gene flow from genetically modified crops

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DOI: 10.1039/b108604a Pesticide Outlook – October 2001 177 This journal is © The Royal Society of Chemistry 2001 Currently in the UK there is a programme of ‘Farm Scale Evaluations’ of genetically modified (GM) crops. The programme is designed to compare the effects on biodiver- sity of GM herbicide tolerant oilseed rape, sugar beet and maize with those of conventional varieties of these crops. The evaluations have highlighted concerns about gene flow from the GM plants to conventional crops or wild relatives. Dispersal and gene flow Gene flow is the movement of genes between populations of a species. In plants, gene flow can occur via dispersal of seeds or pollen. However, gene flow is more than simply the movement of a seed or a pollen grain; pollen grains must achieve fertilisation and seeds must germinate and produce sexually mature plants. Therefore the presence of GM pollen on the leaves of another plant or GM seed in a batch of non- GM is strictly not gene flow, but dispersal. The distinction is important because dispersal without gene flow is a ‘dead end’ for the spread of genes, although the consequences of dispersal might be important. For example, the presence of GM oilseed rape pollen on organic maize might be regarded as unacceptable “contamination”. However, the situation will not continue once the GM oilseed rape is not grown. On the other hand, if the GM rape were to pollinate wild relatives then the genetic modification could persist in the environment. Routes for gene flow from GM crops Crop seeds can give rise to plants in a following or neigh- bouring crop (volunteer weeds), or in semi-natural habitats close to farmland or transport routes (feral populations) (Figure 1). Crops usually cannot persist in semi-natural habitats without continual disturbance and fresh immigration of seed because they are easily overgrown by perennial grasses and shrubs. For example, Crawley and Brown (1995) showed that seed spilled from lorries en route to processing plants in Kent, rather than self-sustaining populations, maintained the presence of oilseed rape populations surrounding the M25. Apart from dispersal associated with agricultural activity, pollen generally has a much higher capacity than seeds for bulk long distance dispersal. However as described above, to have a lasting effect in the environment pollen must achieve fertilisation. Gene flow through GM pollen can occur to other varieties of the same crop (crop-to-crop gene flow) or to wild plants that are sexually compatible with the crop. Gene flow can also occur over time through seed dormancy. For example, seeds of oilseed rape spilled in fields or onto roadsides can survive in the soil and germinate when the ground is disturbed, giving rise to volunteer weeds or feral populations. New feral populations of oilseed rape have been found up to 10 years after the variety had been withdrawn from sale. Variation among crops for gene flow potential Gene flow is to a large extent dependent on the breeding system of the crop (Table 1). Some crops, such as wheat and barley, are ‘inbreeders’, in which pollen is usually transferred to stigmas of the same plant, or even the same flower. These species generally have a low capacity for gene flow. Conversely in ‘outbreeders’, pollination usually occurs by transfer of pollen to stigmas of flowers on a different plant. Many specialised mechanisms exist to promote the transfer of pollen, such nectar production to attract pollinating insects. As well as having mechanisms to promote cross-pollination, many outbreeders have systems to prevent self-fertilisation. For example, pollen and stigmas may ripen at different times or pollen may be prevented from germinating if self-pollination occurs. This latter mechanism is called self-incompatibility. Cabbage is an insect pollinated self-incompatible species and sugar beet and ryegrass are examples of wind pollinated, self-incompat- ible species. Outbreeders have a high capacity for gene flow. A third category of plants has a so-called ‘mixed’ mating system, where seeds are set by a mixture of self- and cross- fertilisation. Oilseed rape is an example of this kind of plant. The proportion of cross- to self- fertilisation can vary depending on crop variety and environmental conditions, and in these species gene flow can occur over long distances. Another factor determining the amount of gene flow is the presence of sexually compatible wild relatives near to the crop. Again, three categories can be defined (Raybould and Gray, 1993). A group of crops with no compatible wild relatives in the UK, such as maize and potato, have a minimal risk of gene flow to wild species. Some crops, sugar beet and ryegrass for instance, have wild relatives that are essentially the same species. Here the likelihood of gene flow from crop to wild relative is high. Finally, there is an inter- mediate group of crops that have local wild relatives of the same genus. In the UK, oilseed rape (Brassica napus) has several wild relatives of the same species such as wild GENE FLOW FROM GENETICALLY MODIFIED CROPS Alan Raybould from the Centre for Ecology and Hydrology (Winfrith Technology Centre) at Dorchester, UK, reports on a controversial issue concerning the field testing of GM crops GM CROPS Published on 01 January 2001. Downloaded on 25/10/2014 17:27:29. View Article Online / Journal Homepage / Table of Contents for this issue

