impacts Feeding the world in the twenty-first century

Gordon Conway and Gary Toenniessen

The gains in production provided by the have reached their ceiling while world population continues to rise. To ensure that the world’s poorest people do not still go hungry in the twenty-first century, advances in plant biotechnology must be deployed for their benefit by a strong public-sector agricultural research effort.

he Green Revolution was one of the As well as gross undernourishment, lack 90 great technological success stories of of protein, vitamins, minerals and other 1965–74 80 1975–84 the second half of the twentieth centu- micronutrients in the diet is also wide- ) 70 1985–94 T –1 ry. Because of the introduction of scientifi- spread3. About 100 million children under 60 cally bred, higher-yielding varieties of , five suffer from vitamin A deficiency, which 50 40 wheat and maize beginning in the 1960s, can lead to eye damage. Half a million chil- 30 overall food production in the developing dren become partly or totally blind each year, yield (kg Ha 20 countries kept pace with population growth, and many subsequently die. Recent research in increase Average 10 0 with both more than doubling. The benefits has shown that lack of vitamin A has an even Rice Wheat Maize of the Green Revolution reached many of the more pervasive effect, weakening the protec- world’s poorest people. Forty years ago there tive barriers to infection put up by the skin, Figure 1 Average annual increase in yields of were a billion people in developing countries the mucous membranes and the immune rice, wheat and maize in developing countries who did not get enough to eat, equivalent to system4. Iron deficiency is also common, by periods. 50 per cent of the population of these coun- leading to about 400 million women of tries. If this proportion had remained childbearing age (15–49 years) being afflict- unchanged, the hungry would now number ed by anaemia. As a result they tend to pro- who lack access to adequate food today will over two billion — more than double the duce stillborn or underweight children and be any better served by future world markets. current estimate of around 800 million, or are more likely to die in childbirth. Anaemia Food aid programmes are also no solution, around 20 per cent of the present population has been identified as a contributing factor in except in cases of specific short-term emer- of the developing world. Since the 1970s, over 20 per cent of all maternal deaths after gency. They reach only a small portion of world food prices have declined in real terms childbirth in Asia and Africa. those suffering chronic hunger and, if by over 70 per cent. Those who benefit most If nothing new is done, the number of the prolonged, create dependency and have a are the poor, who spend the highest propor- poor and hungry will grow. The populations negative impact on local food production. tion of their family income on food. of most developing countries are increasing About 130 million of the poorest 20 per The Green Revolution brought benefits rapidly and by the year 2020 there will be cent of people in developing countries live in too for the industrialized world. The high- an additional 1.5 billion mouths to feed, cities. For them, access to food means cheap yielding varieties of staple plants bred by mostly in the developing world. What is the food from any source. But 650 million of the the international agricultural research cen- likelihood that they will be fed? poorest live in rural areas where tres of the CGIAR (the Consultative Group is the primary economic activity, and as is the on International Agricultural Research) have The end of the Green Revolution case in much of Africa, many live in regions been incorporated into the modern varieties The prognosis is not good. As indicated in where agricultural potential is low and nat- grown in the United States and Europe. The Fig. 1, there is widespread evidence of decline ural resources are poor8. They are distant additional wheat and rice produced in the in the rate of increase of crop yields5–7. This from markets and have limited purchasing United States alone from these improved slowdown is due to a combination of causes. power. For them, access means local produc- varieties is estimated to have been worth over On the best lands many farmers are now tion of food that generates employment and $3.4 billion from 1970 to 1993 (ref. 1). obtaining yields close to those produced on income, and is sufficient and dependable Yet today, despite these demonstrable experimental stations, and there has been enough to meet local needs throughout the achievements, over 800 million people con- little or no increase in the maximum possible year, including years that are unfavourable sume less than 2,000 calories a day, live a life yields of rice and maize in recent years. A for agriculture. of permanent or intermittent hunger and are second factor is the cumulative effect of All these arguments point to the need for a chronically undernourished2. Most of the environmental degradation, partly caused second Green Revolution, yet one that does hungry are the women and young children of by agriculture itself. not simply reflect the successes, and mistakes, extremely poor families in developing coun- Simply exporting more food from the of the first. In effect, we require a ‘Doubly tries. More than 180 million children under industrialized countries is not a solution. Green Revolution’, an agricultural revolution five years of age are severely underweight: The world already produces more than that is both more productive and more ‘green’ that is, they are more than two standard devi- enough food to feed everyone if the food in terms of conserving natural resources and ations below the standard weight for their were equally distributed, but it is not. Market the environment than the first. We believe age. Seventeen million children under five economies are notoriously ineffective in that this can be achieved by a combination die each year and malnourishment con- achieving equitable distribution of benefits. of: ecological approaches to sustainable agri- tributes to at least a third of these deaths. There is no reason to believe that the poor culture; greater participation by farmers in

