Ralstonia solanacearum Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment

Dalsing, Beth L.; Truchon, Alicia N.; Gonzalez-Orta, Enid T.; Milling, Annett; Allen, Caitilyn

doi:10.1128/mbio.02471-14

Cited by 77 publications

(142 citation statements)

References 69 publications

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“…In E. coli , these subunits are involved in electron transport only when oxygen is very limited in the environment (Miller & Gennis, 1983; Anraku & Gennis, 1987). This suggests the corn xylem and/or bacterial biofilm is an oxygen-limited environment for the bacteria, which supports previous conclusions from studies performed with other vascular pathogens (Pegg, 1985; Dalsing et al., 2015). …”

Section: Discussionsupporting

confidence: 90%

Analysis of thein plantatranscriptome expressed by the corn pathogenPantoea stewartiisubsp.stewartiivia RNA-Seq

Packard

Burke

Jensen

et al. 2017

PeerJ

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Pantoea stewartii subsp. stewartii is a bacterial phytopathogen that causes Stewart’s wilt disease in corn. It uses quorum sensing to regulate expression of some genes involved in virulence in a cell density-dependent manner as the bacterial population grows from small numbers at the initial infection site in the leaf apoplast to high cell numbers in the xylem where it forms a biofilm. There are also other genes important for pathogenesis not under quorum-sensing control such as a Type III secretion system. The purpose of this study was to compare gene expression during an in planta infection versus either a pre-inoculum in vitro liquid culture or an in vitro agar plate culture to identify genes specifically expressed in planta that may also be important for colonization and/or virulence. RNA was purified from each sample type to determine the transcriptome via RNA-Seq using Illumina sequencing of cDNA. Fold gene expression changes in the in planta data set in comparison to the two in vitro grown samples were determined and a list of the most differentially expressed genes was generated to elucidate genes important for plant association. Quantitative reverse transcription PCR (qRT-PCR) was used to validate expression patterns for a select subset of genes. Analysis of the transcriptome data via gene ontology revealed that bacterial transporters and systems important for oxidation reduction processes appear to play a critical role for P. stewartii as it colonizes and causes wilt disease in corn plants.

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Section: Discussionsupporting

confidence: 90%

Analysis of thein plantatranscriptome expressed by the corn pathogenPantoea stewartiisubsp.stewartiivia RNA-Seq

Packard

Burke

Jensen

et al. 2017

PeerJ

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“…Tomato xylem sap contains ∼ 1 mM total amino acids and 40 mM nitrate (Dixon and Pegg, ; Zuluaga et al ., ; Dalsing et al ., ). In the oxygen‐limited xylem, R. solanacearum uses nitrate primarily as an alternate electron acceptor (Dalsing et al ., ). Our study suggests the key nitrogen sources fueling bacterial growth in the xylem are alanine, β‐alanine, glycine and proline.…”

Section: Discussionmentioning

confidence: 97%

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Lowe‐Power

Hendrich

Roepenack‐Lahaye

et al. 2017

Environmental Microbiology

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127

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Ralstonia solanacearum thrives in plant xylem vessels and causes bacterial wilt disease despite the low nutrient content of xylem sap. We found that R. solanacearum manipulates its host to increase nutrients in tomato xylem sap, enabling it to grow better in sap from infected plants than in sap from healthy plants. Untargeted GC/MS metabolomics identified 22 metabolites enriched in R. solanacearum-infected sap. Eight of these could serve as sole carbon or nitrogen sources for R. solanacearum. Putrescine, a polyamine that is not a sole carbon or nitrogen source for R. solanacearum, was enriched 76-fold to 37 µM in R. solanacearum-infected sap. R. solanacearum synthesized putrescine via a SpeC ornithine decarboxylase. A ΔspeC mutant required ≥ 15 µM exogenous putrescine to grow and could not grow alone in xylem even when plants were treated with putrescine. However, co-inoculation with wildtype rescued ΔspeC growth, indicating R. solanacearum produced and exported putrescine to xylem sap. Intriguingly, treating plants with putrescine before inoculation accelerated wilt symptom development and R. solanacearum growth and systemic spread. Xylem putrescine concentration was unchanged in putrescine-treated plants, so the exogenous putrescine likely accelerated disease indirectly by affecting host physiology. These results indicate that putrescine is a pathogen-produced virulence metabolite.

