Science & Society

Special Issue: Systems Biology

How should we tackle the global risks to plant health? Robin Fears1, Eva-Mari Aro2, Maria Salome Pais3,4, and Volker ter Meulen5 1

Biosciences Programme Secretariat, EASAC, German National Academy of Sciences Leopoldina, 06019 Halle, Germany Molecular Plant Biology, Department of Biochemistry, University of Turku, 20520 Turku, Finland 3 Plant Systems Biology Laboratory, Centre of Biodiversity, Functional and Integrative Genomics, Science Faculty of Lisbon University, 1749-016 Lisbon, Portugal 4 Academy of Sciences of Lisbon, Lisbon, Portugal 5 Biosciences Programme Chairman, EASAC, German National Academy of Sciences, Leopoldina, 06019 Halle, Germany 2

The introduction and spread of plant pests and diseases has significant consequences for agriculture, horticulture, forestry, and natural habitats. Opportunities arising from scientific advances must be better used to inform regulation of trade and underpin chemical and alternative controls and breeding of plants resistant to biotic stress. According to the latest estimates from the FAO (Food and Agriculture Organisation of the United Nations), 840 million people, 12% of the global population, were unable to meet their dietary energy requirements (http://www. fao.org/publications/sofi/en). At least as many more lack essential vitamins and minerals. Agriculture faces major challenges to deliver food and nutrition security at a time of increasing pressures from climate change, social and economic inequity and instability, and the continuing need to avoid further losses in ecosystem biodiversity. The introduction and spread of pests and diseases among food crops and other plant species, in forestry, horticulture, and natural habitats, has significant consequences for sustainable agriculture, environmental protection, and ecosystem services. Accurate information on crop losses from pests and diseases is often not available, but 30–40% loss in developing countries annually has been estimated [1]. Among recent major problems are wheat stem rust, coffee wilt, rice bacterial blight, potato late blight, maize smut, and soybean wilt [2]. Global problems require global action. One necessary instrument is the International Plant Protection Convention (IPPC), a multilateral treaty overseen by the FAO to secure coordinated action to prevent and control the crossborder entry and spread of pests of plants and plant products. According to World Trade Organisation rules, countries can choose their own phytosanitary standards to protect plant health as long as they are non-discriminatory and justifiable by science. However, this discretion has resulted in some national and regional regulations that become a significant barrier to trade. In the European Union Corresponding author: Aro, E.-M. ([email protected]). 1360-1385/$ – see front matter ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.02.010

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(EU), the European Commission is currently reforming legislation to reinforce certain aspects of quarantine and other technical measures to control movement of plants and plant products. It is vital that such reform is based on sound science for assessing and managing risks. Constraints on trade across borders can only be part of the solution to tackling the risks to plant health. Significant problems are also occasioned by the natural dispersal and movement of pests, diseases, and their vectors and there is accumulating evidence for the multiple impacts of climate change as a global threat to plant health [3]. A 2014 report prepared by EASAC, the European Academies Science Advisory Council [EASAC (2014) Risks to Plant Health: EASAC Statement on European Union Priorities for Tackling Emerging Plant Pests and Diseases (http:// www.easac.eu)], draws attention to the importance of developing an integrated strategy, based on scientific excellence, combining efforts to control international trade in plant and plant products with actions to develop improved plant varieties resistant to biotic stress, new crop protection controls, and other integrated pest management (IPM). EASAC was formed by the national science academies of the EU Member States to enable them to collaborate in giving advice to policy makers; the common element in the various dimensions of this broad strategy is the imperative to generate and implement new knowledge, capitalising on the opportunities now coming within range, for example, in genomics. Although EASAC’s remit is to advice on options for European policy makers, the issues and remedies are of global relevance. In this article we expand on the 2014 EASAC report and other recent analysis [EASAC (2013) Planting the Future: Opportunities and Challenges for Using Crop Genetic Improvement Technologies for Sustainable Agriculture (http://www.easac.eu/ home/reports-and-statements.html)] to discuss global aspects of the challenges ahead. We emphasise the need for an international framework with coherent policy objectives and explore the emerging opportunities for science and technology. Control of trade in plants and plant products The current controls on plant movement have been only partially effective in preventing entry, establishment, and spread of harmful organisms into new territories. Decision making has often been too slow and concentrates on known threats, whereas all countries need to prepare to cope with

