August 11, 2011 | 46
By the turn of the century, the number of people on Earth is expected to increase from the current 6.7 billion to 10 billion. How can we feed the growing population without further degrading the environment?
Because the amount of land and water is limited, it is no longer possible to simply expand farmland to produce more food. Instead, increased food production must largely take place on the same land area, while using less water. Compounding the challenges facing agricultural production are the predicted effects of climate change: flooding in some places, droughts in others and new pests and disease outbreaks.
Thus, an important goal for the US and other countries is to develop more effective land and water use policies, improved integrated pest management approaches, reduce harmful inputs, and create new crop varieties tolerant of diverse stresses.
These strategies must be evaluated in light of their environmental, economic, and social impacts—the three pillars of sustainable agriculture (Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability and National Research Council 2010).
WHAT ARE GENETICALLY ENGINEERED CROPS?
Genetic engineering differs from conventional methods of genetic modiﬁcation in two major ways: (1) genetic engineering introduces one or a few well-characterized genes into a plant species and (2) genetic engineering can introduce genes from any species into a plant. In contrast, most conventional methods of genetic modiﬁcation used to create new varieties (e.g., artiﬁcial selection, forced interspeciﬁc transfer, random mutagenesis, marker-assisted selection, and grafting of two species, etc.) introduce many uncharacterized genes into the same species. Conventional modiﬁcation can in some cases transfer genes between species, such as wheat and rye or barley and rye.
In 2008, the most recent year for which statistics are available, 30 genetically engineered crops were grown on almost 300 million acres in 25 countries (nearly the size of the state of Alaska), 15 of which were developing countries (James 2009). By 2015, 120 genetically engineered crops (including potato and rice) are expected to be cultivated worldwide (Stein and Rodriguez-Cerezo 2009). Half of the increase will be crops designed for domestic markets from national technology providers in Asia and Latin America.
SAFETY ASSESSMENT OF GENETICALLY ENGINEERED CROPS
There is broad scientiﬁc consensus that genetically engineered crops currently on the market are safe to eat. After 14 years of cultivation and a cumulative total of 2 billion acres planted, no adverse health or environmental effects have resulted from commercialization of genetically engineered crops (Board on Agriculture and Natural Resources, Committee on Environmental Impacts Associated with Commercialization of Transgenic Plants, National Research Council and Division on Earth and Life Studies 2002). Both the U.S. National Research Council and the Joint Research Centre (the European Union’s scientiﬁc and technical research laboratory and an integral part of the European Commission) have concluded that there is a comprehensive body of knowledge that adequately addresses the food safety issue of genetically engineered crops (Committee on Identifying and Assessing Unintended Effects of Genetically Engineered Foods on Human Health and National Research Council 2004; European Commission Joint Research Centre 2008).
These and other recent reports conclude that the processes of genetic engineering and conventional breeding are no different in terms of unintended consequences to human health and the environment (European Commission Directorate-General for Research and Innovation 2010). This is not to say that every new variety will be as benign as the crops currently on the market. This is because each new plant variety (whether it is developed through genetic engineering or conventional approaches of genetic modiﬁcation) carries a risk of unintended consequences. Whereas each new genetically engineered crop variety is assessed on a case-bycase basis by three governmental agencies, conventional crops are not regulated by these agencies.
Still, to date, compounds with harmful effects on humans or animals have been documented only in foods developed through conventional breeding approaches. For example, conventional breeders selected a celery variety with relatively high amounts of psoralens to deter insect predators that damage the plant. Some farm workers who harvested such celery developed a severe skin rash—an unintended consequence of this breeding strategy (Committee on Identifying and Assessing Unintended Effects of Genetically Engineered Foods on Human Health and National Research Council 2004).
“A truly extraordinary variety of alternatives to the chemical control of insects is available. Some are already in use and have achieved brilliant success. Others are in the stage of laboratory testing. Still others are little more than ideas in the minds of imaginative scientists, waiting for the opportunity to put them to the test. All have this in common: they are biological solutions, based on the understanding of the living organisms they seek to control and of the whole fabric of life to which these organisms belong. Specialists representing various areas of the vast ﬁeld of biology are contributing—entomologists, pathologists, geneticists, physiologists, biochemists, ecologists—all pouring their knowledge and their creative inspirations into the formation of a new science of biotic controls.” (Carson 1962, p. 278)
In the 1960s, the biologist Rachel Carson brought the harmful environmental and human health impacts resulting from overuse or misuse of some insecticides to the attention of the wider public. Even today, thousands of pesticide poisonings are reported each year (1200 illnesses related to pesticide poisoning in California, 300,000 pesticide-related deaths globally).
