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

José S L Patané,Leandro M Moreira,Nalvo F Almeida,Agda Paula Facincani,Nian Wang,Joaquim Martins,Luiz Thiberio Rangel,Alessandro M Varani,Luciano A Digiampietri,Fabrício José Jaciani,Rafael Marini Ferreira,José Belasque,Jesus A Ferro,João C Setubal,Yunzeng Zhang

doi:10.1186/s12864-019-6007-4

Abstract

BackgroundXanthomonas 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.ResultsBased 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.ConclusionsOur 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.

Highlights

Xanthomonas citri subsp. citri pathotypes cause bacterial citrus canker, being responsible for severe agricultural losses worldwide
These results suggest that a homogeneous and reversible process of evolution is a reasonable assumption across the genomes studied, validating model choice among reversible likelihood models included in IQTree
It is interesting to know the timeframe of evolution of known lineages, since this may provide clues for the likelihood of a highly resistant strain emerging in the near future

Summary

Introduction

Xanthomonas citri subsp. citri pathotypes cause bacterial citrus canker, being responsible for severe agricultural losses worldwide. Citri pathotypes cause bacterial citrus canker, being responsible for severe agricultural losses worldwide. Two previous phylogenomic studies led to contrasting well-supported clades for sequenced genomes of these pathotypes. Citrus canker is a bacterial disease affecting all commercial citrus varieties. This disease has been intensively studied in the past several decades, given the widespread cultivation of citrus in many regions of the world and the economic importance of the orange juice industry [1,2,3]. The causal agent of canker A is Xanthomonas citri subsp. Citri (XCC), which was the first Xanthomonas genome to be sequenced (strain 306) [9] The causal agent of canker A is Xanthomonas citri subsp. citri (XCC), which was the first Xanthomonas genome to be sequenced (strain 306) [9]

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Conclusion