DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment

Abstract

The bacterial microbiota of plants is diverse, with ~1000s of operational taxonomic units (OTUs) associated with any individual plant. In this work we investigate how 19 sequenced Pseudomonas fluorescens strains representing a single OTU isolated from Populus deltoides rhizosphere and endosphere differ using phenotypic analysis, comparative genomics, and metabolic models. While no traits were exclusive to either endosphere or rhizosphere P. fluorescens isolates, multiple pathways relevant for bacterial-plant interactions are enriched in endosphere isolate genomes and growth phenotypes such as phosphate solubilization, protease activity, denitrification and root growth promotion are biased towards endosphere isolates. Endosphere isolates have more metabolic pathways for plant signaling compounds and an increased metabolic range that includes utilization of energy rich nucleotides and sugars, consistent with endosphere colonization. Rhizosphere P. fluorescens have fewer pathways important for bacterial-plant interactions but show metabolic bias towards chemical substrates often found in root exudates. This work reveals the diverse functions that may contribute to colonization of the endosphere by bacteria that are enriched in event he most closely related isolates.

Authors:
 [1];  [2];  [1];  [1];  [3];  [3];  [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Northwest Missouri State Univ., Maryville, MS (United States)
  3. Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1234335
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Timm, Collin M., Campbell, Alicia G., Utturkar, Sagar M., Jun, Se Ran, Parales, Rebecca E., Tan, Mesa, Robeson, Michael S., Lu, Tse-Yuan S., Jawdy, Sara, Schadt, Christopher Warren, Doktycz, Mitchel John, Weston, David, and Pelletier, Dale A. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.01118.
Timm, Collin M., Campbell, Alicia G., Utturkar, Sagar M., Jun, Se Ran, Parales, Rebecca E., Tan, Mesa, Robeson, Michael S., Lu, Tse-Yuan S., Jawdy, Sara, Schadt, Christopher Warren, Doktycz, Mitchel John, Weston, David, & Pelletier, Dale A. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. United States. https://doi.org/10.3389/fmicb.2015.01118
Timm, Collin M., Campbell, Alicia G., Utturkar, Sagar M., Jun, Se Ran, Parales, Rebecca E., Tan, Mesa, Robeson, Michael S., Lu, Tse-Yuan S., Jawdy, Sara, Schadt, Christopher Warren, Doktycz, Mitchel John, Weston, David, and Pelletier, Dale A. Wed . "Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment". United States. https://doi.org/10.3389/fmicb.2015.01118. https://www.osti.gov/servlets/purl/1234335.
@article{osti_1234335,
title = {Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment},
author = {Timm, Collin M. and Campbell, Alicia G. and Utturkar, Sagar M. and Jun, Se Ran and Parales, Rebecca E. and Tan, Mesa and Robeson, Michael S. and Lu, Tse-Yuan S. and Jawdy, Sara and Schadt, Christopher Warren and Doktycz, Mitchel John and Weston, David and Pelletier, Dale A.},
abstractNote = {The bacterial microbiota of plants is diverse, with ~1000s of operational taxonomic units (OTUs) associated with any individual plant. In this work we investigate how 19 sequenced Pseudomonas fluorescens strains representing a single OTU isolated from Populus deltoides rhizosphere and endosphere differ using phenotypic analysis, comparative genomics, and metabolic models. While no traits were exclusive to either endosphere or rhizosphere P. fluorescens isolates, multiple pathways relevant for bacterial-plant interactions are enriched in endosphere isolate genomes and growth phenotypes such as phosphate solubilization, protease activity, denitrification and root growth promotion are biased towards endosphere isolates. Endosphere isolates have more metabolic pathways for plant signaling compounds and an increased metabolic range that includes utilization of energy rich nucleotides and sugars, consistent with endosphere colonization. Rhizosphere P. fluorescens have fewer pathways important for bacterial-plant interactions but show metabolic bias towards chemical substrates often found in root exudates. This work reveals the diverse functions that may contribute to colonization of the endosphere by bacteria that are enriched in event he most closely related isolates.},
doi = {10.3389/fmicb.2015.01118},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Wed Oct 14 00:00:00 EDT 2015},
month = {Wed Oct 14 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 40 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Bacterial volatiles promote growth in Arabidopsis
journal, April 2003

  • Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
  • DOI: 10.1073/pnas.0730845100