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Table 1 Biotechnology research useful in developing countries Traits now in greenhouse or field tests Traits now in laboratory tests Input traits Input traits Resistance to insects, nematodes, viruses, bacteria and fungi in Drought and salinity tolerance in cereals such as rice, maize, potato, papaya and sweet potato Seedling vigour in rice Delayed senescence, dwarfing, reduced shade avoidance and early flowering in rice Enhanced phosphorus and nitrogen uptake in rice and maize

Tolerance of aluminium, submergence, chilling and freezing in cereals Resistance to the parasitic weed Striga in maize, rice and sorghum, to viruses in cassava and banana, and to bacterial blight in cassava Male sterility/restorer for hybrid seed production in rice, maize, oil-seed rape and wheat Nematode resistance and resistance to the disease black sigatoka in banana

New plant types for weed control and for increased yield potential in rice Rice with the alternative C4 photosynthetic pathway and the ability to carry out nitrogen fixation

Output traits Output traits Increased ȋ-carotene in rice and oil-seed rape Increased ȋ-carotene, delayed post-harvest deterioration and reduced content of toxic cyanides in cassava Lower phytates in maize and rice to increase bioavailable iron Increased vitamin E in rice Modified starch in rice, potato and maize and modified fatty-acid content in oil-seed rape Apomixis (asexual seed production) in maize, rice, millet and cassava

Increased bioavailable protein, essential amino acids, seed weight and Delayed ripening in banana sugar content in maize Use of genetically engineered plants such as potato and banana as vehicles Lowered lignin content of forage crops for production and delivery of recombinant vaccines to humans

Improved amino-acid content of forage crops agricultural analysis, design and research; insecticides and herbicides. However, as which are the most important constraint on and the application of modern biotechnolo- with many agricultural inputs, the benefits crop production in Africa; Fig. 2a) but gy directed towards the needs of the poor in received by farmers vary from year to year. becomes more like Asian rice as it reaches developing countries, which is the subject of Most of the GM crops currently being maturity, thus giving higher yields with few the rest of this article. grown in developing countries are cash crops; inputs. Marker-aided selection is being used Bt cotton, for example, has reportedly been to breed rice containing two or more genes The price of biotechnology taken up by over a million farmers in China. for resistance to the same pathogen, thereby The application of advances in plant breed- But despite claims to be ‘feeding the world’, increasing the durability of the resistance, ing — including tissue culture, marker- the big life-science companies have little and to accumulate several different genes aided selection (which uses DNA technology interest in poor farmers’ food crops, because contributing to drought tolerance. to detect the transmission of a desired gene to the returns are too low. National govern- a seedling arising from a cross) and genetic ments, the international research centres of Potential of engineering — are going to be essential if the CGIAR, and a variety of western donors For some time to come, tissue culture and farmers’ yields and yield ceilings are to be are, and will continue to be, the primary sup- marker-aided selection are likely to be the raised, excessive pesticide use reduced, the porters of work that produces advances in most productive uses of biotechnology for nutrient value of basic increased and biotechnology useful to poor farmers. New cereal breeding. However, progress is being farmers on less favoured lands provided with forms of public–private collaboration could made in the production of transgenic crops varieties better able to tolerate drought, help to ensure that all farmers and consumers for the developing countries. As in the salinity and lack of soil nutrients. benefit from the genetic revolution and, over industrialized countries, the focus has been In the industrialized countries the new time, this should increase the number of largely on traits for disease and pest resis- life-science companies, notably the big six farmers who can afford to buy new seeds tance, but genes that confer tolerance of multinationals — Astra-Zeneca, Aventis, from the private sector. high concentrations of aluminium (found Dow, Dupont, Monsanto and Novartis — The cost of accomplishing this will not be in many tropical soils) have been added dominate the application of biotechnology insignificant but it should not be excessive. by Mexican scientists to rice and maize to agriculture. In 1998, ‘genetically modified For example, over the past 15 years, the (Fig. 2c), and Indian scientists have added (GM)’ crops, more accurately referred to as Rockefeller Foundation has funded some two genes to rice which may help the plant transgenic or genetically engineered crops, US$100 million of rice biotechnology tolerate prolonged submergence. There is mostly marketed by these companies or their research and trained over 400 scientists from also the possibility of increasing yield subsidiaries, were grown on nearly 29 Asia, Africa and Latin America. In several ceilings, through more efficient photosyn- million hectares worldwide (excluding places in Asia there is now a critical mass of thesis, for example, or by improved control China)9. That year, 40 per cent of all cotton, talented scientists who are applying the new of water loss from leaves through regulation 35 per cent of soya beans and 25 per cent of tools of biotechnology to rice improvement. of stomatal opening and closing10. maize grown in the United States were GM To date, most of the new varieties are the In addition to generating new traits that varieties. result of tissue culture and marker-aided enable the plant to grow better (input traits), So far, the great majority of the commer- selection techniques. For example, scientists which are useful to poor farmers, GM tech- cial applications of plant genetic engineering at the West Africa Rice Development Associ- nology can also generate plants with have been for crops with single-gene ation have used anther culture to cross the improved nutritional features (output alterations that confer agronomic benefits high-yielding Asian with traditional traits) of benefit to poor consumers. One of such as resistance to pests or to herbicides. African rices. The result is a new plant type the most exciting developments so far has These agronomic traits can reduce costs to that looks like African rice during its early been the introduction of genes into rice that the farmer by minimizing applications of stages of growth (it is able to shade out weeds, result in the production of the vitamin A

