Copyright © 2011 by the Geneti Copyright Genetics cs Society of Amer America ica DOI: 10.1534/genetics.111.128553
Review Plant Genetics, Sustainable Agriculture and Global Food Security Pamelaa Ronald Pamel
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University Universi ty of Califo California, rnia, Davis, Califo California rnia 95616
ABSTRACT The United States and the world face serious societal challenges in the areas of food, environment, energy, and health. Historically, advances in plant genetics have provided new knowledge and technologies needed to address these challenges. Plant genetics remains a key component of global food security, peace, and prosperity prosperity for the foreseeable foreseeable future. Millions of lives depend depend upon the extent to which crop genetic improv imp roveme ement nt can kee keep p pac pacee wit with h the gro growin wing g glob global al pop popula ulatio tion, n, cha changi nging ng cli climat mate, e, and shr shrink inking ing environmental resources. While there is still much to be learned about the biology of plant –environment interactions, the fundamental technologies of plant genetic improvement, including crop genetic engineering, are in place, and are expected to play crucial roles in meeting the chronic demands of global food security. However, genetically improved seed is only part of the solution. Such seed must be integrated into ecologically based farming systems and evaluated in light of their environmental, economic, and social impacts—the three pillars of sustainable agriculture. In this review, I describe some lessons learned, over the last decad decade, e, of how genetically genetically engin engineere eered d crops have been integr integrated ated into agricu agricultura lturall pract practices ices around the world and discuss their current and future contribution to sustainable agricultural systems.
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HE number of people on Earth is expected to increase from the current 6.7 billion to 9 billion by 2050. To accommodate the increased demand for food, world agricultural production needs to rise by 50% by 2030 (R oyal oyal Society 2009). Because the amount of arable land is limited and what is left is being lost to urbanization, urbaniz ation, salini salinization, zation, desertification, and environmental men tal deg degrad radati ation, on, it no lon longer ger pos possibl siblee to simp simply ly open up more undeveloped land for cultivation to meet prod pr oduc ucti tion on ne need eds. s. An Anoth other er ch chal alle leng ngee is tha thatt wa wate terr systems are under severe strain in many parts of the world. world. The fres fresh h wat water er ava availa ilable ble per pers person on has decreased fourfold in the past 60 years (U nited Nations Environmental Programme 2002). Of the water that is available for use, 70% is already used for agriculture (V orosmarty orosmarty et al. 2000). Many rivers no longer flow all the way to the sea; 50% of the world's wetlands have disa disappea ppeared, red, and majo majorr groun groundwat dwater er aqui aquifers fers are bei being ng mi mined ned uns unsust ustain ainabl ably, y, wit with h wat water er tab tables les in pa parts rts of Mex Mexic ico, o, Ind India, ia, Chi China na,, an and d Nor North th Af Afric ricaa declining by as much as 1 m/year (S omerville and Briscoe 2001). Thus, increased food production must largely take place on the same land area while using less water. Compounding the challenges facing agricultural productio duc tion n are the pre predic dicted ted effe effects cts of cli climat matee cha change nge
Address for correspondence: Department of Plant Pathology, University of California, One Shields Avenue, Davis, CA 95616. E-mail:
[email protected] 1
Genetics 188: 11–20 (May 2011)
(Lobell et al. 2008). As the sea level rises and glaciers melt, low-lying croplands will be submerged and river systems will experience shorter and more intense seasonal flows,aswellasmore floodi ooding ng (Intergovernmental Panel on Climate Change 2007). Yields of our most important food, feed, and fiber crops decline precipitously at temperatures much .30 , so heat and drought will increasingly limit crop production (Schlenker and R oberts 2009). 9). In add additi ition on to thes thesee envi environm ronmenta entall oberts 200 stresses, losses to pests and diseases are also expected to increase. increas e. Much of the losses caused by these abiotic and biotic bio tic stre stresses sses,, whic which h alr alread eadyy resu result lt in 30–60% yiel yield d reduct red uctions ions glo global bally ly eac each h yea year, r, occ occur ur afte afterr the pla plants nts are fully grown: a point at which most or all of the land and water required to grow a crop has been invested (Dhlamini et al 2005 05). ). Fo Forr th this is rea reason son,, a re redu ducti ction on in lo losse ssess al.. 20 to pes pests, ts, pat pathoge hogens, ns, and envi environ ronmen mental tal stre stresses ssesis is equ equiva ivalent lent to creating more land and more water. Thus, an important goal for genetic improvement of agricultural crops is to adapt our existing food crops to increasing increas ing tempera temperatures, tures, decreased water availa availability bility in some places and flooding in others, rising salinity, and changing pathogen and insect threats (W orld orld Bank 2007; Gregory et al. 2009; R oyal oyal Society 2009). Such improvements will require diverse approaches that will enhance the sustainability of our farms. These include more effective land and water use policies, integrated pest mana managemen gementt approaches, approaches, reductio reduction n in harmf harmful ul input inputs, s, and the development of a new generation of agricultural °
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crops tolerant of diverse stresses (Somerville and Briscoe 2001). These strategies must be evaluated in light of their environmental, environmenta l, economic, and social impacts—the three pillars pill ars of susta sustainab inable le agri agricult culture ure (Com Committ mittee ee on the Impact of Biotechnology on Farm-Level Economics Economics and Sustainability and National Research Council
2010). This review discusses the current and future contribution of genetically engineered crops to sustainable agricultural agricultu ral systems. WHAT ARE GENETICALLY ENGINEERED CROPS?
