Public Reactions and Scientific Responses to Transgenic Crops Commentary Philip J Dale

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Public reactions and scientific responses to transgenic crops Commentary Philip J Dale

There is currently intense debate in parts of Europe about the isolate genes from any class of living organism and introduce commercial production of transgenic food crops. Information them into most of our crop plants using either the bacterial from the press and lobbying groups has not encouraged an method (Agrobacterium) [1] or the gene gun [2]. Plants mod- informed and balanced consideration of the issues. In marked ified in this way are termed transgenic, and are frequently contrast, there is widespread acceptance of transgenic food referred to as the products of genetic modification, even crops in North America. though traditional breeding is also a form of genetic modification. Intense research activities in genetic mapping, DNA Addresses sequencing and the characterisation of genes are providing John Innes Centre, Colney Lane, Norwich NR4 7UH, UK; valuable insights into how genes are organised within the e-mail: [email protected] genome [3••]. Current research is also increasing our under- Current Opinion in Biotechnology 1999, 10:203–208 standing of the ways genes act and interact to regulate complex biosynthetic pathways. These modern methods of http://biomednet.com/elecref/0958166901000203 genetic modification are making it possible to modify crops © Elsevier Science Ltd ISSN 0958-1669 in a variety of ways [4••,5•,6] (Table 1).

Abbreviations The critics EU European Union GM genetically modified Opponents of genetic modification often argue that it is imprecise, unpredictable, may produce superweeds and risks introducing toxins. They also maintain that to move genes Introduction across sexual barriers is unnatural, undesirable and equiva- About 28 million hectares of transgenic crops were grown lent to ‘playing God’ [7–13]. People often forget that it is worldwide in 1998 and the area is expected to be about 60 perfectly natural to die of smallpox but unnatural, and an ero- million hectares in the year 2000. In North America, where sion of the world’s biodiversity, to try to eradicate the most transgenic crops are grown, public opinion is fairly smallpox virus. We live in a highly managed and, in that relaxed about the widespread introduction of transgenic sense, unnatural world. Our agriculture is directed and artifi- crops and their use in food. Within Europe, various con- cial. Organic farming, for example, uses copper-based sprays cerns have been expressed, and in the UK during 1998 (Bordeaux Mixture) and sulphur dusts to control fungal dis- there has been a great deal of activity by various lobbying eases. Sprays made with the bacterium Bacillus thuringiensis groups who take a negative view of these developments in are used to control insect pests [14•]. Human health is also biotechnology. The aim in this paper is to discuss the sci- highly managed: we inject people with weakened (attenuat- ence and perceptions of the technology and to reflect on ed) viruses for immunisation; we treat bacterial infections why there are concerns. with antibiotics; we transfer blood and organs from one per- son to another; and we implant electrical devices to sustain Progress in genetic modification life. All methods of intervention in crop improvement are to During the past two decades there have been considerable some degree artificial and engineered, to provide crops that advances in methods of crop improvement. We can now are better able to serve the needs of people and animals.

Table 1

Some of the crop characters being modified by genetic modification.

• Pest resistance • Resistance to viral, bacterial and fungal diseases • Oil, starch and protein modification to provide sustainable supplies of raw materials for biodegradable plastics, detergents, lubricants, paper making and packaging, in addition to improvements in baking and brewing qualities • Herbicide tolerance to enable certain crop varieties to tolerate specific herbicides and in many cases reduce the number of herbicide applications to achieve effective weed control • Plant architecture and flowering, including plant height, flowering time and flower colour • Reduction in seed losses through shedding at harvest time • Modifications in fruit and tuber ripening and storage; research in potatoes is likely to reduce dependence on the use of anti-sprouting compounds applied to stored tubers • Increased tolerance to environmental stresses including cold, heat, water, and saline soils • Increase in the ability of certain plants to remove toxic metals from soils (bioremediation), such as on mining waste sites • The elimination of allergens from certain crops, for example, rice • The enhancement of vitamins, minerals and anticancer substances • The production of pharmaceutical substances (e.g. anticoagulant compounds, edible vaccines) 204 Commentary

