First Report of Copper-resistant <i>Xanthomonas citri</i> pv. <i>citri</i> Pathotype A Causing Asiatic Citrus Canker in Réunion, France

Although some plant pathogenic bacteria represent a significant threat to agriculture, the determinants of their ecological success and evolutionary potential are still poorly understood. Refining our understanding of bacterial strain circulation at small spatial scales and the biological significance and evolutionary consequences of co‐infections are key questions. The study of bacterial population biology can be challenging, because it requires high‐resolution markers that can be genotyped with a high throughput. Here, we overcame this difficulty for Xanthomonas citri pv. citri , a genetically monomorphic bacterium causing Asiatic citrus canker (ACC). Using a genotyping method that did not require cultivating the bacterium or purifying DNA, we deciphered the pathogen's spatial genetic structure at several microgeographic scales, down to single lesion, in a situation of ACC endemicity. In a grove where copper was recurrently applied for ACC management, copper‐susceptible and copper‐resistant X. citri pv. citri coexisted and the bacterial population structured as three genetic clusters, suggesting a polyclonal contamination. The range of spatial dependency, estimated for the two largest clusters, was four times greater for the cluster predominantly composed of copper‐resistant bacteria. Consistently, the evenness value calculated for this cluster was indicative of increased transmission. Linkage disequilibrium was high even at a tree scale, probably due to a combination of clonality and admixture. Approximately 1% of samples exhibited within‐lesion multilocus polymorphism, explained at least in part by polyclonal infections. Canker lesions, which are of major biological significance as an inoculum source, may also represent a preferred niche for horizontal gene transfer. This study points out the potential of genotyping data for estimating the range of spatial dependency of plant bacterial pathogens, an important parameter for guiding disease management strategies.

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“…Copper resistance, first reported in Reunion Island in 2014 (Richard et al, 2017), was detected in grove 2, but not in grove 1.…”

Section: A More Efficient Transmission Of Copperresistant Strainsmentioning

confidence: 85%

“…The copper-resistant X. citri pv. citri strain LH201 was used as a positive control in each experiment (Richard et al, 2017).…”

Section: Cop Pcr Amplificationmentioning

confidence: 99%

Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity

Pruvost

Boyer

Ravigné

et al. 2019

Evolutionary Applications

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“…citri copper resistance until it was discovered in the French islands of Réunion (a French territory in the South West Indian Ocean) and Martinique (a French territory in the Eastern Caribbean Sea) in 2014, two decades later (Richard et al . , ). The causative genes of Argentinian X. citri pv.…”

Section: Introductionmentioning

confidence: 99%

Adaptation of genetically monomorphic bacteria: evolution of copper resistance through multiple horizontal gene transfers of complex and versatile mobile genetic elements

et al. 2017

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Copper-based antimicrobial compounds are widely used to control plant bacterial pathogens. Pathogens have adapted in response to this selective pressure. Xanthomonas citri pv. citri, a major citrus pathogen causing Asiatic citrus canker, was first reported to carry plasmid-encoded copper resistance in Argentina. This phenotype was conferred by the copLAB gene system. The emergence of resistant strains has since been reported in Réunion and Martinique. Using microsatellite-based genotyping and copLAB PCR, we demonstrated that the genetic structure of the copper-resistant strains from these three regions was made up of two distant clusters and varied for the detection of copLAB amplicons. In order to investigate this pattern more closely, we sequenced six copper-resistant X. citri pv. citri strains from Argentina, Martinique and Réunion, together with reference copper-resistant Xanthomonas and Stenotrophomonas strains using long-read sequencing technology. Genes involved in copper resistance were found to be strain dependent with the novel identification in X. citri pv. citri of copABCD and a cus heavy metal efflux resistance-nodulation-division system. The genes providing the adaptive trait were part of a mobile genetic element similar to Tn3-like transposons and included in a conjugative plasmid. This indicates the system's great versatility. The mining of all available bacterial genomes suggested that, within the bacterial community, the spread of copper resistance associated with mobile elements and their plasmid environments was primarily restricted to the Xanthomonadaceae family.

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“…Resistance to copper‐based bactericides is also a challenge in the control of phytopathogens . Copper resistance has been observed in several phytopathogens including Pseudomonas and Xanthomonas spp . One study reported that 80% of 35 Pseudomonas syringae pv.…”

Section: Introductionmentioning

confidence: 99%

Biocontrol of phytobacteria with bacteriophage cocktails

Kering

Kibii

Wei

2019

Pest Management Science

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Crop loss due to plant pathogens has provoked renewed interest in bacteriophages as a feasible biocontrol strategy of plant diseases. Phage cocktails in particular present a viable option for broadening the phage host range, limiting the emergence of bacterial resistance while maintaining the lytic activity of the phages. It is therefore important that the design used to formulate a phage cocktail should result in the most effective cocktail against the pathogen. It is also critical that certain factors are considered during the formulation and application of a phage cocktail: their stability, the production time and cost of complex cocktails, the potential impact on untargeted bacteria, the timing of phage application, and the persistence in the plant environment. Continuous monitoring is required to ensure that the efficacy of a cocktail is sustained due to the dynamic nature of phages. Although phage cocktails are considered as a plausible biocontrol strategy of phytobacteria, more research needs to be done to understand the complex interaction between phages and bacteria in the plant environment, and to overcome the technical obstacles.

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First Report of Copper-resistant Xanthomonas citri pv. citri Pathotype A Causing Asiatic Citrus Canker in Réunion, France

Cited by 30 publications

References 5 publications

Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity

Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity

Adaptation of genetically monomorphic bacteria: evolution of copper resistance through multiple horizontal gene transfers of complex and versatile mobile genetic elements

Biocontrol of phytobacteria with bacteriophage cocktails

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