Assessing weediness of transgenic crops: industry plays plant ecologist

PERSPECTIVES Evaluating the petitions

Assessing weediness of transgenic industry plays plant ecologist Colin B. Purrington Joy Bergelson After years of experimentation and limited field testing of genetically modifled crop plants, biotechnology companies in many countries are now beginning to commercialize their transgenic products. This development has shlfted the focus of public concern to the procedures that governments employ in determining that a particular transgenlc crop poses no risk to the environment. In this article we discuss the information required by the US Animal and Plant Health Inspection Service (APHIS) in making this determination, and compare this with the data that have been called for by ecologists and the data presented by companies in their petitions for nonregulated status.

Colin Purrington and Joy Bergelson are at the Dept of Ecology and Evolution, University of Chicago, 1101 E.57th Street, Chicago, IL 60637, USA.

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n the USA, most transgenic crops are regulated by several government entities, but the greatest hurdle towards commercialization is the Department of Agriculture’s Animal and Plant Health Inspection Service (USDA APHIS). Successful commercialization depends upon the crop being completely removed from regulatory oversight -a determination that requires, among other things, proof that the transgenie crop is no more likely to generate a weed problem than its untransformed counterpart. Because the USA is poised to be a large exporter of biotechnology products, and because it is active in establishing biosafety regulations for developing countries’, the careful assessment of current procedures for deregulating transgenic crops in the USA is of general importance.

crops:

both the transformed and untransformed genotypes. In contrast to the freedom afforded by APHIS’ guidelines, the ecological literature is replete with recommendations about traits that should be measureds-5, although there is no clear understanding of which character or subset of characters can accurately predict weediness potential. Some of the characters most commonly discussed include seed production, competitive ability, seed dormancy, germination ability and pollen dispersal. There is a general consensus that we must measure the magnitude of these performance traits for the transgenic plant in question, rather than for related genotypes or species. There is further consensus that the reciprocal hybrids of crops and wild species must also be studied, even if sexually compatible relatives are rare or absent in the USA. These comparisons are necessary to evaluate the threat posed by the distribution of transgenic crops to foreign countries that contain wild relatives yet often lack even rudimentary laws governing importation of biotechnology product@.

Seed viability

0

Seed dormancy

0 Seed production

Seed dispersal

Inspection of Fig. 1 leads quickly to several conclusions. First is that few companies have presented quantitative data on differences between transgenic lines and nontransformed. oarental varieties. Considering that one of APHIS’ few guidelines is that such comparisons be performed, their rarity is astonishing. Second, a large fraction of experimental data is obtained from experiments that are critically flawed (for instance, they do not include the parental variety as a control). Consequently, investigators are usually unable to test the null hypothesis that plant performance is unchanged by the addition of a transgene. Third, there is a remarkable reliance on heuristic arguments. For example, several petitions take the position that weediness can be ascertained by examining the DNA sequence of the inserted fragment (not surprisingly, no weediness potential has been detected!). Finally, several performance characters were not even mentioned in many of the petitions. For instance, it is remarkable that petitions can be written and approved without the inclusion of even a claim (however unsubstantiated) that lifetime survivorship is not increased by the possession of a transgene. In addition to serious shortcomings of the content of the petitions, there are several issues that are typically ignored in discussions about biotechnology risk

Growth rate

Competitiveness

a Growth period

0 Geographic

0 Fitness of hybrids with wild species

range

0

0

Lifetime survivorship

Pollen performance

Clonal reproduction

Fitness of hybrids with other cultivars

0

Demonstrating non-weediness APHIS presents companies with the challenge of verifying that the ‘regulated article is unlikely to pose a greater plant pest risk than the unmodified plant from which it was derived’z. Little guidance is offered as to the data that are acceptable, although APHIS emphasizes that field testing is desirable and that relevant comparisons must involve 340

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Fig. 1. Approved petitions (as of 15 March 1995) for nonregulated status for transgenic crops, categorized for their treatment of 14 issues relating to performance of plants containing transgenes. Possible types of evidence are shown in four categories, those containing quantitative comparisons (based on experimental comparison of transgenic and nontransformed genotypes), imperfect comparisons (based on observations or flawed experiments), heuristic arguments (unsubstantiated suppositions that experimentally derived data are not needed), and those lacking any discussion of the issue. When present at all, discussions of hybrid fitness in the petitions were typically restricted to one or two characters; the figures relating to fitness of hybrids therefore substantially overestimate the attention paid to this issue. A// petitions provided by USDA APHIS.

