Playing on a Pathogen's Weakness: Using Evolution to Guide Sustainable Plant Disease Control Strategies

Abstract

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. To be effective and durable, sustainable disease management requires a significant shift in emphasis to overtly include ecoevolutionary principles in the design of adaptive management programs aimed at minimizing the evolutionary potential of plant pathogens by reducing their genetic variation, stabilizing their evolutionary dynamics, and preventing dissemination of pathogen variants carrying new infectivity or resistance to agrochemicals.

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…Unlike intragenic recombination, the direction and magnitude of selection on plant pathogens can be manipulated through the change in agricultural practices. To slow down the evolution of plant pathogens and achieve durable resistance in hosts in modern agriculture, it is important to create field conditions favoring disruptive selection through the evolutionary deployment of host resistance such as a cultivar mixture (Zhan et al., 2014, 2015). In addition, elevated air temperature associated with anthropogenic activities may greatly threaten food security due to extended seasonality supporting more plant diseases or enhanced pathogen growth thereby driving more intense disease epidemics.…”

“…Pathogens and their host plants are engaged in a never‐ending battle, in which pathogens are continuously evolving invasive mechanisms to break plant defense systems and host plants responding with the constant development of new protection to prevent or mitigate damage (Zhan, Thrall, & Burdon, 2014; Zhan, Thrall, Papaïx, Xie, & Burdon, 2015). Many plant pathogens interact with their hosts following the widely accepted gene‐for‐gene model.…”

Spatio‐temporal connectivity and host resistance influence evolutionary and epidemiological dynamics of the canola pathogen Leptosphaeria maculans

“…On the one hand, diversifying selection has been proposed as a way of exploiting pathogens, for example, via disruptive evolutionary dynamics (Zhan et al., 2015). Alternatively, stacking genes or QTLs in pyramids is also advocated (Djian‐Caporalino et al., 2014; Fukuoka et al., 2015).…”

“…It is worth noting that while stacking might be of interest when the corresponding infectivity profiles are absent from pathogen populations (Lof et al., 2017), this strategy does not allow the possibility of leveraging decreases in unnecessary infectivity as documented in our study. To allow such a decrease, the benefit of removing genes from varieties rather than stacking newly available ones into previous material should be incorporated in breeding strategies (Brown, 2015; Zhan et al, 2015). …”

“…While the solutions to this problem will be multifaceted, one important but frequently neglected area of focus revolves around management strategies that explicitly manipulate the epidemiological and evolutionary trajectories of pathogenic organisms. Any strategy that reduces the size of epidemics and the transfer of inoculum between seasons should also reduce the effective size of pathogen populations, limit evolutionary potential and increase resistance durability (Bousset & Chèvre, 2012, 2013; McDonald & Linde, 2002; Zhan, Thrall, & Burdon, 2014; Zhan, Thrall, Papaïx, Xie, & Burdon, 2015). …”