Genetic engineering differs from conventi conventional onal methodss of gen od geneti eticc mo modi dificat cation ion in two maj major or way ways: s: (1) gen geneti eticc engineering introduces one or a few well-characterized genes ge nes int into o a pl plan antt spe speci cies es an and d (2 (2)) ge genet netic ic en engi ginee neeri ring ng ca can n introduce introd uce genes from any species species into a plant. plant. In contrast, contrast, most conventional conventional method methodss of genetic modification used to create new varieties (e.g., artificial selection, forced interspecific transfer, random mutagenesis, marker-assisted selecti sele ction, on, and gra grafti fting ng of two spec species, ies,etc etc.) .) intr introdu oduce ce man many y unchar unc haracte acterize rized d gene geness int into o the sam samee spec species ies.. Conv Convenentional 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 neer ed crop cropss (in (inclu cludin ding g pota potato to and rice rice)) are exp expecte ected d to be cultivated worldwide (Stein and R odriguezodriguez- 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 The re is bro broad ad sci scient entiific conse consensus nsus that gene genetica tically lly 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 geneticall neti callyy engi engineere neered d crops (Boa Board rd on Ag Agric ricult ulture ure and Natural Resources, Committee on Environmental Impact Imp actss Ass Assoc ociat iated ed wit with h Com Commer mercia cializ lizat ation ion of Transg Tra nsgeni enic c Pla Plants nts,, Na Natio tional nal Res Resear earch ch Cou Counci ncil l 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 nic al res resear earch ch lab labora orator toryy and an int integr egral al pa part rt of the European Commission) have concluded that there is a compreh com prehensi ensive ve bod bodyy of kno knowled wledge ge tha thatt ade adequa quately tely addresses the food safety issue of genetically engineered crops (Commit Committee tee on Ident Identifying ifying and Assess Assessing ing Unintended Effects of Genetically Engineered
Foods on Hum Foods Human an Hea Health lth 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 conseque conse quences nces to huma human n heal health th and the envi environm ronment ent (Euro European pean Commis Commission sion Direc Directora torate-Ge te-Genera neral l 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 beca use each new plant var variety iety (whether (whether it is dev develeloped ope d thr through ough gene genetic tic eng enginee ineerin ring g or conv convent entiona ionall 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 ha ve be been en do docu cume ment nted ed on only ly in fo food odss de deve velo lope ped d through conventional breeding approaches. For example, conventional conventional breeders selected a celery variety with relative rela tively ly hig high h amo amount untss of pso psorale ralens ns to det deter er ins insect ect predators that damage the plant. Some farm workers who who ha harv rvest ested ed su such ch cel celer eryy de deve velo loped ped a se sever veree ski skin n rash—an uni uninten ntended ded con consequ sequence ence of this bree breeding ding strategy (Committee on Identifying and Assessing Unintended Unintend ed Effe Effects cts of Gen Genetic etically ally Engi Engineer neered ed Foods on Human Health and National Research Council 2004).
INSECT-RESISTANT CROPS A tr trul ulyy ex extr trao aord rdin inar aryy va vari riet etyy of al alte tern rnat ativ ives es to th thee chemical control of insects is available. Some are already in use and have achieved brilliant success. Others are in the stage of labora laboratory tory testing. 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 —entomol entomologists, ogists, pathologists, genetic geneticists, ists, physiolo physiologists, gists, biochemists, ecologists—all pouring pourin g their knowledge and their creative inspirations into the form formatio ation n of a new science science of biot biotic ic controls. controls. (Carson 1962, p. 278)
In the 1960s the biologist Rachel Carson brought the detrimental environmental and human health impacts resulting resultin g from overuse or misuse of some insecticides insecticides to the attention of the wider public. Even today, thousands of pesticide poisonings are reported each year (300, (300,000 000 deaths globally, 1200 each year in California alone). This is one reason some of the first genetically engineered nee red cro crops ps wer weree de desig signe ned d to red reduc ucee re reli lianc ancee on sprays of broad-spectrum insecticides for pest control. Corn and cotton have been genetically engineered to produce proteins from the soil bacteria Bacillus
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thuringiensis (Bt ) that kill some key caterpillar and beetle pests of these crops. Bt toxins cause little or no harm to mo most st no nont ntarg arget et or orga gani nisms sms in inclu cludi ding ng be bene neficial insects, wildlife, and people (Mendelsohn et al. 2003). Bt crops produce Bt toxins in most of their tissues. These 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 nubilal ), which bores into stems, and the pink nubilalis is ), bollworm (Pectinophora gossypiella ), ), which bores into bolls of cotton. First commercialized in 1996, Bt crops are the second most widely planted type of transgen transgenic ic crop. In 2009, Bt crops covered .50 million hectares worldwide (James 2009). The genes encoding hundreds of Bt toxins have been sequenced sequenced (Crickmore 20 2011 11). ). Mo Most st of the Bt toxins used in transgen transgenic ic crops are called Cry toxins because they occur as crytalline proteins in nature (Carriere /www.biology. ology.ed.ac.uk/r ed.ac.uk/resear esearch/ ch/ et al. 2010; Deacon, http://www.bi groups/jdeacon/microbes/bt.htm). groups/jdeacon/microbes/bt.htm ). Mor Moree rece recently ntly,, som somee Bt crop cr opss al also so produc producee a se seco cond nd ty type pe of Bt tox toxin in called called a veg vegeta eta-tive insecticidal protein (Carriere et al. 2010; Crickmore 2011). 