Comparative Genomics of Pathogenic and Nonpathogenic Strains of Xanthomonas arboricola Unveil Molecular and Evolutionary Events Linked to Pathoadaptation

Sophie Cesbron,Martial Briand,Marion Fischer-Le Saux,Marie-Agnès Jacques,Sophie Gironde,Charles Manceau,Tristan Boureau,Salwa Essakhi

doi:10.3389/fpls.2015.01126

Sophie Cesbron, Martial Briand + Show 6 more

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https://doi.org/10.3389/fpls.2015.01126

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Abstract

The bacterial species Xanthomonas arboricola contains plant pathogenic and nonpathogenic strains. It includes the pathogen X. arboricola pv. juglandis, causing the bacterial blight of Juglans regia. The emergence of a new bacterial disease of J. regia in France called vertical oozing canker (VOC) was previously described and the causal agent was identified as a distinct genetic lineage within the pathovar juglandis. Symptoms on walnut leaves and fruits are similar to those of a bacterial blight but VOC includes also cankers on trunk and branches. In this work, we used comparative genomics and physiological tests to detect differences between four X. arboricola strains isolated from walnut tree: strain CFBP 2528 causing walnut blight (WB), strain CFBP 7179 causing VOC and two nonpathogenic strains, CFBP 7634 and CFBP 7651, isolated from healthy walnut buds. Whole genome sequence comparisons revealed that pathogenic strains possess a larger and wider range of mobile genetic elements than nonpathogenic strains. One pathogenic strain, CFBP 7179, possessed a specific integrative and conjugative element (ICE) of 95 kb encoding genes involved in copper resistance, transport and regulation. The type three effector repertoire was larger in pathogenic strains than in nonpathogenic strains. Moreover, CFBP 7634 strain lacked the type three secretion system encoding genes. The flagellar system appeared incomplete and nonfunctional in the pathogenic strain CFBP 2528. Differential sets of chemoreceptor and different repertoires of genes coding adhesins were identified between pathogenic and nonpathogenic strains. Besides these differences, some strain-specific differences were also observed. Altogether, this study provides valuable insights to highlight the mechanisms involved in ecology, environment perception, plant adhesion and interaction, leading to the emergence of new strains in a dynamic environment.

Highlights

Xanthomonads are bacteria associated to plants and are commonly pathogens of plants (Vauterin et al, 2000)
We present genomic comparisons of four X. arboricola strains isolated from walnut tree that are representative of the bacterial diversity encountered on J. regia and that were previously analyzed by MLSA, MLVA, and T3Es repertoire (Hajri et al, 2012; Essakhi et al, 2015; FischerLe Saux et al, 2015)
integrative and conjugative element (ICE) and Copper Resistance We showed that strain CFBP 7179 and 36 X. arboricola pv. juglandis strains harbor an ICE with copper resistant genes and are copper resistant

Summary

Introduction

Xanthomonads are bacteria associated to plants and are commonly pathogens of plants (Vauterin et al, 2000). These strains are unable to cause any disease on walnut tree and other plant species (Essakhi et al, 2015) Such xanthomonads, nonpathogenic strains on their host of isolation, have already been isolated from a range of different plants (Vauterin et al, 1996; Vandroemme et al, 2013a; Triplett et al, 2015). Within X. arboricola, nonpathogenic strains from Juglans regia and from Fragaria × ananassa are phylogenetically diverse and do not cluster according to their host of isolation contrary to pathogenic strains from pathovars pruni, corylina, and juglandis (Vandroemme et al, 2013a; Essakhi et al, 2015; Fischer-Le Saux et al, 2015)

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