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Effects of tobacco genetically modified to express protease inhibitor bovine spleen trypsin inhibitor on non-target soil organisms

Published online by Cambridge University Press:  16 November 2007

Maureen O'Callaghan ,
Michael Brownbridge ,
Wendy B. Stilwell ,
Emily M. Gerard ,
Elisabeth P.J. Burgess ,
Emma I. Barraclough  and
John T. Christeller
Maureen O'Callaghan
Affiliation:
Biocontrol, Biosecurity and Bioprocessing Section, AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch, New Zealand
Michael Brownbridge
Affiliation:
Biocontrol, Biosecurity and Bioprocessing Section, AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch, New Zealand Previous address: University of Vermont, Entomology Research Lab, 661 Spear St, Burlington, VT 05405, USA
Wendy B. Stilwell
Affiliation:
Biocontrol, Biosecurity and Bioprocessing Section, AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch, New Zealand
Emily M. Gerard
Affiliation:
Biocontrol, Biosecurity and Bioprocessing Section, AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch, New Zealand
Elisabeth P.J. Burgess
Affiliation:
HortResearch, Private Bag 92 169, Auckland, New Zealand
Emma I. Barraclough
Affiliation:
HortResearch, Private Bag 92 169, Auckland, New Zealand
John T. Christeller
Affiliation:
HortResearch, Private Bag 11 030, Palmerston North, New Zealand

Abstract

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Effects of tobacco genetically modified to express the protease inhibitor bovine spleen trypsin inhibitor (BSTI) were examined in laboratory assays against three earthworm and one collembolan species. BSTI is a serine protease inhibitor that can bind to the digestive trypsins of insects feeding on modified plants, resulting in reduced growth and survival. Protease inhibitors are active against a broad range of insects, so may have a large impact on non-target organisms. Survival and fecundity of the collembolan Folsomia candida were unaffected by consumption of artificial diet containing BSTI-expressing tobacco leaf or powdered freeze-dried BSTI-expressing tobacco leaf that was added to soil. Similarly, mortality and growth of earthworms Aporrectodea caliginosa and Lumbricus rubellus did not differ significantly between soil augmented with BSTI-expressing tobacco leaves or unmodified control leaves. The redworm Eisenia fetida gained less weight when provided with BSTI-expressing leaves in one assay, but when the experiment was repeated, there was no significant difference between treatments. BSTI-expressing tobacco and unmodified control leaves decomposed at the same rate, indicating that the inhibitor had no effect on the overall function of the decomposer community of micro-flora and fauna in soil.

Keywords

environmental impactsearthwormsprotease inhibitorGM plantCollemboladecomposition
Type
Research Article
Information
Environmental Biosafety Research , Volume 6 , Issue 3 , July 2007 , pp. 183 - 195
Copyright
© ISBR, EDP Sciences, 2007