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Page 1: Gene Flow from Genetically Modified Crops

DOI: 10.1039/b108604a Pest ic ide Outlook – October 2001 177

This journal is © The Royal Society of Chemistry 2001

Currently in the UK there is a programme of ‘Farm ScaleEvaluations’ of genetically modified (GM) crops. Theprogramme is designed to compare the effects on biodiver-sity of GM herbicide tolerant oilseed rape, sugar beet andmaize with those of conventional varieties of these crops.The evaluations have highlighted concerns about gene flowfrom the GM plants to conventional crops or wild relatives.

Dispersal and gene flowGene flow is the movement of genes between populations ofa species. In plants, gene flow can occur via dispersal ofseeds or pollen. However, gene flow is more than simply themovement of a seed or a pollen grain; pollen grains mustachieve fertilisation and seeds must germinate and producesexually mature plants. Therefore the presence of GM pollenon the leaves of another plant or GM seed in a batch of non-GM is strictly not gene flow, but dispersal. The distinction isimportant because dispersal without gene flow is a ‘deadend’ for the spread of genes, although the consequences ofdispersal might be important. For example, the presence ofGM oilseed rape pollen on organic maize might be regardedas unacceptable “contamination”. However, the situationwill not continue once the GM oilseed rape is not grown.On the other hand, if the GM rape were to pollinate wildrelatives then the genetic modification could persist in theenvironment.

Routes for gene flow from GM cropsCrop seeds can give rise to plants in a following or neigh-bouring crop (volunteer weeds), or in semi-natural habitatsclose to farmland or transport routes (feral populations)(Figure 1). Crops usually cannot persist in semi-naturalhabitats without continual disturbance and freshimmigration of seed because they are easily overgrown byperennial grasses and shrubs. For example, Crawley andBrown (1995) showed that seed spilled from lorries en routeto processing plants in Kent, rather than self-sustainingpopulations, maintained the presence of oilseed rapepopulations surrounding the M25.

Apart from dispersal associated with agricultural activity,pollen generally has a much higher capacity than seeds forbulk long distance dispersal. However as described above, tohave a lasting effect in the environment pollen must achievefertilisation. Gene flow through GM pollen can occur toother varieties of the same crop (crop-to-crop gene flow) orto wild plants that are sexually compatible with the crop.

Gene flow can also occur over time through seeddormancy. For example, seeds of oilseed rape spilled in fieldsor onto roadsides can survive in the soil and germinate whenthe ground is disturbed, giving rise to volunteer weeds orferal populations. New feral populations of oilseed rapehave been found up to 10 years after the variety had beenwithdrawn from sale.

Variation among crops for gene flow potentialGene flow is to a large extent dependent on the breedingsystem of the crop (Table 1). Some crops, such as wheat andbarley, are ‘inbreeders’, in which pollen is usuallytransferred to stigmas of the same plant, or even the sameflower. These species generally have a low capacity for geneflow. Conversely in ‘outbreeders’, pollination usually occursby transfer of pollen to stigmas of flowers on a differentplant. Many specialised mechanisms exist to promote thetransfer of pollen, such nectar production to attractpollinating insects. As well as having mechanisms topromote cross-pollination, many outbreeders have systemsto prevent self-fertilisation. For example, pollen and stigmasmay ripen at different times or pollen may be preventedfrom germinating if self-pollination occurs. This lattermechanism is called self-incompatibility. Cabbage is aninsect pollinated self-incompatible species and sugar beetand ryegrass are examples of wind pollinated, self-incompat-ible species. Outbreeders have a high capacity for gene flow.

A third category of plants has a so-called ‘mixed’ matingsystem, where seeds are set by a mixture of self- and cross-fertilisation. Oilseed rape is an example of this kind of plant. The proportion of cross- to self- fertilisation can vary depending on crop variety and environmentalconditions, and in these species gene flow can occur overlong distances.

