Whole-Genome Sequences of Xanthomonas euvesicatoria Strains Clarify Taxonomy and Reveal a Stepwise Erosion of Type 3 Effectors

Barak, Jeri D.; Vancheva, Taca; Lefeuvre, Pierre; Jones, Jeffrey B.; Timilsina, Sujan; Minsavage, Gerald V.; Vallad, Gary E.; Koebnik, Ralf

doi:10.3389/fpls.2016.01805

Cited by 58 publications

(56 citation statements)

References 37 publications

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“…Both species form sister lineages within the larger X. euvesicatoria species complex, as initially described by Parkinson et al . () and consists of a heterogeneous group of bacteria that share ≥98% average nucleotide identities (Barak et al ., ; Constantin et al ., ; Bansal et al ., ). Being a seed‐borne pathogen, introduction of contaminated transplants into fields is considered a primary source of Xanthomonas inoculum (Abrahamian et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Genome‐resolved metagenomics to study co‐occurrence patterns and intraspecific heterogeneity among plant pathogen metapopulations

Newberry

Bhandari

Kemble

et al. 2020

Environmental Microbiology

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Summary Assessment of pathogen diversity in agricultural fields is essential for informing management decisions and the development of resistant plant varieties. However, many population genomic studies have relied on culture‐based approaches that do not provide quantitative assessment of pathogen populations at the field‐level or the associated host microbiome. Here, we applied whole‐genome shotgun sequencing of microbial DNA extracted directly from the washings of pooled leaf samples, collected from individual tomato and pepper fields in Alabama that displayed the classical symptoms of bacterial spot disease caused by Xanthomonas spp. Our results revealed that while the occurrence of both X. perforans and X. euvesicatoria within fields was limited, evidence of co‐occurrence of up to three distinct X. perforans genotypes was obtained in 7 of 10 tomato fields sampled. These population dynamics were accompanied by the corresponding type 3 secreted effector repertoires associated with the co‐occurring X. perforans genotypes, indicating that metapopulation structure within fields should be considered when assessing the adaptive potential of X. perforans. Finally, analysis of microbial community composition revealed that co‐occurrence of the bacterial spot pathogens Pseudomonas cichorii and Xanthomonas spp. is common in Alabama fields and provided evidence for the non‐random association of several other human and plant opportunists.

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Section: Introductionmentioning

confidence: 99%

Genome‐resolved metagenomics to study co‐occurrence patterns and intraspecific heterogeneity among plant pathogen metapopulations

Newberry

Bhandari

Kemble

et al. 2020

Environmental Microbiology

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“…Other studies have found atypical bacterial spot strains in Europe, Asia, and Africa (34)(35)(36). The genomes of two of these strains have been sequenced previously: X. perforans strain 4P1S2, from Italy, and X. euvesicatoria strain LMG918, from India (36,37). Preliminary analysis of the genome of strain 4P1S2 showed that it contained regions that were identical in sequence to regions of genomes of other Xanthomonas species, suggesting recombination (34).…”

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confidence: 94%

“…Preliminary analysis of the genome of strain 4P1S2 showed that it contained regions that were identical in sequence to regions of genomes of other Xanthomonas species, suggesting recombination (34). Strain LMG918 was identified as X. euvesicatoria but is amylolytic, which is not typical of X. euvesicatoria strains, and sequencing of its genome revealed unique effector gene content relative to other X. euvesicatoria strains (37). Together with our initial analysis of the strains from Nigeria, these findings suggest that there are genetic groups of X. euvesicatoria and X. perforans that are not represented in genome studies of U.S. strains.…”

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confidence: 99%

Genomic Inference of Recombination-Mediated Evolution in Xanthomonas euvesicatoria and X. perforans