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 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 Plantin g of Bt crops has resulted in the application application of fewer pounds of chemical insecticides and thereby has provided environmental and economic bene fits that are key to sustai sustainable nable agricultural agricultural produc production. tion. Although the benefits vary depending on the crop and pest pressure, su re, ov overa erall ll,, th thee U. U.S. S. Dep Depart artme ment nt of Ag Agri ricul cultu ture re (USDA) Economic Economic Researc Research h Service found that insecticide use in the United States was 8% lower per planted acre ac re fo forr ad adop opter terss of Bt corn tha than n for nonnon-adop adopters ters (Fernandez- Cornejo and Caswell 2006). Fewer insecticide treatments, lower costs, and less insect damage led to significant profit increases when pest pressures were high (Fernandez- Cornejo and Caswell 2006). When pest pressures are low, farmers may not be able to make up for the increased cost of the genetically engineered seed by increased yields. In Arizona, where an integra inte grated ted pest man manage agement ment prog program ram for Bt cotton continues to be effective, growers reduced insecticide
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use by 70% and saved .$200 million from 1996 to 2008 (Naranjo and Ellsworth 2009). A recent study indicates that the economic benefits resulting resulti ng 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 Illinois,, Minnesot Minnesota, a, and Wisconsi Wisconsin, n, cumul cumulative ative 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 som someti etimes mes asso associa ciated ted wit with h pla plantin nting g 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 biologica log icall div diversi ersity. ty. An ana analysi lysiss of 42 field experim experiments ents 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 (M arvier et al. 2007). Benefitsof Bt crops ps hav havee also bee been n well well-do -docum cumente ented d in Bt cro less-developed less-de veloped countries. 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; Q aim aim 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 cide-relat ed injuries (Huang et al. 2005). Despite initial declines in insecticide use associated with Bt cotton in China, a survey of 481 Chinese households in fi ve major cotton-producing provinces indicates that insecticide insecticide use on Bt cotton increased from 1999 to 2004, resulting in only 17% fewer sprays on Bt cotton compar com pared ed with non-Bt co cotto tton n in 20 2004 04 (W ang al.. ang et al 2008). A separate survey of 38 locations in six cottonproducing provinces in China showed that the number of sp spray rayss on al alll co cotto tton n field eldss drop dropped ped by 20 20% % fro from m 19 1996 96 (before widepread cultivation of Bt cotton) to 1999 (2 years years aft after er wide widespr spread ead cul cultiv tivatio ation n of Bt cott cotton) on) (Lu et al. 2010). This study also indicated a slight increase in insecticide insectic ide use on all cotton fields from 1999 to 2008. Although Bt co cotto tton n ha hass eff effec ectiv tively ely con contro trolle lled d its primary target pest in China (the cotton bollworm ), redu reduced ced use of broa broad-sp d-spectr ectrum um Helicoverpa armigera ), insectic inse cticides ides has app appare arently ntly inc increas reased ed the abu abunda ndance nce of so some me pe pest stss tha thatt are not kil kille led d by Bt cot cotton ton ( Wu
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et al. 2008; Lu et al. 2010). In particular, mirids, which are hemipteran insects not targeted by Bt cotton, have become more serious pests in China ( Lu et al. 2010). These results confirm the need to integrate Bt crops wit with h ot othe herr pe pest st co cont ntro roll ta tact ctic icss (Tabashnik et al al.. 2010). In Arizona, such an integrated pest management (IPM) approach has been implemented (N aranjo and Ellsworth 2009). In Arizona's cotton IPM system, key pests pes ts not cont controll rolled ed by Bt cott cotton on are man manage aged d with limited use of narrow-spectrum insecticides that promote mo te co conse nserva rvati tion on of ben beneefici cial al in inse sect ctss (Naranjo and Ellsworth 2009). Mirids such as the Lygus bug (Lygus hespe hesperus rus ) are controlled with a feeding inhibiBemisia ia taba tabaci ci ) is tor,, an tor and d th thee swe sweet et po pota tato to whi white tefl y (Bemis contr co ntroll olled ed wi with th in insec sectt gro growth wth re regul gulat ator orss (Naranjo and Ellsworth 2009). One limitation of using any insecticide, whether it is organic, orga nic, syn synthet thetic, ic, or gen genetic eticall allyy eng enginee ineered red,, is tha that t insects inse cts can evolve resistance resistance to it. For exa exampl mple, e, one crop pest, the diamondback moth ( Plutella xylostella ), ), has evo evolved lved resi resistan stance ce to Bt tox toxins ins und under er ope open n field conditions. This resistance occurred in response to repeated sprays of Bt toxins to control this pest on con ventional (nongenetically engineered) vegetable crops (Tabashnik 1994). Part Pa rtly ly on th thee ba basi siss of th thee ex expe peri rien ence ce wi with th th thee diamondback moth and because Bt crops cause a season-long exposure of target insects to Bt toxins, some scientis scie ntists ts pred predicte icted d tha thatt pest resi resista stance nce to Bt crops would occur in a few years. However, global pest monitoring data suggest that Bt crops have remained effective ti ve aga gain inst st mo most st pes ests ts fo forr mor oree th thaan a de deca cade de (Tabashnik et al. 2008; Carriere et al. 2010). Nonetheless, after more than a dozen years of widespread Bt crop use, resistance to Bt crops has been reported in some field populations of at least four major species of target pests (Bagla 2010; Carriere et al. 2010; Storer et al. 2010). Retrosp Ret rospecti ective ve ana analyse lysess sug suggest gest tha thatt the refuge strategy —i.e ., ., creating refuges of crop plants that do not make Bt toxins to promote survival of susceptible insects—has helped to delay evolution of pest resistance to Bt crops (Carriere et al. 2010). The theory underlying the refuge strategy is that most of the rare resistant pests pes ts surv survivi iving ng on Bt crop cropss will mate with abundant abundant suscept susc eptible ible pests fro from m refu refuges ges of host plants wit withou hout t Bt toxins. If inheritance of resistance is recessive, the hybr hy brid id of offs fspr prin ing g pr prod oduc uced ed by su such ch ma mati ting ngss wi will ll be killed by Bt crops, markedly slowing the evolution of resistanc resistance. e. In case casess wher wheree resi resistan stance ce to Bt crop cropss has evol evolved ved quickly, one or more conditions of the refuge strategy have not been met. For example, resistance occurred rapidly to the Bt toxin Cry1Ac in transgenic cotton in U.S. populations of Helicoverpa zea , which is consistent with the theory underlying the refuge strategy because this resistance is not recessive (Tabashnik et al. 2008). “
