D. G Lindsay, CEBAS-CSIC, Murcia
12.2 Risk assessment and avoidance: general principles
12.2.1 Principles of risk assessment
As previously mentioned, GM crops have a number of potential benefits for growers, processors and eventually the consumer, but it is also recognised that there are likely to be environmental impacts and implications for food quality and safety. For example, exploitation of novel GM pest-, disease- and herbicide- resistant crops will require different (often reduced) pesticide and herbicide applications. These modified management systems will have an impact upon current agricultural systems and the agricultural environment. Such impacts are best analysed by risk assessments.
The basic concepts of risk assessment for genetically modified crops are similar to those applied to chemical pesticides where the risk is equal to the frequency and the hazard. For example no exposure (frequency) would equate to zero hazard. Risk assessments study both the severity and extent of the hazard or damage as well as the likelihood and frequency at which the damage will occur.
Risk is defined as:
Risk (impact) Frequency (exposure) Hazard
Clearly the ideal situation would be one of zero risk. Since in reality the likelihood of risk is always greater than zero, acceptable risk levels for GM crops must be defined, as with all new technology. What is defined as acceptable is based upon cultural values and may well differ globally. Indeed the current climate of controversy surrounding GM crops signifies strong cultural differences between European and North American consumers in what is defined as acceptable levels of risk for the utilisation of GM crops.
While there are differences in the regulatory procedures controlling the development and commercialisation of GM crops in North America and Europe, both systems apply the same broad principles to assessing the safety of GM crop usage for food, animal feed and in terms of environmental impact. The first step involves thoroughly assessing the procedure for modifying the plant tissue. In the UK, for example, the Advisory Committee on Genetic Modification (ACGM) is the regulatory authority responsible for contained use evaluation; that is, the initial experimental work ‘contained’ within the laboratory or glasshouse. The risk evaluation procedure must be specific to each product. Broadly drawn conclusions, for example based on inter-species comparisons, are unacceptable.
Most importantly the information requested in a risk assessment must be derived scientifically, with experiments designed to provide clear, interpretable, unequivocal and reproducible results. A recent addition to the risk-assessment procedure has occurred in the UK, in response to public pressure, where there is now a move towards assessing the societal and cultural impacts of this new technology alongside the environmental and human health risks.
Risk assessment can be divided into four steps (Nickson and McKee 1998):
1. problem formulation 2. risk analysis 3. risk characterisation 4. risk management.
Problem formulation requires that all available information concerning the plant, the trait and the experimental information is gathered in the context of the most likely hazards, such as toxicity/allergenicity. Once all the data are available, they can be analysed for characterisation of the likelihood and/or severity of the risk. In the final phase of the assessment procedure, the acceptability or otherwise of the identified risk must be determined and effective plans set out for its management. The risk assessment procedure is an iterative one and must continue throughout the use of the product, including post-market monitoring.
In the case of GM crops there are a number of variables/risk types to consider including impacts on the agricultural environment, closely related species, insects and animals and human health. To analyse the consequences of GM crop impact upon the agricultural environment requires a detailed understanding of the characteristics of the GM crop in question. This involves determining which wild relative, if any, it may hybridise with and studying the management
systems involved in growing the GM crop itself. It also involves recognising any potential effects on other GM or non-GM crops which are likely to be grown in rotation with the variety being assessed. As an example, GM herbicide tolerant (HT) crops will be treated with different herbicides, with different activity spectra, at different crop development stages, leading to effects on the botanical diversity in the GM-HT crop which are the product of the interaction between the GM crop and the herbicide treatment.
The nature of any hazard is dependent upon the characteristics of both the crop that is modified and of the GM trait. Risk assessments require measurement and study of the hazard or impact of both. Numerous studies have concentrated on measuring frequency phenomena such as gene flow and inter-specific hybridisation without considering the impact of the transgene when it has dispersed or introgressed into other populations or species. In addition the impact of the release of the GM plant will depend on the type and location of the environment into which it is being released. To be truly effective, risk assessments may have to be carried out for a range of locations as they are not necessarily transferable from one site, area, region or country to another.
12.2.2 Impact of plant species
Plants vary in the degree to which they are dominant or are invasive in certain environments and in their ability to disperse genes to different populations and species. They will therefore have different environmental impacts when genetically modified. For any particular country or region, plants can be classified as potentially being high, medium or low impact.
Plants in the high-impact group are generally hardy, perennial, competitive, open-pollinating and prolific having a wide range of relatives with which they hybridise and an ability to colonise a range of natural and semi-natural habitats.
Examples include perennial rye grasses (Lolium perenne) and certain indigenous and introduced trees and shrubs that form a significant proportion of forests and woodlands, e.g.Populusspp. Modifications of these plants, which affect their competitiveness, could have significant impacts upon the ecology of a range of environments.
Medium-impact plants are open-pollinating, hybridise with some wild relatives, are prolific and colonise a limited range of habitats. Examples of such plants include oilseed rape, oats, sugar beet and rice, all of which have closely related wild relatives with which they hybridise and an ability to colonise disturbed ground. These plants and their close relatives rarely form climax populations except in particular environments such as coastal areas or in disturbed ground. Low-impact plants are usually annual or biennial species, are largely self-pollinating with few hybridising relatives that are poorly adapted (or not native) to the area in which they are cultivated. In the UK, examples include maize and sunflower.
It is important to appreciate that the impact of a plant species will depend upon the environment into which it is being released. Maize and potato are
considered low-impact plants in England. However in Central and South America, where their centres of genetic diversity occur, their impact would be considered very high.