Extreme genome reduction in symbiotic bacteria
journal, November 2011

  • McCutcheon, John P.; Moran, Nancy A.
  • Nature Reviews Microbiology, Vol. 10, Issue 1
  • DOI: 10.1038/nrmicro2670

Genomics of Secondary Metabolism in Populus : Interactions with Biotic and Abiotic Environments
journal, October 2009

  • Chen, Feng; Liu, Chang-Jun; Tschaplinski, Timothy J.
  • Critical Reviews in Plant Sciences, Vol. 28, Issue 5
  • DOI: 10.1080/07352680903241279

Is l-arabinose important for the endophytic lifestyle of Pseudomonas spp.?
journal, September 2012

  • Malfanova, Natalia; Kamilova, Faina; Validov, Shamil
  • Archives of Microbiology, Vol. 195, Issue 1
  • DOI: 10.1007/s00203-012-0842-x

Iron acquisition and its control in pseudomonas aeruginosa many roads lead to rome
journal, January 2003

  • Poole, Keith
  • Frontiers in Bioscience, Vol. 8, Issue 4
  • DOI: 10.2741/1051

Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, December 2010

  • Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
  • Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1
  • DOI: 10.1002/jpln.201000085

Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Aerobic degradation of aromatic compounds
journal, June 2013

  • Díaz, Eduardo; Jiménez, José Ignacio; Nogales, Juan
  • Current Opinion in Biotechnology, Vol. 24, Issue 3
  • DOI: 10.1016/j.copbio.2012.10.010

Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture
journal, April 2011

  • Pérez-García, Alejandro; Romero, Diego; de Vicente, Antonio
  • Current Opinion in Biotechnology, Vol. 22, Issue 2
  • DOI: 10.1016/j.copbio.2010.12.003

Modeling Phosphorus Uptake by a Growing and Exuding Root System
journal, January 2012

  • Schnepf, A.; Leitner, D.; Klepsch, S.
  • Vadose Zone Journal, Vol. 11, Issue 3
  • DOI: 10.2136/vzj2012.0001

The Aerobic Pseudomonads a Taxonomic Study
journal, May 1966

  • Stanier, R. Y.; Palleroni, N. J.; Doudoroff, M.
  • Journal of General Microbiology, Vol. 43, Issue 2
  • DOI: 10.1099/00221287-43-2-159

Plant growth promoting activities of phosphate-solubilizing Enterobacter asburiae as influenced by fungicides
journal, January 2010


Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age
journal, October 2004

  • Dechassa, Nigussie; Schenk, Manfred K.
  • Journal of Plant Nutrition and Soil Science, Vol. 167, Issue 5
  • DOI: 10.1002/jpln.200420424

What lies beneath: belowground defense strategies in plants
journal, February 2015


Pseudomonas fluorescens Induces Strain-Dependent and Strain-Independent Host Plant Responses in Defense Networks, Primary Metabolism, Photosynthesis, and Fitness
journal, June 2012

  • Weston, David J.; Pelletier, Dale A.; Morrell-Falvey, Jennifer L.
  • Molecular Plant-Microbe Interactions, Vol. 25, Issue 6
  • DOI: 10.1094/MPMI-09-11-0253

Soil properties are key determinants for the development of exudate gradients in a rhizosphere simulation model
journal, February 2010


Metabolic Activity and Phosphate-Dissolving Capability of Bacterial Isolates from Wheat Roots, Rhizosphere, and Non-Rhizosphere soil
journal, February 1959

  • Katznelson, H.; Bose, B.
  • Canadian Journal of Microbiology, Vol. 5, Issue 1
  • DOI: 10.1139/m59-010

Bacteria and fungi controlling plant growth by manipulating auxin: Balance between development and defense
journal, January 2015


Short-term physiological and developmental responses to nitrogen availability in hybrid poplar
journal, April 2005


Genome-scale metabolic reconstructions of multiple Escherichia coli strains highlight strain-specific adaptations to nutritional environments
journal, November 2013

  • Monk, J. M.; Charusanti, P.; Aziz, R. K.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
  • DOI: 10.1073/pnas.1307797110

Plant hormone cross-talk: the pivot of root growth
journal, January 2015

  • Pacifici, Elena; Polverari, Laura; Sabatini, Sabrina
  • Journal of Experimental Botany, Vol. 66, Issue 4
  • DOI: 10.1093/jxb/eru534