This is one reason some of the ﬁrst genetically engineered crops were designed to reduce reliance on sprays of broad-spectrum insecticides for pest control. Corn and cotton have been genetically engineered to produce proteins from the soil bacteria Bacillus thuringiensis (Bt) that kill some key caterpillar and beetle pests of these crops. Bt toxins cause little or no harm to most beneﬁcial insects, wildlife, and people (Mendelsohn et al. 2003).
Bt toxins kill susceptible insects when they eat Bt crops. This means that Bt crops are especially useful for controlling pests that feed inside plants and that cannot be killed readily by sprays, such as the European corn borer (Ostrinia nubilalis), which bores into stems, and the pink bollworm (Pectinophora gossypiella), which bores into bolls of cotton.
First commercialized in 1996, Bt crops are the second most widely planted type of transgenic crop. Bt toxins in sprayable formulations were used for insect control long before Bt crops were developed and are still used extensively by organic growers and others. The long-term history of the use of Bt sprays allowed the Environmental Protection Agency and the Food and Drug Administration to consider decades of human exposure in assessing human safety before approving Bt crops for commercial use. In addition, numerous toxicity and allergenicity tests were conducted on many different kinds of naturally occurring Bt toxins. These tests and the history of spraying Bt toxins on food crops led to the conclusion that Bt corn is as safe as its conventional counterpart and therefore would not adversely affect human and animal health or the environment (European Food Safety Authority 2004).
Planting of Bt crops has resulted in the application of fewer pounds of chemical insecticides and thereby has provided environmental and economic beneﬁts that are key to sustainable agricultural production. In Arizona, where an integrated pest management program for Bt cotton continues to be effective, growers reduced insecticide use by 70% and saved .$200 million from 1996 to 2008 (Naranjo and Ellsworth 2009).
A recent study indicates that the economic beneﬁts resulting from Bt corn are not limited to growers of the genetically engineered crop (Hutchison et al. 2010). In 2009, Bt corn was planted on .22.2 million hectares, constituting 63% of the U.S. crop. For growers of corn in Illinois, Minnesota, and Wisconsin, cumulative beneﬁts over 14 years are an estimated $3.2 billion. Importantly, $2.4 billion of this total beneﬁt accrued to non-Bt corn (Hutchison et al. 2010). This is because area-wide suppression of the primary pest, O. nubilalis, reduced damage to non-Bt corn. Comparable estimates for Iowa and Nebraska are $3.6 billion in total, with $1.9 billion for non-Bt corn. These data conﬁrm the trend seen in some earlier studies indicating that communal beneﬁts are sometimes associated with planting of Bt crops (Carriere et al. 2003; Wu et al. 2008; Tabashnik 2010).
Planting of Bt crops has also supported another important goal of sustainable agriculture: increased biological diversity. An analysis of 42 ﬁeld experiments indicates that nontarget invertebrates (i.e., insects, spiders, mites, and related species that are not pests targeted by Bt crops) were more abundant in Bt cotton and Bt corn ﬁelds than in conventional ﬁelds managed with insecticides (Marvier et al. 2007). The conclusion that growing Bt crops promotes biodiversity assumes a baseline condition of insecticide treatments, which applies to 23% of corn acreage and 71% of cotton acreage in the United States in 2005 (Marvier et al. 2007).
Beneﬁts of Bt crops have also been well-documented in less-developed countries. For example, Chinese and Indian farmers growing genetically engineered cotton or rice were able to dramatically reduce their use of insecticides (Huang et al. 2002, 2005; Qaim and Zilberman 2003; Bennett et al. 2006). In a study of precommercialization use of genetically engineered rice in China, these reductions were accompanied by a decrease in insecticide-related injuries (Huang et al. 2005).
Although Bt cotton is effective in reducing cotton bollworm outbreaks in China other pests that are not killed by Bt cotton are increasingly problematic (Wu Review 13et al. 2008; Lu et al. 2010). These results conﬁrm the need to integrate Bt crops with other pest control tactics (Tabashnik et al.
