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2. Potential Environmental and Human Health Implications of Pest-Protected Plants
Pages 40-103

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From page 40...
... The bulk of the chapter discusses potential environmental and human health impacts of conventional and transgenic pest-protected plants, such as human toxicity and allergenicity, nontarget effects, hybridization with weedy relatives, and evolution of pest adaptation to pest-protected plants. Scientific data on the potential for adverse environmental and health effects are presented and discussed.
From page 41...
... which is expressed or changed as a result of genetic modification. The effects of gene flow or the effects on nontarget organisms could be considered potential hazards for ecological risk assessments.
From page 42...
... Because the fundamental elements of risk assessment, such as hazard identification, dose-response assessment, exposure assessment, and risk characterization, can also be applied to risk assessments for transgenic pest-protected plants, the committee found that Health and ecological risk assessments of transgenic pest-protected plants do not differ in principle from the assessment of other health and ecological risks. 2.2 REVIEW OF PREVIOUS NATIONAL ACADEMY OF SCIENCES AND NATIONAL RESEARCH COUNCIL REPORTS 2.2.1 Introduction of Recombinant DNA-engineered Organisms Into the Environment (1987)
From page 43...
... The 1987 NAS report noted that the risks associated with rDNAengineered organisms are "the same in kind" as those associated with unmodified organisms and organisms modified by other methods. The committee agrees with that statement for pest-protected plants in that both transgenic and conventional plants may pose certain risks and the resulting plant phenotypes are often similar.
From page 44...
... 44 GENETICALLY MODIFIED PEST-PROTECTED PLANTS: SCIENCE AND REGULATION The committee recognizes that the magnitude of the risk varies on a product by product basis. The committee also agrees with points 1 and 2 in the sense that the potential hazards and risks associated with the organisms produced by conventional and transgenic methods fall into the 2A molecular technique known as marker-assisted selection can speed the identification of polygenic or single-gene traits in the plant's own genome, and rapid advances in genomics are expected to speed the identification of additional single-gene resistance traits in plants and other organisms.
From page 45...
... The greater diversity of genes that can be transferred by transgenic methods, their enhanced effectiveness, and the ability to insert the same gene into many cultivated species have led to concerns about transgenic crops. Does the potential of transgenic methods to expand on the diversity of transferred genes mean that there is a greater chance for unintended risks from transgenic plants than those from conventionally bred plants?
From page 46...
... To expand on the general principles outlined above, NRC published a more detailed report on how genetically modified plants and microorganisms should be regulated for small-scale, experimental field tests (NRC 1989~. The recommendations proved useful and remain well-founded with regard to how federal agencies regulate field testing of genetically engineered organisms.
From page 47...
... To understand the rationale of current and future directions of transgenic breeding for pest-protection and to assess risks of transgenic pestprotected plants relative to those that may be posed by conventional pestprotected plants, this section reviews mechanisms of conventional and transgenic resistance to insects and pathogens. 2.3.1 Natural Pest-protection Mechanisms Preformed Chemical Defenses Plants constitutively produce a variety of antimicrobial or insecticidal chemicals that are known or suspected to provide pest-protection (Mansfield 1983; Rosenthal and Berenbaum 1991~.
From page 48...
... In this report, these pathogen-specific resistance genes will be referred to as race-specific R genes, or simply, R genes. The more general term, defensive genes, will be used to describe natural plant genes specifying antibiotic or insecticidal factors that have broad specificity.
From page 49...
... The "gene-forgene" concept was proposed to explain the interaction between a plant R gene and a pathogen avirulence gene, and this concept is used in agriculture to develop pest-protected crop varieties that are resistant to damage by pathogen races that have known virulence properties. A feature of race-specific R genes, and one of the major limitations associated with their use, is the occurrence of pathogen races that are unaffected by a given plant R gene; these can be pre-existing races that lack the corresponding avirulence genes or new races that have lost avirulence gene function.
From page 50...
... An important component of this wound-induced response is activation of genes that encode proteins, such as proteinase inhibitors, that have insecticidal activity. Proteinase inhibitors prevent digestion of plant material in the insect gut, and so result in starvation.
