Secrete or perish: The role of secretion systems in Xanthomonas biology

Martı́nez, Consuelo; Sgro, Germán G.; Araujo, Gabriel Guarany de; Paiva, Mateus R.N.; Matsuyama, Bruno Y.; Guzzo, Cristiane R.; Andrade, Maxuel O.; Farah, Chuck S.

doi:10.1016/j.csbj.2020.12.020

Cited by 50 publications

(50 citation statements)

References 352 publications

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“…In Xanthomonas species, virulence factors generally depend on the type II and type III secretion systems (T2SS and T3SS, respectively). These secretion systems allow the bacteria to export virulence factors in order to enable or facilitate their proliferation and survival in the host by targeting specific host components ( Büttner and Bonas, 2010 ; Alvarez-Martinez et al, 2021 ). Identifying which virulence factors are involved in the pathogen’s virulence and which host components are the targets of these virulence factors is crucial, as these host components can then be the focus of resistance breeding.…”

Section: Introductionmentioning

confidence: 99%

“…In addition to the T2SS and T3SS, the type IV and type VI secretion systems (T4SS and T6SS, respectively) also secrete proteins that may affect the virulence of the pathogen. However, while the T2SS and the T3SS target host components, the T4SS and the T6SS are involved in the defense against microbial predators such as amoeba, as well as in the competition with other microorganisms ( Büttner and Bonas, 2010 ; Alvarez-Martinez et al, 2021 ). The T4SS is evolutionarily related to bacterial conjugation systems and is involved in the competition with other bacteria by injecting protein effectors or protein–DNA complexes into their cells ( Sgro et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Complete Genome Assemblies of All Xanthomonas translucens Pathotype Strains Reveal Three Genetically Distinct Clades

et al. 2022

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The Xanthomonas translucens species comprises phytopathogenic bacteria that can cause serious damage to cereals and to forage grasses. So far, the genomic resources for X. translucens were limited, which hindered further understanding of the host–pathogen interactions at the molecular level and the development of disease-resistant cultivars. To this end, we complemented the available complete genome sequence of the X. translucens pv. translucens pathotype strain DSM 18974 by sequencing the genomes of all the other 10 X. translucens pathotype strains using PacBio long-read technology and assembled complete genome sequences. Phylogeny based on average nucleotide identity (ANI) revealed three distinct clades within the species, which we propose to classify as clades Xt-I, Xt-II, and Xt-III. In addition to 2,181 core X. translucens genes, a total of 190, 588, and 168 genes were found to be exclusive to each clade, respectively. Moreover, 29 non-transcription activator-like effector (TALE) and 21 TALE type III effector classes were found, and clade- or strain-specific effectors were identified. Further investigation of these genes could help to identify genes that are critically involved in pathogenicity and/or host adaptation, setting the grounds for the development of new resistant cultivars.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Complete Genome Assemblies of All Xanthomonas translucens Pathotype Strains Reveal Three Genetically Distinct Clades

et al. 2022

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“…In this cluster, mobABC is necessary for the initiation and termination stages of conjugal transfer while mobD and mobE act as accessory genes by drastically increasing conjugation efficiency (Perwez and Meyer, 1996;Zhang and Meyer, 1997;Bravo-Angel et al, 1999;van Zyl et al, 2003). In addition, the type IV secretion system (T4SS) located on the chromosome of xanthomonads also contributes to conjugation (Wallden et al, 2010;Guglielmini et al, 2013;Cenens et al, 2020;Alvarez-Martinez et al, 2021). Therefore, mobilization of these small plasmids is likely the outcome from the interplay of the repAC and mobABCDE genes, T4SS genes, and selection pressure from OTC sprays (Guglielmini et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach

