Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343

Estenson, Kasey N.; Hurst, Gregory B.; Standaert, Robert F.; Bible, Amber N.; Garcia, David C.; Chourey, Karuna; Doktycz, Mitchel J.; Morrell-Falvey, Jennifer L.

doi:10.1021/acs.jproteome.7b00708

Title: Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343

Abstract

Here, indole-3-acetic acid (IAA) plays a central role in plant growth and development, and many plant-associated microbes produce IAA using tryptophan as the precursor. Using genomic analyses, we predicted that Pantoea sp. YR343, a microbe isolated from Populus deltoides, synthesizes IAA using the indole-3-pyruvate (IPA) pathway. To better understand IAA biosynthesis and the effects of IAA exposure on cell physiology, we characterized proteomes of Pantoea sp. YR343 grown in the presence of tryptophan or IAA. Exposure to IAA resulted in upregulation of proteins predicted to function in carbohydrate and amino acid transport and exopolysaccharide (EPS) biosynthesis. Metabolite profiles of wild-type cells showed the production of IPA, IAA, and tryptophol, consistent with an active IPA pathway. Finally, we constructed an ΔipdC mutant that showed the elimination of tryptophol, consistent with a loss of IpdC activity, but was still able to produce IAA (20% of wild-type levels). Although we failed to detect intermediates from other known IAA biosynthetic pathways, this result suggests the possibility of an alternate pathway or the production of IAA by a nonenzymatic route in Pantoea sp. YR343. The ΔipdC mutant was able to efficiently colonize poplar, suggesting that an active IPA pathway is not required for plant association.

Authors:

Estenson, Kasey N. ^[1];

^[2];

^[3];

^[4]; Garcia, David C. ^[1]; Chourey, Karuna ^[2];

^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States); Shull Wollan Center - a Joint Institute for Neutron Sciences, Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States)

Publication Date:: Wed Feb 21 00:00:00 EST 2018

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1435312

Grant/Contract Number:: AC05-00OR22725

Resource Type:: Accepted Manuscript

Journal Name:: Journal of Proteome Research

Additional Journal Information:: Journal Volume: 17; Journal Issue: 4; Journal ID: ISSN 1535-3893

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; indole-3-acetic acid; indole-3-pyruvate decarboxylase; Pantoea sp. YR343; plant colonization; poplar; tryptophol

Citation Formats


                    Estenson, Kasey N., Hurst, Gregory B., Standaert, Robert F., Bible, Amber N., Garcia, David C., Chourey, Karuna, Doktycz, Mitchel J., and Morrell-Falvey, Jennifer L. Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343.  United States: N. p., 2018. 
Web.  doi:10.1021/acs.jproteome.7b00708.

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                    Estenson, Kasey N., Hurst, Gregory B., Standaert, Robert F., Bible, Amber N., Garcia, David C., Chourey, Karuna, Doktycz, Mitchel J., & Morrell-Falvey, Jennifer L. Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343.  United States.  https://doi.org/10.1021/acs.jproteome.7b00708

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                    Estenson, Kasey N., Hurst, Gregory B., Standaert, Robert F., Bible, Amber N., Garcia, David C., Chourey, Karuna, Doktycz, Mitchel J., and Morrell-Falvey, Jennifer L. Wed .  
"Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343".  United States.  https://doi.org/10.1021/acs.jproteome.7b00708.  https://www.osti.gov/servlets/purl/1435312.

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@article{osti_1435312,

  title        = {Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343},

  author       = {Estenson, Kasey N. and Hurst, Gregory B. and Standaert, Robert F. and Bible, Amber N. and Garcia, David C. and Chourey, Karuna and Doktycz, Mitchel J. and Morrell-Falvey, Jennifer L.},

  abstractNote = {Here, indole-3-acetic acid (IAA) plays a central role in plant growth and development, and many plant-associated microbes produce IAA using tryptophan as the precursor. Using genomic analyses, we predicted that Pantoea sp. YR343, a microbe isolated from Populus deltoides, synthesizes IAA using the indole-3-pyruvate (IPA) pathway. To better understand IAA biosynthesis and the effects of IAA exposure on cell physiology, we characterized proteomes of Pantoea sp. YR343 grown in the presence of tryptophan or IAA. Exposure to IAA resulted in upregulation of proteins predicted to function in carbohydrate and amino acid transport and exopolysaccharide (EPS) biosynthesis. Metabolite profiles of wild-type cells showed the production of IPA, IAA, and tryptophol, consistent with an active IPA pathway. Finally, we constructed an ΔipdC mutant that showed the elimination of tryptophol, consistent with a loss of IpdC activity, but was still able to produce IAA (20% of wild-type levels). Although we failed to detect intermediates from other known IAA biosynthetic pathways, this result suggests the possibility of an alternate pathway or the production of IAA by a nonenzymatic route in Pantoea sp. YR343. The ΔipdC mutant was able to efficiently colonize poplar, suggesting that an active IPA pathway is not required for plant association.},

