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.
Highlights
Understanding the population biology of plant pathogens, that is, their population genetic structure and dynamics, is important for an informed management of plant diseases in agro‐ecosystems (Burdon & Thrall, 2008; Milgroom, 2015; Stukenbrock & McDonald, 2008)
DNA release and amplification are combined in a single step. It is performed directly from biological samples without the need for bacterial cultivation or genomic DNA extraction. By using this genotyping method, we addressed the following questions: How often do genetically distinct strains co‐occur at the field scale, at the tree scale, and in the same lesion? At the lesion scale, is this diversity strictly related to the population's clonal diversification and/or does it reveal the existence of polyclonal infections, which involve genetically distant strains? what is the spatial genetic structure of X. citri pv. citri populations and what does it reveal about the heterogeneity of inoculum and the pathogen's transmission capability in citrus groves?
We investigated the epidemiological dynamics of X. citri pv. citri at microgeographic scales using a molecular epidemiology approach combining microsatellite genotyping and an extensive hierarchical sampling of two citrus groves
Summary
Understanding the population biology of plant pathogens, that is, their population genetic structure and dynamics, is important for an informed management of plant diseases in agro‐ecosystems (Burdon & Thrall, 2008; Milgroom, 2015; Stukenbrock & McDonald, 2008). Citri) is the causal agent of Asiatic citrus canker (ACC), a striking example of a plant bacterial pathogen that poses a major economic risk to agriculture on several continents It affects crop profitability, both directly (i.e., fruit yield and reduced quality) and indirectly (restrictions of fresh fruit exports because of quarantine regulations in countries not exposed to ACC; Graham, Gottwald, Cubero, & Achor, 2004). Apart from surface biofilms, which possibly represent a more minor inoculum source, the pathogen cannot survive outside canker lesions for extended periods (Cubero, Gell, Johnson, Redondo, & Graham, 2011; Graham et al, 2004) It is dispersed naturally within individual trees or between neighboring trees in droplets, by splashing or wind‐driven dispersal, resulting in aggregated disease patterns (Danos, Berger, & Stall, 1984). By using this genotyping method, we addressed the following questions: How often do genetically distinct strains co‐occur at the field scale, at the tree scale, and in the same lesion? At the lesion scale, is this diversity strictly related to the population's clonal diversification (i.e., the observed diversity of descendants from the original haplotype, which initiated infection) and/or does it reveal the existence of polyclonal infections, which involve genetically distant strains? what is the spatial genetic structure of X. citri pv. citri populations and what does it reveal about the heterogeneity of inoculum and the pathogen's transmission capability in citrus groves?
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