How Ralstonia solanacearum Exploits and Thrives in the Flowing Plant Xylem Environment

Lowe‐Power, Tiffany M.; Khokhani, Devanshi; Allen, Caitilyn

doi:10.1016/j.tim.2018.06.002

Cited by 152 publications

(146 citation statements)

References 93 publications

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“…Amino acid fragments reporting on central metabolic pathways identified. The tertiary butyl dimethyl silane (TBDMS)-derivatized protein hydrolysate of cells fed with [ 12 C]glucose, [1-13 C]glucose, [1,[2][3][4][5][6][7][8][9][10][11][12][13] C]glucose, and 40% [ 13 C 6 ]glucose were subjected to GC-MS for accurate analysis of mass isotopomer distribution in amino acids. The total ion chromatogram of protein hydrolysate resulted in 15 amino acids ( Table S2.…”

Section: Resultsmentioning

confidence: 99%

“…Chemicals. The labeling substrates, [1-13 C]glucose (99 atom%), [1,[2][3][4][5][6][7][8][9][10][11][12][13] C]glucose (99 atom%), and [ 13 C 6 ]glucose (99 atom%), were purchased from Sigma-Aldrich. Derivatization agents TBDMS [N-methyl-N-(t-butyldimethylsilyl) trifluoroacetamide plus 1% t-butyl-dimethylchlorosilane] and MSTFA [N-methyl-N-(trimethylsilyl) trifluroacetamide] were also purchased from Sigma-Aldrich.…”

Section: Methodsmentioning

confidence: 99%

“…IMPORTANCE Understanding the metabolic versatility of Ralstonia solanacearum is important, as it regulates the trade-off between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on the potential roles of glycolysis and the oxidative pentose phosphate pathway (OxPPP) in R. solanacearum (3,4). This work provided evidence from 13 C stable isotope feeding and genome annotation-based comparative metabolic network analysis that the Entner-Doudoroff pathway and non-OxPPP bypass glycolysis and OxPPP during the oxidation of glucose, a component of the host xylem pool that serves as a potential carbon source (5).…”

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confidence: 99%

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The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

et al. 2020

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In Ralstonia solanacearum, a devastating phytopathogen whose metabolism is poorly understood, we observed that the Entner-Doudoroff (ED) pathway and nonoxidative pentose phosphate pathway (non-OxPPP) bypass glycolysis and OxPPP under glucose oxidation. Evidence derived from 13 C stable isotope feeding and genome annotation-based comparative metabolic network analysis supported the observations. Comparative metabolic network analysis derived from the currently available 53 annotated R. solanacearum strains, including a recently reported strain (F1C1), representing the four phylotypes, confirmed the lack of key genes coding for phosphofructokinase (pfk-1) and phosphogluconate dehydrogenase (gnd) enzymes that are relevant for glycolysis and OxPPP, respectively. R. solanacearum F1C1 cells fed with [ 13 C]glucose (99% [1-13 C]glucose or 99% [1,2-13 C]glucose or 40% [ 13 C 6 ]glucose) followed by gas chromatography-mass spectrometry (GC-MS)-based labeling analysis of fragments from amino acids, glycerol, and ribose provided clear evidence that rather than glycolysis and the OxPPP, the ED pathway and non-OxPPP are the main routes sustaining metabolism in R. solanacearum. The 13 C incorporation in the mass ions of alanine (m/z 260 and m/z 232), valine (m/z 288 and m/z 260), glycine (m/z 218), serine (m/z 390 and m/z 362), histidine (m/z 440 and m/z 412), tyrosine (m/z 466 and m/z 438), phenylalanine (m/z 336 and m/z 308), glycerol (m/z 377), and ribose (m/z 160) mapped the pathways supporting the observations. The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13 C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. IMPORTANCE Understanding the metabolic versatility of Ralstonia solanacearum is important, as it regulates the trade-off between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on the potential roles of glycolysis and the oxidative pentose phosphate pathway (OxPPP) in R. solanacearum (3,4). This work provided evidence from 13 C stable isotope feeding and genome annotation-based comparative metabolic network analysis that the Entner-Doudoroff pathway and non-OxPPP bypass glycolysis and OxPPP during the oxidation of glucose, a component of the host xylem pool that serves as a potential carbon source (5). The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13 C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. The study highlights the need to critically examine phytopathogens whose metabolism is poorly understood. on July 10, 2020 by guest http://msystems.asm.org/ Downloaded from R alstonia solanacearum is one of the most destructive plant pathogens as it infects over 450 plant species (6-8), and its metabolism is poorly understood. It is a soilborne pathogen that enters plan...