References

Ahl Goy P, Warren G, White J, Privalle L, Fearing P (1995) Interaction of an insect tolerant maize with organisms in the ecosystem. Proceedings of the Key Biosafety Aspects of Genetically Modified Organisms, Blackwell, Berlin, Berlin-Dahlem, pp 50–53 (cited in Ahmad et al. below)
Ahmad A, Wilde GE, Yan Zhu K (2006) Evaluation of effects of soil containing corn roots or biomass from transgenic corn expressing the coleopteran-specific Cry3Bb1 protein on earthworms. Environ. Entomol. 35: 976–985
Allsopp PG, Nutt KA, Geijskes RJ, Smith GR, Suasa AW (2000) Transgenic sugarcane with increased resistance to canegrubs. In Allsopp PG, ed, Sugarcane Pest Management in the New Millennium, 4th Sugarcane Entomology Workshop, International Society for Sugar Cane Technology, Khon Kaen, Thailand, pp 63–67
Ashouri A, Michaud D, Cloutier C (2001) Unexpected effects of different potato resistance factors to the Colorado potato beetle (Coleoptera: Chrysomelidae) on the potato aphid (Homoptera: Aphididae). Environ. Entomol. 30: 524–532
Berg MP, Stoffer M, van den Heuvel HH (2004) Feeding guilds in Collembola based on digestive enzymes. Pedobiologia 48: 589–601
Bewley GC, DeVillez EJ (1968) Isolation and characterization of the digestive proteinases in the earthworm Lumbricus terrestris Linneus. Comp. Biochem. Physiol. 25: 1061–1066
Bitzer RJ, Buckelew LD, Pedigo LP (2002) Effects of transgenic herbicide-resistant soybean varieties and systems on surface-active springtails (Entognatha: Collembola). Environ. Entomol. 31: 449–461
Burgess EPJ, Main CA, Stevens PS, Christeller JT, Gatehouse AMR, Laing WA (1994) Effects of protease inhibitor concentration and combinations on the survival, growth and gut enzyme activities of the black field cricket, Teleogryllus commodus. J. Insect Physiol. 40: 803–811 CrossRef
Burgess EPJ, Lövei GL, Malone LA, Nielsen IW, Gatehouse HS, Christeller JT (2002) Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis. J. Insect Physiol. 48: 1093–1101
Chari MS, Rao RSN, Prabhu SR (1992) Bio-efficacy of nicotine sulphate against pests of different crops. Tobacco Res. 18: 113–116
Christeller JT, Burgess EPJ, Mett V, Gatehouse HS, Markwick NP, Murray C, Malone LA, Wright MA, Philip BA, Watt D, Gatehouse LN, Lövei GL, Shannon AL, Phung MM, Watson LM, Laing WA (2002) The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor in tobacco and its effects on Helicoverpa armigera larvae. Transgenic Res. 11: 161–173
Christeller JT, Malone LM, Todd JH, Marshall RM, Burgess EPJ, Philip BA (2005) 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. J. Insect Physiol. 51: 1117–1126
Christeller JT, Markwick NP, Poulton J, O'Callaghan M (2006) Binding of an insecticidal transgene protein product to soil: Biological activity of soil-bound avidin and the effects of time and microbial activity. Soil Biol. Biochem. 38: 2043–2052
Clark BW, Coats JR (2006) Subacute effects of Cry 1Ab Bt corn litter on the earthworm Eisenia fetida and the springtail Folsomia candida. Environ. Entomol. 35: 1121–1129
Cowgill SE, Bardgett RD, Kiezebrink DT, Atkinson HJ (2002) The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere. J. Appl. Ecol. 39: 915–923
de Leo F, Bonade-Bottino M, Ceci LR, Gallerani RM, Jouanin L (2001) Effects of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests. Insect Biochem. Mol. Biol. 31: 593–602
Delledonne M, Allegro G, Belenghi B, Balestrazzi A, Picco F, Levine A, Zelasco S, Calligari P, Confalonieri M (2001) Transformation of white poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine proteinase inhibitor and analysis of insect pest resistance. Molec. Breed. 7: 35–42
Donegan K, Seidler R, Fieland V, Schaller D, Palm C, Ganio L, Cardwell D, Steinberger Y (1997) Decomposition of genetically engineered tobacco under field conditions: persistence of the proteinase inhibitor I product and effects on soil microbial respiration and protozoa, nematode and microarthropod populations. J. Appl. Ecol. 34: 767–777
El-Gayar F, El-Shazli A, Khafagy S, Watson W (1975) Studies on the alkaloidal contents of Nicotiana rustica var. brasilia, and its insecticidal activity against Culex pipiens L. (Dipt.: Culicidae) and Spodoptera littoralis Boisd. (Lep.: Noctuidae). Z. Angew. Entomol. 78: 49–55