12.2.3 Impact of transgenes
Transgene expression in GM plants will have different impacts in different environments. Since genes often operate uniquely it is not easy to classify transgenes as having high or low impact. In addition their impact is also dependent upon the nature of the receiving environment (agricultural impact).
High-impact transgenes generally encode genetic modifications that improve the fitness of the GM plants by increasing their reproduction, competitiveness, invasiveness and/or persistence and will therefore also have the greatest environmental impact. Thus transformations that significantly increase plant productivity by overcoming constraints such as broad-spectrum pest, disease and stress tolerance will have the highest impact. Many pest- and disease-resistant genes will have effects on non-target species either directly or indirectly by altering relationships between pests and beneficial organisms. It is important that these non-target effects are thoroughly understood before commercialisation progresses.
Low-impact transgenes are genes that do not noticeably enhance the fitness of the modified plant so that the modified plant’s role and behaviour in a given ecosystem is not altered. Examples would include genes that modify seed composition, e.g. high lauric acid genes in oilseed rape and high starch content genes in potato. However, in preparing a comprehensive risk assessment it would be important to confirm that low-impact genes might not, uninten- tionally, confer an environmental advantage. As an example, in the case of high starch content genes in potato, it would be important to assess that the transgenes do not significantly increase potato seed tuber over-wintering survival rates through enhanced frost resistance. In the case of oilseed rape, it would be important to ensure, for example, that there is no increase in the dormancy characteristics of oilseed rape which may confer enhanced soil survival characteristics.
12.2.4 Mechanisms of transgene transmission
Gene flow is an important consideration in evaluating the risks associated with growing GM crops. Transgene dispersal could lead to contamination of neighbouring crops, a particular worry since the UK organic authority amended its rules to include a zero tolerance to the presence of GM material. Transgene flow from crops to closely related wild relatives is also of concern as an environmental risk. Gene flow between different species is, however, not a new concept and has in fact been occurring between natural plant species, leading to a range of hybrids in the UK flora including amongst others the Salix, Lolium and Rumex genera (Daniels and Sheail 1999).
In order for gene transfer from one species of plant to another closely related wild relative to occur a number of barriers, both physical and genetic, must be overcome. These include dispersal (either of pollen or seed), longevity of the pollen grain, sexual compatibility, competition with other pollen sources and events post-fertilisation. Most gene dispersal occurs as a result of pollen transported either on the wind or via vectors such as bees (Ramsayet al. 1999) or, less commonly, by seed dispersal. The distances over which pollen dispersal occurs varies depending upon the plant species, the prevailing weather conditions, in the case of wind-borne pollen, or the insect vector (Moyes and Dale 1999). As discussed by Moyes and Dale (1999), although most studies have concentrated on the range of pollen dispersal, the survivability over time of the pollen grain is actually the most important aspect of potential gene transfer and cross-contamination.
Assuming that pollination is successful and gene transfer has occurred, the barriers to successful introgression of a gene from the original donor species to the recipient will be dependent upon what the gene might offer the recipient. If, for example, the gene induces a lethal effect, the seed of the recipient plant will die and gene introgression into the recipient species will go no further. If, however, the transgene confers a selective advantage such as cold tolerance, drought or disease resistance or the ability to thrive in low-light conditions, seed from the recipient plant will thrive. This is especially true for native species, with the greatest opportunity for transgene movement occurring within the crop- weed complex (Whitton et al. 1997). However, in assessing the scale of transgene movement, it is important to consider whether those plants containing genes conferring an adaptive advantage in the agricultural environment might lose that selective advantage in the differing environmental conditions outside of the farm field. If the transgene provides no selective advantage to the recipient plant, such as herbicide-resistant genes present in plants growing in an environment where herbicide spraying will not occur, the transgene will have a neutral impact upon the recipient species. There will be no increase in fitness of the population.
12.2.5 Multiple transgenes and transgene stability
One of the major issues surrounding GM crops containing multiple transgenes encoding a variety of traits is the question of stability of gene expression. Might the introduction of a second transgene affect expression of the original transgene and thus the phenotype of the GM variety? In particular, genetic homology between the two transgenes may cause down regulation of gene expression and suppression of the phenotype. How this effect is caused is complex and thought to be affected by factors such as the position of the transgene within the genome, i.e. point of insertion during the transformation procedure, transgene copy number within the genome and by other factors such as reproduction and even environmental conditions. The results may be unpredictable resulting in instability or silencing of gene expression (Senior and Dale 1996). The
production of GM varieties involves evaluation of transgenic lines over a number of generations, during which any unstable lines would generally be identified and discarded. One possible exception to this would be instability arising from environmental interaction. This instability is also observed in conventionally bred varieties, providing a basis for further analysis of GM varieties (Qianet al. 1986).
From the perspective of risk assessment and environmental impact the most significant issue arises from gene flow between closely related species. Instability of gene expression generally leads to suppression of gene expression, in which case the phenotype of the GM variety would revert to the wild type, with no expression of the transgene. The implications for agronomic practice are significant, as suppression of gene expression would render a herbicide-tolerant GM variety susceptible to that particular herbicide, with consequent loss of yield if the farmer were to spray unwittingly. While the effect of transgene instability on the natural environment is likely to be minimal, there may be important issues at stake in the case of transgenic plants engineered to remove the synthesis of harmful toxins. In this situation suppression of gene expression arising from gene flow leading to multiple transgene insertions could prove a serious human or animal health problem if undetected.