Studying Wild Plant Pathosystems to Understand Crop Plant Pathosystems: Status, Gaps, Challenges, and Perspectives.

Phytopathology is a highly complex scientific discipline. Initially, its focus was on the study of plant-pathogen interactions in agricultural and forestry production systems. Host-pathogen interactions in natural plant communities were generally overlooked until the 1970s when plant pathologists and evolutionary biologists started to take an interest in these interactions, and their dynamics in natural plant populations, communities, and ecosystems.

Optimizing Plant Disease Management in Agricultural Ecosystems Through Rational In-Crop Diversification.

Biodiversity plays multifaceted roles in societal development and ecological sustainability. In agricultural ecosystems, using biodiversity to mitigate plant diseases has received renewed attention in recent years but our knowledge of the best ways of using biodiversity to control plant diseases is still incomplete. In term of in-crop diversification, it is not clear how genetic diversity in host populations interacts with identifiable resistance and other functional traits of component genotypes to mitigate disease epidemics and what is the best way of structuring mixture populations.

Metapopulation Structure Predicts Population Dynamics in the - Host-Pathogen Interaction.

AbstractIn symbiotic interactions, spatiotemporal variation in the distribution or population dynamics of one species represents spatial and temporal heterogeneity of the landscape for the other. Such interdependent demographic dynamics result in situations where the relative importance of biotic and abiotic factors in determining ecological processes is complicated to decipher. Using a detailed survey of three metapopulations of the succulent plant and the necrotrophic fungus located along the southeastern Australian coast, we developed a series of statistical analyses-namely, synchrony analysis, patch occupancy dynamics, and a spatially explicit metapopulation model-to understand how habitat quality, weather conditions, dispersal, and spatial structure determine metapopulation dynamics.

Climate change and disease in plant communities.

Climate change is triggering similar effects on the incidence and severity of disease for crops in agriculture and wild plants in natural communities. The complexity of natural ecosystems, however, generates a complex array of interactions between wild plants and pathogens in marked contrast to those generated in the structural and species simplicity of most agricultural crops. Understanding the different impacts of climate change on agricultural and natural ecosystems requires accounting for the specific interactions between an individual pathogen and its host(s) and their subsequent effects on the interplay between the host and other species in the community.

Genetic analysis reveals long-standing population differentiation and high diversity in the rust pathogen Melampsora lini.

A priority for research on infectious disease is to understand how epidemiological and evolutionary processes interact to influence pathogen population dynamics and disease outcomes. However, little is understood about how population adaptation changes across time, how sexual vs. asexual reproduction contribute to the spread of pathogens in wild populations and how diversity measured with neutral and selectively important markers correlates across years.

Lessons from a Life in Time and Space.

A research career investigating epidemiological and evolutionary patterns in both natural and crop host-pathogen systems emphasizes the need for flexibility in thinking and a willingness to adopt ideas from a wide diversity of subdisciplines. Here, I reflect on the pivotal issues, research areas, and interactions, including the role of science management, that shaped my career in the hope of demonstrating that career paths and collaborations in science can be as diverse and unpredictable as the natural world in which we study our organisms of choice.

Mosaics, mixtures, rotations or pyramiding: What is the optimal strategy to deploy major gene resistance?

Once deployed uniformly in the field, genetically controlled plant resistance is often quickly overcome by pathogens, resulting in dramatic losses. Several strategies have been proposed to constrain the evolutionary potential of pathogens and thus increase resistance durability. These strategies can be classified into four categories, depending on whether resistance sources are varied across time (rotations) or combined in space in the same cultivar (pyramiding), in different cultivars within a field (cultivar mixtures) or among fields (mosaics).

Differential impact of landscape-scale strategies for crop cultivar deployment on disease dynamics, resistance durability and long-term evolutionary control.