2010). In Arizona, such an integrated pest management (IPM) approach has been implemented (Naranjo and Ellsworth 2009). In Arizona’s cotton IPM system, key pests not controlled by Bt cotton are managed with limited use of narrow-spectrum insecticides that promote conservation of beneﬁcial insects (Naranjo and Ellsworth 2009). Mirids such as the Lygus bug (Lygus hesperus) are controlled with a feeding inhibitor, and the sweet potato whiteﬂy (Bemisia tabaci) is controlled with insect growth regulators (Naranjo and Ellsworth 2009).
One limitation of using any insecticide, whether it is organic, synthetic, or genetically engineered, is that insects can evolve resistance to it. For example, one crop pest, the diamondback moth (Plutella xylostella), has evolved resistance to Bt toxins. This resistance occurred in response to repeated sprays of Bt toxins to control this pest on conventional (nongenetically engineered) vegetable crops (Tabashnik 1994).
These results underscore a well-known paradigm in agriculture: pest resistance will evolve is the selection pressure is high. Why then, have most Bt crops remained effective against most pests for more than a decade (Tabashnik et al. 2008; Carriere et al. 2010)? The answer is genetic diversity. The inclusion in farmers fields of crop plants that do not make Bt toxins has helped to delay evolution of pest resistance to Bt crops (Carriere et al. 2010).
In cases where insect resistance to Bt crops has evolved, one or more conditions of this crop diversity strategy have not been met. For example, failure to provide adequate refuges of non-Bt cotton appears to have hastened resistance of pink bollworm in India (Bagla 2010). In contrast, Arizona cotton growers complied with this strategy from 1996 to 2005, and no increase in pink bollworm resistance occurred (Tabashnik et al. 2010).
In the United States, Bt cotton producing only Cry1Ac is no longer registered and has been replaced primarily by Bt cotton that produces two toxins (Carriere et al. 2010). More generally, most newer cultivars of Bt cotton and Bt corn produce two or more toxins. These multitoxin Bt crops are designed to help delay resistance an to kill a broader spectrum of insect pests (Carriere et al. 2010). For example, a new type of Bt corn produces ﬁve Bt toxins—three that kill caterpillars and two that kill beetles (Dow Agrosciences 2009).
Despite the success of the crop diversity strategy in delaying insect resistance to Bt crops, this approach has limitations, including the fact that not all farmers will comply. An alternative strategy entails release of sterile insects to mate with resistant insects (Tabashnik et al. 2010). Incorporation of this strategy in a multi-tactic eradication program in Arizona from 2006 to 2009 reduced pink bollworm abundance by 99%, while eliminating insecticide sprays against this pest. The success of such creative multidisciplinary integrated approaches, involving entomologists, geneticists, physiologists, biochemists, and ecologists, provides a roadmap for the future of agricultural production and attests to the foresight of Rachel Carson.
African Agricultural Technology Foundation, 2010 Scientists prepare for conﬁned ﬁeld trials of life-saving drought-tolerant transgenic maize. African Agricultural Technology Foundation (AATF), Nairobi, Kenya. (http://www.aatf-africa.org/userﬁles/PressRelease-WEMA-CFT.pdf).
Arcadia Biosciences, 2010 Nitrogen use efﬁcient crops. Available at http://www.arcadiabio.com/nitrogen.php.
Bennett, R. M., U. S. Kambhampati, S. Morse and Y. Ismael, 2006 Farm-level economic performance of genetically modiﬁed cotton in Maharashtra, India. Rev. Agric. Econ. 28: 59–71.
Bagla, P., 2010 Hardy cotton-munching pests are latest blow to GM crops. Science 327: 1439.
Board on Agriculture and Natural Resources, Committee on Environmental Impacts Associated with Commercialization of Transgenic Plants, National Research Council and Division on Earth and Life Studies (Editors), 2002 Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation. National Academies Press, Washington, DC.
Borlaug, N. E., 2008 Stem rust never sleeps. The New York Times, April 26, 2008 (http://www.nytimes.com/2008/04/26/opinion/26borlaug.html).
Brookes, G., and P. Barfoot, 2006 Global impact of biotech crops: socio-economic and environmental effects in the ﬁrst ten years of commercial use. AgBio Forum 9:139–151.