Another factor determining the amount of gene flow isthe presence of sexually compatible wild relatives near to thecrop. Again, three categories can be defined (Raybould andGray, 1993). A group of crops with no compatible wildrelatives in the UK, such as maize and potato, have aminimal risk of gene flow to wild species. Some crops, sugarbeet and ryegrass for instance, have wild relatives that areessentially the same species. Here the likelihood of gene flowfrom crop to wild relative is high. Finally, there is an inter-mediate group of crops that have local wild relatives of thesame genus. In the UK, oilseed rape (Brassica napus) hasseveral wild relatives of the same species such as wild

GENE FLOW FROM GENETICALLY MODIFIED CROPS

Alan Raybould from the Centre for Ecology and Hydrology (Winfrith Technology Centre) at Dorchester, UK,reports on a controversial issue concerning the field testing of GM crops

GM CROPS

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cabbage (Brassica oleracea) (Figure 2) and wild turnip(Brassica rapa). This group of crops can transfer genes to

wild relatives, but with low and variable frequency that ishard to predict (e.g. Wilkinson et al., 2000).

Consequences of crop-to-crop gene flowCrop-to-crop gene flow from GM crops has already hadserious consequences in North America. One incidentinvolves a variety of maize called StarLink. This variety hasbeen genetically modified with a gene from a soil bacterium,Bacillus thuringiensis. The product of the gene, a proteincalled Cry9C, protects the maize against insect pests such asthe European corn borer. The US Environmental ProtectionAgency restricted the commercial use of this variety toanimal feed and industrial use; the variety was not approvedfor human consumption because of concerns that the Cry9Cprotein might be allergenic.

Last year, DNA from StarLink was detected in taco shellsand the manufacturer voluntarily recalled the affectedproducts. Eventually the US Food and Drug Administrationofficially recalled the taco shells, and many other manufac-turers of foods containing maize also recalled products.

The initial contamination problem seems to have been

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Table 1. Examples of UK crops with different potential for gene flow to other crops or wild relatives

Crop Breeding system Wild relatives in the UK Potential for gene flow

Potato Mixed: Cultivated species are self- Woody nightshade (Solanum dulcamara), no Low crop-to crop(Solanum tuberosum) compatible, but crossing can occur hybrids produced even with artificial Minimal to wild relatives

via insect pollinators pollination

Maize Mixed: Usually self-compatible, but None Crop-to-crop gene flow over (Zea mays) cross pollination promoted by having distances <200 m

separate male (tassel) and female Minimal to wild relatives(silk) inflorescences

Wheat Inbreeding None Very low crop-to crop(Triticum aestivum) Minimal to wild relatives

Barley Inbreeding Many wild Hordeum species, but none known Low crop-to crop(Hordeum vulgare) to hybridise under natural conditions Low to wild relatives

Oilseed rape Mixed: Self-compatible, but but Can cross naturally with Brassica rapa (wild Moderate-high crop-to-crop(Brassica napus) crossing can occur via insect and turnip). Unconfirmed reports of natural crosses Moderate to wild relatives

wind pollination with Brassica oleracea (wild cabbage). Can be made to cross with several other wild Brassica species under laboratory conditionsMany other species of Brassica & related genera (e.g. Raphanus [radish]) with various degrees of compatibility†

Linseed Mixed: Self-compatible, but crossing Pale flax (L. bienne), perennial flax (L. perenne) Moderate crop-to-crop(Linum usitatissimum) can occur via insect pollination and fairy flax (L. catharticum). No hybrids with Low to wild relatives

linseed recorded in the UK

Ryegrass Outbreeder: self-incompatible, wind Many: e.g. species of Lolium & Festuca High crop-to-crop and to wild (Lolim perenne) pollinated relatives

Sugar beet Outbreeder: self-incompatible, Weed beet – plants that flower (bolt) before High to weed beet and sea beet(Beta valugaris) mainly wind pollination, though harvest

insects may act as pollinators Sea beet (Beta vulgaris ssp. maritima) can cross with bolters in the beet crop

†See Scheffler & Dale (1994) for a detailed review of gene flow from oilseed rape

Figure 1. A feral population of wheat, which probablyestablished from wheat straw used to stabilise the sides of theroad cutting

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due to mixing of seed before or during processing. However,there are several reports of the gene for Cry9C beingdetected in other maize varieties. It seems likely, therefore,that gene flow has occurred from StarLink to other maizevarieties, and may also have played a part in the contamina-tion of the maize used to make the taco shells (e.g. Ellstrand,2001). The company that sold StarLink agreed to payfarmers for StarLink maize and other varieties that hadbecome contaminated with StarLink if the maize was notdestined for animal feed. The incident has raised questionsabout food labelling and liability in cases where GM andnon-GM varieties are accidentally mixed.