A multitude of resistance deployment strategies have been proposed to tackle the evolutionary potential of pathogens to overcome plant resistance. In particular, many landscape-based strategies rely on the deployment of resistant and susceptible cultivars in an agricultural landscape as a mosaic. However, the design of such strategies is not easy as strategies targeting epidemiological or evolutionary outcomes may not be the same.

Climate change accelerates local disease extinction rates in a long-term wild host-pathogen association.

Pathogens are a significant component of all plant communities. In recent years, the potential for existing and emerging pathogens of agricultural crops to cause increased yield losses as a consequence of changing climatic patterns has raised considerable concern. In contrast, the response of naturally occurring, endemic pathogens to a warming climate has received little attention.

In situ conservation-harnessing natural and human-derived evolutionary forces to ensure future crop adaptation.

Ensuring the availability of the broadest possible germplasm base for agriculture in the face of increasingly uncertain and variable patterns of biotic and abiotic change is fundamental for the world's future food supply. While ex situ conservation plays a major role in the conservation and availability of crop germplasm, it may be insufficient to ensure this. In situ conservation aims to maintain target species and the collective genotypes they represent under evolution.

Addressing the Challenges of Pathogen Evolution on the World's Arable Crops.

Advances in genomic and molecular technologies coupled with an increasing understanding of the fine structure of many resistance and infectivity genes, have opened up a new era of hope in controlling the many plant pathogens that continue to be a major source of loss in arable crops. Some new approaches are under consideration including the use of nonhost resistance and the targeting of critical developmental constraints. However, the major thrust of these genomic and molecular approaches is to enhance the identification of resistance genes, to increase their ease of manipulation through marker and gene editing technologies and to lock a range of resistance genes together in simply manipulable resistance gene cassettes.

Trade-offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans.

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases.

Epidemiological and Evolutionary Outcomes in Gene-for-Gene and Matching Allele Models.

Gene-for-gene (GFG) and matching-allele (MA) models are qualitatively different paradigms for describing the outcome of genetic interactions between hosts and pathogens. The GFG paradigm was largely built on the foundations of Flor's early work on the flax-flax rust interaction and is based on the concept of genetic recognition leading to incompatible disease outcomes, typical of host immune recognition. In contrast, the MA model is based on the assumption that genetic recognition leads to compatible interactions, which can result when pathogens require specific host factors to cause infection.

Specialization for resistance in wild host-pathogen interaction networks.

Properties encompassed by host-pathogen interaction networks have potential to give valuable insight into the evolution of specialization and coevolutionary dynamics in host-pathogen interactions. However, network approaches have been rarely utilized in previous studies of host and pathogen phenotypic variation. Here we applied quantitative analyses to eight networks derived from spatially and temporally segregated host (Linum marginale) and pathogen (Melampsora lini) populations.

Playing on a pathogen's weakness: using evolution to guide sustainable plant disease control strategies.

Wild plants and their associated pathogens are involved in ongoing interactions over millennia that have been modified by coevolutionary processes to limit the spatial extent and temporal duration of disease epidemics. These interactions are disrupted by modern agricultural practices and social activities, such as intensified monoculture using superior varieties and international trading of agricultural commodities. These activities, when supplemented with high resource inputs and the broad application of agrochemicals, create conditions uniquely conducive to widespread plant disease epidemics and rapid pathogen evolution.

Crop pathogen emergence and evolution in agro-ecological landscapes.

Remnant areas hosting natural vegetation in agricultural landscapes can impact the disease epidemiology and evolutionary dynamics of crop pathogens. However, the potential consequences for crop diseases of the composition, the spatial configuration and the persistence time of the agro-ecological interface - the area where crops and remnant vegetation are in contact - have been poorly studied. Here, we develop a demographic-genetic simulation model to study how the spatial and temporal distribution of remnant wild vegetation patches embedded in an agricultural landscape can drive the emergence of a crop pathogen and its subsequent specialization on the crop host.

Below-ground abiotic and biotic heterogeneity shapes above-ground infection outcomes and spatial divergence in a host-parasite interaction.

