A <i>Bacillus subtilis</i> sensor kinase involved in triggering biofilm formation on the roots of tomato plants

Chen, Yun; Cao, Shugeng; Chai, Yunrong; Clardy, Jon; Kolter, Roberto; Guo, Jianhua; Losick, Richard

doi:10.1111/j.1365-2958.2012.08109.x

Cited by 211 publications

(192 citation statements)

References 52 publications

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“…The authors further demonstrated that infection of Arabidopsis leaves up-regulated root ALUMINUM-ACTIVATED MALATE TRANSPORTER1 (ALMT1). These findings were further validated by Chen et al (2012), wherein exudates of tomato roots strongly stimulated B. subtilis biofilm formation ex planta and that an abundant small molecule in the exudates, L-MA, was able to stimulate biofilm formation at high concentrations in a manner that was dependent on the KinD CACHE domain.…”

supporting

confidence: 53%

“…Among these PGPR strains, FB17 rhizoinoculated onto the roots of Arabidopsis plants reduced disease severity, thus inhibiting the proliferation of foliar pathogen Pst DC3000 through induction of JA/ET-mediated ISR and SAmediated SAR (Rudrappa et al, 2010). The magnitude of colonization on the root by beneficial microbes is limited by several factors that include root surface biochemistry and composition of root exudates (Rudrappa et al, 2008a;Doornbos et al, 2011;Chen et al, 2012). It has been speculated that components of root exudates may play a critical role in establishing a beneficial microbiome in the rhizosphere (Lugtenberg et al, 1999;Bais et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

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Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

et al. 2012

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This study demonstrated that foliar infection by Pseudomonas syringae pv tomato DC3000 induced malic acid (MA) transporter (ALUMINUM-ACTIVATED MALATE TRANSPORTER1 [ALMT1]) expression leading to increased MA titers in the rhizosphere of Arabidopsis (Arabidopsis thaliana). MA secretion in the rhizosphere increased beneficial rhizobacteria Bacillus subtilis FB17 (hereafter FB17) titers causing an induced systemic resistance response in plants against P. syringae pv tomato DC3000. Having shown that a live pathogen could induce an intraplant signal from shoot-to-root to recruit FB17 belowground, we hypothesized that pathogen-derived microbe-associated molecular patterns (MAMPs) may relay a similar response specific to FB17 recruitment. The involvement of MAMPs in triggering plant innate immune response is well studied in the plant's response against foliar pathogens. In contrast, MAMPs-elicited plant responses on the roots and the belowground microbial community are not well understood. It is known that pathogen-derived MAMPs suppress the root immune responses, which may facilitate pathogenicity. Plants subjected to known MAMPs such as a flagellar peptide, flagellin22 (flg22), and a pathogen-derived phytotoxin, coronatine (COR), induced a shoot-to-root signal regulating ALMT1 for recruitment of FB17. Micrografts using either a COR-insensitive mutant (coi1) or a flagellin-insensitive mutant (fls2) as the scion and ALMT1 pro :b-glucuronidase as the rootstock revealed that both COR and flg22 are required for a graft transmissible signal to recruit FB17 belowground. The data suggest that MAMPs-induced signaling to regulate ALMT1 is salicylic acid and JASMONIC ACID RESISTANT1 (JAR1)/JASMONATE INSENSITIVE1 (JIN1)/MYC2 independent. Interestingly, a cell culture filtrate of FB17 suppressed flg22-induced MAMPsactivated root defense responses, which are similar to suppression of COR-mediated MAMPs-activated root defense, revealing a diffusible bacterial component that may regulate plant immune responses. Further analysis showed that the biofilm formation in B. subtilis negates suppression of MAMPs-activated defense responses in roots. Moreover, B. subtilis suppression of MAMPs-activated root defense does require JAR1/JIN1/MYC2. The ability of FB17 to block the MAMPselicited signaling pathways related to antibiosis reflects a strategy adapted by FB17 for efficient root colonization. These experiments demonstrate a remarkable strategy adapted by beneficial rhizobacteria to suppress a host defense response, which may facilitate rhizobacterial colonization and host-mutualistic association.