  doi          = {10.1021/acs.jproteome.7b00708},

  journal      = {Journal of Proteome Research},

  number       = 4,

  volume       = 17,

  place        = {United States},

  year         = {Wed Feb 21 00:00:00 EST 2018},

  month        = {Wed Feb 21 00:00:00 EST 2018}

}

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Journal Article:

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https://doi.org/10.1021/acs.jproteome.7b00708

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Cited by: 16 works

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Figures / Tables:

Figure 1: Tryptophan-dependent IAA biosynthetic pathways in Pantoea sp. YR343. The pathways are color-coded based on genomic analyses with green lines and checks indicating the presence of genes encoding candidate enzymes for each step in the pathway, orange lines and questions marks indicating the presence of possible candidate gene products,more »

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Syntheses of the plant auxin conjugate 2- O -(indole-3-acetyl)- myo -inositol IAInos
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Silva, Saúl; Ascenso, Osvaldo S.; Lourenço, Eva C.
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Table 1: Part 1 (p. 13)

Table 1: Part 2 (p. 14)

Table 1: Part 3 (p. 15)

Table 2: Part 1 (p. 16)

Table 2: Part 2 (p. 17)

Table 3: Part 1 (p. 19)

Table 3: Part 2 (p. 20)

Table 3: Part 3 (p. 21)

Table 3: Part 4 (p. 22)

Table 3: Part 5 (p. 23)

Figure 2 (p. 24)

Figure 3 (p. 27)

Figure 4 (p. 29)

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Identification of a diguanylate cyclase expressed in the presence of plants and its application for discovering candidate gene products involved in plant colonization by Pantoea sp. YR343

Journal Article Bible, Amber N. ; Chang, Mang ; Morrell-Falvey, Jennifer L. ; ... - PLoS ONE

Microbial colonization of plant roots is a highly complex process that requires the coordination and regulation of many gene networks, yet the identities and functions of many of these gene products have yet to be discovered. Pantoea sp. YR343, a gamma-proteobacterium isolated from the rhizosphere of Populus deltoides , forms robust biofilms along the root surfaces of Populus and possesses plant growth-promoting characteristics. In this work, we identified three diguanylate cyclases in the plant-associated microbe Pantoea sp. YR343 that are expressed in the presence of plant roots. One of these diguanylate cyclases, DGC2884, localizes to discrete sites in the cellsmore »« less
https://doi.org/10.1371/journal.pone.0248607

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Title: Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343

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Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types journal, July 2011

Towards a holistic understanding of the beneficial interactions across the Populus microbiome journal, November 2014

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

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

Soil beneficial bacteria and their role in plant growth promotion: a review journal, August 2010

Indole-3-acetic acid in plant–microbe interactions journal, January 2014

Auxin and Plant-Microbe Interactions journal, November 2010

Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria journal, September 2012

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

Indole-3-acetic acid biosynthetic pathway and aromatic amino acid aminotransferase activities in Pantoea dispersa strain GPK journal, March 2013

Role of Pseudomonas putida Indoleacetic Acid in Development of the Host Plant Root System journal, August 2002

Aromatic Amino Acid-Dependent Expression of Indole-3-Pyruvate Decarboxylase Is Regulated by TyrR in Enterobacter cloacae UW5 journal, November 2008

Production of indole-3-acetic acid, aromatic amino acid aminotransferase activities and plant growth promotion by Pantoea agglomerans rhizosphere isolates journal, July 2007

Transcriptional Analysis of the Azospirillum brasilense Indole-3-Pyruvate Decarboxylase Gene and Identification of a cis -Acting Sequence Involved in Auxin Responsive Expression journal, April 2005

Identification and Isolation of the Indole-3-Pyruvate Decarboxylase Gene from Azospirillum brasilense Sp7: Sequencing and Functional Analysis of the Gene Locus journal, June 1998

