Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-11T04:38:20.988Z Has data issue: false hasContentIssue false

Tiered tests to assess the environmental risk of fitness changes in hybrids between transgenic crops and wild relatives: the example of virus resistant Brassica napus

Published online by Cambridge University Press:  16 March 2006

Alan Raybould
Affiliation:
Syngenta, Jealott’s Hill International Research Centre, Bracknell, Berkshire RG42 6EY, UK
Ian Cooper
Affiliation:
Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR, UK

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Over the last 20 years, there has been much research aimed at improving environmental risk assessment of transgenic crops. Despite large amounts of data, decisions to allow or prohibit the release of transgenic crops remain confused and controversial. We argue that part of the reason for confusion is the lack of clear definitions of components of the environment that should be protected, and, as a consequence, there is no way to judge the relevance of data collected under the auspices of ‘environmental risk assessment’. Although this criticism applies to most aspects of environmental risk assessment of transgenic crops, it is most pertinent to effects that might result from an increase in plant fitness, often referred to as increased weediness. Environmental risk assessment of weediness is regarded as complicated: an increase in the fitness of a transgenic plant compared with non-transgenic counterparts will be the result of an interaction between the altered plant phenotype and an enormous number of environmental variables. This has led to the idea that risk assessment of weediness needs to “understand” these interactions, with the implication that exhaustive data are required. Here we argue that environmental risk assessment of the weediness of transgenic plants need not be complicated. Analysis of the conditions that must be met for increased weediness to occur suggests a series of studies that starts with simple tests in the laboratory under “worst case” assumptions, and becomes increasingly complex and realistic should the simpler studies not indicate negligible risk with sufficient certainty. We illustrate how the approach might work for assessing the risks of increased weediness using the example of possible introgression of a gene for Turnip mosaic virus (TuMV) resistance from oilseed rape to certain wild Brassica species.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2006

