<i>Pantoea ananatis</i>defeats<i>Allium</i>chemical defenses with a plasmid-borne virulence gene cluster

Stice, Shaun; Kk, Thao; Khang, Chang Hyun; Baltrus, David A.; Dutta, Bhabesh; Bh, Kvitko

doi:10.1101/2020.02.12.945675

Cited by 8 publications

(36 citation statements)

References 46 publications

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“…It is intriguing to speculate that the syntenic region might help overcome the oxidative burst associated with plant defense, as well as protecting against more specifically redox-active sulfur-containing plant defense substances such as allicin, and it would be interesting to see if loss of syntenic genes other than dsbA in Pst DC3000 also leads to a reduction of virulence. Moreover, a recent study reported plasmid-born onion virulence regions in Pantoea ananatis strains that are pathogenic on onion (Stice et al, 2018, 2020. The OVRA region contained a subset of genes that we describe in our present study as allicin resistance genes.…”

Section: Discussionmentioning

confidence: 50%

Genetic and molecular characterization of multicomponent resistance ofPseudomonasagainst allicin

et al. 2020

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The common foodstuff garlic produces the potent antibiotic defense substance allicin after tissue damage. Allicin is a redox toxin that oxidizes glutathione and cellular proteins and makes garlic a highly hostile environment for non-adapted microbes. Genomic clones from a highly allicin-resistant Pseudomonas fluorescens (PfAR-1), which was isolated from garlic, conferred allicin resistance to Pseudomonas syringae and even to Escherichia coli. Resistance-conferring genes had redox-related functions and were on core fragments from three similar genomic islands identified by sequencing and in silico analysis. Transposon mutagenesis and overexpression analyses revealed the contribution of individual candidate genes to allicin resistance. Taken together, our data define a multicomponent resistance mechanism against allicin in PfAR-1, achieved through horizontal gene transfer.

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Section: Discussionmentioning

confidence: 50%

Genetic and molecular characterization of multicomponent resistance ofPseudomonasagainst allicin

et al. 2020

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“…In this scenario, the alt cluster helps P. ananatis survive and colonize onion plants. P. ananatis uses 11 alt cluster genes associated with sulfur metabolism to impart tolerance to the thiosul nate 'allicin' that is produced by damaged onion cells [26]. The presence of the alt cluster in 80% (n = 41) of the onion pathogenic strains, and its absence in 67% (n = 20) of the non-pathogenic strains, suggests some potential involvement in bacterial virulence.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, Stice et al [25] showed that a megaplasmid-borne onion virulence region (OVR) in P. ananatis is correlated with onion virulence. In a recent study, Stice et al [26] showed that the OVRA cluster contains 11 genes that are critical for colonizing necrotized bulb tissue. This gene cluster was described as the 'alt' cluster that imparts bacterial tolerance to the thiosul nate 'allicin' in onion bulbs.…”

Section: Introductionmentioning

confidence: 99%

Pan-Genome-Wide Analysis of Pantoea Ananatis Identified Genes Linked to Pathogenicity in Onion

Agarwal¹,

Choudhary²,

Stice³

et al. 2020

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Background: Pantoea ananatis is a member of a Pantoea spp. complex that causes center rot of onion, which significantly affects onion yield and quality. This pathogen does not have typical virulence factors like type II or type III secretion systems but appears to require a biosynthetic gene-cluster, HiVir/PASVIL (located chromosomally), for a phosphonate secondary metabolite, and the onion-virulence regions, OVR (localized on a megaplasmid), for onion pathogenicity and virulence, respectively. Results: We conducted a deep pan-genome-wide association study (pan-GWAS) to predict additional genes associated with pathogenicity in P. ananatis using a panel of diverse strains (n = 81). We utilized a red-onion scale necrosis assay as an indicator of pathogenicity. Based on this assay, we differentiated pathogenic (n = 51) - vs. non-pathogenic (n = 30)-strains phenotypically. Pan-GWAS revealed a large core genome of 3,153 genes and a flexible accessory genome of ≤5,065 genes. Phylogenomic analysis using pan-GWAS and presence and absence variants (PAVs) distinguished red-scale necrosis inducing (pathogenic) strains from non-scale necrosis inducing (non-pathogenic) strains of P. ananatis. The pan-GWAS also predicted 42 genes, including 14 from the previously identified HiVir/PASVIL cluster associated with pathogenicity, and 28 novel genes that were not previously associated with pathogenicity in onion. Of the 28 novel genes identified, eight have annotated functions of site-specific tyrosine kinase, N-acetylmuramoyl-L-alanine amidase, TraR/DksA family transcriptional regulator, and HTH-type transcriptional regulator. The remaining 20 genes are currently hypothetical. Conclusions: This is the first report of using pan-GWAS on P. ananatis for the prediction of novel genes contributing to pathogenicity in onion, which will be utilized for further functional analyses. Pan-genomic differences (using PAVs) differentiated onion pathogenic from non-pathogenic strains of P. ananatis, which has been difficult to achieve using single or multiple gene-based phylogenetic analyses. The pan-genome analysis also allowed us to evaluate the presence and absence of HiVir/PASVIL genes and 11 megaplasmid-borne OVR-A genes regarded as the ‘alt’ cluster that aid in P. ananatis colonization in onion bulbs. We concluded that HiVir/PASVIL genes are associated with pathogenic P. ananatis strains and the alt gene cluster alone is not responsible for pathogenicity on onion. The pan-genome also provides clear evidence of constantly evolving accessory genes in P. ananatis that may contribute to host-range expansion and niche-adaptation.