The Bacterial Oxidation of Tryptophan: A Study in Comparative Biochemistry
journal, September 1951


Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization
journal, May 2010


Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
journal, January 2009

  • Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.
  • Genome Biology, Vol. 10, Issue 5
  • DOI: 10.1186/gb-2009-10-5-r51

Phosphate solubilization by Rhizobium strains
journal, March 2009


Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

Analysis of the plant growth-promoting properties encoded by the genome of the rhizobacterium Pseudomonas putida  BIRD-1 : PGPR properties
journal, December 2012

  • Roca, Amalia; Pizarro-Tobías, Paloma; Udaondo, Zulema
  • Environmental Microbiology, Vol. 15, Issue 3
  • DOI: 10.1111/1462-2920.12037

Linking Plant Nutritional Status to Plant-Microbe Interactions
journal, July 2013


Genome Survey and Characterization of Endophytic Bacteria Exhibiting a Beneficial Effect on Growth and Development of Poplar Trees
journal, December 2008

  • Taghavi, S.; Garafola, C.; Monchy, S.
  • Applied and Environmental Microbiology, Vol. 75, Issue 3
  • DOI: 10.1128/AEM.02239-08

Functional analyses of genes involved in the metabolism of ferulic acid in Pseudomonas putida KT2440
journal, March 2003

  • Plaggenborg, R.; Overhage, J.; Steinbüchel, A.
  • Applied Microbiology and Biotechnology, Vol. 61, Issue 5-6
  • DOI: 10.1007/s00253-003-1260-4

Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440
journal, December 2002


Modelling root–soil interactions using three–dimensional models of root growth, architecture and function
journal, June 2013

  • Dunbabin, Vanessa M.; Postma, Johannes A.; Schnepf, Andrea
  • Plant and Soil, Vol. 372, Issue 1-2
  • DOI: 10.1007/s11104-013-1769-y

Microbial metabolism of pyridine, quinoline, acridine, and their derivatives under aerobic and anaerobic conditions.
journal, January 1996


The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006


Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria
journal, September 1991

  • Alexander, D. B.; Zuberer, D. A.
  • Biology and Fertility of Soils, Vol. 12, Issue 1
  • DOI: 10.1007/BF00369386

Interactions between proteolytic and non-proteolytic Pseudomonas fluorescens affect protein degradation in a model community
journal, April 2000


Bacterial degradation of pyridine, indole, quinoline, and their derivatives under different redox conditions
journal, March 1998


The Effect of Phylogenetically Different Bacteria on the Fitness of Pseudomonas fluorescens in Sand Microcosms
journal, March 2015


Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase
journal, October 2005


Physiology and Molecular Biology of Phenylpropanoid Metabolism
journal, June 1989


Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator
journal, June 2008

  • Calisti, C.; Ficca, A. G.; Barghini, P.
  • Applied Microbiology and Biotechnology, Vol. 80, Issue 3
  • DOI: 10.1007/s00253-008-1557-4

Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440
journal, December 2002


Phenol biosynthesis in higher plants. Gallic acid
journal, July 1969

  • Dewick, P. M.; Haslam, E.
  • Biochemical Journal, Vol. 113, Issue 3
  • DOI: 10.1042/bj1130537

The role of auxin in shaping shoot architecture
journal, May 2013

  • Gallavotti, Andrea
  • Journal of Experimental Botany, Vol. 64, Issue 9
  • DOI: 10.1093/jxb/ert141

Molecular characterization of genes of Pseudomonas sp. strain HR199 involved in bioconversion of vanillin to protocatechuate.
journal, April 1997


Linking Plant Nutritional Status to Plant-Microbe Interactions
journal, July 2013


Recent advances and emerging trends in plant hormone signalling
journal, June 2009


p-Cymene pathway in Pseudomonas putida: ring cleavage of 2,3-dihydroxy-p-cumate and subsequent reactions.
journal, January 1977


Evaluation and validation of de novo and hybrid assembly techniques to derive high-quality genome sequences
journal, June 2014


MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012

  • Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
  • Systematic Biology, Vol. 61, Issue 3
  • DOI: 10.1093/sysbio/sys029

Structure and Evolution of Streptomyces Interaction Networks in Soil and In Silico
journal, October 2011


Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture
journal, April 2011

  • Pérez-García, Alejandro; Romero, Diego; de Vicente, Antonio
  • Current Opinion in Biotechnology, Vol. 22, Issue 2
  • DOI: 10.1016/j.copbio.2010.12.003

Markers and signals associated with nitrogen assimilation in higher plants
journal, January 2003

  • Foyer, C. H.; Parry, M.; Noctor, G.
  • Journal of Experimental Botany, Vol. 54, Issue 382
  • DOI: 10.1093/jxb/erg053

Genome-scale metabolic reconstructions of multiple Escherichia coli strains highlight strain-specific adaptations to nutritional environments
journal, November 2013

  • Monk, J. M.; Charusanti, P.; Aziz, R. K.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
  • DOI: 10.1073/pnas.1307797110

Short-term physiological and developmental responses to nitrogen availability in hybrid poplar
journal, April 2005


Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
journal, January 2009

  • Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.
  • Genome Biology, Vol. 10, Issue 5
  • DOI: 10.1186/gb-2009-10-5-r51

Cloning, Sequence, and Expression of Kynureninase fromPseudomonas fluorescens
journal, August 1997

  • Koushik, Srinagesh V.; Sundararaju, Bakthavatsalam; McGraw, Royal A.
  • Archives of Biochemistry and Biophysics, Vol. 344, Issue 2
  • DOI: 10.1006/abbi.1997.0220

Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age
journal, October 2004

  • Dechassa, Nigussie; Schenk, Manfred K.
  • Journal of Plant Nutrition and Soil Science, Vol. 167, Issue 5
  • DOI: 10.1002/jpln.200420424

Phosphate solubilization of Paenibacillus polymyxa and Paenibacillus macerans from mycorrhizal and non-mycorrhizal cucumber plants
journal, June 2012

  • Yanli Wang,
  • African Journal of Microbiology Research, Vol. 6, Issue 21
  • DOI: 10.5897/AJMR12.261

Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica
journal, January 2014

  • Hunter, Paul J.; Teakle, Grahams R.; Bending, Gary D.
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00027

Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013


Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from a forest soil
journal, November 1998

  • Di Simine, C. D.; Sayer, J. A.; Gadd, G. M.
  • Biology and Fertility of Soils, Vol. 28, Issue 1
  • DOI: 10.1007/s003740050467

Bacterial volatiles promote growth in Arabidopsis
journal, April 2003

  • Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
  • DOI: 10.1073/pnas.0730845100

Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants
journal, March 2013


Plant growth promoting activities of phosphate-solubilizing Enterobacter asburiae as influenced by fungicides
journal, January 2010


Functional analyses of genes involved in the metabolism of ferulic acid in Pseudomonas putida KT2440
journal, March 2003

  • Plaggenborg, R.; Overhage, J.; Steinbüchel, A.
  • Applied Microbiology and Biotechnology, Vol. 61, Issue 5-6
  • DOI: 10.1007/s00253-003-1260-4

Relative involvement of nitrate and nitrite reduction in the competitiveness of Pseudomonas fluorescens in the rhizosphere of maize under non-limiting nitrate conditions
journal, February 2002


Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, December 2010

  • Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
  • Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1
  • DOI: 10.1002/jpln.201000085

Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization
journal, May 2010


Degradation of 2,3-Dihydroxybenzoate by a Novel meta-Cleavage Pathway
journal, May 2012

  • Marin, M.; Plumeier, I.; Pieper, D. H.
  • Journal of Bacteriology, Vol. 194, Issue 15
  • DOI: 10.1128/jb.00430-12

Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

Analysis of the plant growth-promoting properties encoded by the genome of the rhizobacterium Pseudomonas putida  BIRD-1 : PGPR properties
journal, December 2012

  • Roca, Amalia; Pizarro-Tobías, Paloma; Udaondo, Zulema
  • Environmental Microbiology, Vol. 15, Issue 3
  • DOI: 10.1111/1462-2920.12037

Extreme genome reduction in symbiotic bacteria
journal, November 2011

  • McCutcheon, John P.; Moran, Nancy A.
  • Nature Reviews Microbiology, Vol. 10, Issue 1
  • DOI: 10.1038/nrmicro2670

Inside the root microbiome: Bacterial root endophytes and plant growth promotion
journal, September 2013

