Genetic Modification for Disease Resistance: A Position Paper PDF

Genetic modification for disease resistance: a position paper Peter Scott, Jennifer Thomson, David Grzywacz, Serge Savary, Richard Strange, Jean B. Ristaino & Lise Korsten Food Security The Science, Sociology and Economics of Food Production and Access to Food ISSN 1876-4517 Food Sec. DOI 10.100...

Genetic modification for disease resistance: a position paper Peter Scott, Jennifer Thomson, David Grzywacz, Serge Savary, Richard Strange, Jean B. Ristaino & Lise Korsten Food Security The Science, Sociology and Economics of Food Production and Access to Food ISSN 1876-4517 Food Sec. DOI 10.1007/s12571-016-0591-9 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht and International Society for Plant Pathology. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23  Author's personal copy Food Sec. DOI 10.1007/s12571-016-0591-9 ORIGINAL PAPER Genetic modification for disease resistance: a position paper Peter Scott 1 & Jennifer Thomson 2 & David Grzywacz 3 & Serge Savary 4 & Richard Strange 5 & Jean B. Ristaino 6 & Lise Korsten 7 Received: 6 June 2016 / Accepted: 10 June 2016 # Springer Science+Business Media Dordrecht and International Society for Plant Pathology 2016 Abstract This Position Paper was prepared by members of GM crops is outlined. GM could make an additional contri- the Task Force on Global Food Security of the International bution to food security but its potential has been controversial, Society for Plant Pathology. An objective approach is pro- sometimes because of fixed views that GM is unnatural and posed to the assessment of the potential of genetic modifica- risky. These have no factual basis: GM technology, where tion (GM) to reduce the impact of crop diseases. The addition adopted, is widely regulated and no evidence has been report- of GM to the plant breeder’s conventional toolbox facilitates ed of adverse consequences for human health. The potential gene-by-gene introduction into breeding programmes of well- benefits of GM could be particularly valuable for the devel- defined characters, while also allowing access to genes from a oping world but there are numerous constraints. These include greatly extended range of organisms. The current status of cost, inadequate seed supply systems, reluctance to adopt This Position Paper was prepared by members of the Task Force on Global Food Security (http://www.isppweb.org/foodsecurity_tf.asp) of the International Society for Plant Pathology. A Position Paper of the Task Force on Global Food Security is a factual summary of the principal aspects of a topic, from the perspective of plant pathology, to present a position from which the merits and drawbacks of particular issues that arise within that topic can be rationally discussed. * Peter Scott Lise Korsten [email protected] [email protected] 1 Jennifer Thomson International Society for Plant Pathology, Oxford, UK [email protected] 2 Department of Molecular and Cell Biology, University of Cape Town, Rondebosch 7701, Republic of South Africa 3 David Grzywacz NRI - Department of Agriculture Health and Environment, [email protected] University of Greenwich, Old Royal Naval College, Park Row, Greenwich, London SE10 9LS, UK 4 INRA, UMR1248 AGIR, Université Toulouse, 24 Chemin de Borde Serge Savary Rouge, Auzeville, F-31326 Toulouse, Castanet-Tolosan, France [email protected] 5 Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK Richard Strange 6 USAID Senior Science Advisor, Department of Plant Pathology, [email protected] North Carolina State University, Raleigh, NC 27695, USA 7 Department of Microbiology and Plant Pathology, University of Jean B. Ristaino Pretoria, Lynnwood Road, Hillcrest, Pretoria, Republic of South [email protected] Africa  Author's personal copy Scott P. et al. unfamiliar technology, concern about markets, inadequacy of pathogens and the emergence of new plant diseases, and by local regulatory systems, mismatch between research and the need for crops to be grown more intensively as global growers’ needs, and limited technical resources. The lower population grows with only limited opportunities for increas- cost of new gene-editing methods should open the practice of ing the area of cultivated land. GM beyond multinational corporations. As yet there are few Management of plant diseases can be effected through crop examples of utilization of GM-based resistance to plant diseases. husbandry and phytosanitary measures, through the use of Two cases, papaya ringspot virus and banana xanthomonas wilt, pesticides, and through plant breeding. But these measures are outlined. In the developing world there are many more po- have limitations: for example the diversity of pesticides is tential cases whose progress is prevented by the absence of ad- declining under more rigorous regulatory control, and resis- equate biosafety regulation. It is concluded that there is untapped