Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T00:54:13.473Z Has data issue: false hasContentIssue false

The responses of crop – wild Brassica hybrids to simulated herbivory and interspecific competition: Implicationsfor transgene introgression

Published online by Cambridge University Press:  19 September 2006

Jamie P. Sutherland
Affiliation:
Ecology and Evolutionary Biology, School of Biological Sciences, Bassett Crescent East, University of Southampton, Southampton, SO16 7PX, UK
Lenka Justinova
Affiliation:
Ecology and Evolutionary Biology, School of Biological Sciences, Bassett Crescent East, University of Southampton, Southampton, SO16 7PX, UK
Guy M. Poppy
Affiliation:
Ecology and Evolutionary Biology, School of Biological Sciences, Bassett Crescent East, University of Southampton, Southampton, SO16 7PX, 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.

Brassica rapa grows as a wild and weedy species throughout the world and is the most likely recipient of transgenes from GM oilseed rape. For transgene introgression to occur, the critical step which must be realized, is the formation of an F1 hybrid. Concerns exist that hybrid populations could be more vigorous and competitive compared to the parental species. This study examines the effect of simulated herbivory and interspecific competition on the vegetative and reproductive performance of non-transgenic F1 hybrids and their parental lines. Several vegetative and reproductive performance measures were used to determine the effect of simulated herbivory and competition on the Brassica lines, including leaf length and biomass for herbivory and seedling height and biomass for competition. For defoliation experiments, B. rapa showed little response in terms of leaf length but B. napus and the F1 hybrid responded negatively. Brassica rapa showed elevated biomass responses, but B. napus and the hybrid demonstrated negative responses to defoliation. Defoliation at the cotyledon stage had a slight effect upon final biomass with the F1 hybrid performing significantly worse than B. napus, although seed counts were not significantly different. For the series of competition experiments, hybrids seemed to be more similar to B. rapa in terms of early seedling growth and reproductive measures. The underperformance of hybrid plants when challenged by herbivory and competition, could potentially decrease survivorship and explain the rarity of hybrids in field surveys. However, should transgene introgression occur, the dynamics of hybrids could change radically thus increasing the risk of gene flow from a transgenic oilseed rape crop to the wild recipient.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2006