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In other words, the concentration of Cry1Ac in Bt cotton was not high enough to kill the hybrid offspring produced by matings between susceptible and resistant Thus,, the soso-cal called led hig high h dos dosee requirement H. ze zea a . Thus was not met (Tabashnik et al. 2008). In a related case, failure to provide adequate refuges of non-Bt cotton appears to have hastened resistance to this same type of Bt cotton by pink bollworm in India ( Bagla 2010). In contras cont rast, t, Ariz Arizona ona cot cotton ton grow growers ers com compli plied ed 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 and to kill a broader spectrum of insect pests (C arriere et al. 2010). For example, a new type of Bt corn produces fi ve thre reee th that at ki kill ll ca cate terp rpil illa lars rs an and d tw two o th that at Bt toxins—th kill beetles (Dow A grosciences grosciences 2009). Despite the success of the refuge strategy in delaying insect resistance to Bt crops, this approach has limitations, including variable compliance by farmers with the requirement to plant refuges of non-Bt host plants. An alternative strategy, where refuges are scarce or absent, 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 integrat ed appro approaches, aches, involving entomolo entomologists, gists, geneticists, physiologists, biochemists, and ecologists, provides a roa roadma dmap p for the futu future re of agr agricu icultur ltural al pro produc duction tion and attests to the foresight of Rachel Carson. “
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HERBICIDE-TOLERANT HERBICIDE-TOL ERANT CROPS
Weeds Weeds are a maj major or lim limitat itation ion of crop productio production n globally because they compete for nutrients and sunligh li ght. t. On Onee me meth thod od to co cont ntro roll we weed edss is to sp spra ray y herbicides that kill them. Many of the herbicides used over the past 50 years are classi fied as toxic or slightly toxic to animals and humans (classes I, II, and III). Some newer herbicides, however, are considered nontoxic (class IV). An example of the latter, the herbicide glyphosate (trade name Roundup), is essentially a modified am amin ino o ac acid id th that at bl bloc ocks ks a chl chlor oropl oplas astt en enzy zyme me [called 5-enolp 5-enolpyruvoyl yruvoyl-shikima -shikimate-3-p te-3-phosphat hosphatee synthetase (EPSPS)] (EPSPS)] that is required for plant, but not animal, production of tryptophan. Glyphosate has a very low acute acu te toxi toxicit city, y, is not car carcino cinogeni genic, c, and brea breaks ks dow down n quickly in the environment and thus does not persist in groundwater. Some crop plants have been genetically engineered for tolerance to glyphosate. In these herbicide-tolerant crops,
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a gene, isolated from the bacterium Agrobacterium encoding cod ing an EPS EPSPS PS pro protei tein n resi resistan stantt to gly glyphos phosate ate,, is engineered into the plant. Growers of herbicide-tolerant crops can spray glyphosate to control weeds without harming their crop. Althou Although gh herb herbici icidede-tole toleran rantt crop cropss do not dire directl ctly y benefit organic farmers, who are prohibited from using herbicid herb icides, es, or poor farm farmers ers in dev develop eloping ing cou countri ntries, es, who often cannot afford to buy the herbicides, there are clear cle ar adv advanta antages ges to conv conventi entiona onall grow growers ers and to the environment environm ent in develop developed ed countri countries. es. One importa important nt environmental benefit is that the use of glyphosate has displaced the use of more toxic (classes I, II, and III) herbicides (Fernandez- Cornejo and Caswell 2006). For example, in Argentina, soybean farmers using herbicide-tolerant crops were able to reduce their use of toxic to xicit ityy cla class ss II an and d III he herbi rbicid cides es by 83–10 100% 0%.. In North Carolina, the pesticide leaching was 25% lower in herbicide-tolerant cotton fields compared with those having conventional cotton (Carpenter 2010). Before the advent of genetically engineered soybean, convent conv entiona ionall soy soybean bean gro growers wers in the Unit United ed Sta States tes applied app lied the mor moree toxi toxicc herb herbicid icide, e, meto metolac lachlo hlorr (cl (class ass III), to control weeds. Metolachlor, known to contaminate groundwater, is included in a class of herbicides with suspected toxicological problems. Switching from metolachlor to glyphosate in soybean production has had lar large ge envi environm ronmenta entall benefits an and d lik likely ely he heal alth th benefits fo forr fa farmw rmwork orker erss (Fernandez- Cornejo and McBride 2002). In the Cen Central tral Valley of Cal Califor ifornia nia,, mos mostt conv convenentional alfalfa farmers use diuron (class III) to control weeds. Diuron, which also persists in groundwater, is toxic tox ic to aqu aquati aticc inve inverteb rtebrate ratess (U. (U.S. S. Environmental Protection A gency gency 1983, 1988). Planting of herbicide-tolerant alfalfa varieties is therefore expected to improve water quality in the valley and enhance biodi versity (Strandberg and Pederson 2002). The USDA Animal and Plant Health Inspection Service recently prepared a final environmental impact statement evaluating the potential environmental effects of planting this crop (Usda Animal and Plant Health Inspection Service 2010). Another benefit in terms of sustainable agriculture is that herbicide-tolerant corn and soybean have helped foster use of low-till and no-till agriculture, agriculture, which leaves the fertile topsoil intact and protects it from being removed by wind or rain. Thus, no-till methods can improve pro ve wate waterr qua qualityand lityand red reduce uce soilerosion soilerosion.. Als Also, o, beca because use tractor tilling is minimized, less fuel is consumed and greenhouse gas emissions are reduced (F arrell et al. 2006; Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability and National Nationa l Research Council 2010). In Argentina and the United States, the use of herbicide-tolerant soybeans was associated with a 25–58% decrease in the number of tillage operations (Carpenter 2010). Such reduced till-
