Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

Vascular pathogens travel long distances through host veins leading to life-threatening, systemic infections. In contrast, non-vascular pathogens remain restricted to infection sites, triggering localized symptom development. The contrasting features of vascular and non-vascular diseases suggest distinct etiologies, but the basis for each remains unclear. Here, we show that the hydrolase CbsA acts as a phenotypic switch between vascular and non-vascular plant pathogenesis. cbsA was enriched in genomes of vascular phytopathogenic bacteria in the Xanthomonadaceae family and absent in most non-vascular species. CbsA expression allowed non-vascular Xanthomonas to cause vascular blight while cbsA mutagenesis resulted in reduction of vascular or enhanced non-vascular symptom development. Phylogenetic hypothesis testing further revealed that cbsA was lost in multiple non-vascular lineages and more recently gained by some vascular subgroups, suggesting that vascular pathogenesis is ancestral. Our results overall demonstrate how the gain and loss of single loci can facilitate the evolution of complex ecological traits.