  • Gaiero, Jonathan R.; McCall, Crystal A.; Thompson, Karen A.
  • American Journal of Botany, Vol. 100, Issue 9
  • DOI: 10.3732/ajb.1200572

Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica
journal, January 2014

  • Hunter, Paul J.; Teakle, Grahams R.; Bending, Gary D.
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00027

Phosphate solubilization by Rhizobium strains
journal, March 2009


Metabolic Activity and Phosphate-Dissolving Capability of Bacterial Isolates from Wheat Roots, Rhizosphere, and Non-Rhizosphere soil
journal, February 1959

  • Katznelson, H.; Bose, B.
  • Canadian Journal of Microbiology, Vol. 5, Issue 1
  • DOI: 10.1139/m59-010

Indole-3-acetic acid in microbial and microorganism-plant signaling
journal, July 2007


The Aerobic Pseudomonads a Taxonomic Study
journal, May 1966

  • Stanier, R. Y.; Palleroni, N. J.; Doudoroff, M.
  • Journal of General Microbiology, Vol. 43, Issue 2
  • DOI: 10.1099/00221287-43-2-159

Plant hormone cross-talk: the pivot of root growth
journal, January 2015

  • Pacifici, Elena; Polverari, Laura; Sabatini, Sabrina
  • Journal of Experimental Botany, Vol. 66, Issue 4
  • DOI: 10.1093/jxb/eru534

Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013


Phenol biosynthesis in higher plants. Gallic acid
journal, July 1969

  • Dewick, P. M.; Haslam, E.
  • Biochemical Journal, Vol. 113, Issue 3
  • DOI: 10.1042/bj1130537

Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp.
journal, October 2004


Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids
journal, September 2011


Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Effects of Bacterial ACC Deaminase on Brassica napus Gene Expression
journal, May 2012

  • Stearns, Jennifer C.; Woody, Owen Z.; McConkey, Brendan J.
  • Molecular Plant-Microbe Interactions, Vol. 25, Issue 5
  • DOI: 10.1094/mpmi-08-11-0213

A More Sensitive Plate Assay for Detection of Protease Production by Pseudomonas aeruginosa
journal, April 1979

  • Sokol, Pamela A.; Ohman, Dennis E.; Iglewski, Barbara H.
  • Journal of Clinical Microbiology, Vol. 9, Issue 4
  • DOI: 10.1128/jcm.9.4.538-540.1979

Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil
journal, April 2010


Is l-arabinose important for the endophytic lifestyle of Pseudomonas spp.?
journal, September 2012

  • Malfanova, Natalia; Kamilova, Faina; Validov, Shamil
  • Archives of Microbiology, Vol. 195, Issue 1
  • DOI: 10.1007/s00203-012-0842-x

Physiology and Molecular Biology of Phenylpropanoid Metabolism
journal, June 1989


The β-Ketoadipate Pathway And The Biology Of Self-Identity
journal, October 1996


Modeling Phosphorus Uptake by a Growing and Exuding Root System
journal, January 2012

  • Schnepf, A.; Leitner, D.; Klepsch, S.
  • Vadose Zone Journal, Vol. 11, Issue 3
  • DOI: 10.2136/vzj2012.0001

What lies beneath: belowground defense strategies in plants
journal, February 2015


Plant-driven selection of microbes
journal, November 2008


Biological nitrogen fixation and phosphate solubilization by bacteria isolated from tropical soils
journal, March 2012

  • Marciano Marra, Leandro; Fonsêca Sousa Soares, Cláudio Roberto; de Oliveira, Silvia Maria
  • Plant and Soil, Vol. 357, Issue 1-2
  • DOI: 10.1007/s11104-012-1157-z

A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013


Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens
journal, December 1992


Evaluation and validation of de novo and hybrid assembly techniques to derive high-quality genome sequences
journal, June 2014


The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006


Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase
journal, October 2005


Interactions between proteolytic and non-proteolytic Pseudomonas fluorescens affect protein degradation in a model community
journal, April 2000


Microbial metabolism of pyridine, quinoline, acridine, and their derivatives under aerobic and anaerobic conditions
journal, September 1996


The Effect of Phylogenetically Different Bacteria on the Fitness of Pseudomonas fluorescens in Sand Microcosms
journal, March 2015


Brassica Seed Meal Soil Amendments Transform the Rhizosphere Microbiome and Improve Apple Production Through Resistance to Pathogen Reinfestation
journal, April 2015


