Bremia lactucae populations on cultivated lettuce originate from prickly lettuce and are interconnected with the wild pathosystem

Bremia lactucae is a devastating pathogen causing heavy yield losses in lettuce production worldwide. Long time it was thought to infect various members of the Asteraceae but recent phylogenetic investigations revealed that B. lactucae is restricted to cultivated Lactuca sativa and its wild progenitor Lactuca serriola . Many resistance genes in cultivated lettuce were crossbred from L. serriola , but often a fast overcoming of the resistance in the crop by new downy mildew races was observed. Consequently, it seems important to investigate the population genetic relationships of wild prickly lettuce and cultivated lettuce, in order to determine, if the Bremia lineages infecting these hosts are distinct or intermingled. In the first case, searching for resistance in prickly lettuce is straightforward, in the second case it would rather be futile. Bremia belongs to the genera of downy mildews with pyriform haustoria, which feature highly variable ITS-repeats that can be used as high-resolution markers for population genetics studies. Here we report that Bremia lactucae on Lactuca sativa is not homogeneous but emerged from several host shifts from Lactuca serriola and that Bremia accessions from both species are not forming distinct genepools. While the pathogen population from L. serriola showed a balanced pattern, the pathogen population from L. sativa has a directional selection pattern reflecting founder effects after host shifts, resulting in a fast colonisation of susceptible lettuce cultivars. Thus, the wild population of Bremia lactucae seems to play a major role in the epidemiology of downy mildew on cultivated lettuce. This also explains, why resistance breeding using resistance genes from prickly lettuce had little success for achieving durable resistance in cultivated lettuce and calls for both more detailed research into Bremia on wild lettuce and new breeding strategies using less closely related lettuce species.