Genome shuffling in a globalized bacterial plant pathogen: Recombination-mediated evolution in Xanthomonas euvesicatoria and X. perforans

Bacterial recombination and clonality underly the evolution and epidemiology of pathogenic lineages as well as their cosmopolitan spread. While the spread of stable clonal bacterial pathotypes drives disease epidemics, recombination leads to the evolution of new bacterial lineages. Recombinant lineages of plant bacterial pathogens are typically associated with colonization of novel hosts and emergence of new diseases. Here, we show that recombination between evolutionarily and phenotypically distinct plant pathogenic lineages has generated new recombinant lineages with unique combinations of pathogenicity and virulence factors.X. euvesicatoria(Xe) andX. perforans(Xp) are two closely related monophyletic species causing bacterial spot disease on tomato and pepper worldwide. We sequenced the genomes of strains representing populations on tomato in Nigeria and found shuffling of secretion systems and effectors such that these strains contain genes from bothXeandXp. Multiple strains, from populations in Nigeria, Italy, and Florida, USA, exhibited extensive genomewide homologous recombination and both species exhibited dynamic open pangenomes. Our results show that recombination is generating new lineages of bacterial spot pathogens on tomato with consequences for disease management strategies.ImportanceTheXanthomonaspathogens that cause bacterial spot of tomato and pepper have been model systems for plant-microbe interactions. Two of these pathogens,X. euvesicatoriaandX. perforans, are very closely related. Genome sequences of bacterial spot field strains from Nigeria, Italy, and the United States showed varying levels of homologous recombination that changed the amino sequence of effectors, secretion systems, and other proteins. This shuffling of genome content occurred betweenX. euvesicatoriaandX. perforans, while a Nigerian lineage also contained the lipopolysaccharide cluster of a distantly relatedXanthomonasspecies. Gene content varied among strains and the affected genes are important in the establishment of disease, therefore our findings point to global variation in the host-pathogen interaction driven by gene exchange among evolutionarily distinct lineages.