tance to pesticides is increasing. New disease management potential for using GM to introduce disease resistance. An methodologies are needed in compensation. objective approach to mobilizing this potential is recommended, Genetic improvement of crop plants by selective breeding to address the severe impact of plant disease on food security. presents a particularly cost-effective and easily adopted means of disease management, as the only action required of the Keywords Genetic modification. Genetic engineering. grower is to use appropriate seed or other planting material Plant breeding. Food security. Disease resistance. (Evenson and Gollin 2003). Developing countries. Biosafety Genetic improvement of plants has been practised since the beginning of agriculture through selection of improved vari- ants, occurring either spontaneously or amongst the progeny Initial statement of cross-breeding, or sometimes through treatment to induce mutations. The normal multiplication processes of crops then The ISPP Task Force on Global Food Security recognizes the allow stocks of improved cultivars to be built up. potential of genetic modification (GM) to reduce the impact of Conventional plant breeding, which is the basis of nearly plant diseases on the productivity, safety and quality of crops all modern crop cultivars, has been typified as Bcrossing the in agriculture, horticulture and forestry, and advocates an ob- best with the best and hoping for the best^. For all its limita- jective approach to the assessment of that potential. tions and despite the typical uncertainty of what genetic change is actually responsible for the improved performance of its products, plant breeding retains its importance and ac- Definition ceptance as a key element in crop husbandry (Tester and Langridge 2010). It is taken for granted as a central and safe Genetic modification (GM), also known as genetic engineer- man-made contribution to food security and has a special im- ing, is here defined as alteration of the genetic material of a portance in the development of cultivars with improved resis- plant through human intervention using methods other than tance to crop pests and diseases. cross-fertilization. The products of genetic modification are referred to here as genetically modified (GM) plants. GM as a tool for plant breeding Food security, plant diseases and the value of plant The plant breeder’s toolbox traditionally contained devices for breeding effecting hybridization between stocks of promising plant ma- terial for cross-breeding, and systems of selection of improved Global crop production needs to be substantially increased to variants among progeny for multiplication. The versatility of meet the demands of a growing population. Of the population the toolbox has been greatly increased by the tools of genetic of more than 7 billion people, some 800 million do not have modification (GM). GM facilitates gene-by-gene introduction enough to eat today. The vast majority of these people live in into breeding programmes of well-defined characters, while developing countries (FAO 2015). By 2050, the global popula- also allowing access to genes from a greatly extended range of tion is expected to exceed 9 billion (US Census Bureau 2015). organisms since there is no reliance on compatibility in hy- It has been estimated that some 15 % of global food production bridization. Not only is the pool of available variation enor- is lost to plant disease (Oerke and Dehne 2008). In developing mously increased (notably for resistance to pathogens) but far countries losses might be much higher. Plant pathologists can- greater precision is achievable in the introduction of each de- not ignore the juxtaposition of these figures for food shortage sirable genetic trait, without other unwanted genes. and the damage to food production caused by plant pathogens. Furthermore the release of unwanted variation through genetic The impact of plant diseases is exacerbated by increasing recombination that is an inherent feature of hybridization is globalization and trade, which facilitate the spread of avoided. Consequently the time needed to breed improved  Author's personal copy Genetic modification for disease resistance cultivars bearing specific traits is shortened. It should be rec- the contention that GM technology per se is more likely than ognized, however, that the cost to a breeder of acquiring GM conventional plant breeding to create dangerous new pheno- capability is likely to be significant. GM as defined here in- types. Indeed the reverse can be argued, since GM should cludes the use of gene-editing tools such as CRISPRs allow far greater control over genetic change than convention- (Ledford 2015). al breeding. As a precaution against risk, the use of GM technology is officially regulated in most countries, at the laboratory The current status of GM crops level and in the deployment of the products