A second problem that arose because of crop-to cropgene flow was the development of volunteer oilseed rapethat was resistant to 3 herbicides. In Alberta in 1997, afarmer sowed part of a field with a GM oilseed raperesistant to glufosinate; in the remainder, he planted aconventional variety resistant to imidazolinone. In anadjacent field, he planted a GM oilseed rape resistant toglyphosate. The following year, the farmer grew imidazoli-none resistant rape in the field that had the glyphosateresistant rape the previous year and left the other fieldfallow. In this field, he tried to control volunteer rape weedswith glyphosate, but without success. Hall et al. (2000)found that the glyphosate resistant weeds were also resistantto either imidazolinone or glufosinate. This indicated thatgene flow via pollen, rather than seed movement was thesource of the resistant volunteers. In addition, two volunteersgave progeny resistant to all three herbicides; the imidazoli-none rape crop had probably crossed with a glufosinate andglyphosate resistant weed. Hall et al. (2000) point out thatthis situation should be avoided by not growing varieties withdifferent herbicide resistance mechanisms so close together. Inaddition, herbicides with a different mode of action should beused to control volunteers.

Consequences of crop to wild relative geneflowThe hazards of crop-to-crop gene flow are fairly clear: adul-teration of harvested seed and novel traits in volunteer

weeds. There is less agreement about the hazards of geneflow to wild relatives. Some people have ethical concerns,considering gene flow to wild plants to be ‘genetic pollution’(Daniels and Sheail, 1999). Other hazards are the potentialfor changes in the persistence, abundance or distribution(‘weediness’) of wild relatives, which might alter thecomposition of plant communities, and effects on other(‘non-target’) organisms.

It is difficult to generalise about the traits that make aplant a successful weed. Several attempts have been made,but none is very successful (e.g. Gray, 1986 and Williamson,1993 for the problems involved). Unfortunately, this meansthat risk assessments must proceed on a case-by-case (cropand modification) basis, at least until more data areavailable.

It is likely that herbicide tolerance will not increase theweediness of plants in non-agricultural habitats whereherbicides are not applied. Crawley et al. (2001) sowedseeds of GM herbicide resistant potato, oilseed rape, maizeand sugar beet, along with non-GM controls in 12 semi-natural habitats throughout the UK. For all GM crops,recruitment was very low (<4% of seed sown) and in nocase was it greater than conventional controls. Allpopulations were extinct after 4 years, except one non-GMpotato that still persists after 10 years.

Traits that are more likely to change the weediness ofplants are resistance to physical stresses such as drought,salinity, high temperature and pollution. Resistance to pestsand diseases may also increase weediness if the size of plantpopulations is controlled by these factors. Up to a point,laboratory experiments may help to predict the environ-mental impacts of resistance genes. Suppose that in anexperiment a GM plant with insect resistance produces moreseed than a non-GM plant when attacked by insects, it doesnot follow that the GM plant will become a worse weed.Factors other than insects might be much more important incontrolling seed output in the field. Also seed output mightnot be a factor limiting the size of a population, so althoughresistant plants produce more seed, the population size doesnot increase because the previously susceptible populationproduced sufficient seed to keep the population at itscarrying capacity (e.g. Bergelson, 1994). However, while thesize of the population may not change, its geneticcomposition may change from susceptible plants to resistantones, which could have a knock-on effect on non-targetinsects.

Non-target effects occur when, for example, a gene forresistance against a pest or disease has detrimental effects onharmless or beneficial organisms. Laboratory experimentshave shown that ladybirds feeding on aphids feeding on GMinsect resistant potatoes show lower survival and fecunditythan ladybirds feeding on aphids on conventional potatoes(Birch et al., 1999). Similar results have been found withgreen lacewings fed with European corn borer larvae rearedon GM insect resistant maize.

