Origin and diversification of Xanthomonas citri subsp. citri pathotypes revealed by inclusive phylogenomic, dating, and biogeographic analyses

Abstract

Background Xanthomonas citri subsp. citri pathotypes cause bacterial citrus canker, being responsible for severe agricultural losses worldwide. The A pathotype has a broad host spectrum, while A* and Aw are more restricted both in hosts and in geography. Two previous phylogenomic studies led to contrasting well-supported clades for sequenced genomes of these pathotypes. No extensive biogeographical or divergence dating analytic approaches have been so far applied to available genomes. Results Based on a larger sampling of genomes than in previous studies (including six new genomes sequenced by our group, adding to a total of 95 genomes), phylogenomic analyses resulted in different resolutions, though overall indicating that A + AW is the most likely true clade. Our results suggest the high degree of recombination at some branches and the fast diversification of lineages are probable causes for this phylogenetic blurring effect. One of the genomes analyzed, X. campestris pv. durantae, was shown to be an A* strain; this strain has been reported to infect a plant of the family Verbenaceae, though there are no reports of any X. citri subsp. citri pathotypes infecting any plant outside the Citrus genus. Host reconstruction indicated the pathotype ancestor likely had plant hosts in the family Fabaceae, implying an ancient jump to the current Rutaceae hosts. Extensive dating analyses indicated that the origin of X. citri subsp. citri occurred more recently than the main phylogenetic splits of Citrus plants, suggesting dispersion rather than host-directed vicariance as the main driver of geographic expansion. An analysis of 120 pathogenic-related genes revealed pathotype-associated patterns of presence/absence. Conclusions Our results provide novel insights into the evolutionary history of X. citri subsp. citri as well as a sound phylogenetic foundation for future evolutionary and genomic studies of its pathotypes.

Development and comparative validation of genomic-driven PCR-based assays to detect Xanthomonas citri pv. citri in citrus plants

“…citri strain collection, a feature that most earlier studies failed to achieve. Indeed, we assayed representative samples of all the lineages/sublineages of this bacterium, which have been reported to date throughout the world [11,[16][17][18]38]. The selected target gene, XAC1051, encodes for a hypothetical transmembrane protein and is present on the chromosome of strains for which a complete genome sequence is available.…”

“…cajani was identified as the closest relative to X. citri pv. citri in a recent phylogenomic analysis [38], suggesting that this DNA region may have been present in their most recent common ancestor. If necessary, suspect samples can be confirmed by performing the XAC1051-F/R PCR assay.…”

“…citri strain collection, a feature that most earlier studies failed to achieve. Indeed, we assayed representative samples of all the lineages/sublineages of this bacterium, which have been reported to date throughout the world [ 11 , 16 – 18 , 38 ].…”

“…citri pathotype A* strain was recently authenticated by WGS data, after initially being mislabeled as X. campestris pv. durantae [38].…”

Comparative Genomics of Xanthomonas citri pv. citri A* Pathotype Reveals Three Distinct Clades with Varying Plasmid Distribution

“…citri phylogeny has been inconsistent with multiple studies observing different evolution of the A, A*, and A w pathotypes. Patané et al (2019) attribute these inconsistencies in lineages of X. citri pv. citri to be due to fast diversification, causing a "blurring effect" of the phylogeny [13].…”