Resistance genes introgressed into cultivated plants are frequently overcame by pathogens, causing outbreaks and economic losses. Therefore, understanding the evolutionary strategies involved in the adaptation of pathogen populations is needed to improve the sustainable management of resistance. Bremia lactucae, the lettuce downy mildew, is under strong selection pressure exerted by host resistance genes. Under this selection pressure, B. lactucae populations showed a rapid adaptation to host resistance. The study of pathogen genetic structure may help to understand the evolutionary mechanisms involved in the overcoming of resistant genes. Study of the genetic structure (neutral and potentially selected markers) of B. lactucae populations in France was conducted in order to identify the evolutionary forces involved in the adaptation of the plant pathogen and to determine the influence of selective pressure of host resistance genes on the population structure. We developed 12 microsatellites markers, to study genetic structure of B. lactucae populations in France. Over 800 isolates were collected from the most important production areas of the host plant, Lactuca sativa. These isolates were taken from different cultivars grouped according to their resistance gene combinations. Moreover, a prospection in the wild compartment allowed sampling isolates of B. lactucae on the wild host L. serriola. The polymorphism of several RxLR candidate effectors was studied in several Bremia populations. Our results showed clonality in Bremia populations but rare events of sexual reproduction are also suggested. Weak genetic differentiation between populations suggested important gene flow between populations at French regional scale. Gene flow was also found between the wild and the crop pathosystems indicating a possible role of wild host plants as genetic reservoir. Moreover, analyzing the population genetic structure suggests the presence of different clonal lineages, resulting probably from selection pressure of resistance genes. Characterizing the population structure of B. lactucae allowed to highlight the strong evolutionary potential (significant gene flow, mixed mating system, selection by resistance genes) of B. lactucae explaining its rapid adaptation to host resistance. Thus, we can suggest some management strategies of resistance genes as promoting the use of quantitative resistance and use of crop association to improve the durability of resistance.