From page 51...
... The application of transgenic resistance should be most useful where natural conventional breeding has failed due to lack of resistance genes in sexually compatible plants or due to undesirable agronomic traits in conventional pest-protected crops. For example, the oat Pc-2 resistance gene which controls crown rust disease caused by the fungus Puccinia coronata is coinherited with a trait that confers sensitivity to an unrelated fungal pathogen, Cochliobolus victoriae, so it would not be useful to deploy this gene in oat cultivars by conventional breeding methods (Walton 1996~.
From page 52...
... The resistance can occur through a number of mechanisms. Expression of a normal or altered form of a pathogen protein in transgenic plants can disrupt the pathogen's normal pattern or timing of expression of that protein, or interfere with the interaction between a host and the pathogen.
From page 53...
... For example, constitutive or localized expression of a variety of genes that encode proteinase inhibitors, chitinases, and lectins in transgenic plants can provide protection against some chewing insects, sucking insects, or nematodes (Iohnson et al. 1989; Kramer and Muthukrishnan 1997; Rao et al.
From page 54...
... Development of strategies that enhance the effective life span, or durability, of transgenic pest-protection mechanisms is also of vital importance. 2.4 POTENTIAL HEALTH EFFECTS OF DIVERSE GENE PRODUCTS AND BREEDING METHODS Sections 2.1 and 2.2 discussed standard risk-assessment terminology for GMPP plants and the 1987 NAS principles.
From page 55...
... R genes for protection against pathogens are routinely transferred between plants by conventional breeding. There are no known toxic or nontarget effects of R gene products aside from their role in triggering localized and systemic defense responses in the presence of specific pathogens.
From page 56...
... It is reasonable to predict that manipulation of those pathways can enhance resistance to insects and pathogens. The known toxicity of many protective natural products to nontarget organisms, however, means that such strategies could pose a risk.
From page 57...
... New cultivars, regardless of how they were produced, could be tested for known or suspected toxicants and compared with established cultivars that are already being consumed. Pathogen-Der~ved Protective Genes Virus-derived transgenes Because viruses of edible plants are common components of the food supply and no associations between such viral infections and adverse health effects have emerged, transgenic plants that express parts of viral genomes are generally considered not to represent an important human health risk because there is little chance of exposure to a novel virus gene product.
From page 58...
... Therefore, genetic modification methods, both conventional and transgenic, are discussed below with regard to their potential for adding novel extraneous genes and their potential for causing unanticipated pleiotropic effects. Conventional Breeding Methods that Involve Sexual Hybridization The choice of parents used in the crosses and the mating structure of the plant species are important in determining the potential for inadvertent health effects associated with the progeny (hybrid, inbred line, or population)
From page 59...
... Interspecific crosses are usually between a cultivar and a wild species that has a pest-protective gene of interest. Inasmuch as most of the wild relative's genes are removed by backcrossing, with the exception of those genes linked to the selected protective gene (known as a linkage block)
From page 60...
... that remove most of one genus's genes from the commercial product. However, because of poor chromosome pairing, there is often little homologous recombination, and large linkage blocks of DNA are retained in the progeny (for example, the whole chromosome arms mentioned above)
From page 61...
... The reason for interest in somaclonal variation is that it increases the genetic variation in plants regenerated from tissue culture; one of the general procedures used to develop transgenic plants. Its potential for unfamiliar health effects would be similar to that of mutagenesis.
From page 62...
... It is important to point out, however, that these pleiotropic effects are not peculiar to transgenic plants. Crops resulting from conventional breeding and other nontransgenic methods can contain potentially hazardous concentrations of naturally occurring toxic compounds, as has been documented in new or established varieties.
From page 63...
... In the regulation of recently approved transgenic pest-protected plant products (that is plant products with Bt and viral coat proteins) , the emphasis has not been on detailed assessments of safety for humans or domestic animals.
From page 64...
... . In general, oral toxicity testing for Bt endotoxins is based on the presumption that there is unlikely to be a problem inasmuch as a number of Bt toxins have been widely used for many years in microbial sprays without human toxicity.
From page 65...