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PERSPECTIVES assessment. One concern involves the tendency for companies to request that multiple transgenic lines be exempt from regulation. Although technically each transgenic line should be compared independently to the nontransformed control, companies generally compare controls to the aggregate of all transformed lines. This effectively increases the variance within the transgenic category and thereby decreases the probability of detecting a significant difference between the transformed and untransformed plants. This procedure obscures the fact that some lines outperform the control, a problem that is compounded when a company restricts experiments, as is often the case, to a subset of its transgenic lines. This sloppiness in accounting for individual transgenic lines plays down the importance of insertion site7 and the number of insertions8 in the performance of transgenie plants. APHIS,too, is apparently unconcerned with position effects, as shown by its rapid acceptance of additional transgenie lines after those in the original petition are deregulated. One company has already obtained approval for 10 additional lines in this manner. In general, petitions do not clarify whether plots contain homozygous plants or individuals segregating for the transgene. Clearly, petitions should describe data on homozygous and heterozygous forms of each transgenic line, as well as an indication of the expected zygosity of the crop when marketed. This information is needed because transgene expression level can vary between plants homozygous and heterozygous for the same transgeneg. Furthermore, such data will become even more critical if and when researchers produce crops with recessive transgenes. Similarly, there has been surprisingly little concern voiced that the transgenic plants discussed in the petitions are not always the plants that will eventually be commercialized. The inbred lines of original transformants are expected to have low fitness because of the deleterious mutations that are associated with transformation and regeneration of plantlets. Most petitions readily acknowledge this fact and, not surprisingly, have commenced breeding programs to remove these mutations through repeated backcrossing to the parental variety. In addition, companies attempt to breed the transgene into a variety of genetic backgrounds in the hopes of optimizing yield. Traditional breeding programs have found that a resistance trait can have highly variable effects when bred into multiple genetic backgroundslo, and there is evidence suggesting that breeding programs involving transgenes will encounter similar effects TREE

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Table 1. Transgenic crops approved for commercialization Crop

Altered trait

Company

APHIS petition no.

Approved

Flavr Savr’” tomato ZW-20 squash BXT” cotton Roundup Ready” soybean Laurate canola Fruit-ripening altered tomato BT potato

Ripening time Virus resistance Herbicide tolerance

Calgene Upjohn Calgene “Monsanto Calgene DNA Plant Technology Monsanto

P92-196-01 P92-204-01 P93-196-01 P93-258-01 P94-090-01 P94-228-01 P94-257-01

act Dee Feb May Sept Jan Mar

Oil profile Ripening time Insect resistance

(e.g. Monsanto Petition P93-258-01; see Table 1). It is important to note that attainment of nonregulated status allows companies and third-party seed corporations to engage freely in both backcrossing and hybridization programs. Finally, even when transgenic crops are shown to perform differently than untransformed crops in an agricultural setting, these differences might not be reflected in their relative invasiveness in natural habitats. This was recently illustrated in a comparison of experimental populations of resistant and susceptible thale cress (Arabidopsis thaliunu)~i. Even though re sistant plants produced substantially fewer seeds than susceptible plants in a common-garden experiment, no differences in invasiveness could be discerned. The lack of association between reproductive output and population growth rate was because these populations of A. thaliana were limited by interspecific competition, not seed production. That is, populations of resistant plants reached the same size as populations of susceptible plants despite a reduction in seed number. A similar, and striking, dependence of population growth rates on interspecific competition was also found in the PROSAMO trials of transgenic oil-seed rape (Brassicu nupus)l2. As Abbott4 has recently argued, we must first understand the factors limiting population size before we can hope to anticipate changes in invasiveness. Improving regulatory guidelines It is probable that most ecologists do not view the seven crops slated for commercialization as alarming ecological threats. However, an aim of many biotechnology companies is to produce transgenie organisms that have higher fitness under a broader range of environmental and biotic stresses, and inevitably, they will succeed in their goals. Accordingly, it may be wise to view today’s transgenic plants (largely crops) as practice organisms for the regulatory machinery that is being trusted to catch future transgenic plants (for instance, weeds for bioremediation projects) exhibiting clear potentials for weediness.

