Genomic Inference of Recombination-Mediated Evolution in Xanthomonas euvesicatoria and X. perforans

Abstract

Recombination is a major driver of evolution in bacterial populations, because it can spread and combine independently evolved beneficial mutations. Recombinant lineages of bacterial pathogens of plants are typically associated with the colonization of novel hosts and the emergence of new diseases. Here we show that recombination between evolutionarily and phenotypically distinct plant-pathogenic lineages generated recombinant lineages with unique combinations of pathogenicity and virulence factors. and are two closely related lineages causing bacterial spot disease on tomato and pepper worldwide. We sequenced the genomes of atypical strains collected from tomato in Nigeria and observed recombination in the type III secretion system and effector genes, which showed alleles from both and Wider horizontal gene transfer was indicated by the fact that the lipopolysaccharide cluster of one strain was most similar to that of a distantly related pathogen of barley. This strain and others have experienced extensive genomewide homologous recombination, and both species exhibited dynamic open pangenomes. Variation in effector gene repertoires within and between species must be taken into consideration when one is breeding tomatoes for disease resistance. Resistance breeding strategies that target specific effectors must consider possibly dramatic variation in bacterial spot populations across global production regions, as illustrated by the recombinant strains observed here. The pathogens that cause bacterial spot of tomato and pepper are extensively studied models of plant-microbe interactions and cause problematic disease worldwide. Atypical bacterial spot strains collected from tomato in Nigeria, and other strains from Italy, India, and Florida, showed evidence of genomewide recombination that generated genetically distinct pathogenic lineages. The strains from Nigeria and Italy were found to have a mix of type III secretion system genes from and, as well as effectors from These genes and effectors are important in the establishment of disease, and effectors are common targets of resistance breeding. Our findings point to global diversity in the genomes of bacterial spot pathogens, which is likely to affect the host-pathogen interaction and influence management decisions.

Recently emerged and diverse lineages of Xanthomonas perforans have independently evolved through plasmid acquisition and homologous recombination originating from multiple Xanthomonas species

“…To examine patterns of homologous recombination between Xp , Xeu , and other closely related Xanthomonas spp., a second core genome alignment was constructed utilizing the strains sequenced in this study and respective genome assemblies available from GenBank ( n = 68). A maximum likelihood phylogeny generated from the resulting 3.98 Mb alignment was largely congruent to the population structure inferred by previous studies (18, 20) and showed Xp and Xeu branching from each other into two distinct phylogenetic groups, while other related Xanthomonas spp. displayed considerably longer branch lengths and clustered into a paraphyletic group of strains.…”

“…The strains that belong to this larger phylogenetic group were classified into several species including X. alfalfae , X. axonopodis , X. perforans and X. euvesicatoria and are associated with diseases of diverse monocot and dicotyledonous plant families (23). While the importance of homologous recombination in facilitating the emergence of novel X. perforans lineages has been established (18, 19), the extent of genetic exchange across the larger X. euvesicatoria species complex and specific functional pathways affected by homologous recombination remains to be explored.…”

The Green Revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae

“…4a), but because each recombination event introduces approximately six substitutions, recombination introduced substitution over mutation is 2.82 (95% CI: 2.81-2.83) times higher within recombinant fragments. These values were similar to those found in Indian Xoo populations [53] or what has been reported for other Xanthomonas species [59,60].…”

Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogenXanthomonas

“…nov.) associated with watercress production in Florida were defined. Sequencing genomes of diverse strains belonging to closely related species infecting tomato and/or pepper indicated the admixture of strains arising due to frequent genetic exchange among different strains of the closely related species (Barak, Koike and Gilbertson 2002;Jibrin et al 2018). These hybrid strains pose a challenge to the current taxonomic definitions of a species based on average nucleotide identity (ANI).…”

“…Recombination-mediated evolution of bacterial plant pathogens is important for the colonisation in novel hosts and new disease emergence. Jibrin et al (2018) compared two newly sequenced Nigerian Xanthomonas strains (N1 and N38) with 70 previously published X. perforans and X. euvesicatoria strains. Recombination was identified as the major driving force of evolution of X. perforans and X. euvesicatoria strains, with X. perforans showing more evidence for recombination than X. euvesicatoria (Jibrin et al 2018).…”