It must be remembered that laboratory experiments areusually ‘worst case scenarios’, because the predator specieshas no choice over its food. In addition, the effects tend tobe compared with ‘no treatment’, rather with insecticide orother control methods that the GM crop might replace.

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Figure 2. A population of wild cabbage, a relative of oilseedrape, growing on limestone cliffs at St. Aldhelm’s Head on thecoast of Dorset.

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Page 4: Gene Flow from Genetically Modified Crops

However, laboratory experiments do provide a useful guideto variables that should be measured in field experiments.

ConclusionsCrop-to-crop gene flow has already had serious conse-quences for agriculture. For seed crops, which requirepollination, it is unlikely that unwanted gene flow betweencrops could be avoided. The degree of separation (in spaceor time) between GM and non-GM crops will depend uponthe permitted thresholds for extraneous gene flow agreed byregulators and other interested parties. Wider environmentalimpacts are harder to predict as the population dynamics ofspecies are controlled by many interacting factors. Fieldtrials, guided by laboratory experiments, are required toassess these risks.

ReferencesBergelson, J. (1994) Changes in fecundity do not predict invasive-

ness – a model study of transgenic plants. Ecology 75, 249-252.Birch, A. N. E.; Geoghegan, I. E.; Majerus, M. E. N.; McNicol, J.

W.; Hackett, C. A.; Gatehouse, A. M. R.; Gatehouse, J. A.(1999) Tri-trophic interactions involving pest aphids, predatory2-spot ladybirds and transgenic potatoes expressing snowdroplectin for aphid resistance. Molecular Breeding 5, 75–83.

Crawley, M. J.; Brown, S. L. (1995) Seed limitation and thedynamics of feral oilseed rape on the M25 motorway.Proceedings of the Royal Society of London Series B 259,49–54.

Crawley, M. J.; Brown, S. L.; Hails, R. S.; Kohn, D. D.; Rees, M.(2001) Transgenic crops in natural habitats. Nature 409,682–683.

Daniels, R. E.; Sheail, J. (1999) Genetic pollution: concepts,concerns and transgenic crops. In: Gene Flow and Agriculture –Relevance for Transgenic Crops. Farnham, British CropProtection Council. pp. 65–72.

Ellstrand, N. C. (2001) When transgenes wander, should weworry? Plant Physiology 125, 1543–1545.

Gray, A. J. (1986) Do invading species have definable genetic char-acteristics? Philosophical Transactions of the Royal Society ofLondon Series B, 314, 655–674.

Hall, L.; Topinka, K.; Huffman, J.; Davis, L.; Good, A. (2000)Pollen flow between herbicide resistant Brassica napus is thecause of multiple-resistant B. napus volunteers. Weed Science48, 688–694.

Raybould, A. F.; Gray, A. J. (1993) Genetically modified crops andhybridization with wild relatives – a UK perspective. Journal ofApplied Ecology. 30, 199–219.

Scheffler, J. A.; Dale, P. J. (1994) Opportunities for gene transferfrom transgenic oilseed rape (Brassica napus) to related species.Transgenic Research 3, 263–278.

Wilkinson, M. J.; Davenport, I. J.; Charters, Y. M.; Jones, A. E.;Allainguillaume, J.; Butler, H. T.; Mason, D. C.; Raybould, A. F.(2000) A direct regional scale estimate of transgene movementfrom genetically modified oilseed rape to its wild progenitors.Molecular Ecology 9, 983–991.

Williamson, M. (1993) Invaders, weeds, and the risks fromGMOs. Experientia 49, 219–224

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Alan Raybould is head of the Molecular Ecology Group at CEHDorset. His research is focussed on predicting the impact of geneflow from genetically modified crops to their wild relatives. His maininterest is the effects of plant secondary chemistry on disease andpest resistance.

PREVIOUS PESTICIDE OUTLOOK ARTICLES ON GM CROPS

How to engineer a crop plant (Dunwell) – Pesticide Outlook 1998, 9(4), 29

GM crops – is there a future? (Halford) – Pesticide Outlook 1999, 10(6), 246

Farm scale evaluations of GM crops (Firbank) – Pesticide Outlook 2001, 12(3), 116

Bt maize and monarch butterflies (McLaren) – Pesticide Outlook 2001, 12(4), 136

Do GM crops mean less pesticide? (Benbrook) – Pesticide Outlook, this issue, p. 204

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