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Abstract

Crop disease outbreaks are often associated with clonal expansions of single pathogenic lineages. Unlike in most agricultural populations, wild plant populations are composed of plants with genetically diverse immune systems. While these wild plant pathosystems are predicted to be less susceptible to clonal epidemics, pathogen evolution in a genetically diverse host remains largely uncharacterized. To determine whether boom-and-bust scenarios similar to those in agriculture hold for wild pathosystems, we carried out a multi-year, multi-site survey of Pseudomonas in its natural host Arabidopsis thaliana. The most common Pseudomonas lineage corresponded to a ubiquitous pathogenic clade. Sequencing of 1,524 genomes revealed this lineage to have diversified approximately 300,000 years ago, containing dozens of genetically identifiable pathogenic sublineages. There is differentiation at the level of both gene content and disease phenotypes and genome-wide association mapping is revealing those variable genes that contribute to evolving pathogenicity. The coexistence of sublineages indicates that in contrast to crop systems, no single strain has been able to overtake the studied A. thaliana populations in the recent past. Our results suggest that genetically diverse host populations can drive the diversification of the pathogen population, preventing any single pathogen from overtaking the host.