of GM in agriculture. Such regulation may need to be rationalized, GM crops were first used in agriculture in 1996 when 1.7 for example in some countries where it precludes research million hectares were planted (James 2015). There has been on GM or the deployment of research outputs, or in others an increasing trend since then, to a total of 180 million hect- that lack robust objective oversight. However, the value of ares in 2015, principally of four crops: soybean, maize, cotton appropriate and proportionate regulation of GM is widely and oilseed rape (canola). Of the 28 countries in which GM recognized. crops have been deployed, 20 are developing countries. The No evidence has been reported of adverse consequences for principal traits introduced into GM crops up to 2015 are tol- human health from consuming the products of crops devel- erance of the herbicide glyphosate, and resistance to insects oped using GM technology (World Health Organization 2014; from Bacillus thuringiensis. New GM crops of the principal Suzie et al. 2008; National Academies of Sciences, four species and also potato, beans, eggplant, papaya, squash, Engineering, and Medicine 2016). This fact is based on a sugar beet, eucalyptus, poplar and apple are now being devel- substantial and growing body of scientific publications. oped with these characters, and with drought tolerance, dis- There is a case for adoption of a system of objective collec- ease resistance, salt tolerance, nitrogen use efficiency, speed of tion, evaluation and dissemination of such evidence as a pre- ripening, storage quality, nutritional versatility and other char- caution against misleading assertions of risk. acteristics. Field trials of GM potato are being conducted in Concerns have been raised about the impact of GM on the Bangladesh, India, Indonesia and Uganda to assess their resis- environment, though these are often associated with the intro- tance to late blight, caused by Phytophthora infestans. duced trait rather than with the use of GM to introduce it. Reservations about the safety of GM crops continue to limit However, there is also evidence of environmental benefit, for their use, notably in Europe where a majority of the Member example through reduced pesticide use and (with herbicide- States of the European Union have opted to prohibit their tolerant cultivars) conservation tillage (Sanvido et al. 2007). cultivation (European Commission 2015). Evidence-based evaluation Benefits and risks Decision making on the use of GM, like decision making on any There is a strong case for exploring the use of such potentially other technology for plant disease management, should be valuable tools which present new possibilities to meet the based on scientific evidence through critical and independent challenge of food security, extending the widely valued prac- evaluation of potential cost/benefit on a case-by-case basis, tice of plant breeding. Nevertheless, the potential of GM for taking into consideration economic, social and environmental crop improvement has been the subject of much controversy, issues. There is not yet an accepted structure for such evalua- sometimes based on fixed views that GM is unlike other tools tion, which should be rigorously science-based, and should in being unnatural and inherently risky. Thus it has been ar- preferably involve the public in its development and use. gued that the widespread use of GM to introduce insect resis- Such a structure would facilitate evidence-based decisions. tance derived from the bacterium Bacillus thuringiensis (Bt) into crops brings with it the risk of selection in insect popula- tions for the capacity to thrive in the presence of the genetic GM in the developing world resistance. Furthermore this could apply to non-target insects as well as those that are the target of the breeding programme. The potential benefits of GM-based cultivars in disease man- Such risks have been ascribed to the use of GM but are in fact agement could be considerable in the developing world. There a consequence of deploying the trait, not the technology used are however many constraints to be overcome (Adenle et al. to introduce it. 2013), including: The choice of traits for introduction by GM should be made with due consideration for the consequences of their deploy- – The high cost of development and deployment of GM- ment. There seems however to be no factual basis to support based cultivars. Because costs must be recouped,  Author's personal copy Scott P. et al. developers focus on major traits in globally significant Approval for their cultivation in Hawaii was granted by US crops.1** Government agencies. Their resistance to PRSV was substan- – Inadequate capacity of local seed supply systems to mul- tial and has enabled production of papaya to continue in tiply GM seed. Hawaii, where it had been threatened. The GM produce is – Growers’ reluctance to adopt an unfamiliar