92 94 94 94 94 95 95

From this point of view, it is beneficial to assess the efficacy of current procedures for deregulation. It seems clear from Fig. 1 that both industry and government must improve their collection and interpretation of data. Improvement on the side of industry could be aided with the introduction of more specific guidelines by APHIS. It is less clear how to improve the regulations that frequently reflect the past influence of the President’s Council on Competitiveness, a powerful governmental entity charged with assuring that US companies are competitive in international marketsIs. President Clinton abolished the Council early in 1993, but it is difficult to predict how new governmental directives, particularly the planned reorganization of the USDA,will affect attempts at modifying existing statutes. With biotechnology as one of the hopes for US economic growth, there is likely to be resistance to the promulgation of stricter guidelines across the board. It is expected that organizations supporting and opposing stronger regulation will increase their efforts as the number of submitted petitions begins to grow. The most realistic means of handling this expected flood is through the establishment of guidelines that can efficiently concentrate oversight on those transgenic plants with high potential for weedinessi4J5. Such an outcome will necessarily involve cooperation among industry, government and the scientific community and require significant compromise from all. Acknowledgements We gratefully acknowledge the help provided by M.K. Peterson, USDA APHIS, in obtaining petitions and related information. Support for this research was provided in part by USDA grant No. 92-33120-8232 to J.B.

References 1 Chambers, J.A. (1993) in The USAIDLatin America

Caribbean

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pp. 6, US Agency for International Development 2 United States Department of Agriculture (1992) Fed. Regist. 57,53036-53043 3 Tiedje, J.M. eta/. (1989) Ecology 70,298-315 4 Abbott, R.J.(1994) Trends Ecol. Euol. 9,280-282

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5 Raybould, A.F. and Gray, A.J. (1994) Trends Ecol. Evol. 9,85-89 6

Wiegele, T.C. (1991) Biotechnology International Dimensions,

Relations:

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University of Florida Press 7 Meyer, P. and Heidmann, I. (1994) Mol. Gen. Genet. 243,390-399

8 Assaad, F.F.,Tucker, K.L. and Signer, E.R. (1993)

Plant Mol. Biol. 22,1067-1085

9 de Carvalho, F. et al. (1992) EMBO J. 11,2595-2602 10 Cooper, R.L. and Waranyuwat, A. (1985) 11 Bergelson, J. (1994) Ecology 75,249-252 12 Crawley, M.J., Hails, R.S.,Rees, M., Kohn, D. and Buxton, .I. (1993) Nature 363, 620-623 13 President’s Council on Competitiveness (1991) on National