Burney, J. A., S. J. Davis and D. B. Lobell, 2010 Greenhouse gas mitigation by agricultural intensiﬁcation. Proc. Natl. Acad. Sci. USA 107: 12052–12057.
Carpenter, J. E., 2010 Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nat. Biotechnol. 28: 319–321.
Carriere, Y., C. Ellers-Kirk, M. Sisterson, L. Antilla, M. Whitlow et al., 2003 Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. USA 100: 1519–1523.
Carriere, Y., D. W. Crowder and B. E. Tabashnik, 2010 Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3: 561–573.
Carson, R., 1962 Silent Spring. Houghton Mifﬂin, Boston.
Cattaneo, M. G., C. Yafuso, C. Schmidt, C.-Y. Huang, M. Rahman et al., 2006 Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use and yield. Proc. Natl. Acad. Sci. USA 103: 7571–7576.
Committee on Identifying and Assessing Unintended Effects of Genetically Engineered Foods on Human Health, and National Research Council (Editors), 2004 Safety of Genetically Engineered Foods: Approaches to Assessing Unintended Health Effects. National Academies Press, Washington, DC.
Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability, and National Research Council (Editors), 2010 Impact of Genetically Engineered Crops on Farm Sustainability in the United States. National Academies Press, Washington, DC.
Crickmore, N. 2011 Bacillus thuringiensis toxin nomenclature. Available at http://www.lifesci.sussex.ac.uk/home/Neil_Crickmore/Bt/
Deacon, J. The Microbial World: Bacillus thuringiensis, edited by Institute of Cell and Molecular Biology. Archival. University of Edinburgh, Edinburgh, UK (http://www.biology.ed.ac.uk/research/groups/jdeacon/microbes/bt.htm).
Dhlamini, Z., C. Spillane, J. P. Moss, J. Ruane, N. Urquia et al., 2005 Status of Research and Application of Crop Biotechnologies in Developing Countries. Food and Agriculture Oganization of the United Nations Natural Resources Management and Environment Department. Rome, Italy.
Dow AgroSciences, 2009 SmartStax TM: leading through technology, Available at http://www.dowagro.com/science/product_updates/smartstax.htm.
European Commission Directorate-General for Research, 2010 EUR 24473 – A Decade of EU-Funded GMO Research 2001–2010. European Commission, Communication Unit, Brussels, Belgium.
European Commission Joint Research Centre, 2008 Scientiﬁc and Technical Contribution to the Development of an Overall Health Strategy in the Area of GMOs. European Commission, EU Publications, Luxembourg.
European Food Safety Authority, 2004 Opinion of the Scientiﬁc Panel on Genetically Modiﬁed Organisms. EFSA Journal, 1–25.
Farrell, A. E., R. J. Plevin, B. T. Turner, A. D. Jones, M. O’Hare et al., 2006 Ethanol can contribute to energy and environmental goals. Science 311: 506–508.
Fernandez-Cornejo, J., and M. Caswell, 2006 The ﬁrst decade of genetically engineered crops in the United States, pp. 1–30 in Economic Information Bulletin, edited by United States Department of Agriculture Economic Research Service. USDA, Washington, DC.
Fernandez-Cornejo, J., and W. D. McBride, 2002 Adoption of bioengineered crops, p. 67 in U.S. Department of Agriculture Agricultural Economic Report No. AER810. U.S. Department of Agriculture, Washington, DC.
Golden Rice Project, 2010 Golden Rice is part of the solution: biofortiﬁed rice as a contribution to the alleviation of life-threatening micronutrient deﬁciencies in developing countries. Available at http://Goldenrice.org.
Green, R. E., S. J. Cornell, J. P. W. Scharlemann and A. Balmford, 2005 Farming and the fate of wild nature. Science 307: 550–555.
Gregory, P. J., S. N. Johnson, A. C. Newton and J. S. I. Ingram, 2009 Integrating pests and pathogens into the climate change/ food security debate. J. Exp. Bot. 60: 2827–2838.
Huang, J., S. Rozelle, C. Pray and Q. Wang, 2002 Plant biotechnology in China. Science 295: 674–676.
Huang, J., R. Hu, S. Rozelle and C. Pray, 2005 Insect-resistant GM rice in farmers’ ﬁelds: assessing productivity and health effects in China. Science 308: 688–690.