Genetic modification placed in the context of many parts of the world [25]. Again, if we are concerned other methods of crop improvement about the transfer of weediness characteristics in crop Crop domestication improvement, it should be noted that this can happen in Crops have been improved for thousands of years [15,16]. traditional plant breeding, because thousands of genes are This was first done by selection of plants by people who often transferred from the gene donor species. needed them for food, feed, fibre and pharmaceuticals. People collected and cultivated the plants that were most Induced mutations productive. This process of selection was the driving force Another procedure used in traditional plant breeding is the in crop domestication, long before people began to under- artificial induction of mutations by chemicals or irradiation. stand the scientific principles underlying heredity. Mutagenesis has the potential to cause random and undi- rected genetic changes in all plant characteristics. These Following the widespread recognition of Mendel’s studies changes can be associated with single DNA base changes, on heredity early this century, we have come to understand with chromosomal inversions, translocations and rearrange- much more about the science of genetics. Early in the ments [26]. The process is rather like taking a million 1900s, plant breeding programmes became established watches and hitting each of them with a hammer and then across the world to direct the process of crop improvement sorting through them, for those watches with improved towards meeting the increasing demand for food [17,18]. timekeeping. Critics of modern genetic modification who During the history of traditional plant breeding, through to consider it to be imprecise, and capable of disturbing the current methods of genetic modification, a major motiva- natural genetic balance of organisms, should reflect on the tion has been to identify genes which confer characteristics considerable imprecision and unpredictability of mutation that are desirable in crops. breeding. This technique has, however, made a valuable contribution to plant breeding; induced mutations are To understand the relationship between modern methods found in the pedigrees of many crops that are well estab- of genetic modification and traditional plant breeding, it is lished in the human and animal food chain [27]. important to highlight a few comparisons. Induced polyploidy Wide hybridisation Induced polyploidy has similarly become well established Genes have traditionally been moved into crops from relat- in traditional plant breeding. The process uses colchicine, ed species, or genera. In some cases, this is by forced obtained from the autumn crocus (Colchicum autumnale). pollination and sexual hybridisation between plants that This natural plant extract is a potent mutagen and is capa- would not, or are very unlikely to, hybridise in nature. In ble of doubling the total number of chromosomes (a these cases, hand pollination followed by embryo culture chromosome mutation). Some forage grasses, for example, and sometimes ovary culture, is used to rescue hybrid have had their number of chromosomes doubled from 14 embryos that would otherwise degenerate and die to 28, a change from the diploid to the tetraploid state [28]. [16,19,20]. Those people who take a fundamentalist view Induced polyploidy, a fundamental genetic change result- that moving genes across natural sexual barriers is unac- ing in a doubling of the total amount of DNA in each plant ceptable, should be aware that this has been carried out in cell, is used in traditional plant breeding and the crop vari- plant breeding for many decades. eties obtained have been used over many decades for human and animal food, for example, titicale (wheat-rye Another feature of wide hybridisation is that unwanted hybrids), rye grasses and clovers. genes are often transferred along with the gene or genes of interest. In some cases, we may transfer between 1000 and The point of these examples from traditional plant breed- 4000 genes from the donor species. Because of the way ing is to illustrate the considerable lack of precision in genetic recombination works, it is usual to transfer a quar- techniques that are widely used and accepted in tradition- ter, a half, or even a whole chromosome from the donor al plant breeding, and that plant breeders have developed species, along with the one or few genes that control the testing, evaluation and selection procedures to eliminate important agricultural characteristic [21,22]. In the history plants with undesirable characteristics. A substantial of plant breeding, for example, wild potatoes have been amount of the abundant food supply that we now enjoy used as a source of genes to modify the potato crop. Wild when we trolley around our supermarket is a product, potatoes, which include relatives of the nightshade family, directly or indirectly, of these methods of crop improve- frequently contain high levels of toxic alkaloids [23]. ment. For those of us who have no personal experience of Those people concerned about the transfer of toxins into hunger it is difficult fully to appreciate the value of an ade- our crop plants, should note that this is possible in tradi- quate and reliable food supply. tional methods of breeding. Genetic modification breeding Similarly, wild oat species have been used as a source of In genetic modification breeding we usually introduce one mildew resistance for modifying the oat crop [24]. Wild or a few genes into a plant. The introduction of two genes oats are among the most important weeds in agriculture in into a wheat plant with about 80,000 genes is a change in the Public reactions and scientific responses to transgenic crops Dale 205

Table 2

Some of the questions considered during biosafety assessment.

