Maximizing World Food Production through Disease Control

In the debate about the ability of global agriculture to provide food and nutritional security for the world's rising population, it is frequently stated that, by 2050, when the world's population will exceed 9.7 billion, 50%–60% more food than that produced at the end of the first decade of the twenty-first century will be needed. More agricultural land, more fertilizer, more water, and higher-yielding crops will therefore be needed to secure food supplies. These and related statements that are focused on increasing production fail to recognize that more reliable means of disease control could substantially improve the balance of the production–demand equation. Plant diseases caused or transmitted by a wide array of fungi, oomycetes, bacteria, viruses, nematodes, and insects inflict enormous annual crop production losses on a global scale. Among the world's most important food crops—rice, wheat, maize, potatoes, and soybeans—losses to pathogens are estimated to average 13%–22% annually (Oerke 2006, Savary et al. 2019), even after the use of resistant varieties and the application of large amounts of fungicide. However, epidemics are patchy in time and space—a phenomenon that confounds crop loss estimates, because losses at one spatial scale and location are extrapolated to greater and greater scales. Even if published estimates are scaled back twofold, losses are still very substantial and are likely to be particularly concentrated in food insecure hotspots that are least able to respond to shortages (Savary et al. 2019). Moreover, the consequences of the impact of diseases go deeper than simple yield losses, creating further economic costs and social concerns through reductions in food quality and safety (Savary et al. 2012). On the basis of the current population and levels of production, preventing a 10% loss in the world's food crop yield would provide sustenance for an additional 700 million people without the need to use additional resources. For most consumers, the possibility that plant diseases have such an impact and pose a continuing threat to food security goes unrecognized. However, the effectiveness of disease control approaches in agriculture is under constant threat because current approaches strongly focus on the widespread deployment of large scale, genetically uniform crops grown in high density stands. These conditions impose prolonged directional selection on pathogen populations, strongly favoring the emergence of novel variants with the ability to overcome resistance genes in the crops themselves or to counter the effect of fungicides. Indeed, since the advent of genetic and chemical methods of disease control in the first half of the twentieth century, a complex coevolutionary battle between crops and pathogens has developed into a war of attrition. Crop varieties carrying new resistance genes and fungicides with new modes of action give some short-term respite before evolutionary changes result in pathogens gaining the genetic advantage and defeating both genes and chemistry (Zhan et al. 2015). To minimize this continuous loss of food production requires a major rethink—a change of approach by scientists and recognition by governments and consumers that current expectations that society can limit the tools available for disease control while simultaneously demanding food quality to rise and prices to fall is unsustainable. Pricing food fairly and ensuring that the benefits flow back to the growers will allow the deployment of sustainable, integrated pathogen control strategies that require greater investment by those growers. Sustainable, integrated control requires adopting a variable, disruptive approach in which the deployment of resistance varies across both time and space. In contrast to genetically uniform monocultures, such use of genetic diversity presents pathogen populations with a shifting evolutionary target, leading to reduced population size and evolutionary potential (Burdon et al. 2016). Furthermore, such control will have major environmental benefits through reductions in the use of fungicides and in pressures on scarce land and water resources. Molecular technologies have increased the efficiency of plant breeding by speeding the incorporation of many traits including pathogen and pest resistance into modern cultivars, enhancing opportunities to develop multiresistance gene pyramids or cassettes (Steuernagel et al. 2016), introduced precision gene-editing techniques (Yin et al. 2017) and revolutionizing the concept of whole genome selection (De los Campos et al. 2013, Burdon et al. 2016). At the same time, recognition of the need to broaden the available resistance arsenal has stimulated exploration of the intricacies of cellular and subcellular interactions between pathogens and their hosts, raising hopes that resistance based on nonhost interactions, altered host susceptibility factors, or the use of resistance that targets specific pathogen effectors important for primary metabolisms may prove more durable or at least provide a greater diversity of genes to use in pyramiding (Dangl et al. 2013). However, this first wave of benefits continues a high-risk, brute-force approach that maintains strong directional selection to control organisms that have long been regarded as shifty enemies (Stakman 1947). Certainly, simultaneously stacking multiple R genes in a single