Climate change impacts on plant pathogens, food security and paths forward

Abstract

Plant disease outbreaks pose significant risks to global food security and environmental sustainability worldwide, and result in the loss of primary productivity and biodiversity that negatively impact the environmental and socio-economic conditions of affected regions. Climate change further increases outbreak risks by altering pathogen evolution and host-pathogen interactions and facilitating the emergence of new pathogenic strains. Pathogen range can shift, increasing the spread of plant diseases in new areas. In this Review, we examine how plant disease pressures are likely to change under future climate scenarios and how these changes will relate to plant productivity in natural and agricultural ecosystems. We explore current and future impacts of climate change on pathogen biogeography, disease incidence and severity, and their effects on natural ecosystems, agriculture and food production. We propose that amendment of the current conceptual framework and incorporation of eco-evolutionary theories into research could improve our mechanistic understanding and prediction of pathogen spread in future climates, to mitigate the future risk of disease outbreaks. We highlight the need for a science-policy interface that works closely with relevant intergovernmental organizations to provide effective monitoring and management of plant disease under future climate scenarios, to ensure long-term food and nutrient security and sustainability of natural ecosystems.

Fig. 1. A new angle in the disease triangle paradigm that considers the plant microbiome as a pivotal factor influencing plant disease.

Intimate interactions among the plant, the environment, the soil and plant microbiomes, and invading pathogens impact the outcome of infection processes, disease severity and productivity of the plant. Environmental change and human activities (for example, global commodity and climate change) drive pathogen evolution and have increased disease threats to global crops. Genetically uniform crop monocultures and high planting density in modern agriculture have accelerated the emergence of virulent pathogens capable of overcoming disease-resistant crop varieties and promote the pathogen’s population size and genetic variability. Similarly, overreliance on pesticides has also fostered rapid emergence of new strains of pathogens. Pathogen transmission and anthropogenic pathogen movement due to, for example, international trade spreads pathogens to places free of natural enemies, and allows exchange of genetic material via horizontal gene transfer, facilitating adaptation to local hosts. Depletion of natural resources and natural landscapes has caused deterioration of the agroecosystem diversity. Emerging evidence suggests that soil and plant microbiomes influence the three angles of the disease paradigm — the host, the pathogen and the environment — by either facilitating or supressing pathogen attacks, by affecting plant physiology and immune response, and providing a line of defence and manipulating environmental conditions. For example, in disease-suppressive soils, indigenous microbiomes can reduce disease incidence, even in the presence of a pathogen, a susceptible host and a conductive environment. Explicit consideration of the role of the microbiome can improve our mechanistic understanding of disease outbreaks, which may lead to more effective prediction, monitoring and management of disease outbreaks. Better land management practices can improve overall soil health by influencing the diversity and functions of soil microbial communities, and could potentially be used to steer microbiomes that suppress diseases.

Fig. 2. Projected shifts in relative abundance of soil-borne pathogens from current to future climates.

a,b, Current relative abundance of soil-borne potential plant pathogens: Phytophthora spp. and Pythium spp. (panel a) and Penicillium sp. (panel b). c,d, The projected change in their abundance under predicted future climates (2050): Phytophthora spp. and Pythium spp. (panel c) and Penicillium sp. (panel d) (also see Supplementary Table 1). Previously developed models were implemented to project each map of the current and future relative abundance of plant pathogenic taxa worldwide. To implement these models, we performed exploratory correlation analyses to identify the most important factors associated with potential plant pathogen distributions from available data (see Supplementary Information). We used available data sets of climate variables, vegetation type, elevation and soil variables to identify the global distribution^,. To perform projections of these pathogens in future climates, we used climatic and land use available data sets^–. The prediction can be improved, as data from other locations will become available in the future. Areas of the projection away from the sampling points have been marked in white. The masking criterion was P < 0.01 to show the areas generated by the model in the projection that are closer to the sampling points (see Supplementary Information).

Fig. 3. Responses of plant microbiomes to novel climates and their consequences on disease occurrences.

Four scenarios are proposed for microbiome responses to climate change. Green plants symbolize the healthy state of plants prior to climate change, whereas yellow plants indicate the effect of climate change and pathogen infection on plants. a, Plants employ an array of mechanisms that depend on optimal immune response, root exudates and hormonal balance to assemble complex microbiomes. Plant-associated microbiomes in soil, particularly in the rhizosphere, provide the first line of defence against pathogens. Climate change will likely alter the structure of the microbial reservoir in the bulk soil. This together with changes in the plant immunity may alter the rhizosphere microbiome assembly and change the first line of defence, which would allow the pathogen to breach. b, Plants maintain homeostasis of associated (leaf, root, stem, endophytes) microbiomes via tight and complex regulation of immune systems. Climate change can alter plant physiology and immune response, such as the production of the root exudates, volatile organic carbons and phytohormones, which may constrain the ability of plants to recruit and assemble beneficial microbiomes and promote dysbiosis of the plant leading to diseases. c, Plant migration to new locations (niche range shift) may interrupt the plant immune system and its mutualistic coevolution with indigenous soil microbiomes that support healthy plant growth and disease tolerance. As such, plant migration may expose them to local pathogens to which they are susceptible, whereas in some cases, migrating plants will escape local pathogens. Similarly, niche range shift in pathogens (along with evolutionary processes) can make the pathogen more transmissible and virulent in new regions in the absence of an effective immune response of local plants and resistance by local microflora. d, The ‘cry for help’ strategy of the plant, which refers to the plant recruiting beneficial microorganisms when under pathogen attack, is also likely be altered under climate change. Climate change may constrain the abilities of plants to produce signal molecules (for example, root exudates, volatiles and so on) to attract beneficial microorganisms and/or shift microbial composition and traits, or their ability to respond to these signals. Climate change could also reduce the burden of pathogen attacks where a shift in microbiomes has either enriched beneficial microorganisms or primed the plant immune response. MAMP, microorganism-associated molecular pattern; PRR, pattern recognition receptor.