• What is the function of the gene in the donor organism? • What is the effect of the introduced gene(s) on the modified plant? • Is there evidence of a change in allergenicity or toxicity? • Will there be non-target effects on friendly organisms within the environment? • Is there a change in the plant’s ability to persist in an agricultural habitat (weediness) or its invasiveness in natural habitats? • Can the introduced gene be transferred to other plants (e.g. by pollination) or organisms, and what would be the likely consequences?

genetic makeup of about 0.0025%. Some variables within comparable data are required or possible to produce from genetic modification breeding that cannot be controlled at mutagenesis breeding (or from most other traditional present are the number of transgene copies introduced and breeding procedures) where the changes are usually in their position on the chromosomes. In practice, biotechnol- unknown genes and may potentially involve chromosome ogists make many transgenic lines (e.g. 100 for each gene rearrangements or translocations. While I am a supporter of construct) and select those that have the desired number of the international regulatory process, there seems to be an transgene copies (one copy is usually preferred), along with inconsistency in that the full weight of regulatory oversight optimal levels and patterns of transgene expression through- falls on the products of genetic modification breeding out the plant, and stability of inheritance. while there is minimal comparable oversight of the products of traditional breeding. Another feature of genetically modified (GM) plants is that a selectable marker gene (often, an antibiotic resistance If we believe there is a need to ask questions about the gene) is used to select transgenic cells during the transfor- long term impact of herbicide tolerance or particular kinds mation process, and is therefore present in the GM crop. of insect resistance on agricultural practice, then it is illog- The use of antibiotic resistance marker genes for some ical to concentrate regulatory oversight on crops modified people is contentious, and various research programmes by one particular breeding method. In the broadening are studying ways to avoid or eliminate them. Extensive debate about the impact of agriculture on the wider envi- studies have concluded, however, that the use of certain ronment [32], it is important to take account of the effect antibiotic resistance genes (e.g. kanamycin resistance) pre- of all crops, whichever method of genetic improvement sent no enhanced risk to human health and the was used to produce them. environment [29,30]. Why is there public concern? Biosafety assessment I believe there are various reasons for the current concerns Because it is possible by genetic modification breeding to about the introduction of GM crops. introduce genes into crops from any class of living organism, there is international agreement that anyone wishing to Throughout the history of the application of technologies develop GM crops should go through a safety assessment there have been opponents; for example, following the process [31•]. In practice, therefore, all of the tests from con- introduction of the bicycle, the train, the car, immunisation ventional plant breeding are carried out, plus a substantial and blood transfusion. An increasing awareness of the biosafety assessment that considers potential impacts on potential of genetics in the 1930s led to debate and fright- human health and the environment (Table 2). This addi- ening scenarios of eugenics at that time [33]. There is tional assessment is a statutory requirement in most currently the propagation of a considerable amount of mis- countries (including the European Union [EU], USA and information and the use of deliberately frightening, Canada) and various organisations (e.g. Organisation for emotive language by some lobbying groups that are active- Economic Cooperation and Development [OECD], United ly against development of the technology [11,12,34]. Nations Environment Programme [UNEP]) are working to Terms like ‘genetic pollution’, ‘Frankenstein food’, are harmonise standards and criteria across the world. used deliberately to disturb people and, I suspect, by some as a ploy to try to increase market share of their products. An important feature of transgenic crops is that we can analyse them with a molecular precision that is impossible Some of the views expressed are blatantly anti-science. for characteristics modified by traditional plant breeding One of the major biases in the debate is that people often methods. This is a major advantage of transgenic plants concentrate on the issues that have gone tragically wrong but, perversely, because we are technically able to analyse (e.g. Salmonella and Escherichia coli food poisoning, bovine transgenes in detail (including their expression, their sta- spongiform encephalopathy [BSE] and thalidomide), but bility, and even their precise position in the plant genome), forget the successes; for example, the production of an the risk assessment procedure often requires abundant supply of food, and the control of diseases that a biotechnologists to provide much of these data. No generation ago were major killers (e.g. diphtheria, smallpox 206 Commentary