Science & Society the consequences of globalisation in terms of new trade routes, as well as climate challenges and a more diverse range of pests and diseases [2,3]. This flexibility in preparedness should encompass the following four strategies: (i) Increased collaboration between countries and regions to identify potential threats to plant health, with increased sharing of epidemiological and other intelligence, and the comparison of mitigation strategies. (ii) Raising public awareness of the risks to plant health and the need to prepare for future challenges. (iii) Putting in place the necessary scientific infrastructure and scientific advisory capabilities to support modernisation of the surveillance and regulatory systems, based on rapid developments in diagnostic, information technology (IT), modelling, and communication methodologies. (iv) Risk-based assessment of priorities, focusing on those organisms posing the greatest threat of incursion and establishment with the greatest environmental, social, and economic consequences. For each strategy, the capability of the national authorities involved would be strengthened by increasing the contribution from university departments and public research institutes. Durable protection of plant health Control of plant movement across borders must be accompanied by commitment to improving plant health durably in other ways: by decreasing the vulnerability of plants and ecosystems and by mitigating the impact once a hazard is established. This requires research and its translation in order to develop improved plant varieties, new chemical control measures, and novel approaches, such as the encouragement of associated microbial communities that naturally counter plant pests and diseases. No single approach will be a panacea; all technological options should be kept open and new approaches must be integrated within good agronomic practice. Pesticides Pesticides bring great benefits yet many also pose significant threats to human health and the environment. Pesticides lack selectivity and do not discriminate between beneficial and pathogenic organisms. For fungicides the problem is compounded by the high levels that have customarily been applied, leading to accelerated genetic change in pathogen populations and the evolution of fungicide resistance that has reduced effective control [4]. There is scope for finding new classes of agrochemicals as well as smart alternatives to chemical control [5]. There is also room for improved policy coherence. The recent introduction of pesticide legislation in Europe means that fewer approved chemical control options will be available. The current policy objective to reduce pesticide use, although set with the best of intentions, is likely to have adverse consequences for maintaining crop productivity unless crops can be protected in other ways, in particular by conferring genetic resistance.

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Breeding and biotechnology for improved resistance to biotic stress The genetic improvement of plants, to acquire greater resilience and resistance, can be accomplished by more precise breeding techniques (in particular, markerassisted selection), by genetic modification to introduce desirable traits, and by other, newer crop genetic improvement technologies [see EASAC (2013) report cited above]. For example, disease resistance can be engineered based on advances in understanding the plant immune system [6]. It is critically important that genetically modified (GM) crops are introduced as part of IPM systems rather than as isolated, stand-alone solutions. More than 25 years of experience worldwide has accrued, on the impact of the first generation GM crops that are endowed with traits for herbicide tolerance or insect resistance or both. Although some regions are still very cautious in their attitude to these crops, most notably Europe, dramatic advances in science and innovation are occurring. For example, in African countries, engineered pest/disease resistance and/or herbicide tolerance is being studied in banana/ plantain (Musa), cabbage (Brassica oleracea), cassava (Manihot esculenta), coconut (Cocus nucifera), cotton (Gossypium ssp.), cowpea (Vigna unguiculata), maize (Zea mays), potato (Solanum tuberosum), rice (Oryza sativa), sorghum (Sorghum vulgare), sweet potato (Ipomea batatas), sugar cane (Saccharum), and tomato (Solanum lycopersicum), among other crops [see EASAC (2013) report cited above]. It is vital that regulatory systems governing the approval and introduction of GM crops are calibrated to be science-based, proportionate, and predictable, addressing benefit versus risk and regulating specific traits and products rather than the technology. Unfortunately, there are still problems in the EU where approval remains slow, expensive, and subject to political pressures and does not properly take into account the worldwide accumulating evidence on benefit and safety. There are other important techniques that have emerged from advances in biotechnology, for use in programmes of crop improvement [7]. For several of these new breeding techniques, the commercialised crop would be free of genes foreign to the species. For example, cisgenesis allows for the specific transfer of genes between closely related, crossable plant species, and current research is evaluating resistance to disease in apples (Malus domestica), bananas (Musa), grapes (Vitis vinifera), and potatoes (S. tuberosum). However, in some regions, including the EU, there is confusion on how the new breeding techniques might be regulated and, until legal clarity is reached, application is hampered. It is important for regulatory authorities to confirm that the products of new breeding techniques, when they do not contain foreign DNA, do not fall within the scope of legislation on GM organisms [see EASAC (2013) and (2014) reports cited above]. Promoting, sharing, and using research Strategic objectives for a multidisciplinary, evidence-based strategy include: (i) to analyse and tackle the effects of globalisation on plant health (in particular trade, climate change, and potential for bioterrorism); (ii) to model disease 207

Science & Society Box 1. Scientific priorities for action to underpin the broad strategic objectives for tackling risks to plant health Surveillance systems Long-term and new forms of monitoring; collection of standardised data; extension of surveillance systems to the natural environment; and early-warning systems. Research agenda Support for IPPC and regional implementation; augmenting scientific infrastructure; pest and disease diagnosis and characterisation; ecology and epidemiology of plant pests and pathogens and their relationships with hosts and vectors; mechanisms of plant disease resistance; and biological and cultural strategies for sustainable pest and disease management. Innovation Translation of research findings to overcome limitations of current crop protection chemical approaches; breeding improved plants, resistance to biotic stress; using sound science, evidence-based approaches to inform options for regulation; and public engagement to articulate the implications of research findings and the value of innovation.

