Summary• The deployment of resistant crops often leads to the emergence of resistance-breaking pathogens that suppress the yield benefit provided by the resistance. Here, we theoretically explored how farmers' main leverages (resistant cultivar choice, resistance deployment strategy, landscape planning and cultural practices) can be best combined to achieve resistance durability while minimizing yield losses as a result of plant viruses.• Assuming a gene-for-gene type of interaction, virus epidemics are modelled in a landscape composed of a mosaic of resistant and susceptible fields, subjected to seasonality, and a reservoir hosting viruses year-round. The model links the genetic and the epidemiological processes, shaping at nested scales the demogenetic dynamics of viruses.• The choice of the resistance gene (characterized by the equilibrium frequency of the resistance-breaking virus at mutation-selection balance in a susceptible plant) is the most influential leverage of action. Our results showed that optimal strategies of resistance deployment range from 'mixture' (where susceptible and resistant cultivars coexist) to 'pure' strategies (with only resistant cultivar) depending on the resistance characteristics and the epidemiological context (epidemic incidence and landscape connectivity).• We demonstrate and discuss gaps concerning virus epidemiology across the agro-ecological interface that must be filled to achieve sustainable disease management.

The management of genes conferring resistance to plant–pathogens should make it possible to control epidemics (epidemiological perspective) and preserve resistance durability (evolutionary perspective). Resistant and susceptible cultivars must be strategically associated according to the principles of cultivar mixture (within a season) and rotation (between seasons). We explored these questions by modeling the evolutionary and epidemiological processes shaping the dynamics of a pathogen population in a landscape composed of a seasonal cultivated compartment and a reservoir compartment hosting pathogen year-round. Optimal deployment strategies depended mostly on the molecular basis of plant–pathogen interactions and on the agro-ecological context before resistance deployment, particularly epidemic intensity and landscape connectivity. Mixtures were much more efficient in landscapes in which between-field infections and infections originating from the reservoir were more prevalent than within-field infections. Resistance genes requiring two mutations of the pathogen avirulence gene to be broken down, rather than one, were particularly useful when infections from the reservoir predominated. Combining mixture and rotation principles were better than the use of the same mixture each season as (i) they controlled epidemics more effectively in situations in which within-field infections or infections from the reservoir were frequent and (ii) they fulfilled the epidemiological and evolutionary perspectives.

By combining high-throughput sequencing (HTS) with experimental evolution, we can observe the within-host dynamics of pathogen variants of biomedical or ecological interest. We studied the evolutionary dynamics of five variants of Potato virus Y (PVY) in 15 doubled-haploid lines of pepper. All plants were inoculated with the same mixture of virus variants and variant frequencies were determined by HTS in eight plants of each pepper line at each of six sampling dates. We developed a method for estimating the intensities of selection and genetic drift in a multi-allelic Wright-Fisher model, applicable whether these forces are strong or weak, and in the absence of neutral markers. This method requires variant frequency determination at several time points, in independent hosts. The parameters are the selection coefficients for each PVY variant and four effective population sizes Ne at different time-points of the experiment. Numerical simulations of asexual haploid Wright-Fisher populations subjected to contrasting genetic drift (Ne ∈ [10, 2000]) and selection (|s| ∈ [0, 0.15]) regimes were used to validate the method proposed. The experiment in closely related pepper host genotypes revealed that viruses experienced a considerable diversity of selection and genetic drift regimes. The resulting variant dynamics were accurately described by Wright-Fisher models. The fitness ranks of the variants were almost identical between host genotypes. By contrast, the dynamics of Ne were highly variable, although a bottleneck was often identified during the systemic movement of the virus. We demonstrated that, for a fixed initial PVY population, virus effective population size is a heritable trait in plants. These findings pave the way for the breeding of plant varieties exposing viruses to stronger genetic drift, thereby slowing virus adaptation.