C56 © 1999 Macmillan Magazines Ltd NATURE | VOL 402 | SUPP | 2 DECEMBER 1999 | www.nature.com impacts precursor ȋ-carotene in the rice grain11. ȋ- replant new varieties from the public sector. proprietary seed and restrict its use for carotene is a pigment required for photosyn- But if the companies tie up enabling tech- further breeding, the public sector will be thesis and is synthesized in the green tissues nologies and DNA sequences of important severely constrained in using biotechnology of all plants, including rice, but is not usually genes with patents, and then use terminator to meet the needs of the poor. present in non-photosynthetic tissues such technologies to control the distribution of Rather than using the terminator tech- as those of seeds. Traditional nology to protect their intellectual property has given us some plants that produce ȋ- in developing countries, it would be better if a carotene in non-photosynthetic tissue, such seed companies focused on producing as the roots of carrots, but despite decades of hybrid seed combined with plant variety searching no rice mutants had been found protection (PVP) to protect the commercial that produce ȋ-carotene in the grain, so con- production of the seed. Hybrid plants do ventional breeding was not an option. To get produce viable seed but it is not genetically the cells of the grain to produce ȋ-carotene, identical to the original hybrid seed; it may genetic engineers added three genes for key lack some of the desirable characteristics. enzymes for ȋ-carotene biosynthesis to the Hence, there is still an incentive (for exam- rice genome. The grain of the transgenic rice ple, increased yield) for farmers to purchase has a light golden-yellow colour (Fig. 2b) hybrid seed for each planting. However, if and contains sufficient ȋ-carotene to meet such purchase is not possible, farmers can human vitamin A requirements from rice still use a portion of their harvest as seed and alone. This ‘golden’ rice offers an opportuni- b obtain a reasonable crop. Such recycling of ty to complement vitamin A supplementa- hybrids is not uncommon in developing tion programmes, particularly in rural areas countries and is an important element of that are difficult to reach. These same scien- . And with PVP, new varieties tists and others have also added genes to rice can be protected while also becoming a that increase the grain’s nutritionally avail- resource that both the private and public able iron content by more than threefold. sectors can use in further breeding for the Over the next decade we are likely to see benefit of all farmers. much greater progress in multiple gene introductions that focus on output traits or Intellectual property rights on difficult-to-achieve input characteristics Even assuming that terminator technologies (Table 1). c are not used, there is cause for concern about The potential benefits of plant biotech- the rights of developing countries to use their nology are considerable, but are unlikely to own genetic resources, the freedom of their be realized unless seeds are provided free or plant breeders to use new technologies to at nominal cost. This will require heavy pub- develop locally adapted varieties, and the lic investment by national governments and protection of poor farmers from exploita- donors, at times in collaboration with the tion. In part, these concerns result from the private sector, both in the research and in the privatization of crop genetic improvement, subsequent distribution of seed and techni- the rapid expansion of corporate ownership cal advice. Breeding programmes will also of key technologies and genetic information need to include crops such as cassava, upland and materials, and the competitive pressure rice, African maize, sorghum and millet, on these companies to capture world market which are the food staples and provide share as rapidly as possible employment for the 650 million rural poor It is only recently that intellectual proper- who need greater stability and reliability of ty rights (IPR) have become an important yield as much as increased yield. factor in plant breeding, primarily through the greater use of utility patents. Such patents The role of the public sector have stimulated greater investment in crop None of this will happen through marketing improvement research in industrialized by multinational seed companies, particu- countries, but they are also creating major larly if they decide to deploy gene-protection problems and potentially significant addi- technologies, commonly referred to as ter- tional expense for the already financially con- minator gene technologies, which will mean strained public-sector breeding programmes that farmers cannot save seed from the crop that produce seeds for poor farmers. and sow it to get the next crop. In developing Figure 2 Biotechnology products of value in The success of the Green Revolution was countries roughly 1.4 billion farmers still developing countries. a, Interspecific progenies based on international collaboration which rely on saving seed for their planting materi- of Asian ǂ African rice. Rows 3 and 4 from the included the free exchange of genetic diversi- als and many gain access to new varieties right have vigorous growth with droopy lower ty and information. Most of the ‘added value’ through farmer-to-farmer trade. Much of leaves that suppress weeds. (Courtesy of M. present in modern crops has been accumu- the success of the Green Revolution was due Jones.) b, Transgenic rice grain containing ȋ- lated over the centuries by farmers them- to the true-breeding nature of the higher- carotene (provitamin A). (Courtesy of I. selves as they selected their best plants as the yielding rice and wheat varieties. Potrykus and P. Beyer.) c, Transgenic rice (left) source of seed for the next planting. These While terminator technology is clearly with increased citrate production and exudation ‘land races’ have traditionally been provided designed to prevent rather than encourage by roots, tolerates aluminium (100 ȖM at pH free of charge by developing countries to the such spread of proprietary varieties among 4.5) better than control. (Courtesy of L. Herrera world community. The CGIAR centres add poor farmers, some argue that it will do them Estrella.) value through selective breeding, and the no harm because they can still use and superior varieties they generate are widely