... However, the committee recognizes that it is often difficult to obtain enough plant-expressed protein; in these cases, the committee recommends that The EPA should provide clear, scientifically justifiable criteria for establishing biochemical and functional equivalency when registrants request permission to test non plant-expressed proteins in lieu of plantexpressed proteins. The strong likelihood that gene products currently found in commercial transgenic pest-protected plants are not allergens does not remove the need for a minimum of properly planned and executed tests.
From page 66...
... Furthermore, it is well established that allergenic proteins can be found in many food plants, of which some, such as soybeans and potatoes, have been genetically modified for pest-protection, and many others are or will be candidates for this type of genetic modification. Those two sources also summarize the problems in protein allergenicity testing.
From page 67...
... ) No \ Sequence Similarity /r I Stability to Digestion and Processing If any tests indicate potential allergenicity: Label as to Source Consult with Regulatory Agency FIGURE 2.1 Tests for Potential Allergenicity.
From page 68...
... 1999~. It is important to ask whether any such threats have resulted from more conventional genetic modification of agricultural crop plants (conventional pest-protected plants)
From page 69...
... , and therefore pleiotropic effects of the genetic modification cannot be monitored. If proper controls are used, feeding whole plants to the test animals might allow for the detection of potential toxicity due to pleiotropic effects.
From page 70...
... and Rizek 1974) , and the concentrations of these chemicals can be changed, either purposely or inadvertently, by conventional or transgenic genetic modifications.
From page 71...
... Overall increases in the concentrations of secondary plant chemicals in the total plant might cause toxic chemicals that are normally present only in trace amounts in edible parts to be increased to the point where they pose a toxic hazard. In some cases, genes transferred by conventional breeding can also change the distribution of secondary plant compounds among plant parts.
From page 72...
... show that allergens can be inadvertently changed during conventional breeding, and there is no substantial body of information on this possibility. There are some examples of assessments of endogenous allergens in transgenic plants (Burke and Fuchs 1995; Metcalfe et al.
From page 73...
... 2.6 POTENTIAL EFFECTS ON NONTARGET ORGANISMS In addition to human health concerns, there is concern that gene products of some transgenic and conventional plants may be toxic to nontarget species in the ecosystem. This section reviews and discusses relevant data on such potential nontarget effects of transgenic and conventional pest-protected plants.
From page 74...
... 1998~. However, a considerable number of studies have examined direct and indirect effects of conventional pest-protected crops and of wild host plants that differ in their pesticidal properties.
From page 75...
... , which are common in and along edges of corn fields in the midwestern United States where about half the population of US monarchs spend some of the summer (Wassenaar and Hobson 1998~. Milkweed is the only food of monarch
From page 76...
... obtained similar results when monarch larvae were placed on milkweed leaves that had been collected at the edges of Bt and non-Bt corn fields in Iowa and brought into the laboratory. Although both studies should be viewed as preliminary and actual
From page 77...
... Further field-based research is needed to determine whether dispersed Bt pollen could have detectable effects on the population dynamics of nontarget organisms. 2.6.3 Indirect Effects Studies in which predators were fed insects that developed on pestprotected cultivars have often produced adverse effects on the predator.
From page 78...
... Parasitoid populations in the chemically treated potato fields were, on the average, 58.4% lower than in Bt potato fields. Insecticidal treatment of potatoes to control Colorado potato beetles with conventional insecticides often results in secondary outbreaks of aphids because the aphids are released from biological control.
From page 79...
... This could result in lower biodiversity of species at higher trophic levels that depend on herbivorous insects as food. 2.6.4 Summary Conventional and transgenic pest-protected crops can adversely affect nontarget organisms through direct contact with or ingestion of the plant or pollen by the nontarget organisms and through indirect contact when the pest-protective substances (or their effects)
From page 80...
... The committee recommends that Criteria for evaluating the merit of commercializing a new transgenic pest-protected plant should include the anticipated impacts on nontarget organisms compared with those of currently used5 pest control techniques. 2.7 GENE FLOW FROM TRANSGENIC PEST-PROTECTED PLANTS Genes from one crop plant may be spread to other plants of the same or related species when pollen is transported by wind, bees, or other animal pollinators.