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age practices correlate with a significant reduction in greenhouse gas emissions which, in 2005, was equivalent to removing 4 million cars from the roads ( Brookes and Barfoot 2006). One drawback to the application of herbicides is that overuse of a single herbicide can lead to the evolution of we weed edss th that at are res resist istant ant to th that at her herbi bicid cide. e. Th Thee evolution of resistant weeds has been documented for herbicid herb icide-t e-toler olerant ant trai traits ts dev develop eloped ed thro through ugh sel selecti ective ve breeding bree ding,, mut mutagen agenesis esis,, and gene genetic tic engi engineer neering. ing. To mitigate the evolution of weed resistance and prolong the usefulness of herbicid herbicide-tolera e-tolerant nt crops, a sustai sustainable nable manage man agemen mentt syst system em is need needed. ed. Suc Such h app approac roaches hes require qui re swi switch tching ing to an anoth other er her herbic bicide ide or mix mixtur tures es of herbicides or employing alternative weed control methods (Commit Committee tee on the Impac Impact t of Biote Biotechnol chnology ogy on Farm-L Farm-Level evel Econo Economics mics and Susta Sustainab inability ility and Implementation ation National Natio nal Resea Research rch Coun Council cil 2010). Implement of a mandatory crop diversity strategy would also greatly reduce weed resistance. Newer herbicide-tolerant varietiess wil tie willl hav havee tol tolera erance nce to mo more re tha than n one her herbic bicid ide, e, which which wil willl all allow ow ea easie sierr her herbic bicide ide rot rotati ation on or mix mixing ing,, and,, in the and theory ory,, hel help p to imp improv rovee the durabil durability ity of the effectiveness of particular herbicides. In addition to environmental issues, economic issues related to pollen flow between genetically engineered, nongeneti nonge neticall callyy engi engineered neered,, and organ organic ic crop cropss and to compa com patib tible le wil wild d rel relati atives ves are als also o im impor porta tant nt to dis discus cussio sions ns of herbicide tolerance due to possible gene flow. These issues are addressed in the USDA report on genetically engineered alfalfa and are also discussed in other reviews (R onald onald and A damchak damchak 2008; McHughen and W ager ager 2010; Usd Usda a Ani Animal mal and Pla Plant nt Hea Health lth Ins Inspec pectio tion n Service 2010). VIRAL-RESISTANT CROPS
Although Bt and herbicide-tolerant crops are by far the largest acreage, genetically engineered crops on the market, other genetically engineered crops have also been commercialized and proven to be effective tools for sustainable agriculture. For example, in the 1950s, the entire papaya production on the Island of Oahu was decimated decima ted by papaya ringspot ringspot virus (PRSV), a potyvi potyvirus rus with single-stranded RNA. Because there was no way to control PRSV, farmers moved their papaya production to the island of Hawaii where the virus was not yet present. By the 1970s, however, PRSV was discovered in the town of Hilo, just 20 miles away from the papaya growing area where 95% of the state's papaya was grown. In 1992, PRSV had invaded the papaya orchards and by 1995 the disease was widespread, creating a crisis for Hawaiian papaya farmers. In anticipation of disease spread, Dennis Gonsalves, a loc local al Haw Hawaiia aiian, n, and co-workers co-workers ini initia tiated ted a gene genetic tic strategy to control the disease (Tripathi et al. 2006). This research was spurred by an earlier observation that
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transgenic transgen ic tob tobacc acco o exp express ressing ing the coa coatt pro protein tein gene from tobacco mosaic virus showed a significant delay in dis disease ease sym sympto ptoms ms cau caused sed by toba tobacco cco mos mosaic aic viru viruss (Powell- A bel bel et al. 1986). Gonsalves's group engineered papaya to carry a transgene from a mild strain of PRSV. The transgene was designed designe d with a premature stop codon in the PRSV coat protein sequence to prevent expression of a functional coat protein because, at the time of engineering, it was thought that the protein itself was an important factor in resistance. RNA analysis later revealed that the plants with the best resistance exhibited the least detectable message, which was suggestive of the involvement of an RNA silencing mechanism (Tripathi et al. 2006). Conceptually Concept ually simila similarr (althou (although gh mechan mechanisticall isticallyy different) to human vaccinations against polio or small pox,, this trea pox treatme tment nt immunized the pa papa paya ya pl plan ant t againstt further infection. The genetica agains genetically lly enginee engineered red papaya yielded 20 times more papaya than the nongenetical neti cally ly engi enginee neered red var variety iety aft after er PRS PRSV V infe infectio ction. n. By Septem Sep tember ber 199 1999, 9, 90% of the Hawa Hawaiia iian n far farmers mers had obtained obta ined gen genetic eticall allyy engi engineer neered ed seed seeds, s, and 76% of them had planted the seeds. After release of genetica genetically lly engineered papaya to farmers, production rapidly increased from 26 million pounds in 1998 to a peak of 40 million pounds in 2001. Today, 80 –90% of Hawaiia Hawaiian n papaya is genetically engineered. There is still no con ventional or organic method to control PRSV. Funded mostl mo stlyy by a gr grant ant from th thee USD USDA, A, the project project cost $60,000, a small sum compared to the amount the papaya industry lost between 1997 and 1998, prior to the introduction of the genetically engineered papaya. “