NATURE | VOL 402 | SUPP | 2 DECEMBER 1999 | www.nature.com © 1999 Macmillan Magazines Ltd C57 impacts distributed without charge, benefiting both rice or Thailand’s Jasmine rice. The granting talking and reaching decisions is required. developing and developed countries. of free licenses to use such materials in We believe a global public dialogue is needed Patents on biotechnology methods and breeding programmes in the country of which will involve everyone on an equal materials, and even on plant varieties, are origin of the trait might gain the apprecia- footing — the seed companies, consumer complicating and undermining these collab- tion of developing country researchers and groups, environmental groups, indepen- orative relationships. Public-sector research governments. dent scientists, and representatives of gov- institutions in industrialized countries no Finally, the current opposition to GM ernments, particularly from the developing longer fully share new information and tech- crops and foods is likely to spread from nations. nology. Rather, they patent and license and Europe to the developing countries and Agriculture in the twenty-first century have special offices charged with maximiz- maybe even to North America unless there is will need to be more productive and less ing their financial return from licensing. greater public reassurance. At the heart of the damaging to the environment than agricul- Commercial production of any genetically debate about the safety of GM crops and ture has been in the twentieth. An increased engineered crop variety requires dozens of their food derivatives is the issue of relative effort is needed to assure that the benefits of patents and licenses. It is only the big compa- benefits and risks. The debate is particularly agricultural research reach the hundreds of nies that can afford to put together the IPR impassioned in Europe. Some of it is moti- millions of poor farmers who have benefited portfolios necessary to give them the free- vated by anti-corporate or anti-American little from previous research. We believe that dom to operate. And now, under the TRIPS sentiment, but underlying the rhetoric are biotechnology has significant potential to (Trade-Related Aspects of Intellectual Prop- genuine concerns about lack of consumer help meet these objectives but that this erty Rights) agreement of the World Trade benefits, about ethics, about the environ- potential is threatened by a polarized debate Organization, most developing countries ment and about the potential impact on that grows increasingly acrimonious. We are required to put in place their own IPR human health12–16. need to reverse this trend, to begin working systems, including IPR for plants. Further- Much of the opposition tends to lump together, to share our various concerns, and more, all of this ‘ownership’ of plant genetic together the various risks — some real, some to assure the new technologies are applied to resources is causing developing countries to imaginary — and to assume there are generic agriculture only when this can be done safely rethink their policies concerning access to hazards17. However, GM organisms are not and effectively in helping to achieve future the national biodiversity they control, and all the same and each provides different food security for our world. new restrictions are likely. potential benefits to different people and dif- Note added in proof: We commend the So far, international negotiations rele- ferent environmental and health risks. Calls Monsanto Company’s recent public vant to agricultural biotechnology and plant for general moratoria are not appropriate. commitment not to commercialize sterile genetic resources have not been effectively Each new transgene and each new GM crop seed technologies and encourage other coordinated. There are inconsistencies, and containing it needs to be considered in its companies to follow their lead. the interests of poor farmers in developing own right. Well planned field tests are cru- Gordon Conway and Gary Toenniessen are at the countries have not been well represented. cial, particularly in the developing countries Rockefeller Foundation, New York, New York The days of unencumbered free exchange of where the risks of using, or not using, a GM 10018, USA. plant genetic materials are no doubt over, crop may be quite different from those in 1. Pardey, P. G. Alston, J. M., Christian, J. E. & Fan, S. Summary of and agreements and procedures need to be industrialized countries. a Productive Partnership: The Benefits from U.S. Participation in the CGIAR (International Food Policy Research Institute, formulated to ensure that public-sector The multinational companies could take Washington DC, 1996). institutions have access to the technological a number of specific decisions in this area 2. Conway, G. R. The Doubly Green Revolution: Food for All in the and genetic resources needed to produce that would improve acceptance of plant 21st Century (Penguin Books, London/Cornell University improved crop varieties for farmers in devel- biotechnology in both the developing and Press, Ithaca NY, 1999). 