Humphrey, J. H., K. P. West, Jr. and A. Sommer, 1992 Vitamin A deﬁciency and attributable mortality among under-5-year-olds. Bull. World Health Organ. 70: 225–232.
Hutchison, W. D., E. C. Burkness, P. D. Mitchell, R. D. Moon, T. W. Leslie et al., 2010 Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330: 222–225.
Intergovernmental Panel on Climate Change, 2007 Climate Change 2007: Impacts, Adaptation and Vulnerability. Cambridge University Press, Cambridge, UK.
James, C., 2009 Global Status of Commercialized Biotech/GM Crops. International SeCarriere, Y., D. W. Crowder and B. E. Tabashnik, 2010 Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3: 561–573.
Lobell, D. B., M. B. Burke, C. Tebaldi, M. D. Mastrandrea, W. P. Falcon et al., 2008 Prioritizing climate change adaptation needs for food security in 2030. Science 319: 607–610.
Lu, Y., K. Wu, Y. Jiang, B. Xia, P. Li et al., 2010 Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328: 1151–1154.
Marin, D. H., R. A. Romero, M. Guzman and T. B. Sutton, 2003 Black Sigatoka: an increasing threat to banana cultivation. Plant Dis. 87: 208–222.
Marvier, M., C. McCreedy, J. Regetz and P. Kareiva, 2007 A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316: 1475–1477.
McHughen, A., and R. Wager, 2010 Popular misconceptions: agricultural biotechnology. New Biotechnol. 27: 724–728.
Mendelsohn, M., J. Kough, Z. Vaituzis and K. Matthews, 2003 Are Bt crops safe? Nature Biotechnol. 21: 1003–1009.
Naranjo, S. E., and P. C. Ellsworth, 2009 Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag. Sci. 65: 1267–1286.
Naylor, R., W. Falcon and C. Fowler, 2007 The conservation of global crop genetic resources in the face of climate change. Bellagio Conference sponsored by the Rockefeller Foundation. Bellagio, Italy. Available at http://www.croptrust.org/documents/WebPDF/Bellagio_ﬁnal1.pdf.
Peed, M., 2011 We have no bananas. The New Yorker, pp. 28–34.
Potrykus, I., 2010 Regulation must be revolutionized. Nature 466: 561.
Powell-Abel, P., R. S. Nelson, B. De, N. Hoffmann, S. G. Rogers et al., 1986 Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232: 738–743.
Qaim, M., and D. Zilberman, 2003 Yield effects of genetically modiﬁed crops in developing countries. Science 299: 900–902.
Qaim, M., A. Subramanian and P. Sadashivappa, 2010 Socioeconomic impacts of Bt (Bacillus thuringiensis) cotton. Biotechnol. Agric. For. 65: 221–224.
Ronald, P., and R. Adamchak, 2008 Tomorrow’s Table: Organic Farming, Genetics and the Future of Food. Oxford University Press, New York.
Royal Society, T., 2009 Reaping the Beneﬁts: Science and the Sustainable Intensiﬁcation of Global Agriculture. The Royal Society, London.
Schlenker, W., and M. J. Roberts, 2009 Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change. Proc. Natl. Acad. Sci
Seo, Y. S., M. S. Chern, L. E. Bartley, T. E. Richter, M. Han et al., 2011 Towards a rice stress response interactome. PloS Genetics (in press).
Somerville, C., and J. Briscoe, 2001 Genetic engineering and water. Science. 292: 2217.
Steffenson, B., B. Alonso and P. Lemaux, 2011 Combating the threat of African stem rust. Podcast of the Cooperative Extension System online interactive learning environment. Available at http://www.extension.org/pages/32536/combating-the-threat-ofafrican-stem-rust-podcast.
Stein, A. J., and E. Rodriguez-Cerezo, 2009 The global pipeline of new GM crops: implications of asynchronous approval for international trade, pp. 1–114 in JRC Scientiﬁc and Technical Reports, edited by Joint Research Centre European Commission,
Institute for Prospective Technological Studies. Joint Research Centre, Institute for Prospective Technological Studies, Seville, Spain.
Stein, A. J., H. P. S. Sachdev and M. Qaim, 2006 Potential impact and cost-effectiveness of Golden Rice. Nat. Biotechnol. 24: 1200–1201.
Stein, A. J., H. P. S. Sachdev and M. Qaim, 2008 Genetic engineering for the poor: Golden Rice and public health in India. World Dev. 36(1): 144–158.