From page 81...
... A few examples of transgenic pest-protected plants from which the consequences of gene flow are serious enough to merit special attention with regard to the weediness of wild relatives are also highlighted. The committee also describes the extent of gene flow from transgenic crops to organically grown crops of the same species.
From page 82...
... 82 GENETICALLY MODIFIED PEST-PROTECTED PUS: SCIENCE ED ~GU~TION TABLE 2.1 Isolation distances required by USDA for producing foundation seed used for seed increase. Note that this is not a complete list of all crops Maximal Proportion Crop Speciesa Distance, it Contaiminated, %b No isolation required: Barley 0 0 05 Bean, field and garden 0 0.05 Broad bean 0 0.05 Cotton 0 0.03 Flax 0 0.05 Millet, selfed 0 0.05 Mung bean 0 0.10 Oat 0 0.02 Pea, field 0 0.50 Peanut 0 0.10 Soybean 0 0.10 Triticale 0 0 05 Wheat 0 0.50 Isolation Required: Alfalfa 600 0.10 Buckwheat 660 0.05 Clover, < 2 ha 600 0.10 Clover, > 2 ha 900 0.10 Corn 660 0.10 Crown vetch, < 2 ha 200 0.10 Crown vetch, > 2 ha 900 0.10 Grasses, cross-pollinated 900 0.10 Grasses, selfed 60 0.10 Lespedeza 10 0.10 Millet, cross-pollinated 1,320 0.005 Mustard 1,320 0.05 Okra 1,320 0.0 Onion 5,280 0.0 Pepper 200 0.0 Rape, cross-pollinated 1,320 0.05 Rape, selfed 660 0.05 Rice 10 0.05 Rye 660 0.05 Safflower 1,320 0.01 Sorghum 900 0.005 Sunflower 2,640 0.02 Tobacco 150 0.01 Tomato 200 0.0 Trefoil, birdsfoot 600 0.10 Vetch 10 0.10 Vetch, milk 600 0.05 Watermelon 2,640 0.0 aCommon name.
From page 83...
... 2.7.2 Crop-to-Wild Gene Flow The escape of novel resistance traits into free-living populations of wild relatives is often cited as an undesirable consequence of growing transgenic crops on a commercial scale (for example, Bergelson et al. in press; Ellstrand and Hoffman 1990; NRC 1989; Parker and Kareiva 1996; Raybould and Gray 1998; Rissler and Mellon 1996; Snow and MoranPalma 1997; Tiedje et al.
From page 84...
... Recently, weed scientists have redoubled their efforts to quantify genetic diversity in weed populations and to gain a better understanding of how weeds adapt to changing conditions. The commercialization of transgenic crops has provided added incentives for studies on crop-towild gene flow because some transgenic phenotypes have never occurred in wild relatives of certain crops.
From page 85...
... . In contrast, some cultivated species survive in feral populations or cross with wild plants of the same species (for example, carrot, sunflower, squash, rice, poplar, certain grasses, oilseed rape, radish, and beet)
From page 86...
... Lactuca saliva (lettuce) Cruciferae Brassica napus (oilseed rape:canola)
From page 87...
... Eventually, wild species will be able to acquire additional beneficial transgenes that are released in different cultivars, and the new traits could accumulate in wild populations. The ecological and evolutionary benefits conferred by crop genes that
From page 88...
... We know little about the extent to which insects and diseases limit wild, weedy populations that are sexually compatible with cultivated species. Critics of biotechnology argue that the spread of beneficial traits could quickly lead to the spread of weeds; advocates of transgenic crops maintain that this risk is small or nonexistent.
From page 89...
... For example, the spread of transgenes to wild relatives that are rare or endangered is sometimes considered as a potential ecological risk, especially in regions that are centers of diversity for crop relatives (for example, Rissler and Mellon 1996~. However, if a portion of wild species's genome is being exchanged for new genetic material by hybridization, this process will occur whether or not the crop is transgenic.
From page 90...