emergence and spread in farmed and other landscapes; (iii) to implement rapid monitoring and detection systems; (iv) to collectively harness the individual tools available, such as movement control, chemical control, biological control, and plant breeding; and (v) to measure impact. There is a broad range of actions required to pursue these objectives (Box 1), relevant not only to applications in agriculture but also to many additional goods and services including biofuels, other products of the bioeconomy, as well as ecosystem services and carbon sequestration. Accomplishing this strategy will depend on better networking across the scientific domains and coordination worldwide to reduce current fragmentation in research objectives and capabilities. In some regions, the capacity to engage in research and to use research outputs is limited by the shortage of skills in key disciplines, including taxonomy, plant pathology, epidemiology, environmental microbiology, and plant breeding [5,6], and these deficits also need to be tackled.

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(iv) Inconsistency between the objectives of industrialised countries to support global development objectives and the spillover from their domestic regulatory policies in influencing decisions by developing countries about innovation. There is a related disconnect with domestic initiatives to support university spinouts and other smaller companies, when the operation of regulatory frameworks may deter all but the biggest companies. Some plant health policy is currently global in orientation (the IPCC) but much is national or regional. It is necessary to learn from what can work globally, in balancing the regulatory role with creating room for innovation, in order to develop new coherence in those policy areas that are currently fragmented. One prerequisite to addressing the policy disconnects is to raise the political and public visibility of plant health issues, for example, in the UN strategy on the post-2015 agenda for sustainable development as part of the broader goals to improve food yield and reduce post-harvest losses [High-level Panel of Eminent Persons on the Post2015 Development Agenda (2013) A New Global Partnership: Eradicate Poverty and Transform Economies Through Sustainable Development, United Nations (http://www. un.org/sg/management/pdf/HLP_P2015_Report.pdf)]. It is also desirable to encompass plant health within the broader framework of disease ecology that links human and animal health, by applying the ‘One Health’ concept [8] to improve understanding of pest and disease (re-)emergence and increase capacity to forecast and tackle outbreaks. Addressing the policy disconnects entails significant responsibilities for the scientific community, meriting support from the academies of science worldwide. Although the evidence may sometimes be uncertain and some of the related policies controversial, what should always be made clear is that the procedures for generating scientific advice have been conducted openly and robustly to share understanding about emerging threats and the means to protect and promote plant health globally. Acknowledgements

Policy disconnects Threats to world agriculture and ecosystem services, associated with risks to plant health, have been posited as among the existential crises facing humanity. If the scientific actions (Box 1) are to be successfully accomplished, it is also necessary to understand and resolve disconnects in the present policy landscape. These disconnects include: (i) Inconsistency between willingness to invest in fundamental plant science research, while neglecting to use the outputs from research for innovation. Efforts worldwide to conserve, characterise, and maintain plant genetic resources are also often disconnected from readiness to use those resources for improved plant breeding. (ii) Incongruence between the objective to reduce chemical pesticide use and the overregulation of alternative genetic approaches to protecting crops. (iii) Lack of coherence when countries have approved the importation of food or feed of GM origin yet have not approved the same GM crop for cultivation. 208

We thank all those who contributed to the discussion for preparing the EASAC report [EASAC (2014) Risks to Plant Health: EASAC Statement on European Union Priorities for Tackling Emerging Plant Pests and Diseases (http://www.easac.eu)].

References 1 Flood, J. (2010) The importance of plant health to food security. Food Secur. 2, 215–231 2 Fisher, M.C. et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 3 Bebber, D.P. et al. (2013) Crop pests and pathogens moving polewards in a warming world. Nat. Clim. Change 3, 985–988 4 Cools, H.J. and Hammond-Koseck, K.E. (2013) Exploitation of genomics in fungicide research: current status and future perspectives. Mol. Plant Pathol. 14, 197–210 5 Lamberth, C. et al. (2013) Current challenges and trends in the discovery of agrochemicals. Science 341, 742–746 6 Dangl, J.L. et al. (2013) Pivoting the plant immune system from dissection to deployment. Science 341, 746–751 7 Lusser, M. et al. (2012) Deployment of new biotechnologies in plant breeding. Nat. Biotechnol. 30, 231–239 8 National Research Council (2011) Fungal Diseases: An Emerging Threat to Human, Animal, and Plant Health: Workshop Summary, The National Academies Press

How should we tackle the global risks to plant health?

The introduction and spread of plant pests and diseases has significant consequences for agriculture, horticulture, forestry, and natural habitats. Op...
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