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“…ananatis uses 11 alt cluster genes associated with sulfur metabolism to impart tolerance to the thiosulfinate 'allicin that is produced by damaged onion cells [26]. In this study, we demonstrated the use of a pan-GWAS approach to predict genes associated with onion-pathogenicity in P. ananatis.…”

Section: Discussionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Pan-genome-wide analysis ofPantoea ananatisidentified genes linked to pathogenicity in onion

Agarwal

Choudhary

Stice

et al. 2020

Preprint

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Pantoea ananatis is a member of a Pantoea spp. complex that causes center rot of onion, which significantly affects onion yield and quality. This pathogen does not have typical virulence factors like type II or type III secretion systems but appears to require a biosynthetic gene-cluster, HiVir/PASVIL (located chromosomally), for a phosphonate secondary metabolite, and the onion-virulence regions, OVR (localized on a megaplasmid), for onion pathogenicity and virulence, respectively. We conducted a deep pan-genome-wide association study (pan-GWAS) to predict additional genes associated with pathogenicity in P. ananatis using a panel of diverse strains (n = 81). We utilized a red-onion scale necrosis assay as an indicator of pathogenicity. Based on this assay, we differentiated pathogenic (n = 51)- vs. non-pathogenic (n = 30)-strains phenotypically. Pan-GWAS revealed a large core genome of 3,153 genes and a flexible accessory genome of ≤5,065 genes. Phylogenomic analysis using pan-GWAS and presence and absence variants (PAVs) distinguished red-scale necrosis inducing (pathogenic) strains from non-scale necrosis inducing (non-pathogenic) strains of P. ananatis. The pan-GWAS also predicted 42 genes, including 14 from the previously identified HiVir/PASVIL cluster associated with pathogenicity, and 28 novel genes that were not previously associated with pathogenicity in onion. Of the 28 novel genes identified, eight have annotated functions of site-specific tyrosine kinase, N-acetylmuramoyl-L-alanine amidase, TraR/DksA family transcriptional regulator, and HTH-type transcriptional regulator. The remaining 20 genes are currently hypothetical. This is the first report of using pan-GWAS on P. ananatis for the prediction of novel genes contributing to pathogenicity in onion, which will be utilized for further functional analyses. Pan-genomic differences (using PAVs) differentiated onion pathogenic from non-pathogenic strains of P. ananatis, which has been difficult to achieve using single or multiple gene-based phylogenetic analyses. The pan-genome analysis also allowed us to evaluate the presence and absence of HiVir/PASVIL genes and 11 megaplasmid-borne OVR-A genes regarded as the ‘alt’ cluster that aid in P. ananatis colonization in onion bulbs. We concluded that HiVir/PASVIL genes are associated with pathogenic P. ananatis strains and the alt gene cluster alone is not responsible for pathogenicity on onion. The pan-genome also provides clear evidence of constantly evolving accessory genes in P. ananatis that may contribute to host-range expansion and niche-adaptation.Author summaryPantoea ananatis is a major bacterial pathogen that causes center rot of onion and diseases of a number of other plant species. In order to understand the genome architecture and identify genes responsible for pathogenicity in onion, a pan-genome analysis was performed. We used 81 strains of P. ananatis collected over 20 years from different regions of the state of Georgia, USA. The pan-genome study identified a core genome with a conserved set of genes and an accessory genome that displayed variation among strains. We conducted pan-GWAS (pan-genome-wide association study) using presence and absence variants (PAVs) in the genomes and associated onion-pathogenic phenotypes based on a red-onion scale necrosis assay. The study resulted in identification of genes, including a cluster of chromosomal HiVir/PASVIL genes, that are significantly associated with the onion pathogenic phenotype. In addition, we identified 28 novel genes, a majority of which (n = 20) have hypothetical functions. We concluded and further substantiated earlier findings that a cluster of genes is responsible for pathogenicity on onion. The pan-genome analysis also allowed us to evaluate the presence and absence of HiVir/PASVIL genes and 11 megaplasmid-borne OVR-A genes regarded as the ‘alt’ cluster that aid in bacterial colonization of onion bulbs by P. ananatis strains. We concluded that HiVir/PASVIL genes are associated with onion-pathogenic strains, and the alt gene cluster alone is not responsible for pathogenicity on onion. This study also provides potential evidence of constantly evolving accessory genes in P. ananatis which may help in host range expansion and adaptation to diverse niches.

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Pantoea ananatisdefeatsAlliumchemical defenses with a plasmid-borne virulence gene cluster

Cited by 8 publications

References 46 publications

Genetic and molecular characterization of multicomponent resistance ofPseudomonasagainst allicin

Genetic and molecular characterization of multicomponent resistance ofPseudomonasagainst allicin

Pan-Genome-Wide Analysis of Pantoea Ananatis Identified Genes Linked to Pathogenicity in Onion

Pan-genome-wide analysis ofPantoea ananatisidentified genes linked to pathogenicity in onion

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