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“…Perhaps, plant root tissues also contribute to NO production (and to NO reduction as well) (29). Likewise, bradyrhizobial genes other than nirK and norB may contribute to NO production and detoxification in the oxygen-limited host environment (30,31).…”

Section: Discussionmentioning

confidence: 99%

Potential of Rice Stubble as a Reservoir of Bradyrhizobial Inoculum in Rice-Legume Crop Rotation

Piromyou

Greetatorn

Teamtisong

et al. 2017

Appl Environ Microbiol

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Bradyrhizobium encompasses a variety of bacteria that can live in symbiotic and endophytic associations with leguminous and nonleguminous plants, such as rice. Therefore, it can be expected that rice endophytic bradyrhizobia can be applied in the rice-legume crop rotation system. Some endophytic bradyrhizobial strains were isolated from rice (Oryza sativa L.) tissues. The rice biomass could be enhanced when supplementing bradyrhizobial strain inoculation with KNO 3 , NH 4 NO 3 , or urea, especially in Bradyrhizobium sp. strain SUTN9-2. In contrast, the strains which suppressed rice growth were photosynthetic bradyrhizobia and were found to produce nitric oxide (NO) in the rice root. The expression of genes involved in NO production was conducted using a quantitative reverse transcription-PCR (qRT-PCR) technique. The nirK gene expression level in Bradyrhizobium sp. strain SUT-PR48 with nitrate was higher than that of the norB gene. In contrast, the inoculation of SUTN9-2 resulted in a lower expression of the nirK gene than that of the norB gene. These results suggest that SUT-PR48 may accumulate NO more than SUTN9-2 does. Furthermore, the nifH expression of SUTN9-2 was induced in treatment without nitrogen supplementation in an endophytic association with rice. The indole-3-acetic acid (IAA) and 1-amino-cyclopropane-1-carboxylic acid (ACC) deaminase produced in planta by SUTN9-2 were also detected. Enumeration of rice endophytic bradyrhizobia from rice tissues revealed that SUTN9-2 persisted in rice tissues until rice-harvesting season. The mung bean (Vigna radiata) can be nodulated after rice stubbles were decomposed. Therefore, it is possible that rice stubbles can be used as an inoculum in the rice-legume crop rotation system under both low-and high-organic-matter soil conditions.IMPORTANCE This study shows that some rice endophytic bradyrhizobia could produce IAA and ACC deaminase and have a nitrogen fixation ability during symbiosis inside rice tissues. These characteristics may play an important role in rice growth promotion by endophytic bradyrhizobia. However, the NO-producing strains should be of concern due to a possible deleterious effect of NO on rice growth. In addition, this study reports the application of endophytic bradyrhizobia in rice stubbles, and the rice stubbles were used directly as an inoculum for a leguminous plant (mung bean). The degradation of rice stubbles leads to an increased number of SUTN9-2 in the soil and may result in increased mung bean nodulation. Therefore, the persistence of endophytic bradyrhizobia in rice tissues can be developed to use rice stubbles as an inoculum for mung bean in a ricelegume crop rotation system. KEYWORDS rice endophytic bradyrhizobia, mung bean, rice-legume crop rotation

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Ralstonia solanacearum Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment

Cited by 77 publications

References 69 publications

Analysis of thein plantatranscriptome expressed by the corn pathogenPantoea stewartiisubsp.stewartiivia RNA-Seq

Analysis of thein plantatranscriptome expressed by the corn pathogenPantoea stewartiisubsp.stewartiivia RNA-Seq

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Potential of Rice Stubble as a Reservoir of Bradyrhizobial Inoculum in Rice-Legume Crop Rotation

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