Intercontinental dissemination and diversification of Xanthomonas perforans in tomato production

Tomato is a high value crop that requires quality seed each season. Tomato production often relies on international breeding and production chains with a global network to deliver seeds to growers. Xanthomonas perforans , one of the causal agents of bacterial spot of tomato, is seedborne and has rapidly emerged and displaced other bacterial spot xanthomonads in tomato production regions around the world. The objectives of this work were to determine if different tomato production regions contain genetically distinct X. perforans populations, examine genetic relatedness of strains collected in tomato seed production areas in East Asia and other production regions, estimate the timing of X. perforans population expansion relative to its first report in 1991, and evaluate variation in type III effectors, which are critical pathogenicity and virulence factors. Our results showed extensive genetic diversity in the pathogen and highly similar strains in distant tomato production regions, which is consistent with global dissemination. Furthermore, we found genetically similar strains in tomato seed production and fruit production regions, as would be expected if the pathogen was being moved through tomato production chains from a common origin. We found waves of diversification of populations in the United States, where our sampling was more extensive, before and since its first detection, consistent with emergence of new X. perforans genotypes from diverse source populations. Variation in gene content, including effector genes, within and between core genome lineages suggests the potential for rapid changes to the accessory genome upon dissemination. Evolution of the X. perforans pangenome, including the acquisition and loss of type III secreted effectors, will continue to challenge sustainable management of tomato bacterial spot.