3. UNICEF. The State of the World’s Children 1998 (Oxford Univ. oping countries who will not be well served the industrialized world. First, consumers Press, Oxford/New York, 1998). by the for-profit sector. If the big life-science have a right to choose whether to eat GM 4. Somer, A. & West, K. P. Vitamin A Deficiency: Health, Survival companies wish to find a receptive and grow- foods or not and although there are serious and Vision (Oxford Univ. Press, New York and Oxford, 1966). ing market in developing countries, they will logistic problems in separating crops all the 5. Mann, C. C. Science 283, 310–314 (1999). 6. Cassman. K. G. Proc. Natl Acad. Sci. USA 96, 5952–5959 (1999). need to work with the public sector to make way from field to retail sale, the agricultural 7. Pingali, P. L. & Heisey, P. W. Cereal Productivity in Developing sure this happens. seed industry should come out immediately Countries: Past Trends and Future Prospects. CIMMYT and strongly in favour of labelling. Second, Economics Paper 99-03 (CIMMYT, Mexico, 1999). Some solutions 8. Leonard, H. J. in Environment and the Poor: Development the industry should disavow use of the termi- Strategies for a Common Agenda (ed. Leonard, H. J.) 3–45 While negotiations are underway, there are a nator technology in developing countries (Overseas Development Council, Washington DC, 1989). number of things that should be done. With and, third, it should phase out the use of 9. James, C. Global Review of Commercialized Transgenic Crops: little competitive loss, seed companies could antibiotic-resistance genes as a means of 1998. ISAAA Briefs No. 8. (International Service for Acquisition of Agri-biotech Applications, Ithaca NY, 1998). agree to use the PVP system (including selecting transgenic plants. Alternatives exist 10.Mann, C. C. Science 283, 314–316 (1999). provisions allowing seed saving and sharing and should be used. 11.Ye, X. D. et al. Science (submitted). by farmers) in developing countries in coop- The Rockefeller Foundation and other 12.The Royal Society of London. Genetically Modified Plants for eration with public plant-breeding agencies, donors have invested significant sums in Food Use (The Royal Society, London, 1998). 13.Nuffield Council on Bioethics. Genetically Modified Crops: The rather than using patents or terminator helping developing countries put in place Ethical and Social Issues (Nuffield Council on Bioethics, technologies to protect their varieties. biosafety regulations and the facilities neces- London, 1999). To speed the development of biotechnol- sary for biosafety testing of new crops and 14.UN Food and Agriculture Organization. Biotechnology and Food Safety. FAO Food and Nutrition Paper 61. (World Health ogy capacity in developing countries, foods, but much more needs to be done. The Organization/FAO, Rome, 1996). companies that have IPR claims over certain big life-science companies could join forces 15.Rissler, J. & Mellon, M. The Ecological Risks of Engineered Crops key techniques or materials might agree to and establish a fellowship programme for (MIT Press, Cambridge MA/London, 1996). license these for use in developing countries training developing country scientists in 16.May, R. Genetically Modified Foods: Facts, Worries, Policies and Public Confidence (http://www.2.dti.gov.uk/ost/ at no cost. crop biotechnology, biosafety, intellectual ostbusiness/gen.html, 1999). We would also like to see an agreement to property rights and international negotia- 17.Pretty, J. The Biochemist (in the press). share the financial rewards from IPR claims tions administered by a neutral fellowship Acknowledgements. We thank M. Lipton, S. Dryden, R. May and on crop varieties or crop traits of distinct agency. colleagues at the Rockefeller Foundation for comments on an national origin, such as South Asian Basmati Most important of all, a new way of earlier draft of this article.

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