Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas

Abstract

Understanding the evolutionary history and potential of bacterial pathogens is critical to prevent the emergence of new infectious bacterial diseases. Xanthomonas axonopodis subsp. citri (Xac) (synonym X. citri subsp. citri), which causes citrus canker, is one of the hardest-fought plant bacterial pathogens in US history. Here, we sequenced 21 Xac strains (14 XacA, 3 XacA* and 4 XacA w ) with different host ranges from North America and Asia and conducted comparative genomic and evolutionary analyses. Our analyses suggest that acquisition of beneficial genes and loss of detrimental genes most likely allowed XacA to infect a broader range of hosts as compared with XacA w and XacA*. Recombination was found to have occurred frequently on the relative ancient branches, but rarely on the young branches of the clonal genealogy. The ratio of recombination/ mutation q/h was 0.0790 ± 0.0005, implying that the Xac population was clonal in structure. Positive selection has affected 14% (395 out of 2822) of core genes of the citrus canker-causing Xanthomonas. The genes affected are enriched in 'carbohydrate transport and metabolism' and 'DNA replication, recombination and repair' genes (Po0.05). Many genes related to virulence, especially genes involved in the type III secretion system and effectors, are affected by positive selection, further highlighting the contribution of positive selection to the evolution of citrus cankercausing Xanthomonas. Our results suggest that both metabolism and virulence genes provide advantages to endow XacA with higher virulence and a wider host range. Our analysis advances our understanding of the genomic basis of specialization by positive selection in bacterial evolution.

Xanthomonas citri pv. citri Pathotypes: LPS Structure and Function as Microbe‐Associated Molecular Patterns

“…However, the genomic differences in the LPS cluster were subsequently shown not to be pathotype‐specific, as the LPS sequence for pathotype A strains was found to be variable, and this variable region corresponds to a region of recombination. Thus, some pathotype A strains (e.g., DAPC1) have an LPS cluster organization identical to that reported by Zhang et al., whereas others have one similar to that of pathotypes A* and A W …”

“…identified genomic differences between these pathotypes, and they suggested several candidate genes associated with host range and various aspects of virulence. Zhang et al . identified a genomic region involved in lipopolysaccharide (LPS) biosynthesis, which was thought specific to pathotype A, with the upstream and downstream genes conserved.…”

“…[11] Ther easons for the differences in host range between the pathotypes are not fully defined. Gordon et al [7] identified genomic differences between these pathotypes, and they suggested several candidate genes associated with host range and various aspects of virulence.Z hang et al [12] identifiedagenomic regioni nvolved in lipopolysaccharide (LPS) biosynthesis, which was thought specific to pathotype A, with the upstream and downstream genes conserved. However,t he genomic differences in the LPS cluster were subsequently shown not to be pathotype-specific, as the LPS sequencef or pathotype As trains wasf ound to be variable, and this variable region corresponds to ar egion of recombination.…”

Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management

“…However, these results differ from other results, which suggest that the strains from each pathotype form monophyletic clades, with a short branch shared by the Xcc‐A w and Xcc‐A pathotypes (Gordon et al ., ). Such differences in the investigations of Xcc phylogeny call for further studies to understand the evolution of Xcc strains (Gordon et al ., ; Zhang et al ., ). It is presumed that the acquisition of beneficial genes and the loss of detrimental genes has most likely allowed Xcc‐A to infect a broader range of hosts relative to Xcc‐A* and Xcc‐A w .…”

Using Ecology, Physiology, and Genomics to Understand Host Specificity inXanthomonas

“…The extensive acquisition of novel T3Es and subsequent shaping of T3E repertoires through HGT events was hypothesized to account for specialization of strains on specific hosts (70,95,97). On top of HGT, selection of advantageous alleles seems to contribute to host adaptation (153).…”