and polio). The immunisation of 93 million children against but the scientific questions asked during the risk assess- polio on one day (20th January 1996) in India [35] justified ment process are similar [31•]. I suggest the reasons for the a few short paragraphs in the middle pages of newspapers. difference in attitude between North America and Europe The successes become part of the wallpaper of life and we are as follows: only remember the inkspots. 1. The procedures within the regulatory process in the EU It is unfortunate that some members of the media seem to are more complicated. There are 15 member states, each believe that science is interesting only if it is scary and with their own specific decision-making process, even emotive. Certain journalists appear to be more interested though all states work under the same EU Directive in creating controversy and drama, rather than presenting (EEC/90/220) [39]; balanced information. Because of this, the debate is often unnecessarily polarised and adversarial. A debate between 2. The people in the US and the EU have a rather differ- the two extremes is rather like asking a socialist and a fas- ent relationship with food and there are variations in the cist to debate the finer points of democracy. Discussions of retail supply system. In the US, for example, supermarkets this kind often degenerate into slanging matches, and more frequently lease shelf space to the major brand name become the intellectual equivalent of a street brawl. suppliers, who largely determine what goes on those shelves. In the UK, at least, the supermarkets frequently There are also those who misrepresent the science and sci- stock their own brand foods, have a major influence on the entists. Mae-Wan Ho [36] argues that the “Genetic foods sold in their supermarket and are very responsive to Engineering Mindset is: firstly, genes determine characters customer preferences; in linear causal chain — one gene gives one function; sec- ondly, genes and genomes are not subject to 3. A particular difference between the UK and several environmental influence; thirdly, genes and genomes are other countries is that the UK has a relatively large propor- stable and unchanging; and finally, genes stay where they tion of its land in some form of agriculture (UK 71%, are put.” I have yet to identify a ‘Genetic Engineer’ any- France 55%, Germany 50%, USA 46%, Canada 8% [40]). where in the world who accepts these four points. I suggest Agricultural practice in the UK, therefore, has the potential that if they do have this ‘mindset’, they were not listening to have a greater influence on the wider environment. to their first-year undergraduate genetics lectures. If people in North America have difficulty in understand- In addition to my scientific research, I also give occasional ing the difference in ‘mindset’ between North America talks on genetic modification to lay-people (village societies, and the EU it may help to consider the following. Imagine consumer groups, etc.). The most frequent comment during that the USA were split into 15 geographical regions, (each question time is about choice. People often argue that they able to make independent decisions about the introduc- don’t understand the details of the science, but would like tion of GM crops) and the EU were to threaten the opportunity to choose between GM and non-modified fundamental damage to trade relations if the US popula- products. Arguably, from the general public’s point of view tion did not accept two GM crops produced on a large scale the introduction into the UK of the tomato puree containing in Europe [41]. GM tomatoes (by Zeneca), was a model for the way products should be offered to the consumer [37,38]. In this case, Challenges for the future tins of tomato puree were clearly labelled as being from GM One unfortunate feature of the current debate is that it has tomatoes and consumers were given a choice of puree from become especially polarised and political. There are very non-GM tomatoes, usually on the same supermarket shelf. important issues that need to be debated among people While acknowledging that the logistics of segregating mil- who are well informed about the science of plant breeding, lions of tonnes of GM and non-GM commodity crops (e.g. agricultural practice, ecology, and food and feed safety. We maize and soybean) across a very large North American need to have more debate about the impact of agriculture landmass presents some major challenges and accepting that on the wider environment, including wildlife biodiversity a thorough scientific risk assessment is a statutory require- [32]. There are also important challenges for agriculture ment before GM crops are marketed, it is difficult not to from the influence of gene patenting issues, business respect the layperson’s desire for choice. monopolies and intensifying international market forces.

Attitudes in North America and Europe The arguments between organic agriculturists and those It is interesting to reflect on why opinions over the use of wishing to grow GM crops need to be resolved [13,42]. GM crops are relatively relaxed in North America. Most of Organic farming can teach the rest of agriculture valuable the GM crops in the world are grown there and people are lessons about how to use management practices to have bet- consuming them with apparently minimal concerns. The ter control over pests, diseases, weeds and soil fertility [12]. regulatory processes in North America and the EU are Organic production in the UK is practised on only 0.5% of both carried out very carefully. There are some differences agricultural land [43], so it is important that farmers managing in the way the regulations operate in the two continents, the 99.5% should be able to grow a range of different crops, Public reactions and scientific responses to transgenic crops Dale 207

whichever breeding methods have been used to produce References and recommended reading them, to enable farmers to compete in world markets. Papers of particular interest, published within the annual period of review, have been highlighted as: Otherwise, Europe risks becoming a major importer (as is cur- • of special interest rently the case for many electrical goods), rather than a •• of outstanding interest producer of GM crops. GM crops have the potential to pro- 1. Gheysen G, Angenon G, Van Montagu M: Agrobacterium-mediated vide a valuable source of pest and disease resistant varieties plant transformation: a scientifically intriguing story with that will eventually find application in all forms of agriculture. significant applications. In Transgenic Plant Research. Edited by Lindsey K. Amsterdam: Harwood Academic Publishers; 1998:1-33. 2. 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