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

Abstract 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 s...

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Main Authors: Olivier Pruvost, Karine Boyer, Virginie Ravigné, Damien Richard, Christian Vernière
Format: Article
Language:English
Published: Wiley 2019-09-01
Series:Evolutionary Applications
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Online Access:https://doi.org/10.1111/eva.12788
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author Olivier Pruvost
Karine Boyer
Virginie Ravigné
Damien Richard
Christian Vernière
author_facet Olivier Pruvost
Karine Boyer
Virginie Ravigné
Damien Richard
Christian Vernière
author_sort Olivier Pruvost
collection DOAJ
description Abstract 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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spelling doaj.art-d7e01900a2c54a2bbe175e13a1c0c5392022-12-22T01:55:49ZengWileyEvolutionary Applications1752-45712019-09-011281523153810.1111/eva.12788Deciphering 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 endemicityOlivier Pruvost0Karine Boyer1Virginie Ravigné2Damien Richard3Christian Vernière4CIRAD UMR PVBMT Saint Pierre, La Réunion FranceCIRAD UMR PVBMT Saint Pierre, La Réunion FranceCIRAD UMR PVBMT Saint Pierre, La Réunion FranceCIRAD UMR PVBMT Saint Pierre, La Réunion FranceCIRAD UMR PVBMT Saint Pierre, La Réunion FranceAbstract 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.https://doi.org/10.1111/eva.12788genotypingmicrosatellitesplant bacterial diseasesspatial structure
spellingShingle Olivier Pruvost
Karine Boyer
Virginie Ravigné
Damien Richard
Christian Vernière
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
Evolutionary Applications
genotyping
microsatellites
plant bacterial diseases
spatial structure
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic genotyping
microsatellites
plant bacterial diseases
spatial structure
url https://doi.org/10.1111/eva.12788
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