We investigated the impact of below-ground and above-ground environmental heterogeneity on the ecology and evolution of a natural plant-pathogen interaction. We combined field measurements and a reciprocal inoculation experiment to investigate the potential for natural variation in abiotic and biotic factors to mediate infection outcomes in the association between the fungal pathogen Melampsora lini and its wild flax host, Linum marginale, where pathogen strains and plant lines originated from two ecologically distinct habitat types that occur in close proximity ('bog' and 'hill'). The two habitat types differed strikingly in soil moisture and soil microbiota.

Guiding deployment of resistance in cereals using evolutionary principles.

Genetically controlled resistance provides plant breeders with an efficient means of controlling plant disease, but this approach has been constrained by practical difficulties associated with combining many resistance genes together and strong evolutionary responses from pathogen populations leading to subsequent resistance breakdown. However, continuing advances in molecular marker technologies are revolutionizing the ability to rapidly and reliably manipulate resistances of all types - major gene, adult plant and quantitative resistance loci singly or multiply into individual host lines. Here, we argue that these advances provide major opportunities to deliberately design deployment strategies in cereals that can take advantage of the evolutionary pressures faced by target pathogens.

Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation.

The extent and speed at which pathogens adapt to host resistance varies considerably. This presents a challenge for predicting when--and where--pathogen evolution may occur. While gene flow and spatially heterogeneous environments are recognized to be critical for the evolutionary potential of pathogen populations, we lack an understanding of how the two jointly shape coevolutionary trajectories between hosts and pathogens.

Evolution of pathogen specialisation in a host metapopulation: joint effects of host and pathogen dispersal.

Metapopulation processes are important determinants of epidemiological and evolutionary dynamics in host-pathogen systems, and are therefore central to explaining observed patterns of disease or genetic diversity. In particular, the spatial scale of interactions between pathogens and their hosts is of primary importance because migration rates of one species can affect both spatial and temporal heterogeneity of selection on the other. In this study we developed a stochastic and discrete time simulation model to specifically examine the joint effects of host and pathogen dispersal on the evolution of pathogen specialisation in a spatially explicit metapopulation.

Achieving sustainable plant disease management through evolutionary principles.

Plants and their pathogens are engaged in continuous evolutionary battles and sustainable disease management requires novel systems to create environments conducive for short-term and long-term disease control. In this opinion article, we argue that knowledge of the fundamental factors that drive host-pathogen coevolution in wild systems can provide new insights into disease development in agriculture. Such evolutionary principles can be used to guide the formulation of sustainable disease management strategies which can minimize disease epidemics while simultaneously reducing pressure on pathogens to evolve increased infectivity and aggressiveness.

Population processes at multiple spatial scales maintain diversity and adaptation in the Linum marginale--Melampsora lini association.

Host-pathogen coevolution is a major driver of species diversity, with an essential role in the generation and maintenance of genetic variation in host resistance and pathogen infectivity. Little is known about how resistance and infectivity are structured across multiple geographic scales and what eco-evolutionary processes drive these patterns. Across southern Australia, the wild flax Linum marginale is frequently attacked by its rust fungus Melampsora lini.

Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation.

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs.

Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems.

Anthropogenic impacts increasingly drive ecological and evolutionary processes at many spatio-temporal scales, demanding greater capacity to predict and manage their consequences. This is particularly true for agro-ecosystems, which not only comprise a significant proportion of land use, but which also involve conflicting imperatives to expand or intensify production while simultaneously reducing environmental impacts. These imperatives reinforce the likelihood of further major changes in agriculture over the next 30-40 years.

Spatial variation in disease resistance: from molecules to metapopulations.

Variation in disease resistance is a widespread phenomenon in wild plant-pathogen associations. Here, we review current literature on natural plant-pathogen associations to determine how diversity in disease resistance is distributed at different hierarchical levels - within host individuals, within host populations, among host populations at the metapopulation scale and at larger regional scales.We find diversity in resistance across all spatial scales examined.