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GENETICALLY ENGINEERED CROPS ON THE HORIZON
Peer-reviewed studies of the genetically engineered crops currently on the market indicate that such crops have contributed to enhancing global agricultural sustainability. As reviewed here, bene fits include massive reduct red uctions ions in inse insecti cticide cidess in the envi environm ronment ent (Q aim and Zilberman 20 2003 03;; Huang et al 2005), 5), imp improve roved d soil qua quallal.. 200 ity and reduced erosion ( Committee on the Impact of Biot Biotechn echnolog ology y on Far Farm-Lev m-Level el Econ Economic omicss and Sustainability and Nat Nationa ional l Rese Researc arch h Cou Council ncil
2010), prevention of the destruction of the Hawaiian papa pa paya ya in indu dust stry ry (Tripathi et al 2006), 6), enha enhanced nced al.. 200 health benefits to farmers and families as a result of reduced exposure to harsh chemicals (Huang et al. 2002, 2005), economic bene fits to local communities (Q aim aim et al. 2010), enhanced biodiversity of beneficial insects (Cattaneo et al. 2006), reduction in the number of pest outbreaks on neighboring farms growing nongenetically engineer engi neered ed crop cropss (Hutchison et al 2010), 0), and inal.. 201 creased profits to farmers (Tabashnik 2010). Genetically engineered crops have also dramatically dramatically increased crop yiel yields ds—.30 30% % in som somee fa farmi rming ng co comm mmun unit itie iess (Q aim aim et al. 2010). As has been well-documented for Bt
cotton in Arizona, the ability to combine innovations in farming practice with the planting of genetically engineered seed has had a huge positive bene fit/cost ratio, far beyo beyond nd what cou could ld be ach achiev ieved ed by inno innovat vating ing far farming ming practic pra ctices es or pla planti nting ng gene genetica tically lly eng enginee ineered red crop cropss alo alone. ne. The benefit/cost ratio of Bt crops is the highest for any agricultural innovation in the past 100 years. There The re are doz dozens ens of use useful ful gen genetic eticall allyy engi engineer neered ed traits in the pipeline, including nitrogen use ef ficiency (A rcadia 2010 10). ). Su Succe ccess ss of cr crop opss enrcadia Biosciences 20 hanced for this ef ficiency would reduce water eutroph eutrophiication caused by nitrogenous compounds in fertilizers and greenhouse gas emissions resulting from the energy required to chemically synthesize fertilizers. Thee US Th USDA DA An Anim imal al an and d Pl Plant ant Hea Health lth In Insp spect ectio ion n Service has developed a transgenic plum variety, the HoneySweet, which is resistant to Plum Pox, a plant disease that infects plum and other stone fruit trees, including peach, nectarine, plum, apricot, and cherries. Although Plum Pox is very rare in the United States, and its out outbrea breaks ks are imm immedi ediatel atelyy era eradica dicated,the ted,the Hone HoneyySweet variety was developed as a precautionary measure to avoid a major disruption in the availability of plums, prunes, and other stone fruits should Plum Pox become wide wi desp sprea read d as is al alre read adyy th thee ca case se in Eu Europ ropee Usda Anim Animal al and Plant Health Inspection Service 2009). Other promising applications of genetic engineering are those that affect staple food crops. For example, rice is grown in .114 countries on six of the seven continents. In countries where rice is the staple food, it is frequent freq uently ly the bas basic ic ingr ingredi edient ent of ever everyy mea meal. l. Thu Thus, s, even mod modest est cha changes nges in tol toleran erance ce to env environ ironmen mental tal stress or enhanced nutrition in rice can have a large impact in the lives of the poor. With Wi th reg regard ard to nut nutriti ritionalenhanc onalenhancemen ements, ts, someefforts havee focu hav focused sed on vita vitamin min de ficie ciencie ncies. s. Vita Vitamin min A deficiency is a public health problem in .100 countries, especially in Africa and Southeast Asia, affecting young children and pregnant women the most ( Golden Rice Project 2010). Worldwide, .124 million children are estimated to be vitamin A-de ficient. Many of these children go blind or become ill from diarrhea, diarrhea, and nearly 8 million mil lion pre prescho school-a ol-age ge chil children dren die eac each h yea yearr as the resu result lt of this deficiency. Researchers estimate that 6000 children and young mothers die every day from vitamin A deficie ciencyncy-rela related ted pro problem blemss (Potrykus 201 2010). 0). The World Health Organization estimates that improved vitamin A nutritional status could prevent the deaths of 1.3–2.5 million late-i late-infancy nfancy and preschoo preschool-age l-age children each year (Humphrey et al. 1992). To combat vitamin A de ficiency, the World Health Organiza Orga nizatio tion n has pro propose posed d an arse arsenal nal of nutr nutritio itional nal well-being well-being weapons weapons,, inc inclu ludi ding ng a com combin binat ation ion of breastfeeding breastfe eding and vitami vitamin n A suppl supplementati ementation, on, coupled with with long long-ter -term m solu solution tions, s, suc such h as prom promotin oting g vit vitami amin n A-r A-rich ich di diet etss an and d fo food od fo forti rtifica cati tion on.. In re resp spons onsee to this cha challe llenge, nge, a grou group p of Roc Rockefe kefeller ller Fou Founda ndation tion-“