References

Agrawal, AA (1998) Induced responses to herbivory and increased plant performance. Science 279: 12011202 CrossRef
Arnold, ML, Hodges, SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol. Evol. 10: 6771 CrossRef
Bardner, R, Fletcher, KE (1974) Insect infestations and their effects on the growth and yield of field crops: A review. B. Entomol. Res. 64: 141160 CrossRef
Cartwright, B, Kok, LT (1990) Feeding by Cassida rubiginosa (Coleoptera: Chrysomelidae) and the effects of defoliation on growth of musk thistles. J. Entomol. Sci. 25: 538547
Davenport, IJ, Wilkinson, MJ, Mason, DC, Charters, YM, Jones, AE, Allainguillaume, J, Butler, HT, Raybould, AF (2000) Quantifying gene movement from oilseed rape to its wild relatives using remote sensing. Int. J. Remote Sens. 21: 35673573 CrossRef
Davis, JM, Svendsgaard, DJ (1990) U-shaped dose-response curves: their occurrence and implications for risk assessment. J. Toxicol. Env. Heal. 30: 7183 CrossRef
Downey RK, Klassen AJ, Stringham GR (1980) Rapeseed and mustard. In Fehr WR, Hadley HH, eds, Hybridization of crop plants. American Society of Agronomy, Madison, Wisconsin, pp 495–509
Gavloski, JE, Lamb, RJ (2000a) Compensation for herbivory in cruciferous plants: Specific responses to three defoliating insects. Environ. Entomol. 29: 12581267 CrossRef
Gavloski, JE, Lamb, RJ (2000b) Compensation by cruciferous plants is specific to the type of simulated herbivory. Environ. Entomol. 29: 12731282 CrossRef
Gressel J (2002) Molecular Biology of Weed Control. Taylor and Francis, London
Guéritaine G, Bazot S, Darmency H (2003) Emergence and growth of hybrids between Brassica napus and Raphanus raphanistrum. New Phytol. 158: 561–567
Halfhill MD, Millwood RJ, Raymer PL, Stewart CN (2002) Bt-transgenic oilseed rape hybridization with its weedy relative, Brassica rapa. Environ. Biosafety Res. 1: 19–28
Halfhill, MD, Zhu, B, Warwick, SI, Raymer, PL, Millwood, RJ, Weissinger, AK, Stewart, CN (2004) Hybridization and backcrossing between transgenic oilseed rape and two related weed species under field conditions. Environ. Biosafety Res. 3: 7381 CrossRef
Halfhill, MD, Sutherland, JP, Moon, HS, Poppy, GM, Warwick, SI, Weissinger, AK, Rufty, TW, Raymer, PL, Stewart, CN (2005) Growth, fitness, and competitiveness of introgressed weedy Brassica rapa hybrids with Bt cry1Ac and gfp transgenes. Mol. Ecol. 14: 31773189 CrossRef
Hansen, LB, Siegismund, HR, Jørgensen, RB (2001) Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population. Genet. Resour. Crop Ev. 48: 621627 CrossRef
Hauser, TP, Østergård H (1999) Precocious germination of Brassica rapa × B. napus seeds within pods. Hereditas 130: 8993 CrossRef
Hauser, TP, Shaw, RG, Østergård H (1998a) Fitness of F1 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81: 429435 CrossRef
Hauser, TP, Jørgensen, RB, Østergård H (1998b) Fitness of backcross and F2 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81: 436443 CrossRef
Jørgensen, RB, Andersen, B (1994) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): A risk of growing genetically modified oilseed rape. Am. J. Bot. 81: 16201626 CrossRef
Jørgensen, RB, Andersen, B, Landbo, L, Mikkelsen, TR (1996) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy relatives. Acta Hort. 407: 193200 CrossRef
Jørgensen, RB, Andersen, B, Snow, A, Hauser, TP (1999) Ecological risks of growing genetically modified crops. Plant Biotechnol. 16: 6971 CrossRef
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, Illinois, USA
Klinger T, Ellstrand NC (1994) Engineered genes in wild populations: Fitness of weed-crop hybrids of Raphanus sativus. Ecol. Appl. 4: 117–120 CrossRef
Landbo L, Andersen B, Jørgensen RB (1996) Natural hybridisation between oilseed rape and a wild relative: hybrids among seeds from weedy B. campestris. Hereditas 125: 89–91
Lewontin R (2004) Building a science of population biology. In Singh RS, Uyenoyama MK, eds, The Evolution of Population Biology. Cambridge University Press, pp 7–20
Linder, CR, Schmitt, J (1994) Assessing the risks of transgene escape through time and crop-wild hybrid persistence. Mol. Ecol. 3: 2330 CrossRef
Linder, CR, Schmitt, J (1995) Potential persistence of escaped transgenes: Performance of transgenic, oil-modified Brassica seeds and seedlings. Ecol. Appl. 5: 10561068 CrossRef
Mauricio, R, Bowers, MD, Bazzaz, FA (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74: 20662071 CrossRef
Poppy, GM (2004) Geneflow from GM plants – towards a more quantitative risk assessment. Trends Biotechnol. 22: 436438 CrossRef
Rabinovitch, PS (1994) Flow cytometry. Method. Cell. Biol. 41: 264496
Raldugina, GN, Gorelova, SV, Kozhemyakin, AV (2000) Stability and inheritance of inserted genes in rapeseed plants. Russ. J. Plant Phys. 47: 386393
Raybould, AF, Gray, AJ (1994) Will hybrids of genetically modified crops invade natural communities? Trends Ecol. Evol. 9: 8589 CrossRef
Raybould AF, Moyes CL, Maskell LC, Mogg RJ, Warman EA, Wardlaw JC, Elmes GW, Edwards ML, Cooper JI, Clarke RT, Gray AJ (1999) Predicting the ecological impacts of transgenes for insect and virus resistance in natural and feral populations of Brassica species. In Ammann K, Jacot Y, Kjellsson G, Simonsen V, eds, Methods for Risk Assessment of Transgenic Plants. III. Ecological risks and prospects of transgenic plants, where do we go from here? Birkhauser Verlag, pp 3–15
Rees, M, Long, MJ (1992) Germination biology and the ecology of annual plants. Am. Nat. 139: 484508 CrossRef
Scheffler, JA, Dale, PJ (1994) Opportunities for gene-transfer from transgenic oilseed rape (Brassica napus) to related species. Transgenic Res. 3: 263278 CrossRef
Scott, SE, Wilkinson, MJ (1998) Transgene risk is low. Nature 393: 320320 CrossRef
Stewart, CN, Adang, MJ, All, JN, Raymer, PL, Ramachandran, S, Parrott, WA (1996) Insect control and dosage effects in transgenic canola containing a synthetic Bacillus thuringiensis crylAc gene. Plant Physiol. 112: 115120 CrossRef
Stewart, CN, All, JN, Raymer, PL, Ramachandran, S (1997) Increased fitness of transgenic insecticidal rapeseed under insect selection pressure. Mol. Ecol. 6: 773779 CrossRef
Strauss, SY, Agrawal, AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol. Evol. 14: 179185 CrossRef
Sutherland JP, Poppy GM (2005) Quantifying exposure. In Poppy GM, Wilkinson MJ, eds, Gene Flow from GM Plants. Blackwell Publishing, pp 186–212
Sylvester-Bradley, R, Makepeace, RJ, Broad, H (1984) A code for stage development in oilseed rape (Brassica napus L.) – Agronomy, physiology, plant breeding and crop protection of oilseed rape. Aspect. Appl. Biol. 6: 399419
Talekar, NT, Shelton, AM (1993) Biology, ecology and management of the diamondback moth. Annu. Rev. Entomol. 38: 275301 CrossRef
Trumble, JT, Kolodny-Hirsch, DM, Ting, IP (1993) Plant compensation for arthropod herbivory. Annu. Rev. Entomol. 38: 93119 CrossRef
Watkinson, AR, Freckleton, RP, Robinson, RA, Sutherland, WJ (2000) Predictions of biodiversity response to genetically modified herbicide-tolerant crops. Science 289: 15541557 CrossRef
Warwick, SI, Simard, MJ, Légère, A, Beckie, HJ, Braun, L, Zhu, B, Mason, P, Séguin-Swartz, G, Stewart, CN Jr (2003) Hybridization between transgenic Brassica napus L. and its wild relatives: B. rapa L., Raphanus raphanistrum L., Sinapsis arvensis L., and Erucastrum gallicum (Willd.) O.E. Schulz. Theor. Appl. Genet. 107: 528539 CrossRef
Weis AE (2005) Assessing the ecological fitness of recipients. In Poppy GM, Wilkinson MJ, eds, Gene Flow from GM Plants. Blackwell Publishing, pp 143–168
Wilkinson, MJ, Elliott, 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, GM (2003b) Risk assessment of GM plants: Avoiding gridlock? Trends Plant Sci. 8: 208212 CrossRef