technology widely sold locally and exported. Like any other kind of re- that may be costly, may require seed to be sourced exter- sistance, it may be rendered less effective by the emergence of nally, and may evoke unfounded perceptions of risk. virulent strains of the pathogen. But as its efficacy is greater – Concern among growers that GM produce may be diffi- when the introduced CP gene is derived from locally damag- cult to sell, for example to EU countries. ing strains, there is scope for adapting the GM crop to the local – The challenge of establishing regulatory systems, and pathogen challenge. Papaya cultivars with CP and other GM- deploying GM in farming systems that differ from those in based forms of resistance to PRSV are now available for cul- developed countries where the technology was developed. tivation in other regions. Their utilization is limited mainly by – Discrepancy between the priorities of donor-funded re- reluctance to adopt GM technology. search and the needs of growers. Some other cases are less successful (Tripathi et al. 2009). In – Limited local research capacity to identify pathogens and East Africa the banana crop may be seriously affected by banana their variants as targets for development of GM cultivars. xanthomonas wilt (BXW) caused by the bacterium – The need to manage GM introductions to minimize po- Xanthomonas campestris pv. musacearum, which has spread tential build-up of pathogen virulence and avoid acciden- invasively since 2001. Yield may be reduced by 90 % within tal transfer of traits to weed species. a year of infection. This is a new disease and is of critical eco- – The risk to GM developers of legal liability for accidental nomic and social importance in Uganda where banana is the introduction of GM material into food chains designated staple crop. Banana cultivars show no resistance to the disease, as non-GM. so the International Institute of Tropical Agriculture (IITA), with – The need for effective seed production and distribution national and African partners, developed GM bananas express- systems to avoid proliferation of poor quality or fake GM ing the Hrap or Pflp genes from Capsicum annuum. These products. exhibited strong resistance to BXW in laboratory tests. The most resistant lines were planted in a Confined Field Trial (CFT) after approval from the National Biosafety Committee. They are Examples of GM-based disease resistance however unable to progress further because official biosafety regulation has not been established in Uganda. Attempts to pass To date, there are few examples of utilization of GM-based new legislation have been stalled by campaigns suggesting resistance to plant diseases. Two cases are outlined here. A health risks and the likelihood of market collapse. basis for evaluating other prospects has been discussed There are many such examples of experimental GM-based (Collinge et al. 2016). lines in developing countries that are prevented from In Hawaii in the 1990s, the increasingly severe effects of progressing beyond the CFT stage by the need for effective papaya ringspot virus (PRSV) were addressed by develop- biosafety regulation, which would allow evidence-based con- ment of GM papaya cultivars with resistance based on the sideration of benefits and risks (Bailey et al. 2014). introduction of coat protein (CP) genes from mild strains of the pathogen (Tripathi et al. 2008; Fermin et al. 2010). Conclusion The ISPP Task Force on Global Food Security considers that 1 ** At present, the costs are such that the choice of GM for disease there is untapped potential for using GM to introduce resis- management in developing countries should be critically compared with tance to more pathogens in a wider variety of crops. The Task alternative strategies for cost effectiveness. The products of commercial Force advocates an objective approach to assessment and investment may however be locally available: for example the African Agricultural Technology Foundation introduces genes donated by multi- application of the potential of GM, as one means of address- nationals into African varieties and provides farmers with assistance in ing the severe impact of plant disease on food security. using them (Delmer et al. 2003). The lower cost of new gene-editing More detailed treatment of the topic can be found here methods should open the practice of GM beyond multinational corpora- (Bennett and Jennings 2014; Qaim 2015; Collinge 2016; tions, reducing the constraint to focus on major crops and increasing the scope for small companies and academic researchers to develop GM National Academies of Sciences, Engineering, and Medicine cultivars (Ledford 2015). 2016).  