Pathological convergence of a bacterial plant pathogen is associated with the horizontal transfer of an effector-containing mobile element

Xanthomonas campestris is a diverse bacterial plant pathogen that causes disease on many critical crops. However, the mechanisms underlying its virulence have remained elusive. We paired a quantitative virulence screen with a bacterial genome-wide association study (GWAS) to uncover the genetic underpinnings of virulence on this model pathogen. We found that a diverse panel of 67 X. campestris strains varied substantially in their ability to grow and cause disease on the model host A. thaliana Col-0. However, its virulence on this host was not a monophyletic trait. This opened the door to the application of a GWAS to test for convergent genetic loci underlying virulence in X. campestris. After correcting for phylogenetic structure, only four accessory gene families were positively associated with X. campestris virulence: a xopJ family effector, a hypothetical gene, and two genes associated with transposable element mobility. These four genes mapped to a Tn3-family transposon that appears to have been horizontally transferred across multiple distinct X. campestris lineages, enabling the emergence of divergent pathogens in these lineages with the same underlying genetic architecture. Further analysis revealed that these transposons were often nested within larger transposons that also contained additional virulence genes, including effectors xopE, avrBs3, and xopAH, which may further contribute to host specific adaptation within independent lineages. This study demonstrates that the horizontal transfer of an effector harbouring transposon is a primary determinant of X. campestris virulence on the model host A. thaliana. It also highlights the utility of GWASs for identifying bacterial loci associated with virulence, which has far-reaching implications for pathogen surveillance and the engineering of resistant crops.