Mobile genetic elements accompany the emergence of clonal crop lineages from weed-associated populations of Xanthomonas campestris

Xanthomonas campestris is a destructive pathogen of cruciferous vegetables and ornamentals and is frequently isolated from related weed species growing near agricultural land. However, the evolutionary relationships, genomic features, and biosecurity significance of weed-associated strains remain poorly understood. Here, we integrate phylogenomic and pangenomic analyses of X. campestris, including nine newly sequenced strains isolated from invasive garlic mustard (Alliaria petiolata), to compare strains from cultivated and non-cultivated hosts across multiple pathovars. Weed-isolated strains predominantly clustered within basal, genetically diverse lineages associated with broad host ranges, whereas crop-isolated strains were concentrated in host-associated clonal lineages. The emergence of specialized crop-associated lineages coincided with multiple inferred acquisitions of large mobile elements, including integrative conjugative and mobilizable elements and plasmids carrying genes previously associated with pathogenicity and host range. Although these elements were enriched in clonal crop-associated lineages, they also occurred in diverse weed-associated strains, indicating that genetic material associated with crop infection is distributed among divergent lineages and persists in wild and weedy systems. These findings identify invasive weeds as ancillary hosts that may harbor pathogen diversity and provide opportunities for genetic exchange, underscoring the importance of surveillance beyond agricultural fields to monitor pathogen diversification and emerging threats. Our pangenomic analysis also identified crop-associated pathogen factors and putative host resistance targets for future investigation, providing a foundation for developing critically needed black rot-resistant cultivars.