Christeller J.T. Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth and light brown apple moth, respectively. Transgenic Research 12 (2003) 671-681
58. Mazumdar-Leighton S., Babu C.R., and Bennett J. Identification of novel serine proteinase gene transcripts in the midguts of two tropical insect pests, Scirpophaga incertulas (Wk.) and Helicoverpa armigera (Hb.). Insect Biochemistry and Molecular Biology 30 (2000) 57-68
59. Meissle M., Vojtech E., and Poppy G.M. Effects of Bt maize-fed prey on the generalist predator Poecilus cupretis L. (Coleoptera: Carabidae). Transgenic Research 14 (2005) 123-132
60. Moller R., Steward D., Phillips L., Flint H., and Wagner A. Gene silencing of cinnamyl alcohol dehydrogenase in Pinus radiata callus cultures. Plant Physiology and Biochemistry 43 (2005) 1061-1066
61. Mulligan E.A., Ferry N., Jouanin L., Walters K.F.A., Port G.R., and Gatehouse A.M.R. Comparing the impact of conventional pesticide and use of a transgenic pest-resistant crop on the beneficial carabid beetle Pterostichus melanarius. Pest Management Science 62 (2006) 999-1012
62. Murray C., Sutherland P.W., Phung M.M., Lester M.T., Marshall R.K., and Christeller J.T. Expression of biotin-binding proteins, avidin and streptavidin, in plant tissues using plant vacuolar targeting sequences. Transgenic Research 11 (2002) 199-214
63. O'Neal M.E., Zontek E.L., Szendrei Z., Landis D.A., and Isaacs R. Ground predator abundance affects prey removal in highbush blueberry (Vaccinium corymbosum) fields and can be altered by aisle ground covers. Biocontrol 50 (2005) 205-222
64. Ostman O., Ekbom B., and Bengtsson J. Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecological Economics 45 (2003) 149-158
65. Philip B.A., and Burgess E.P.J. Observations on the ecology and behaviour of Ctenognathus novaezelandiae (Fairmaire) (Coleoptera: Carabidae). New Zealand Journal of Entomology 31 (2008) 37-41
66. Raybould A., Stacey D., Vlachos D., Graser G., Li X., and Joseph R. Non-target organism risk assessment of MIR604 maize expressing mCry3A for control of corn rootworm. Journal of Applied Entomology 131 (2007) 391-399
67. Riddick E.W., Dively G., and Barbosa P. Effect of a seed-mix deployment of Cry3A-transgenic and nontransgenic potato on the abundance of Lebia grandis (Coleoptera: Carabidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Annals of the Entomological Society of America 91 (1998) 647-653
68. Sehnal F., Habustova O., Spitzer L., Hussein H.M., and Ruzicka V. A biannual study on the environmental impact of Bt maize. Bulletin OILB/SROP 27 (2004) 147-160
69. Stark J.D., Banks J.E., and Vargas R. How risky is risk assessment: the role that life history strategies play in susceptibility of species to stress. Proceedings of the National Academy of Sciences of the United States of America 101 (2004) 732-736
70. Sun J., and Zhang Y. Effects of insecticide application on Oracella acuta (Lobdell) (Homoptera: Pseudococcidae) population and its two dominant parasitoids. Acta Entomologica Sinica 46 (2003) 466-472
71. Symondson W.O.C., Sunderland K.D., and Greenstone M.H. Can generalist predators be effective biocontrol agents?. Annual Review of Entomology 47 (2002) 561-594
72. Szyszko J. Carabids as Efficient Indicators of the Quality and Functioning of Forest Ecosystems Useful in Forestry Management. How to Protect or What we Know about Carabid Beetles: from Knowledge to Application, from Wijster (1969) to Tuczno (2001) (2002), Warsaw Agricultural University Press, Warsaw, Poland pp. 301-318
73. Tarver M.R., Shade R.E., Shukle R.H., Moar W.J., Muir W.M., Murdock L.M., and Pittendrigh B.R. Pyramiding of insecticidal compounds for control of the cowpea bruchid (Callosobruchus maculatus F.). Pest Management Science 63 (2007) 440-446
74. Terra W.R., and Cristofoletti P.T. Midgut proteinases in three divergent species of Coleoptera. Comparative Biochemistry and Physiology B-Biochemistry and Molecular Biology 113 (1996) 725-730
75. Thiele H.U. Carabid Beetles in their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behaviour vol. 10 (1977), Springer, Berlin, New York
76. Thomas L. Retrospective power analysis. Conservation Biology 11 (1997) 276-280
77. Vaje S., Mossakowski D., and Gabel D. Temporal, intra- and inter-specific variation of proteolytic enzymes in carabid beetles. Insect Biochemistry 14 (1984) 313-320
78. Walter C., Grace L.J., Wagner A., White D.W.R., Walden A.R., Donaldson S.S., Hinton H., Gardner R.C., and Smith D.R. Stable transformation and regeneration of transgenic plants of Pinus radiata D. Don. Plant Cell Reports 17 (1998) 460-468
79. Wu Z., Chen P., Yang Y., Xu Y., and Xie H. Evaluation of the resistance of different insect-resistant cotton cultivars to the pink bollworm. Acta Agronomica Sinica 31 (2005) 53-57
80. Yoza K., Imamura T., Kramer K.J., Morgan T.D., Nakamura S., Akiyama K., Kawasaki S., Takaiwa F., and Ohtsubo K. Avidin expressed in transgenic rice confers resistance to the stored-product insect pests Tribolium confusum and Sitotroga cerealella. Bioscience Biotechnology and Biochemistry 69 (2005) 966-971
81. Zwahlen C., and Andow D.A. Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environmental Biosafety Research 4 (2005) 113-117