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supporting

confidence: 53%

Section: Discussionmentioning

confidence: 99%

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

et al. 2012

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“…While this manuscript was in preparation, a study was published that explored the developmental response of B. subtilis to the presence of tomato roots. 35 The authors found that a developmental phenomenon regulated by the sporulation phosphorelay, namely biofilm formation, could be induced by the presence of tomato roots and that this phenomenon was dependent on KinD. They identified malate to be at least partially responsible for induction of biofilm formation mediated by KinD.…”

Section: Is Pyruvate the Physiological Ligand Of Kind?mentioning

confidence: 97%

Insight into the sporulation phosphorelay: Crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD

Wilton

et al. 2013

Protein Science

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The Bacillus subtilis KinD signal-transducing histidine kinase is a part of the sporulation phosphorelay known to regulate important developmental decisions such as sporulation and biofilm formation. We have determined crystal structures of the extracytoplasmic sensing domain of KinD, which was copurified and crystallized with a pyruvate ligand. The structure of a ligandbinding site mutant was also determined; it was copurified and crystallized with an acetate ligand. The structure of the KinD extracytoplasmic segment is similar to that of several other sensing domains of signal transduction proteins and is composed of tandem Per-Arnt-Sim (PAS)-like domains. The KinD ligand-binding site is located on the membrane distal PAS-like domain and appears to be highly selective; a single mutation, R131A, abolishes pyruvate binding and the mutant binds acetate instead. Differential scanning fluorimetry, using a variety of monocarboxylic and dicarboxylic acids, identified pyruvate, propionate, and butyrate but not lactate, acetate, or malate as KinD ligands. A recent report found that malate induces biofilm formation in a KinDdependent manner. It was suggested that malate might induce a metabolic shift and increased secretion of the KinD ligand of unknown identity. The structure and binding assays now suggests that this ligand is pyruvate and/or other small monocarboxylic acids. In summary, this study gives a first insight into the identity of a molecular ligand for one of the five phosphorelay kinases of B. subtilis.

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“…Bacillus sp. was also used as model to study the biological activity of mixed ligand complexes of transition metal with 8-quinolinols and 5-alkoxumethyl-8-quinolinol (Patel et al 2012) and as bio-control agent to protect plants from a variety of pathogens (Chen et al 2012). In this work, B. subtilis 1556WTNC was isolated from treated sewage effluents, exhibited good growth (<5 log 10 CFU mL −1 ), β-lactamase activity, biodegradation of cephalexin and biomass yield in treated sewage effluents, and was resistant against cefuroxime, cephalexin, ampicillin and amoxicillin.…”

Section: Discussionmentioning

confidence: 99%

Biodegradation of Pharmaceutical Wastes in Treated Sewage Effluents by Bacillus subtilis 1556WTNC

Al-Gheethi¹,

Ismail²

2014

Environ. Process.

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The aim of this study was to investigate the potentials for enzymatic biodegradation of pharmaceutical active compounds (β-lactam antibiotics) in treated sewage effluents as a function of β-lactamase produced Bacillus subtilis 1556WTNC. Four β-lactams antibiotics were selected: two of them belong to penicillin's (amoxicillin and ampicillin) and two belong to cephalosporins (cephalexin and cefuroxime); ciprofloxacin (belongs to quinolones) was used as a negative control. The enzymatic biodegradation process was conducted under the optimal conditions for β-lactams production (5.9 log 10 CFU mL −1 ; pH 6.5; temperature 35°C for 12 days) as determined in this research. The maximum biodegradation was 25.03 % at 1 mg mL −1 for amoxicillin, 15.59 % at 0.8 mg mL −1 of ampicillin, 22.59 % at 1 mg mL −1 of cephalexin, 10.62 % at 1 mg mL −1 of cefuroxime, while it was 2.45 % at 0.6 mg mL −1 of ciprofloxacin. B. subtilis 1556WTNC exhibited the potential to produce β-lactamase and biodegrade β-lactam antibiotic genetically and inducibly B. subtilis 1556WTNC could grow and biodegrade β-lactam antibiotics in conditions similar to the characteristics of treated sewage effluents such as pH, temperature, and during short time (12 days), because it was already acclimatized to those conditions. For this reason, treated sewage effluents were used as source to isolate this strain. It can be concluded that B. subtilis 1556WTNC is suitable to remove pharmaceutical residues from the treated sewage effluents and produce effluents at higher quality than that achieved by secondary treatment process.

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A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants

Cited by 211 publications

References 52 publications

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

Insight into the sporulation phosphorelay: Crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD

Biodegradation of Pharmaceutical Wastes in Treated Sewage Effluents by Bacillus subtilis 1556WTNC

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