Author's personal copy Genetic modification for disease resistance References US Census Bureau (2015). US Census Bureau International Database. h t t p s : / / w w w. c e n s u s. g o v / p o p u l a t i o n / i n t e r n a t i o n a l / data/idb/worldpopinfo.php Adenle, A. A., Moris, E. J., & Parayil, G. (2013). Status of development, World Health Organization (2014). Frequently asked questions on genet- regulation and adoption of GM agriculture in Africa: views and ically modified foods. http://www.who.int/foodsafety/areas_ positions of stakeholder groups. Food Policy, 43, 159–166. work/food-technology/faq-genetically-modified-food/en/ Bailey, R., Willoughby, R., & Grzywacz, D. (2014). On trial: agricultural biotechnology in Africa. Chatham House Research Paper: Energy, Environment and Resources July 2014, 1–26. Bennett, D. J., & Jennings, R. C. (2014). Successful Agricultural Innovation in Emerging Economies: New Genetic Technologies for Global Food Production. UK: Cambridge University Press. Peter Scott is a retired director of Collinge, D. B. (Ed.) (2016). Plant pathogen resistance biotechnology. CABI. As a former research sci- Hoboken: Wiley-Blackwell. entist at the Plant Breeding Collinge, D. B., Mullins, E., Jensen, B., & Jørgensen, H. J. L. (2016). The Institute, Cambridge, UK, he status and prospects for biotechnological approaches for attaining studied resistance to facultative sustainable disease resistance. Plant Pathogen Resistance fungal parasites of temperate ce- Biotechnology, 1–20. Hoboken: Wiley-Blackwell. reals. He worked as a plant pa- Delmer, D., Nottenburg, C., Graff, D., & Bennett, A. (2003). Intellectual thologist with plant breeders and property resources for international development in agriculture. geneticists with the aim of im- Plant Physiology, 133, 1666–1670. proving the disease resistance of European Commission (2015). Restrictions of geographical scope of cereal cultivars and the methods GMO applications/authorisations: Member States demands and out- by which resistance is selected in comes. http://ec.europa.eu/food/plant/gmo/authorisation breeding programmes. He was /cultivation/geographical_scope_en.htm. part of a team that introduced re- Evenson, R. E., & Gollin, D. (2003). Assessing the impact of the green sistance to eyespot (Oculimacula revolution, 1960 to 2000. Science, 300, 758–762. yallundae) into wheat from the wild grass Aegilops ventricosa. At CABI FAO (2015). The Millennium Development Goals Report 2015. he was responsible for information management and led the team that h t t p : / / w w w. u n. o r g / m i l l e n n i u m g o a l s / 2 0 1 5 _ M D G _ developed the Crop Protection Compendium. He has been President of Report/pdf/MDG%202015%20rev%20(July%201).pdf the British Society for Plant Pathology and of the International Society for Plant Pathology. Fermin, G. M., Castro, L. T., & Tennant, P. F. (2010). CP-transgenic and non-transgenic approaches for the control of papaya ringspot: current situation and challenges. Transgenic Plant Journal, 4, 1–15. James, C. (2015). Global Status of Commercialized Biotech/GM Crops: 2015. ISAAA Brief no. 51. International Service for the Acquisition of Agri-biotech applications, Ithaca, New York. Ledford, H. (2015). CRISPR, the disruptor. Nature, 522, 20–24. Jennifer A. Thomson has a BSc National Academies of Sciences, Engineering, and Medicine (2016). in Zoology from the University of Genetically Engineered Crops: Experiences and Prospects. Cape Town (UCT), an MA in Washington, DC: The National Academies Press 388 pp. Genetics from Cambridge Oerke, E. C., & Dehne, H. W. (2008). Safeguarding production losses in University and a PhD in major crops and the role of crop protection. Crop Protection, 23, Microbiology from Rhodes 275–285. University, South Africa. After a Qaim, M. (2015). Genetically modified crops and agricultural develop- post-doctoral fellowship at ment. Palgrave Studies in Agricultural Economics and Food Policy. Harvard, she was a Lecturer and London: Palgrave Macmillan. Associate Pro fessor at th e Sanvido, O., Romeis, J., & Bigler, F. (2007). Ecological impacts of ge- University of the Witwatersrand netically modified crops: ten years of field research and commercial and then started and ran the cultivation. Green Gene Technology, Advances in Biochemical Laboratory for Molecular and Engineering/Biotechnology, 107, 235–278. Cell Biology for the Council for Suzie, K., Julian, K.-C. M., & Pascal, M. W. D. (2008). Genetically Scientific and Industrial modified plants and human health. Journal of the Royal Society of Research. She was appointed Professor and Head of the Department of Medicine, 101, 290–298. Microbiology at UCT in 1988, a position she held for 12 years. She won Tester, M., & Langridge, P. (2010). Breeding technologies to increase the L’Oreal/UNESCO prize for Women in Science for Africa in 2004 and crop production in a changing world. Science, 327, 818–822. was awarded an Honorary Doctorate from the Sorbonne University, Paris Tripathi, S., Suzuki, J., Ferreira, S., & Gonsalves, D. (2008). Papaya in 2005. Her main research interests are the development of maize resis- ringspot virus-P: characteristics, pathogenicity, sequence variability tant to the African endemic Maize streak virus and tolerant to drought. and control. Molecular Plant Pathology, 9, 269–280. She has published two books on the subject of Genetically Modified Tripathi, L., Mwangi, M., Aritua, V., Tushemereirwe, W. K., Steffen, A., Organisms: Genes for Africa and Seeds for the Future. She is currently & Ranajit, B. (2009). Xanthomonas wilt: a threat to banana produc- Emeritus Professor in the Department of Molecular and Cell Biology at tion in east and Central Africa. Plant Disease, 93, 440–451. UCT.  