A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013


Aerobic tryptophan degradation pathway in bacteria: novel kynurenine formamidase
journal, October 2003


Unravelling the gallic acid degradation pathway in bacteria: the gal cluster from Pseudomonas putida: Aerobic gallic acid degradation
journal, November 2010


Cloning, Sequence, and Expression of Kynureninase fromPseudomonas fluorescens
journal, August 1997

  • Koushik, Srinagesh V.; Sundararaju, Bakthavatsalam; McGraw, Royal A.
  • Archives of Biochemistry and Biophysics, Vol. 344, Issue 2
  • DOI: 10.1006/abbi.1997.0220

Modelling root–soil interactions using three–dimensional models of root growth, architecture and function
journal, June 2013

  • Dunbabin, Vanessa M.; Postma, Johannes A.; Schnepf, Andrea
  • Plant and Soil, Vol. 372, Issue 1-2
  • DOI: 10.1007/s11104-013-1769-y

Bacterial degradation of pyridine, indole, quinoline, and their derivatives under different redox conditions
journal, March 1998


Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp.
journal, October 2004


Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens.
journal, January 1992


MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012

  • Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
  • Systematic Biology, Vol. 61, Issue 3
  • DOI: 10.1093/sysbio/sys029

Soil properties are key determinants for the development of exudate gradients in a rhizosphere simulation model
journal, February 2010


Markers and signals associated with nitrogen assimilation in higher plants
journal, January 2003

  • Foyer, C. H.; Parry, M.; Noctor, G.
  • Journal of Experimental Botany, Vol. 54, Issue 382
  • DOI: 10.1093/jxb/erg053

Biochemical and Genetic Analyses of Ferulic Acid Catabolism in Pseudomonas sp. Strain HR199
journal, November 1999


The role of auxin in shaping shoot architecture
journal, May 2013

  • Gallavotti, Andrea
  • Journal of Experimental Botany, Vol. 64, Issue 9
  • DOI: 10.1093/jxb/ert141

Structure and Evolution of Streptomyces Interaction Networks in Soil and In Silico
journal, October 2011


Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator
journal, June 2008

  • Calisti, C.; Ficca, A. G.; Barghini, P.
  • Applied Microbiology and Biotechnology, Vol. 80, Issue 3
  • DOI: 10.1007/s00253-008-1557-4

Biotechnology in Flavor Production
book, February 2008


Bacteria and fungi controlling plant growth by manipulating auxin: Balance between development and defense
journal, January 2015


Relative involvement of nitrate and nitrite reduction in the competitiveness of Pseudomonas fluorescens in the rhizosphere of maize under non-limiting nitrate conditions
journal, February 2002


Genomics of Secondary Metabolism in Populus : Interactions with Biotic and Abiotic Environments
journal, October 2009

  • Chen, Feng; Liu, Chang-Jun; Tschaplinski, Timothy J.
  • Critical Reviews in Plant Sciences, Vol. 28, Issue 5
  • DOI: 10.1080/07352680903241279

Inside the root microbiome: Bacterial root endophytes and plant growth promotion
journal, September 2013

  • Gaiero, Jonathan R.; McCall, Crystal A.; Thompson, Karen A.
  • American Journal of Botany, Vol. 100, Issue 9
  • DOI: 10.3732/ajb.1200572

Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids
journal, September 2011


Recent advances and emerging trends in plant hormone signalling
journal, June 2009


The Bacterial Oxidation of Tryptophan: A Study in Comparative Biochemistry
journal, September 1951


Molecular characterization of genes of Pseudomonas sp. strain HR199 involved in bioconversion of vanillin to protocatechuate.
journal, April 1997


Two Distinct Pathways Supply Anthranilate as a Precursor of the Pseudomonas Quinolone Signal
journal, March 2007

  • Farrow, J. M.; Pesci, E. C.
  • Journal of Bacteriology, Vol. 189, Issue 9
  • DOI: 10.1128/jb.00209-07

A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria.
journal, January 1995


A More Sensitive Plate Assay for Detection of Protease Production by Pseudomonas aeruginosa
journal, April 1979

  • Sokol, Pamela A.; Ohman, Dennis E.; Iglewski, Barbara H.
  • Journal of Clinical Microbiology, Vol. 9, Issue 4
  • DOI: 10.1128/jcm.9.4.538-540.1979