References

APHIS (Animal and Plant Health Inspection Service) (1987) 7 CFR Parts 330 and 340, Plant pests; introduction of genetically engineered organisms or products; final rule. Fed. Register 52: 22892–22915
Barrett KL, Grandy N, Harrison EG, Hassan S, Oomen P (1994) Guidance Document on Regulatory Testing Procedures for Pesticides with Non-Target Arthropods. Society for Environmental Toxicology and Chemistry, Brussels
Bedford ID, Briddon RW, Brown JK, Rosell RC, Markham PG (1994) Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Ann. Appl. Biol. 125: 311–325 CrossRef
Bergelson, J (1994) Changes in fecundity do not predict invasiveness – a model study of transgenic plants. Ecology 75: 249252 CrossRef
Bergelson, J, Purrington, CB, Wichmann, G (1998) Promiscuity in transgenic plants. Nature 395: 25 CrossRef
Bing, DJ, Downey, RK, Rakow, G (1996) Hybridizations among Brassica napus, B.rapa, and B. juncea and their weedy relatives B. nigra and Sinapis arvensis under open pollination conditions in the field. Plant Breed. 115: 470473 CrossRef
Burban, C, Fishpool, LDC, Fauquet, C, Fargette, D, Thouvenel, J-C (1992) Host associated biotypes within West African populations of the whitefly Bemisia tabaci (Genn.) (Hom., Aleyrodidae). J. Appl. Ent. 113: 416423 CrossRef
Butler, D, Reichhardt, A (1999) Long-term effect of GM crops serves up food for thought. Nature 398: 654656
Candolfi MP, Barrett KL, Campbell PJ, Forster R, Grandy N, Huet M-C, Lewis G, Oomen PA, Schmuck R, Vogt H (2000) Guidance Document on Regulatory Testing and Risk Assessment Procedures for Plant Protection products with Non-Target Arthropods. Society for Environmental Toxicology and Chemistry, Pensacola, FL
Chèvre, AM, Eber, F, Baranger, A, Boucherie, A, Broucqsault, LM, Bouchet, Y, Renard, M (1998) Risk assessment on crucifer species. Acta Hort. 459: 219224 CrossRef
Chèvre AM, Ammitzboll H, Breckling B, Dietz-Pfeilstetter A, Eber F, Fargue A, Gomez-Campo C, Jenczewski E, Jørgensen R, Lavigne C, Meier MS, den Nijs HCM, Pascher K, Séguin-Swartz G, Sweet J, Stewart Jr CN, Warwick S (2004) A review on interspecific gene flow from oilseed rape to wild relatives. In den Nijs HCM, Bartsch D, Sweet J, eds, Introgression from Genetically Modified plants into Wild Relatives. CAB International, Wallingford, UK, pp 235–251
Cooper, JI, Jones, AT (1983) Responses of plants to viruses: proposals for the use of terms. Phytopathology 73: 127128 CrossRef
Cooper JI, Raybould AF (1997) Transgenes for stress tolerance: consequences for weed evolution. Proceedings of the Brighton Crop Protection ConferenceWeeds, pp 265–272
Cooper JI, Walsh JA (2003) Genetic modification of disease resistance, viral pathogens. In Thomas B, Murphy D, Murray B, eds, Encyclopedia of Applied Plant Sciences. Academic Press, London, UK, pp 257–262
Cross, FB (1996) Paradoxical perils of the precautionary principle. Wash. & L. Law Rev. 53: 851925
Dinant, S, Blaise, F, Kusiak, C, Astier-Manifacier, S, Albouy, J (1993) Heterologous resistance to potato virus Y in transgenic tobacco plants expressing the coat protein of lettuce mosaic potyvirus. Phytopathology 83: 818824 CrossRef
Dinant, S, Maisonneuve, B, Albouy, J, Chupeau, Y, Chupeau, M-C, Bellec, Y, Gaudefroy, F, Kusiak, C, Souche, S, Robaglia, C, Lot, H (1997) Coat protein gene-mediated protection in Lactuca sativa against lettuce mosaic potyvirus strains. Mol. Breeding 3: 7586 CrossRef
Dutton, A, Romeis, J, Bigler, F (2003) Assessing the risks of insect resistant plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. BioControl 48: 611– 636 CrossRef
Ellstrand, NC (2001) When transgenes wander, should we worry? Plant Physiol. 125: 15431545 CrossRef
Ellstrand, NC, Prentice, HC, Hancock, JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30: 539563 CrossRef
Elvin, DE, Welsh, R, Batie, SS, Capentier, CL (2003) Towards an ecological systems approach in public research for environmental regulation of transgenic crops. Agric. Ecosyst. Environ. 99: 114
EPPO (2003) Environmental risk assessment scheme for plant protection products. EPPO Bull. 33: 103111 CrossRef
Gray, AJ (2004) Ecology and government policies: the GM crop debate. J. Appl. Ecol. 41: 110 CrossRef
Hails, RS, Morley, K (2005) Genes invading new populations: a risk assessment perspective. Trends Ecol. Evol. 20: 245252 CrossRef
Hansen, LB, Siegismund, HR, Jørgensen, RB (2001) Introgression between oilseed rape Brassica napus L. and its weedy relative B. rapa in a natural population. Genet. Resour. Crop Evol. 48: 621627 CrossRef
Heritage, J (2003) Will GM rapeseed cut the mustard? Science 302: 401403 CrossRef
Hill, RA, Sendashonga, C (2003) General principles for risk assessment of living modified organisms: lessons from chemical assessment. Environ. Biosafety Res. 2: 8188 CrossRef
Jan, FJ, Fagoaga, C, Pang, SZ, Gonsalves, D (2000) A single transgene derived from two distinct viruses confers multi-virus resistance in transgenic plants through homology-dependent gene silencing. J. Gen. Virol. 81: 21032109 CrossRef
Lehmann, P, Walsh, JA, Jenner, CE, Kozubek, E, Greenland, A (1996) Genetically engineered protection against turnip mosaic virus infection in transgenic oilseed rape (Brassica napus var. oleifera). J. Appl. Gen. 37A: 118121