Author's personal copy Scott P. et al. David Grzywacz is a researcher World in topics directly concerned with plant disease problems affecting on biological control of insect their food security. pests at the Natural Resources Institute of the University of Greenwich, UK. His research fo- cus has been on the use of insect pathogens for the control of pests and developing these as practical Jean Beagle Ristaino is a and commercial biocontrol prod- William Neal Reynolds ucts. This has covered deploying Distinguished Professor at North insect pathogens as conventional Carolina State University, USA, spray products and the develop- in the Department of Plant ment of genetically engineered Pathology where she directs the crops that express pathogen Emerging Plant Disease and genes. He has worked with re- Global Food Security cluster. search institutes, universities, SMEs and private sector clients in Africa, Her research career has focused Asia and South America. on Phytophthora diseases of glob- al importance including the popu- lation genetics and migrations of Serge Savary is a plant patholo- historic and present-day gist with the French institute for Phytophthora infestans. She leads agricultural research (INRA). His diagnostics workshops globally to research addresses botanical epide- improve capacity for rapid and accurate diagnosis and improved manage- miology, risk assessment, crop ment of Phytophthora diseases. She has been science advisor for govern- health management, analysis of ment, industry, foundations and academia in Central and South America, agricultural systems, and research East Africa, Southeast Asia and China. In 2012 the National Academy of prioritization. He has conducted re- Sciences named her a Jefferson Science Fellow to serve as science advisor search in West Africa, Central in the Bureau for Food Security at USAID Washington. She is the 2016 America, France, South-East and recipient of the American Phytopathological Society Excellence in South Asia in ORSTOM, IRD, International Service Award. IRRI, and INRA. His work has ad- dressed plant disease epidemiolo- gy and IPM in vegetables, le- gumes, and cassava in West Africa; plant disease epidemiology and crop loss analysis in coffee and bean in Central America; epidemiology and disease management in wheat and grapevine in France; and management of rice health in tropical Asia. His research involves simulation modelling, epidemiological and crop loss Lise Korsten is Professor of Plant experiments, and multivariate statistical analyses on large databases. This Pathology, Department of Plant perspective includes the agronomic and socio-economic contexts of agri- Science, University of Pretoria. culture and crop health related to sustainable crop health management. He is She is responsible for the food currently Vice-President of the International Society for Plant Pathology. safety programme within the University’s Institute for Food Nutrition and Well-Being. She is also responsible for the food safe- Richard Strange is Editor-in- ty and regulatory control Chief of Food Security. His back- programmes within the Centre of ground is in Plant Pathology, a Excellence Food Security of the subject to which he was attracted Department of Science and by its relevance to food security Technology, South Africa. She is and in which he has published a chief editor of Crop Protection over 100 papers and two books. and chairs the International He currently holds an Honorary Society for Plant Pathology’s Task Force on Global Food Security. She Chair at University College initiated the Food Law focus at the University of Pretoria. Professor London, UK, and is a Fellow of Korsten has addressed Parliament on Food Safety Control and has devel- the International Society for Plant oped a national framework for Government to develop a Food Control Pathology. He has been involved Authority. She developed South Africa‘s first biocontrol agent for fruit in numerous overseas projects, and established a biocontrol research group at the University of Pretoria. several of which were located in She established a fruit health group that focuses on food safety of fresh African countries, and has super- produce and on Sanitary and Phytosanitary aspects related to international vised Ph.D. students from these and other countries of the Developing trade.