Works referencing / citing this record:

Two Poplar-Associated Bacterial Isolates Induce Additive Favorable Responses in a Constructed Plant-Microbiome System
journal, April 2016

  • Timm, Collin M.; Pelletier, Dale A.; Jawdy, Sara S.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00497

Emergence of plant and rhizospheric microbiota as stable interactomes
journal, July 2016

  • Bandyopadhyay, Prasun; Bhuyan, Soubhagya Kumar; Yadava, Pramod Kumar
  • Protoplasma, Vol. 254, Issue 2
  • DOI: 10.1007/s00709-016-1003-x

Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
journal, July 2016

  • Wagner, Maggie R.; Lundberg, Derek S.; del Rio, Tijana G.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12151

Two Poplar-Associated Bacterial Isolates Induce Additive Favorable Responses in a Constructed Plant-Microbiome System
journal, April 2016

  • Timm, Collin M.; Pelletier, Dale A.; Jawdy, Sara S.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00497

Root Associated Bacillus sp. Improves Growth, Yield and Zinc Translocation for Basmati Rice (Oryza sativa) Varieties
journal, November 2015

  • Shakeel, Muhammad; Rais, Afroz; Hassan, Muhammad Nadeem
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01286

Relatively rare root endophytic bacteria drive plant resource allocation patterns and tissue nutrient concentration in unpredictable ways
journal, October 2019

  • Henning, Jeremiah A.; Weston, David J.; Pelletier, Dale A.
  • American Journal of Botany, Vol. 106, Issue 11
  • DOI: 10.1002/ajb2.1373

The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions
journal, September 2017

  • Jacoby, Richard; Peukert, Manuela; Succurro, Antonella
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01617

Root Associated Bacillus sp. Improves Growth, Yield and Zinc Translocation for Basmati Rice (Oryza sativa) Varieties
journal, November 2015

  • Shakeel, Muhammad; Rais, Afroz; Hassan, Muhammad Nadeem
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01286

Using genome-scale metabolic models to compare serovars of the foodborne pathogen Listeria monocytogenes
journal, June 2018


Root bacterial endophytes alter plant phenotype, but not physiology
journal, January 2016

  • Henning, Jeremiah A.; Weston, David J.; Pelletier, Dale A.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2606

Toluene biodegradation in the vadose zone of a poplar phytoremediation system identified using metagenomics and toluene-specific stable carbon isotope analysis
journal, January 2019

  • BenIsrael, Michael; Wanner, Philipp; Aravena, Ramon
  • International Journal of Phytoremediation, Vol. 21, Issue 1
  • DOI: 10.1080/15226514.2018.1523873

The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions
journal, September 2017

  • Jacoby, Richard; Peukert, Manuela; Succurro, Antonella
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01617

Root bacterial endophytes alter plant phenotype, but not physiology
journal, January 2016

  • Henning, Jeremiah A.; Weston, David J.; Pelletier, Dale A.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2606

Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation
journal, May 2018

  • Noirot-Gros, Marie-Francoise; Shinde, Shalaka; Larsen, Peter E.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.00853

Giving back to the community: microbial mechanisms of plant-soil interactions
journal, June 2016


Quantifying the Spatiotemporal Dynamics of Plant Root Colonization by Beneficial Bacteria in a Microfluidic Habitat
journal, April 2018

  • Aufrecht, Jayde A.; Timm, Collin M.; Bible, Amber
  • Advanced Biosystems, Vol. 2, Issue 6
  • DOI: 10.1002/adbi.201800048

Genome variations between rhizosphere and bulk soil ecotypes of a Pseudomonas koreensis population
journal, September 2018

  • Lopes, Lucas Dantas; Pereira e. Silva, Michele de C.; Weisberg, Alexandra J.
  • Environmental Microbiology, Vol. 20, Issue 12
  • DOI: 10.1111/1462-2920.14363

Isolated Bacillus subtilis strain 330-2 and its antagonistic genes identified by the removing PCR
journal, May 2017


Isolated Bacillus subtilis strain 330-2 and its antagonistic genes identified by the removing PCR
journal, May 2017


Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
text, January 2016

  • S., Lundberg, Derek; L., Dangl, Jeffery; G., Del Rio, Tijana
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/18y1-ek17