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supported scientists decided to try to fortify rice plants with higher levels of carotenoids, which are precursors to vita vitamin min A. Usin Using g gen genetic etic eng enginee ineering ring,, they introduced a gene from daffodils (which make carotenoids, the pigment that gives the flower its yellow color) and two genes from a bacterium into rice (Y e et al. 2000). The resulting geneticially engineered golden and carotenoid-rich rice plants were named Golden Rice. Results from human feeding studies indicate that the carotenoids in the second generation of Golden Rice (called (calle d Golden Rice-2 Rice-2)) can be properly metabo metabolized lized into the vitamin A that is needed by children (T ang et al. 2009). One 8-ounce cup of cooked Golden Rice-2 pro vides 450 mgofretinol,whichisequivalentto50–60%of the adu adult lt Rec Recomm ommend ended ed Die Dietary tary All Allowa owance nce of vita vitamin min A. Otherr stu Othe studie diess sup supportthe portthe ide ideaa tha thatt wid widesp espreadconsum readconsumpption of Golden Rice would reduce vitamin A de ficiency, saving thousands of lives (Stein et al. 2006). The positive effects of Golden Rice are predicted to be most pronounced in the lowest income groups at a fraction of thee co th cost st of th thee cu curr rrent ent su supp pplem lemen enta tatio tion n pr progr ogram amss (Stein et al. 2006, 2008). If predictions prove accurate, this rela relative tively ly lowlow-tech tech,, sust sustain ainabl able, e, pub publicl liclyy fund funded, ed, peo peo-ple-centered effort will complement other approaches, such as the development of home gardens with vitamin A-rich crops, such as carrots and pumpkins. In a sense, the resulting nutritionally nutritionally enhanced rice is similar to vitamin D-enriched milk —except the process is different. Vitamin A fortification of rice is also similar to adding iodine to salt, a process credited with drastically reducing iodine iodine-de -deficien ciency cy dis disord orders ers in inf infant ants. s. Worldwide, iodine deficiency affects 2 billion people and is the leading preventable cause of mental retardation. The benefits of iodized salt are particularly apparent in Kaz Kazakhs akhstan tan wher wheree loca locall food supplies supplies seld seldom om contain suf ficient iodine and where fortified salt was initially viewed with suspicion. Campaigns by the government ernm ent and non nonpro profit organizations to educate the public about fortified salt req require uired d both money and political leadership, but they eventually succeeded. Today, da y, 94 94% % of ho hous useh ehold oldss in Ka Kazak zakhs hsta tan n us usee iod iodiz ized ed salt, and the United Nations is expected to certify the country cou ntry of fici cial ally ly fre freee of io iodin dinee-de deficiency disorde disorders rs (R onald onald and A damchak damchak 2008). The dev develop elopmen mentt of gene genetic ticall allyy engi enginee neered red crop cropss tha that t aree to ar toler leran antt of env envir ironm onmen enta tall str stress esses es is al also so pr pred edict icted ed to be br broad oadly ly ben beneefici cial al.. Su Such ch cro crops ps ar aree ex expe pect cted ed to enhance enh ance local foo food d secu security rity,, an iss issue ue of imp importa ortance nce especially especia lly for farmers in poorer nations that have limited acces ac cesss to ma marke rkets ts an and d ar aree no now w of oftendepe tendepend ndenton enton ot other herss for their staple foods (R oyal oyal Society 2009). The development of submergence tolerant rice (Sub1 rice), through a nongenetically engineered process that involved gene cloning and precision breeding, demonstrates the power of genetics to improve tolerance to environ env ironmen mental tal stre stresses sses suc such h as flood ooding, ing, whi which ch is a maj major or constra cons traint int to riceproduc riceproduction tion in Sou South th and Sou Southea theast st Asi Asiaa “
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(Xu et al. 2006). In Bangladesh and India, 4 million tons of rice, enough to feed 30 million people, are lost each year to flooding. Planting of Sub1 rice has resulted in threethre e- to fou fourfol rfold d yiel yield d incr increase easess in far farmers mers field eldss dur during ing floods compared to conventional varieties. Although the Sub1 rice varieties provided an excellent immediate solution lut ion for mos mostt of the sub submer mergenc gence-p e-prone rone area areas, s, a hig higher her and wider range of tolera tolerance nce is require required d for severe conditions and longer periods of flooding. With increasing global warming, unusually heavy rainfall patterns are predicted for rain-fed as well as irrigated agricultural systems. For these reasons, we and others have identified additional genes that improve tolerance (S eo et al. 2011) 201 1).. Su Such ch ge genesmay nesmay be us usefu efull forthe de devel velop opme ment nt of plus Sub1 varieties. In Africa, three-quarters of the world's severe droughts have occurred over the past 10 years. The introduction of geneticallyy engineered drought-tolerant corn, the most imgeneticall portant port antAfri African canstap staple le foodcrop, is pred predicte icted d to dram dramatic aticall ally y increase yields for poor farmers (A frican frican A gricultural gricultural Technology Foundation 2010). Drought-tolerant corn will be broadly beneficial across almost any non-irrigated agricult agri cultura urall situ situatio ation n and in any man managem agement ent syst system. em. Drought-tolerance technologies are likely to benefit other agricul agri cultura turall crop cropss for both deve develope loped d and deve developi loping ng countries. In addition to environmental stresses, plant diseases also threaten global agricultural production (B orlaug 2008). For example, an epidemic of stem rust threatens wheat, a crop that provides 20% of the food calories for the world's people. Because fungal spores travel in the wind, the infection spreads quickly. Stem rust has caused major famines since the beginning of history. In North America, huge grain losses occurred in 1903 and 1905 and from 1950 to 1954. During the 1950s, Norman Borlaug and other scientists developed high-yielding high-yielding wheat varieties that were resistant to stem rust and other diseases. These improved seeds not only enabled farmers around the world to hold stem rust at bay for .50 years but also all allowe owed d for gre greater ater and mor moree dep depend endable able yiel yields. ds. However, new strains of stem rust, called Ug99 because they were discovered in Uganda in 1999, are much more dangerous than those that destroyed as much as 20% of the American wheat crop 50 years ago. Effective resistance does not exist in American wheat and barley varieties,, but rece ties recentl ntlyy resi resistan stance ce was ide identi ntified in African varieties and molecular markers mapped to facilitate introgression of the trait using marker-assisted selection (Steffenson 2011). Bananas and plantains are the world's fourth most impo im porta rtant nt foo food d cro crop p af after ter ric rice, e, wh wheat eat,, an and d ma maiz ize. e. Approximately one-third of the bananas produced globally are grown in sub-Saharan Africa, where the crop provides .25% of the food energy requirements for .100 million people in East Africa alone. Banana Xanthomonas thom onas wilt dis disease ease,, cau caused sed by the Gram Gram-ne -negat gative ive Xanthomonas omonas vasic vasicola ola pv. musacearum , i s a bacterium Xanth ’