Maskell, LC, Raybould, AF, Cooper, JI, Edwards, M-L, Gray, AJ (1999) Effects of turnip mosaic virus and turnip yellow mosaic virus on the survival, growth and reproduction of wild cabbage (Brassica oleracea). Ann. Appl. Biol. 135: 401407 CrossRef
Miller, HI, Conko, G (2005) NGO war on biotechnology. J. Commer. Biotech. 11: 209222 CrossRef
Mitchell, CE, Power, AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421: 625627 CrossRef
Mitchell ND, Richards AJ (1979) Biological Flora of the British Isles No 145, Brassica oleracea ssp. oleracea. J. Ecol. 67: 1087–1096
Naranjo, SE, Head, G, Dively, GP (2005) Field studies assessing arthropod nontarget effects in Bt transgenic crops: introduction. Environ. Ent. 34: 11781180 CrossRef
Newman NC (1998) Fundamentals of Ecotoxicology. Ann Arbor Press, Chelsea, MI
Pallett, DW, Thurston, MI, Cortina-Borja, M, Edwards, M-L, Alexander, M, Mitchell, E, Raybould, AF, Cooper, JI (2002) The incidence of viruses in wild Brassica rapa ssp. sylvestris in Southern England. Ann. Appl. Biol. 141: 163170 CrossRef
Peters RH (1991) A Critique for Ecology. Cambridge University Press
Pimentel, D, McNair, S, Janecka, J, Wightman, J, Simmonds, C, O’Connell, C, Wong, E, Russel, L, Zern, J, Aquino, T, Tsomondo, T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric. Ecosyst. Environ. 84: 120 CrossRef
Poppy, G (2000) GM crops: environmental risks and non-target effects. Trends Plant Sci. 5: 46 CrossRef
Preston CD, Pearman DA, Dines TD (2002) New Atlas of the British & Irish Flora. Oxford University Press
Raybould, AF (2004) A decade of gene flow research: improved risk assessments or missed opportunities? Aspects Appl. Biol. 74: 2733
Raybould AF (2005) Assessing the environmental risks of transgenic volunteer weeds. In Gressel J, ed., Crop Ferality and Volunteerism. CRC Press, Boca Raton, FL, pp 389– 401
Raybould, AF, Gray, AJ (1993) Genetically modified crops and hybridization with wild relatives: a UK perspective. J. Appl. Ecol. 30: 199219 CrossRef
Raybould, AF, Gray, AJ (1994) Will hybrids of genetically modified crops invade natural communities? Trends Ecol. Evol. 9: 8589 CrossRef
Raybould AF, Wilkinson MJ (2005) Assessing the environmental risks of gene flow from genetically modified crops to wild relatives. In Poppy GM, Wilkinson MJ, eds, Gene Flow from GM Plants. Oxford: Blackwell Publishing, pp 169–185
Raybould AF, Maskell LC, Edwards M-L, Cooper JI, Gray AJ (1999a) The prevalence and spatial distribution of viruses in natural populations of Brassica oleracea. New Phytol. 141: 265–275
Raybould AF, Moyes CL, Maskell LC, Mogg RJ, Warman EA, Wardlaw JC, Elmes GW, Edwards M-L, Cooper JI, Clarke RT, Gray AJ (1999b) Predicting the ecological impacts of transgenes for insect and virus resistance in natural and feral populations of Brassica species. In Ammann K, Jacot Y, Simonsen V, Kjellsson G, eds, Methods of Risk Assessment of Transgenic Plants III. Ecological risks and prospects of transgenic plants. Bïrkhäuser Verlag, Basel, pp 3–15
Raybould AF, Edwards M-L, Clarke RT, Pallett D, Cooper JI (2000) Heritable variation for the control of turnip mosaic virus and cauliflower mosaic virus replication in wild cabbage. Beiträge zur Züchtungsforschung – Bundesanstalt für Züchtungsforschung an Kulturpflanzen. Proceedings of the 7th Aschersleben Symposium – New Aspects of Resistance Research on Cultivated Plants, pp 4–8
Raybould AF, Alexander MJ, Mitchell E, Thurston MI, Pallett DW, Hunter P, Walsh JA, Edwards M-L, Jones AME, Moyes CL, Gray AJ, Cooper JI (2003) The ecology of turnip mosaic virus in populations of wild Brassica species. In Beringer J, Godfray CHJ, Hails RA, eds, Ecological Dynamics & Genes, final symposium volume. Blackwell Scientific Press, Oxford, UK, pp 226–244
Rich TCG (1991) Crucifers of Great Britain and Ireland. London: Botanical Society of the British Isles
Scheffler, JA, Dale, PJ (1994) Opportunities for gene transfer from transgenic oilseed rape (Brassica napus) to related species. Transgenic Res. 3: 263278 CrossRef
Shattuck, VI (1992) The biology, epidemiology and control of turnip mosaic virus. Offprints from Plant Breeding Reviews 14: 199238
Thurston, MI, Pallett, DW, Cortina-Borja, M, Edwards, M-L, Raybould, AF, Cooper, JI (2001) The incidence of viruses in wild Brassica nigra in Dorset (UK). Ann. Appl. Biol. 139: 277284 CrossRef
U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and the peculiar mode of fertilization. Shokub utsu Kekyu Zasshi. 7: 389452
US EPA (2001) Biopesticides Registration Action Document – Bacillus thuringiensis Plant Incorporated Protectants. http://www.epa.gov/oppbppd1/biopesticides/pips/bt_brald.htm
Wilkinson, MJ, Davenport, IJ, Charters, YM, Jones, AE, Allainguillaume, J, Butler, HT, Mason, DC, Raybould, AF (2000) A direct regional scale estimate of transgene movement from GM oilseed rape to its wild progenitors. Mol. Ecol. 9: 983991 CrossRef
Wilkinson, MJ, Elliot, LJ, Allainguillaume, J, Shaw, MW, Norris, C, Welters, R, Alexander, M, Sweet, J, Mason, DC (2003a) Hybridization between Brassica napus and B. rapa on a national scale in the United Kingdom. Science 302: 457459 CrossRef
Wilkinson, MJ, Sweet, J, Poppy, G (2003b) Risk assessment of GM plants: avoiding gridlock? Trends Plant Sci. 8: 208212 CrossRef