crop variety may decrease the short-term probability of multiple de novo mutations giving rise to new pathogen strains with matching virulence combinations. However, plant pathogens possess an almost bewildering array of means whereby they generate novel variation. This, coupled with their very short generation times and great fecundity, provides great opportunities for novel variants to emerge quickly. Although molecular approaches providing a greater array of R genes with which to combat pathogens should be an integral part of new disease control strategies, greater consideration must be given to the pathogen's response in the field. To achieve durable resistance, it is essential to implement alternative approaches that explicitly consider epidemiological and evolutionary processes. Sustainable disease management requires a shift in mindset away from a sole focus on yield and productivity to a broader integration of productivity with underlying ecological, economic, and environmental dimensions. Multidisciplinary collaboration is critical for the development of effective and durable strategies. Evolutionary plant pathologists and geneticists need to play a major role in designing management practices that maximize host plant defense while simultaneously minimizing opportunities for pathogens to evolve. To be effective and durable, sustainable disease management must tackle the practices and social constraints that currently make the construction of evolutionarily robust, genetically diverse agricultural landscapes difficult. Intensive agricultural practices, associated commercial imperatives (ease of harvesting, demand for product uniformity), and consumer expectations of cheap food all contribute to this problem. To these must be added social issues, including prejudices among consumers against the use of particular technologies (e.g., genetic modification) and a general unwillingness to factor in the costs to growers of fostering broadly beneficial ecosystem services. The technological revolution occurring at the farm level is rapidly moving to a situation where many market-driven constraints can be overcome. Therefore, the use of gene-editing approaches opens the way for the development of varieties with considerable among-individual diversity in R genes. Similarly, advances in precision agriculture and the application of robotics make the routine use of within-field spatial diversity approaches possible (Zhan et al. 2015). Even simple varietal mixtures have repeatedly been demonstrated to reduce disease levels and pathogen evolution and improve ecosystem services (Yang et al. 2019). More complex strategies involving within and among field and regional variation in varietal deployment has been the subject of intensive modeling studies (Papaïx et al. 2015) frequently backed by small-scale empirical trials (Döring et al. 2015). All of these studies demonstrate the complexity of balancing short-term disease control with longer-term durability, but the underlying message is strong. By combining the opportunities provided by modern molecular genetics with ecologically and evolutionarily informed gene deployment strategies, a far greater degree of reliable long-term disease control than is currently achieved is possible. Enhanced durable disease control offers a wide range of benefits that stretch far beyond the immediate goal of improved global food security and nutritional status. The potential to reduce the footprint of agriculture through better and more efficient use of farmland and reduced pesticide use has significant implications for improved outcomes in global climate change, in the availability of water resources, and in the conservation of biodiversity and associated ecosystem services. Indeed, the propensity for the biological world of agriculture to respond to prolonged directional selection from overuse of the same strategy goes beyond the loss of disease resistance to include the loss of efficacy of herbicides and fungicides. Optimal ecoevolutionary strategies that disrupt these trends can be identified but translating these into changes in breeding and farming strategies needs a mix of incentives, legislation and social change with significant implications for governmental policy settings (Pretty et al. 2018). Governments, researchers, industry and philanthropic bodies must work together to ensure the best possible outcomes are achieved by deploying the outcomes of modern molecular genetics in ecologically and evolutionarily sustainable ways. The authors thank Robert Park, Tim Reeves, and John Thompson for their comments and insights on earlier versions of the manuscript. JZ acknowledges the support of the Chinese National Natural Science Foundation of China (grants no. 31761143010 and no. U1405213). Jeremy J. Burdon (jeremy.burdon@csiro.au) is a post retirement fellow with CSIRO Agriculture and Food in Canberra, Australia, and a visiting fellow at the Fujian Agriculture and Forestry University, in Fuzhou, China. Luke Barrett is a senior research scientist with CSIRO Agriculture and Food in Canberra, Australia. Lina Yang is a research scientist, and Dunchun He an agricultural economist, both working at the Fujian Agricultural and Forestry University in Fuzhou, China. Jiasui Zhan is a senior plant pathologist working at both the Swedish University of Agricultural Sciences, Uppsala, Sweden, and the Fujian Agriculture and Forestry University, Fuzhou, China.