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Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity.

ABSTRACT: Bacterial spot disease of pepper and tomato is caused by four distinct Xanthomonas species and is a severely limiting factor on fruit yield in these crops. The genetic diversity and the type III effector repertoires of a large sampling of field strains for this disease have yet to be explored on a genomic scale, limiting our understanding of pathogen evolution in an agricultural setting. Genomes of 67 Xanthomonas euvesicatoria (Xe), Xanthomonas perforans (Xp), and Xanthomonas gardneri (Xg) strains isolated from diseased pepper and tomato fields in the southeastern and midwestern United States were sequenced in order to determine the genetic diversity in field strains. Type III effector repertoires were computationally predicted for each strain, and multiple methods of constructing phylogenies were employed to understand better the genetic relationship of strains in the collection. A division in the Xp population was detected based on core genome phylogeny, supporting a model whereby the host-range expansion of Xp field strains on pepper is due, in part, to a loss of the effector AvrBsT. Xp-host compatibility was further studied with the observation that a double deletion of AvrBsT and XopQ allows a host range expansion for Nicotiana benthamiana. Extensive sampling of field strains and an improved understanding of effector content will aid in efforts to design disease resistance strategies targeted against highly conserved core effectors.

SUBMITTER: Schwartz AR

PROVIDER: S-EPMC4452888 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity.

Schwartz Allison R AR Potnis Neha N Timilsina Sujan S Wilson Mark M Patané José J Martins Joaquim J Minsavage Gerald V GV Dahlbeck Douglas D Akhunova Alina A Almeida Nalvo N Vallad Gary E GE Barak Jeri D JD White Frank F FF Miller Sally A SA Ritchie David D Goss Erica E Bart Rebecca S RS Setubal João C JC Jones Jeffrey B JB Staskawicz Brian J BJ

Frontiers in microbiology 20150603

Bacterial spot disease of pepper and tomato is caused by four distinct Xanthomonas species and is a severely limiting factor on fruit yield in these crops. The genetic diversity and the type III effector repertoires of a large sampling of field strains for this disease have yet to be explored on a genomic scale, limiting our understanding of pathogen evolution in an agricultural setting. Genomes of 67 Xanthomonas euvesicatoria (Xe), Xanthomonas perforans (Xp), and Xanthomonas gardneri (Xg) strai ...[more]

PMID: 26089818

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Project description:BackgroundThe genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.Methodology/principal findingsTwo hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132 Xanthomonas axonopodis strains representative of 18 different pathovars which display different host range. First, the phylogenetic position of each strain was determined by sequencing the housekeeping gene rpoD. This study showed that many pathovars of Xanthomonas axonopodis are polyphyletic. Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods. Indeed, for pathogenic bacteria T3Es were shown to trigger and to subvert host defences. Our study revealed that T3E repertoires comprise core and variable gene suites that likely have distinct roles in pathogenicity and different evolutionary histories. Our results showed a correspondence between composition of T3E repertoires and pathovars of Xanthomonas axonopodis. For polyphyletic pathovars, this suggests that T3E genes might explain a pathological convergence of phylogenetically distant strains. We also identified several DNA rearrangements within T3E genes, some of which correlate with host specificity of strains.Conclusions/significanceThese data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a "repertoire for repertoire" hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.

Project description:BackgroundBacterial spot of tomato and pepper is caused by four Xanthomonas species and is a major plant disease in warm humid climates. The four species are distinct from each other based on physiological and molecular characteristics. The genome sequence of strain 85-10, a member of one of the species, Xanthomonas euvesicatoria (Xcv) has been previously reported. To determine the relationship of the four species at the genome level and to investigate the molecular basis of their virulence and differing host ranges, draft genomic sequences of members of the other three species were determined and compared to strain 85-10.ResultsWe sequenced the genomes of X. vesicatoria (Xv) strain 1111 (ATCC 35937), X. perforans (Xp) strain 91-118 and X. gardneri (Xg) strain 101 (ATCC 19865). The genomes were compared with each other and with the previously sequenced Xcv strain 85-10. In addition, the molecular features were predicted that may be required for pathogenicity including the type III secretion apparatus, type III effectors, other secretion systems, quorum sensing systems, adhesins, extracellular polysaccharide, and lipopolysaccharide determinants. Several novel type III effectors from Xg strain 101 and Xv strain 1111 genomes were computationally identified and their translocation was validated using a reporter gene assay. A homolog to Ax21, the elicitor of XA21-mediated resistance in rice, and a functional Ax21 sulfation system were identified in Xcv. Genes encoding proteins with functions mediated by type II and type IV secretion systems have also been compared, including enzymes involved in cell wall deconstruction, as contributors to pathogenicity.ConclusionsComparative genomic analyses revealed considerable diversity among bacterial spot pathogens, providing new insights into differences and similarities that may explain the diverse nature of these strains. Genes specific to pepper pathogens, such as the O-antigen of the lipopolysaccharide cluster, and genes unique to individual strains, such as novel type III effectors and bacteriocin genes, have been identified providing new clues for our understanding of pathogen virulence, aggressiveness, and host preference. These analyses will aid in efforts towards breeding for broad and durable resistance in economically important tomato and pepper cultivars.

Project description:Disease outbreaks of bacterial leaf spot and blight of pepper and tomato often occur in both transplant- and field-production systems worldwide. In some cases, the outbreaks are caused by novel bacterial species. Characterization of these novel bacterial species are critical in developing diagnostic assays and identifying management options for pathogen monitoring and sustainable production, respectively. We characterized strains belonging to novel Pseudomonas species that are responsible for outbreaks in pepper and tomato both in transplant-houses and in production fields in Georgia, USA. Phylogenomic analyses and whole genome sequence indices demonstrated that the pepper and tomato strains belonged to P. capsici. The whole-genome comparison revealed that 13 Pseudomonas strains from diverse isolation sources that were curated in NCBI were indeed P. capsici indicating a potential wide-host range for this bacterial species. Our greenhouse-based host-range assay also indicated that P. capsici strains were pathogenic on pepper, tomato, eggplant, cabbage, lettuce, and watermelon corroborating a wide-host-range. A phylogenetic tree inferred from the whole genome sequence data showed that the P. capsici strains from Georgia (pepper and tomato) were genetically diverse, and were closely related to tomato P. capsici strains from Florida. Genomic presence of traditional bacterial virulence factors in P. capsici strains was also determined. Pseudomonascapsici strains encode one set of type I secretion system, two sets of type II secretion systems, one set of type III secretion system, two sets of type V secretion systems, three sets of type VI secretion systems, and various secondary metabolite gene clusters including lipopeptides. In in-vitro assays, it was demonstrated that six out of seven P. capsici strains (pepper and tomato strains from Georgia) were not sensitive to 0.8 mM CuSO4. When the genomes of copper-tolerant strains were compared with the copper-sensitive strains, it was observed that the former strains encode a cluster of genes related to copper tolerance, which were absent in the genomes of copper-sensitive strains. Considering the ability of P. capsici strains to infect a range of vegetable hosts and possession of a wide range of bacterial virulence factors, secondary metabolites, and copper-tolerance genes, we envision that the management of this pathogen might potentially be a challenge.

Dataset Information

Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity.

Publications

Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity.

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