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

et al. 2020

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“…Understanding the metabolic versatility of Ralstonia solanacearum is important as it regulates the tradeoff between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on potential roles of Glycolysis and Oxidative pentose phosphate pathways (OxPPP) in R. solanacearum (3, 4). This work provided evidence from 13 C stable isotopes feeding and genome annotation based comparative metabolic network analysis that Entner-Doudoroff pathway and Non-OxPPP bypasses glycolysis and OxPPP during the oxidation of Glucose, one of the host xylem pool that serves as a potential carbon source (5).…”

Section: Importancementioning

confidence: 99%

Entner–Doudoroff pathway and Non-OxPPP bypasses glycolysis and OxPPP inRalstonia solanacearum

Jyoti

Shree

Joshi

et al. 2020

Preprint

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In Ralstonia solanacearum, a devastating phytopathogen whose metabolism 13 is poorly understood, we observed that Entner-Doudoroff (ED) pathway and Oxidative pentose phosphate pathway (OxPPP) bypasses glycolysis and OxPPP under 15 glucose oxidation. Evidences derived from 13 C stable isotopes feeding and genome 16 annotation based comparative metabolic network analysis supported the observations. 17 Comparative metabolic network analysis derived from the currently available 53 18 annotated R. solanacearum strains also including the recently reported strain (F1C1), 19 representing the four phylotypes confirmed the lack of key genes coding for 20 phosphofructokinase (pfk-1) and phosphogluconate dehydrogenase (gnd) enzymes that 21 are relevant for glycolysis and OxPPP respectively. R. solanacearum F1C1 cells fed 22 with 13 C Glucose (99%[1-13 C]-or 99%[1,2-13 C]-or 40%[ 13 C 6 ]-glucose) followed by GC- 23MS based labelling analysis of fragments from amino acids, glycerol and ribose 24 provided clear evidence that rather than Glycolysis and OxPPP, ED pathway and Non-25 OxPPP are the main routes sustaining metabolism in R. solanacearum. The 13 C 26 incorporation in the mass ions of alanine (m/z 260, m/z 232); valine (m/z 288, m/z 260), 27 glycine (m/z 218), serine (m/z 390, m/z 362), histidine (m/z 440, m/z 412), tyrosine (m/z 28 466, m/z 438), phenylalanine (m/z 336, m/z 308), glycerol (m/z 377) and ribose (m/z 29 160) mapped the pathways supporting the observations. The outcomes help better 30 defining the central carbon metabolic network of R. solanacearum that can be 31 integrated with 13 C metabolic flux analysis as well as flux balance analysis studies for 32 defining the metabolic phenotypes. 33 Importance: Understanding the metabolic versatility of Ralstonia solanacearum is 37 important as it regulates the tradeoff between virulence and metabolism (1, 2) in a wide 38 range of plant hosts. Due to a lack of clear evidence until this work, several published 39 research papers reported on potential roles of Glycolysis and Oxidative pentose 40 phosphate pathways (OxPPP) in R. solanacearum (3, 4). This work provided evidence 41 from 13 C stable isotopes feeding and genome annotation based comparative metabolic 42 network analysis that Entner-Doudoroff pathway and Non-OxPPP bypasses glycolysis 43 and OxPPP during the oxidation of Glucose, one of the host xylem pool that serves as a 44 potential carbon source (5). The outcomes help better defining the central carbon 45 metabolic network of R. solanacearum that can be integrated with 13 C metabolic flux 46 analysis as well as flux balance analysis studies for defining the metabolic phenotypes.47The study highlights the need to critically examine phytopathogens whose metabolism 48 is poorly understood. 50Introduction: Ralstonia solanacearum is one of the most destructive plant pathogen as 51 it infects over 450 plant species (6-8) and its metabolism is poorly understood. It is a 52 soil borne pathogen that enters the plants through natural openings or wounds,...

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“…Unsurprisingly ΔphcA, a global regulator mutant, is avirulent (Khokhani et. al., 2017, Lowe-Power et. al., 2018b.…”

Section: Rs Myo-inositol Consumption Is Required For Root Colonizationmentioning

confidence: 99%

Ralstonia solanacearumdepends on catabolism of myo-inositol, sucrose, and trehalose for virulence in an infection stage-dependent manner

Hamilton

Steidl

MacIntyre

et al. 2019

Preprint

Self Cite

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The soilborne pathogen Ralstonia solanacearum (Rs) causes lethal bacterial wilt disease of tomato and many other crops by infecting host roots and then colonizing the xylem vessels. Tomato xylem sap is nutritionally limiting but it does contain sucrose and trehalose. Transcriptomic analyses revealed that Rs expresses distinct sets of catabolic pathways at low cell density (LCD) and high cell density (HCD). To investigate the links between bacterial catabolism, infection stage, and virulence, we measured the in planta fitness of bacterial mutants lacking carbon catabolic pathways expressed at either LCD or HCD. We hypothesized that the bacterium needs LCD carbon sources early in disease (root infection) while HCD carbon sources are required during late disease (stem colonization). An Rs ΔiolG mutant unable to use the LCD nutrient myo-inositol was defective in root colonization but once it reached the stem, this strain colonized and caused symptoms as well as wild type. In contrast, Rs mutants unable to use sucrose (ΔscrA), trehalose (ΔtreA), or both (∆scrA/treA), infected roots as well as wild type but were defective in colonization and competitive fitness in tomato mid-stems and were reduced in bacterial wilt virulence. Additionally, xylem sap from tomato plants colonized by ΔscrA, ΔtreA, or ΔscrA/treA contained more sucrose than sap from plants colonized by wild-type Rs. Together, these findings suggest Rs metabolism is specifically adapted for success in the different nutritional environments of plant roots and xylem sap.

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How Ralstonia solanacearum Exploits and Thrives in the Flowing Plant Xylem Environment

Cited by 152 publications

References 93 publications

The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

Entner–Doudoroff pathway and Non-OxPPP bypasses glycolysis and OxPPP inRalstonia solanacearum

Ralstonia solanacearumdepends on catabolism of myo-inositol, sucrose, and trehalose for virulence in an infection stage-dependent manner

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