... Popularly known as "terminator" technology, this potential method of containment is highly controversial and has not yet been used commercially. In the future, biotechnology companies might develop transgenic plants with inducible pest resistance traits that require a chemical spray to be "turned on." If these systems work as predicted, resistance genes that spread to wild species would not be expressed in the wild species unless the spray was used, and therefore, would be extremely unlikely to contribute to the wild species' invasiveness.
From page 91...
... Gene flow into row crops can also occur via volunteer crop plants that survive to reproduce and via feral plants that start new populations, for example, when sunflower or oilseed rape seeds are inadvertently spilled along roadsides. Even for selfing species, total containment of crop genes is not considered to be feasible when seeds are distributed and grown on a commercial scale.
From page 92...
... The transfer of resistance traits to weedy relatives could potentially exacerbate weed problems, but such problems have not been observed or adequately studied. The committee recommends that Criteria for evaluating the merit of commercializing a new transgenic pest-protected plant should include whether gene flow to feral plants or wild relatives is likely to have a significant impact on these populations.
From page 93...
... , surveillance of pathogen activity and strain development, deployment of new pest-protected germplasm in response to emerging pest strains, and development and use of longer-lasting forms of pest-protection. With transgenic pestprotected plants that express a pest-protection gene transferred from another plant, the selective pressure for development of resistance-breaking strains should be qualitatively similar to the selective pressure associated with conventionally bred pest-protected plants.
From page 94...
... is well documented (Matthews 1991) , it is highly unlikely that functional coat proteins expressed in transgenic plants pose a significant risk of expansion of host range to new crop or non-crop hosts.
From page 95...
... Thus, it is highly unlikely that transgenic plants with general hyper susceptibility characteristics will pass through a breeding program to commercialization. 2.8.3 Summary In light of the above analysis, the committee found that Most virus-derived resistance genes are unlikely to present unusual or unmanageable problems that differ from those associated with traditional breeding for virus resistance.
From page 96...
... l991~. History also indicates that pests adapt more rapidly to some types of GMPP plants than to others (Lamberti et al.
From page 97...
... For the same reason, scientists investigating pest-resistance management tactics are reluctant to provide regulatory officials or farmers with exact predictions about how many years it will take for a specific pest to adapt to overcome a proposed resistance management plan. However, they can provide information on which of a number of approaches to development and deployment of transgenic and conventional pest-protected plants is likely to be most successful in decreasing the rate of pest evolution to adapt to those plants.
From page 98...
... , the chance that insects will have the proper gene combination to be fully adapted is further decreased compared to the case where only one toxin is produced by the plant. It also increases the efficiency with which refuge-produced insects can break up combinations of resistance genes from the few pests
From page 99...
... Much of the theory of resistance management for GMPP plants has been developed for diploid, sexually reproducing organisms (NRC 1986; Roush and Tabashnik 1990~. The theory is therefore only partially applicable to viruses, bacteria, and even a large group of insects that have different means of reproduction.
From page 100...
... 2.9.3 Future of Resistance Management for GMPP Plants EPA has been active in developing resistance management plans for Bt crops. It has developed an internal group of staff to work on the issue and has consulted formally and informally with researchers (Matter et al.
From page 101...
... A resistance management program could be developed in such a situation to ensure that adaptation does not evolve at a rate or in a manner that causes environmental, economic, or health problems. 2.9.4 Summary In light of the above discussion, the committee found that Evolution of pest strains that can overcome the pest-protection mechanisms of plants can have a number of potential environmental and health impacts.
From page 102...
... , and it should also begin to consider resistance management strategies for other transgenic pest-protected plants. Specifically, If a pest Protestant or its functional equivalent is providing effective pest control, and if growing a new transgenic pest-protected plant variety threatens the utility of the existing uses of the pest-protectant or its functional equivalent, implementation of resistance management practices for all uses should be encouraged (for example, Bt proteins used both in microbial sprays and in transgenic pest-protected plants)
From page 103...
... · If a pest protestant or its functional equivalent is providing effective pest control, and if growing a new transgenic pest-protected plant variety threatens the utility of existing uses of the pest Protestant or its functional equivalent, implementation of resistance management practices for all uses should be encouraged (for example, Bt proteins used both in microbial sprays and in transgenic pest-protected plants)


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