Biotechnology

Policy,

to be written by a single author. The topics that are synthesized and reviewed demonstrate the need to understand and work across disciplines: marine ecology in general, and in polar areas in particular, must be understood in the context of geological The Biology of the Southern time, meteorology, and physical and chemiOcean cal oceanography. Not only that, but biologiby GA. Knox cal systems are inherently variable, and they must be understood through several levels Cambridge University Press, of reduction from evolution and systematics Studies in Polar Research, 1994. to ecosystems to populations to behavior, f90.00/$130.00 hbk (xiv + 444 pages) physiology and biochemistry. Separate sysISBN 0 52132211 1 tems, such as microbial, phytoplankton, he Antarctic Treaty and the determi- krill, benthos, are very different from each nation of scientists to break free from other, but they, also, are interdependent. national politics has made the Antarctic a Thus general understanding must be built unique beacon for scientific cooperation on real integration. Because the science among cold war powers and others since leaders have understood this, all levels the late 1950s. With this spirit of cooper- and systems were funded and studied. It ation, the past four decades have included is the successful integration of all of these an unprecedented scientific investigation of extremely diverse and fast moving subthe continent and its surrounding ocean by jects that makes this book such a useful tens of thousands of well-equipped scientists review. working in difficult and sometimes dangerThe book reviews the evolution and ous conditions. Because this scientific as- changing climate of the southern ocean as sault was based on a remarkably broad and well as the physical driving factors, ocean excellent foundation laid by many heroic, circulation and nutrient dynamics. It then turn of the century expeditions, there has moves into reviews of subjects such as prialways been a focus and direction to the mary production, sea-ice microbial comresearch. Coupled with the spirit of open munities, zooplankton, krill, nekton, each communication and cooperation, this has of several groups of vertebrates, special led to remarkable success. This book communities, ecosystem dynamics and summarizes the accomplishments of the management. Readers will find each chap marine biologists, who represent the largest ter remarkably multidisciplinary. The zoo and perhaps the most multidisciplinary plankton, krill and nekton chapters have particular ecosystem importance, are up group. An interesting observation of this huge to date and are well presented. The seal, international scientific effort is that it has whale and bird chapters are unusually been choreographed by a surprisingly small broad summaries ranging from physiology number of prescient leaders including George to foraging and reproductive behavior, pre Llano, Richard Laws, Cotthilf Hempel, Sayed sented from very appropriate evolutionary El Sayed and George Knox. Each has differ- perspectives. It is unusual for a general book ent styles and different national political to do such a good job synthesizing bio realities, but the unifying theme is that these chemistry and energetics with ecosystem strong and capable managers and leaders of dynamics and behavior of both predator this wonderfully successful scientific legacy and prey into broad understanding of the are professional biologists, not physicists or foraging biology of sea birds, seals and lawyers or political hacks. Not only are they whales. skilled scientific managers and excellent biThe last section of the book focuses ologists, they have each written or edited on ecosystem approaches to specific sysmassive and insightful reviews such as this tems. This is based on the more classical one by Professor Knox. oceanographic data, such as currents, nuThe Biology of the Southern Ocean may trients, primary and secondary productivity, be the best synthesis of Antarctic research sedimentation and resuspension, decompo-

International research at its best

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15 Colwell, R.K. (1988) Safety Assurance

Crop Sci. 25,90-92

Report

US Department of Commerce 14 Simonsen, L. and Levin, B.R. (1988) Trends

for Environmental Intmductions of Genetically-Engineered Organisms

(Vol. C18) (NATO ASI Series) (Fisksel, J. and Covello, V.T., eds), pp. 163-180, Springer-Verlag

sition, as they apply to particular communities such as the benthos, sea-ice and iceshelf systems. As expected from a longtime player in the international political arena, Knox summarizes some of the conservation agreements, particularly those of the Commission on the Conservation of Antarctic Marine Living Resources (CCAMLR). The latter represents a high point in international conservation law, yet some of its objectives such as management based on multispecies models are yet to be implemented. Certainly the broad-scale overview emphasized in this book is most appropriate. An epilogue summarizes both the conceptual advances of these few decades of research and a few of the management prob lems. In addition, Knox reviews the need to understand the many effects of increases in the levels of UV radiation. Readers of this book may contemplate future directions, especially those attendant to global warming and its effects on sea ice. Ice breaker capabilities surely will open new research in the sea-ice zone, as will remote equipment ranging from ocean@ graphic monitoring to undersea exploration to enhanced satellite technology. Increased use of Lagrangian drifters will help define currents and advective processes. With the increased number of countries participating in Antarctic research, there will be more shore-based research, and with proper coordination, this may help make it possible to approach large-scale issues such as biogeographic questions of dispersal and recruitment or regional forcing functions of populations or ecosystem. The international Scientific Committee of Antarctic Research has several groups of specialists including a Coastal and Shelf Zone Systems Group that is coordinating shore-based research by standardizing techniques and focusing on specific questions and species. Such coordinated largescale research represents the best hope of separating real global changes from environmental noise. In all cases, this synthetic book offers valuable background information. Paul K. Dayton Scripps Institution of Oceanography, La Jolla, CA 92093-0201, USA TREE

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