et al. 2022

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Xanthomonas arboricola pv. pruni (Xap) causes bacterial spot, a major worldwide disease of Prunus species. Very few chemical management options are available for this disease and frequent applications of oxytetracycline (OTC) in the United States peach orchards have raised concerns about resistance development. During 2017–2020, 430 Xap strains were collected from ten peach orchards in South Carolina. Seven OTC-resistant (OTCR) Xap strains were found in 2017 and 2020 from four orchards about 20–270 km apart. Interestingly, the seven strains were also resistant to streptomycin (STR). Six strains grew on media amended with ≤100 μg/mL OTC, while one strain, R1, grew on ≤250 μg/mL OTC. Genome sequence analysis of four representative OTCR strains revealed a 14–20 kb plasmid carrying tetC, tetR, and strAB in each strain. These three genes were transferable to Xanthomonas perforans via conjugation, and they were PCR confirmed in all seven OTCR Xap strains. When tetC and tetR were cloned and expressed together in a sensitive strain, the transconjugants showed resistance to ≤100 μg/mL OTC. When tetC was cloned and expressed alone in a sensitive strain, the transconjugants showed resistance to ≤250 μg/mL OTC. TetC and tetR expression was inducible by OTC in all six wild-type strains resistant to ≤100 μg/mL OTC. However, in the R1 strain resistant to ≤250 μg/mL OTC, tetR was not expressed, possibly due to the presence of Tn3 in the tetR gene, and in this case tetC was constitutively expressed. These data suggest that tetC confers OTC resistance in Xap strains, and tetR regulates the level of OTC resistance conferred by tetC. To our knowledge, this is the first report of OTC resistance in plant pathogenic xanthomonads.

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“…The gene coding this protein is in the same genomic region as hppA , a proton pump that utilizes the energy of pyrophosphate hydrolysis as the driving force for proton movement across the membrane to generate a proton motive force. AKJ12_07680 is homologous to the lipoprotein ElpS, a protein involved in the mobilization of inorganic phosphate [ 53 ]. This protein interacts with T2SS, three TBDR, and GuaA and GuaB from the guaAB operon involved in purine salvage pathways for synthesis of DNA and RNA from the host environment [ 54 ].…”

Section: Discussionmentioning

confidence: 99%

A Secreted Chorismate Mutase from Xanthomonas arboricola pv. juglandis Attenuates Virulence and Walnut Blight Symptoms

Assis

Sagawa

Zaini

et al. 2021

IJMS

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Walnut blight is a significant above-ground disease of walnuts caused by Xanthomonas arboricola pv. juglandis (Xaj). The secreted form of chorismate mutase (CM), a key enzyme of the shikimate pathway regulating plant immunity, is highly conserved between plant-associated beta and gamma proteobacteria including phytopathogens belonging to the Xanthomonadaceae family. To define its role in walnut blight disease, a dysfunctional mutant of chorismate mutase was created in a copper resistant strain Xaj417 (XajCM). Infections of immature walnut Juglans regia (Jr) fruit with XajCM were hypervirulent compared with infections with the wildtype Xaj417 strain. The in vitro growth rate, size and cellular morphology were similar between the wild-type and XajCM mutant strains, however the quantification of bacterial cells by dPCR within walnut hull tissues showed a 27% increase in XajCM seven days post-infection. To define the mechanism of hypervirulence, proteome analysis was conducted to compare walnut hull tissues inoculated with the wild type to those inoculated with the XajCM mutant strain. Proteome analysis revealed 3296 Jr proteins (five decreased and ten increased with FDR ≤ 0.05) and 676 Xaj417 proteins (235 increased in XajCM with FDR ≤ 0.05). Interestingly, the most abundant protein in Xaj was a polygalacturonase, while in Jr it was a polygalacturonase inhibitor. These results suggest that this secreted chorismate mutase may be an important virulence suppressor gene that regulates Xaj417 virulence response, allowing for improved bacterial survival in the plant tissues.

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Secrete or perish: The role of secretion systems in Xanthomonas biology

Cited by 50 publications

References 352 publications

Complete Genome Assemblies of All Xanthomonas translucens Pathotype Strains Reveal Three Genetically Distinct Clades

Complete Genome Assemblies of All Xanthomonas translucens Pathotype Strains Reveal Three Genetically Distinct Clades

Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach

A Secreted Chorismate Mutase from Xanthomonas arboricola pv. juglandis Attenuates Virulence and Walnut Blight Symptoms

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