Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants

The efficiency of plant major resistance genes is limited by the emergence and spread of resistance‐breaking mutants. Modulating the evolutionary forces acting on pathogen populations constitutes a promising way to increase the durability of these genes. We studied the effect of four plant traits affecting these evolutionary forces on the rate of resistance breakdown (RB) by a virus. Two of those traits correspond to virus effective population sizes (Ne), either at plant inoculation or during infection. The third trait corresponds to differential selection exerted by the plant on the virus population. Finally, the fourth trait corresponds to within‐plant virus accumulation (VA). These traits were measured experimentally on Potato virus Y (PVY) and a set of 84 pepper doubled‐haploid lines, all carrying the same pvr23 resistance gene but having contrasted genetic backgrounds. The lines showed extensive variation for the rate of pvr23 RB by PVY and for the four other traits of interest. A generalized linear model showed that three of these four traits, with the exception of Ne at inoculation, and several of pairwise interactions between them had significant effects on RB. RB increased when Ne during plant infection or VA increased. The effect of differential selection was more complex because of a strong interaction with VA. When VA was high, RB increased as the differential selection increased. An opposite relationship between RB and differential selection was observed when VA was low. This study provides a framework to select plants with appropriate virus‐evolution‐related traits to avoid or delay resistance breakdown