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major threat to banana productivity in eastern Africa (Tripathi et al. 2009; Studholme et al. 2010). Cavendish banana, which represents 99% of export bananas, is threatened by a virulent form of the soil-borne fungus called led Tro Tropic pical al Rac Racee Fou Fourr (Peed Fusarium Fusa rium oxysp oxysporum orum cal 2011). 201 1). The fun fungal gal lea leaff spot disease disease Blac Black k Sig Sigato atoka, ka, caused cau sed by the asc ascomy omycete cete Mycosphaerella fi jiensis , has spread spre ad to ban banana ana pla planta ntation tionss thro througho ughout ut the trop tropics ics and is increasingly resistant to chemical control (Marin et al. 2003). Research to develop new methods to control these diseases of banana are underway in several laboratories. CONCLUSION
For hu For hund ndre reds ds of ye year ars, s, fa farm rmer erss ha have ve re reli lied ed on genetically improved seed to enhance agricultural productio duc tion. n. Wit Without hout the dev develo elopme pment nt of high high-yi -yieldi elding ng crop varieties over recent decades, two to four times more mo re la land nd wou would ld ha have ve bee been n nee needed ded in the Uni United ted States, China, and India to produce the same amount of food. Looking ahead, without additional yield increases, maintaining current per capita food consumption will necessitate a near doubling of the world's cropland area by 2050. By comparison, raising global average yields to those currently achieved in North America could result in a very considerable considerable sparing of land (W aggoner aggoner 1995; Green et al substantial tial greenhou greenhouse se al.. 2005). Because substan gases gas es are emi emitted tted from agri agricul cultur tural al syst systems, ems, and because the net effect of higher yields is a dramatic reducti du ction on in ca carb rbon on em emiss ission ionss (Burney et al al.. 2010), development develop ment and deploym deployment ent of high-yi high-yielding elding varieties will will be a cri critic tical al com compo ponen nentt of a fu futu ture re su sust stai aina nable ble agriculture. Thus, a key challenge is to raise global yields without further fur ther erod eroding ing the envi environm ronment. ent. Rec Recent ent rep reports orts on food security emphasize the gains that can be made by bringing existing agronomic and food science technology and know-how to people who do not yet have it. These reports also highlight the need to explore the genetic gene tic var variab iabilit ilityy in our existing existing food crops and to develop new genetic approaches that can be used to enhance enha nce mor moree eco ecologi logical cally ly sou sound nd farm farming ing pra practic ctices es (Naylor et al. 2007; W orld orld Bank 2007; R oyal oyal Society 2009). Despite the demonstrated importance of genetically improved seed, there are still agricultural problems that cann ca nnot ot be sol solved ved by im impr prove oved d see seed d al alon one, e, ev even en in combination with innovative farming practices. A premise basic to almost every agricultural system (conventional, organic, and everything in between) is that seed can ca n ta take ke us on only ly so fa far. r. Ec Ecol ologi ogica call llyy ba based sed fa farm rming ing practices used to cultivate the seed, as well as other technological changes and modi fied government policies, clearly are also required. In ma many ny pa parts rts of the wo world rld,, su such ch po polic licies ies inv invol olve ve building local educational, technical, and research cap-
acity, food processing capability, storage capacity, and other oth er as aspe pects cts of ag agrib ribusi usine ness, ss, as we well ll as ru rura rall tra transnsportati por tation on and wat water er and comm communi unicat cations ions infr infrast astruc ruc-ture.. The man ture manyy tra trade, de, sub subsidy sidy,, inte intellec llectua tuall prop property erty,, and an d reg regul ulat atory ory is issu sues es tha thatt in inter terfer feree wi with th tra trade de an and d inhibit the use of technology must also be addressed to assure adequate food availability to all. Despite the complex com plexity ity of many of thes thesee inte interrel rrelated ated issues, issues, it is hard to avoid the conclusion that ecological‐ ecological‐farming practic pra ctices es usi using ng gene genetica tically lly engi engineer neered ed seed wil willl pla play y an increasingly important role in a future sustainable agriculture. Fourteen Fourte en years of extensiv extensivee field studies (Carpenter 2010) have demonstrated that genetically engineered crops are tools that, when integrated with optimal management practices, help make food production more sustainable. The vast benefits accrued to farmers, the environment, environm ent, and consume consumers rs expla explain in the widespr widespread ead popularity of the technology in many regions of the world. The path toward a future sustainable sustainable agriculture lies in harnessing the best of all agricultural technologies, including the use of genetically engineered seed, within the framework of ecological farming. I am grateful to Peggy Lemaux, Kent Bradford, and Bruce Tabshnik for helpful discussions and critical review of the manuscript. This work was supported by National Institutes of Health grant GM055962 and the Department of Energy, Of fice of Science, Of fice of Biological and Environmenta Environ mentall Resea Research, rch, through contra contract ct DE-AC02 DE-AC02-05CH11231 -05CH11231 between Lawrence Berkeley National Laboratory and the Department of Energy Energy..
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