Ferry, N, Edwards, MG, Gatehouse, JA, Gatehouse, AMR (2004) Plant-insect interactions: molecular approaches to insect resistance. Curr. Opin. Biotechnol. 15: 155–161 CrossRef
Fioretti, E, Iacopino, G, Angeletti, M, Barra, D, Bossa, F, Ascoli F (1985) Primary structure and antiproteolytic activity of a Kunitz-type inhibitor from bovine spleen. J. Biol. Chem. 260: 11451–11455
Flores S, Saxena D, Stotzky G (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biol. Biochem. 37: 1073–1082
Fountain MT, Hopkin SP (2005) Folsomia candida (Collembola): a `standard' soil arthropod. Annu. Rev. Entomol. 50: 201–222 CrossRef
Gatehouse JA, Gatehouse AMR, Brown DP (2000) Control of phytophagous insect pests using serine proteinase inhibitors. In Michaud D, ed, Recombinant Protease Inhibitors in Plants, Landes Bioscience, Eurekah.com, Texas, USA, pp 9–26
Hopkins DW, Gregorich EG (2003) Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize. Eur. J. Soil Sci. 54: 793–800
James C (2005) Global Status of Commercialized Transgenic Crops: 2005. The International Service for the Acquisition of Agri-biotech Applications (ISAAA), Ithaca, NY. http://www.isaaa.org/ kc/bin/briefs34/es/index.htm
Kula H, Larink O (1998) Tests on the earthworms Eisenia fetida and Aporrectodea caliginosa. In Lokke H, van Gestel CAM, eds, Handbook of Soil Invertebrate Toxicity Tests, John Wiley and Sons, Chichester, UK, pp 95–112
Laskowski MJ, Kato I (1980) Protein inhibitors of proteinases. Ann. Rev. Biochem. 49: 593–626
Malone LA, Todd JH, Burgess EPJ, Christeller JT (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor. Apidologie 35: 655–664
Markwick NP, Laing WA, Christeller JT, McHenry JZ, Newton MR (1998) Overproduction of digestive enzymes compensates for inhibitory effects of protease and a-amylase inhibitors fed to three species of leafrollers (Lepidoptera: Tortricidae). J. Econ. Entomol. 91: 1265–1276
Rebek EJ, Hogg DB, Young DK (2002) Effect of four cropping systems on the abundance and diversity of epedaphic springtails (Hexapoda: Parainsecta: Collembola) in southern Wisconsin. Environ. Entomol. 31: 37–46
Romeis J, Battini M, Bigler F (2003) Transgenic wheat with enhanced fungal resistance causes no effects on Folsomia candida (Collembola: Isotomidae). Pedobiologia 47: 141–147
Saxena D, Stotzky G (2001a) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria and fungi in soil. Soil Biol. Biochem. 33: 1225–1230
Saxena D, Stotzky G (2001b) Bt corn has a higher lignin content than non-Bt corn. Am. J. Bot. 88: 1704–1706
Snider R (1973) Laboratory observations on the biology of Folsomia candida (Willem) (Collembola: Isotomidae). Rev. Ecol. Biol. Sol 10: 103–124
Stam EM, van de Leemkule MA, Ernsting G (1996) Trade-offs in the life history and energy budget of the parthenogenetic collembolan Folsomia candida (Willem). Oecologia 107: 283–292
Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. 109B: 1–62
van Amelsvoort PAM, Usher MB (1989) Egg production related to food quality in Folsomia candida (Collembola: Isotomidae): effects on life history strategies. Pedobiologia 33: 61–66
Vercesi ML, Krogh PH, Holmstrup M (2006) Can Bacillus thuringiensis (Bt) corn residues and Bt-corn plants affect life-history traits in the earthworm Aporrectodea caliginosa? Appl. Soil Ecol. 32: 180–187
Vincent JP, Lazdunski M (1972) Trypsin-pancreatic trypsin inhibitor association. Dynamics of the interaction and role of disulfide bridges. Biochem. 11: 2967–2977
Voisey CR, Dudas B, Biggs R, Burgess EPJ, Wigley PJ, McGregor PG, Lough TJ, Beck DL, Forster RLS, White DWR, Spangenberg G (2001) Transgenic pest and disease resistant white clover plants. In Spangenberg G, ed, Molecular Breeding of Forage Crops. Developments in Plant Breeding, Kluwer Academic Publishers, London, UK, pp 239–250
Yu L, Berry RE, Croft BA (1997) Effects of Bacillus thuringienesis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Orbatidae). J. Econ. Entomol. 90: 113–118
Zwahlen C, Hilbeck A, Howald R, Nentwig W (2003) Effects of transgenic Bt corn litter on the earthworm Lumbricus terrestris. Molec. Ecol. 12: 1077–1086