Jibrin

Potnis

Timilsina

et al. 2018

Appl Environ Microbiol

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Recombination is a major driver of evolution in bacterial populations, because it can spread and combine independently evolved beneficial mutations. Recombinant lineages of bacterial pathogens of plants are typically associated with the colonization of novel hosts and the emergence of new diseases. Here we show that recombination between evolutionarily and phenotypically distinct plant-pathogenic lineages generated recombinant lineages with unique combinations of pathogenicity and virulence factors. and are two closely related lineages causing bacterial spot disease on tomato and pepper worldwide. We sequenced the genomes of atypical strains collected from tomato in Nigeria and observed recombination in the type III secretion system and effector genes, which showed alleles from both and Wider horizontal gene transfer was indicated by the fact that the lipopolysaccharide cluster of one strain was most similar to that of a distantly related pathogen of barley. This strain and others have experienced extensive genomewide homologous recombination, and both species exhibited dynamic open pangenomes. Variation in effector gene repertoires within and between species must be taken into consideration when one is breeding tomatoes for disease resistance. Resistance breeding strategies that target specific effectors must consider possibly dramatic variation in bacterial spot populations across global production regions, as illustrated by the recombinant strains observed here. The pathogens that cause bacterial spot of tomato and pepper are extensively studied models of plant-microbe interactions and cause problematic disease worldwide. Atypical bacterial spot strains collected from tomato in Nigeria, and other strains from Italy, India, and Florida, showed evidence of genomewide recombination that generated genetically distinct pathogenic lineages. The strains from Nigeria and Italy were found to have a mix of type III secretion system genes from and, as well as effectors from These genes and effectors are important in the establishment of disease, and effectors are common targets of resistance breeding. Our findings point to global diversity in the genomes of bacterial spot pathogens, which is likely to affect the host-pathogen interaction and influence management decisions.

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“…However, these aforementioned tools have significant limitations because they examine only a subset of the bacterial genome of interest and thus restrict molecular epidemiological analyses (12). For instance, virulence-or effector-based typing can be misleading when used to infer ancestry, due to the loss and acquisition of virulence genes (17,18).…”

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confidence: 99%

Molecular Epidemiology ofXanthomonas perforansOutbreaks in Tomato Plants from Transplant to Field as Determined by Single-Nucleotide Polymorphism Analysis

Abrahamian

Timilsina

Minsavage

et al. 2019

Appl Environ Microbiol

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Outbreaks of bacterial spot on tomato (BST) caused by Xanthomonas perforans are a major concern for sustainable crop production. BST is a common occurrence in tomato transplants grown for field production. We hypothesized that BST outbreaks in commercial fields originate from X. perforans strains inadvertently introduced from commercial transplant facilities. To test this hypothesis, we used a genome-wide single-nucleotide polymorphism (SNP) analysis to characterize X. perforans strains recovered from tomato transplant facilities and fields in commercial production areas. X. perforans strains were isolated from symptomatic transplants prior to roguing at two commercial transplant growers. Then, the same groups of transplants were tracked to commercial fields to recover X. perforans strains from diseased plants prior to harvest. Whole-genome sequencing was carried out on 84 strains isolated from transplant and field plants from Florida and South Carolina. SNPs were called using three reference strains that represented the genetic variation of the sampled strains. Field strains showing genetic similarity to transplant strains had a difference of 2 to 210 SNPs. Transplant and field strains clustered together by grower within each phylogenomic group, consistent with expectations. The range of genetic divergence among strains isolated from field plants was similar to the range obtained from strains on transplants. Using the range of genetic variation observed in transplants, we estimate that 60% to 100% of field strains were an extension of the transplant strain population. Our results stress the importance of BST management to reduce X. perforans movement from transplant to field and to minimize subsequent disease outbreaks. IMPORTANCE Current management of Xanthomonas perforans on tomato plants mainly relies on the frequent application of pesticides. However, the lack of effective pesticides and the development of strain tolerance to certain bactericides limit the ability to control outbreaks in production fields. Better knowledge of probable sources of X. perforans inoculum during tomato production is required to refine management strategies. Tomato plants are typically established in the field using transplants. This study aimed to determine if strains from field epidemics were coming from transplant facilities or resulted from local field outbreaks. The overall goal was to identify potential sources of inoculum and subsequently develop strategies to reduce carryover from transplant production to the field. Our results indicate that tomato producers should shift disease management efforts to transplant facilities to reduce disease in the field. Improved transplant health should reduce the likelihood of bacterial spot outbreaks and subsequently reduce pesticide usage in the field.

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Whole-Genome Sequences of Xanthomonas euvesicatoria Strains Clarify Taxonomy and Reveal a Stepwise Erosion of Type 3 Effectors

Cited by 58 publications

References 37 publications

Genome‐resolved metagenomics to study co‐occurrence patterns and intraspecific heterogeneity among plant pathogen metapopulations

Genome‐resolved metagenomics to study co‐occurrence patterns and intraspecific heterogeneity among plant pathogen metapopulations

Genomic Inference of Recombination-Mediated Evolution in Xanthomonas euvesicatoria and X. perforans

Molecular Epidemiology ofXanthomonas perforansOutbreaks in Tomato Plants from Transplant to Field as Determined by Single-Nucleotide Polymorphism Analysis

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