Storer, N. P., J M. Babcock, M. Schlenz, T. Meade, G. D. Thompson et al., 2010 Discovery and characterization of ﬁeld resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Entomol. Soc. Am. 103: 1031.
Strandberg, B., and M. B. Pederson, 2002 Biodiversity of Glyphosate Tolerant Fodder Beet Fields, edited by National Environmental Research Institute. NERI Technical Report 410. Silkeborg, Sweden.
Studholme, D. J., E. Kemen, D. MacLean, S. Schornack, V. Aritua et al., 2010 Genome-wide sequencing data reveals virulence factors implicated in banana Xanthomonas wilt. FEMS Microbiol.
Lett. 310: 182–192.
Tabashnik, B. E., 1994 Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39: 47–79.
Tabashnik, B. E., 2010 Communal beneﬁts of transgenic corn. Science 330: 189–190.
Tabashnik, B., A. J. Gassman, D. W. Crowder and Y. Carriere, 2008 Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26: 199–202.
Tabashnik, B. E., M. S. Sisterson, P. C. Ellsworth, T. J. Dennehy, L. Antilla et al., 2010 Suppressing resistance to Bt cotton with sterile insect releases. Nat. Biotechnol. 28: 1304–1307.
Tang, G., J. Qin, G. G. Dolnikowski, R. M. Russell and M. A. Grusak, 2009 Golden Rice is an effective source of Vitamin A. Am. J. Clin. Nutr. 89: 1776–1783.
Tripathi, L., M. Mwangi, S. Abele, V. Aritua, W. K. Tushemereirwe et al., 2009 Xanthomonas wilt: a threat to banana production in East and Central Africa. Plant Dis. 93: 440–451.
Tripathi, S., J. Suzuki and D. Gonsalves, 2006 Development of genetically engineered resistant papaya for papaya ringspot virus in a timely manner: a comprehensive and successful approach, pp. 197–240 in Methods in Molecular Biology, Vol. 354: Plant–Pathogen Interactions: Methods and Protocols, edited by P. C. Ronald. Humana Press, Totowa, NJ.
United Nations Environment Programme, 2002 State of the environment and policy retrospective: 1972–2002, pp. 1–30. in Global Environment Outlook 3, edited by United Nations Environment Programme. United Nations, New York.
U.S. Department of Agriculture Animal and Plant Health Inspection Service, 2009 HoneySweet plum trees: a transgenic answer to the plum pox problem. U.S. Department of Agriculture Animal and Plant Health Inspection Service, Washington DC (http://www.ars.usda.gov/is/br/plumpox/).
U.S. Department of Agriculture Animal and Plant Health Inspection Service, 2010 USDA announces ﬁnal environmental impact statement for genetically engineered alfalfa. U.S. Department of Agriculture, Washington, DC(http://www.aphis.usda.gov/biotech
U.S. Environmental Protection Agency, 1983 Chemical Information Fact Sheet Number 09: Diuron, pp. 9–11. Ofﬁce of Pesticides and Toxic Substances, Washington, DC.
U.S. Environmental Protection Agency, 1988 Health Advisory Summary: Diuron, pp. 9–33. Ofﬁce of Drinking Water, Washington, DC.
Vorosmarty, C. J., P. Green, J. Salisbury and R. B. Lammers, 2000 Global water resources: vulnerability from climate change and population growth. Science 289: 284–288.
Waggoner, P. E., 1995 How much land can ten billion people spare for nature? Does technology make a difference? Technol. Soc. 17:17–34.
Wang, S., D. R. Just and P. Pinstrup-Anderson, 2008 Bt-cotton and secondary pests. Int. J. Biotechnol. 10: 113–120.
World Bank, 2007 Agriculture for development, pp. in World Development Report, edited by The World Bank. The World Bank, Washington, DC.
Wu, K-M., Y.-H. Lu, H.-Q. Feng, Y.-Y. Jiang and J.-Z. Zhao, 2008 Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321: 16676.
Xu, K., X. Xu, T. Fukao, P. Canlas, R. Maghirang-Rodriguez et al., 2006 Sub1A encodes an ethylene responsive-like factor that confers submergence tolerance to rice. Nature 442: 705–708.
Ye, X., S. Al-Babili, A. Kloti, J. Zhang, P. Lucca et al., 2000 Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287: 303–305.