Transcriptome Analysis of the Rhizosphere Bacterium Azospirillum brasilense Reveals an Extensive Auxin Response journal, February 2011

Physiological evidence for differently regulated tryptophan-dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense journal, November 2000

Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions journal, July 2000

Auxins Upregulate Expression of the Indole-3-Pyruvate Decarboxylase Gene in Azospirillum brasilense journal, February 1999

Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM journal, May 2008

Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae journal, June 2015

Pantoea rodasii sp. nov., Pantoea rwandensis sp. nov. and Pantoea wallisii sp. nov., isolated from Eucalyptus journal, July 2012

A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization journal, April 2016

Improved gfp and inaZ Broad-Host-Range Promoter-Probe Vectors journal, November 2000

NIH Image to ImageJ: 25 years of image analysis journal, June 2012

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics journal, December 2010

Dosage-Dependent Proteome Response of Shewanella oneidensis MR-1 to Acute Chromate Challenge journal, May 2007

Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress journal, March 2006

Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization journal, October 2012

Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT journal, August 2002

MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis journal, February 2007

Twenty-One Genome Sequences from Pseudomonas Species and 19 Genome Sequences from Diverse Bacteria Isolated from the Rhizosphere and Endosphere of Populus deltoides journal, October 2012

IMG 4 version of the integrated microbial genomes comparative analysis system journal, October 2013

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering journal, August 2009

A Model for Random Sampling and Estimation of Relative Protein Abundance in Shotgun Proteomics journal, July 2004

Refinements to Label Free Proteome Quantitation: How to Deal with Peptides Shared by Multiple Proteins journal, March 2010

Statistical Analysis of Membrane Proteome Expression Changes in Saccharomyces c erevisiae journal, September 2006

Label-free Quantitative Proteomics for the Extremely Thermophilic Bacterium Caldicellulosiruptor obsidiansis Reveal Distinct Abundance Patterns upon Growth on Cellobiose, Crystalline Cellulose, and Switchgrass journal, December 2011

The pKNOCK Series of Broad-Host-Range Mobilizable Suicide Vectors for Gene Knockout and Targeted DNA Insertion into the Chromosome of Gram-Negative Bacteria journal, May 1999

Molecular cloning and sequence analysis of an Azospirilium brasilense indole-3-pyruvate decarboxylase gene journal, July 1994

Development of Indole-3-Acetic Acid-Producing Escherichia coli by Functional Expression of IpdC, AspC, and Iad1 journal, December 2013

Indole-3-acetic acid (IAA) synthesis in the biocontrol strain CHA0 of Pseudomonas fluorescens: role of tryptophan side chain oxidase journal, October 1991

The Pho regulon: a huge regulatory network in bacteria journal, April 2015

The PhoU Protein from Escherichia coli Interacts with PhoR, PstB, and Metals To Form a Phosphate-Signaling Complex at the Membrane journal, May 2014

Employment of a Promoter-Swapping Technique Shows that PhoU Modulates the Activity of the PstSCAB 2 ABC Transporter in Escherichia coli journal, February 2009

Characterization of the Escherichia coli AaeAB Efflux Pump: a Metabolic Relief Valve? journal, October 2004

Inactivation of Efflux Pumps Abolishes Bacterial Biofilm Formation journal, October 2008

Biosynthesis of the repeating units of the exopolysaccharides amylovoran from Erwinia amylovora and stewartan from Pantoea stewartii journal, April 2011

Some chemical and physiological properties of 3-indolylpyruvic acid journal, September 1956

Contribution of Indole-3-Acetic Acid Production to the Epiphytic Fitness of Erwinia herbicola journal, September 1998

Differential Involvement of Indole-3-Acetic Acid Biosynthetic Pathways in Pathogenicity and Epiphytic Fitness of Erwinia herbicola pv. gypsophilae journal, July 1998

Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation journal, March 2007

Isolation and Identification of Indole-3-Ethanol (Tryptophol) from Cucumber Seedlings journal, April 1967

Indole-3-ethanol Oxidase: Kinetics, Inhibition, and Regulation by Auxins journal, April 1973

Syntheses of the plant auxin conjugate 2- O -(indole-3-acetyl)- myo -inositol IAInos journal, January 2018

Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants journal, June 2018

Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types
journal, July 2011

Towards a holistic understanding of the beneficial interactions across the Populus microbiome
journal, November 2014

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

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

Soil beneficial bacteria and their role in plant growth promotion: a review
journal, August 2010

Indole-3-acetic acid in plant–microbe interactions
journal, January 2014

Auxin and Plant-Microbe Interactions
journal, November 2010

Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria
journal, September 2012

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

Indole-3-acetic acid biosynthetic pathway and aromatic amino acid aminotransferase activities in Pantoea dispersa strain GPK
journal, March 2013

Role of Pseudomonas putida Indoleacetic Acid in Development of the Host Plant Root System
journal, August 2002

Aromatic Amino Acid-Dependent Expression of Indole-3-Pyruvate Decarboxylase Is Regulated by TyrR in Enterobacter cloacae UW5
journal, November 2008

Production of indole-3-acetic acid, aromatic amino acid aminotransferase activities and plant growth promotion by Pantoea agglomerans rhizosphere isolates
journal, July 2007

Transcriptional Analysis of the Azospirillum brasilense Indole-3-Pyruvate Decarboxylase Gene and Identification of a cis -Acting Sequence Involved in Auxin Responsive Expression
journal, April 2005

Identification and Isolation of the Indole-3-Pyruvate Decarboxylase Gene from Azospirillum brasilense Sp7: Sequencing and Functional Analysis of the Gene Locus
journal, June 1998

Transcriptome Analysis of the Rhizosphere Bacterium Azospirillum brasilense Reveals an Extensive Auxin Response
journal, February 2011

Physiological evidence for differently regulated tryptophan-dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense
journal, November 2000

Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions
journal, July 2000

Auxins Upregulate Expression of the Indole-3-Pyruvate Decarboxylase Gene in Azospirillum brasilense
journal, February 1999

Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM
journal, May 2008

Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae
journal, June 2015

Pantoea rodasii sp. nov., Pantoea rwandensis sp. nov. and Pantoea wallisii sp. nov., isolated from Eucalyptus
journal, July 2012

A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization
journal, April 2016

Improved gfp and inaZ Broad-Host-Range Promoter-Probe Vectors
journal, November 2000

NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics
journal, December 2010

Dosage-Dependent Proteome Response of Shewanella oneidensis MR-1 to Acute Chromate Challenge
journal, May 2007

Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress
journal, March 2006

Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization
journal, October 2012

Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT
journal, August 2002

MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

Twenty-One Genome Sequences from Pseudomonas Species and 19 Genome Sequences from Diverse Bacteria Isolated from the Rhizosphere and Endosphere of Populus deltoides
journal, October 2012

IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009

A Model for Random Sampling and Estimation of Relative Protein Abundance in Shotgun Proteomics
journal, July 2004

Refinements to Label Free Proteome Quantitation: How to Deal with Peptides Shared by Multiple Proteins
journal, March 2010

Statistical Analysis of Membrane Proteome Expression Changes in Saccharomyces c erevisiae
journal, September 2006

Label-free Quantitative Proteomics for the Extremely Thermophilic Bacterium Caldicellulosiruptor obsidiansis Reveal Distinct Abundance Patterns upon Growth on Cellobiose, Crystalline Cellulose, and Switchgrass
journal, December 2011

The pKNOCK Series of Broad-Host-Range Mobilizable Suicide Vectors for Gene Knockout and Targeted DNA Insertion into the Chromosome of Gram-Negative Bacteria
journal, May 1999

Molecular cloning and sequence analysis of an Azospirilium brasilense indole-3-pyruvate decarboxylase gene
journal, July 1994

Development of Indole-3-Acetic Acid-Producing Escherichia coli by Functional Expression of IpdC, AspC, and Iad1
journal, December 2013

Indole-3-acetic acid (IAA) synthesis in the biocontrol strain CHA0 of Pseudomonas fluorescens: role of tryptophan side chain oxidase
journal, October 1991

The Pho regulon: a huge regulatory network in bacteria
journal, April 2015

The PhoU Protein from Escherichia coli Interacts with PhoR, PstB, and Metals To Form a Phosphate-Signaling Complex at the Membrane
journal, May 2014

Employment of a Promoter-Swapping Technique Shows that PhoU Modulates the Activity of the PstSCAB ₂ ABC Transporter in Escherichia coli
journal, February 2009

Characterization of the Escherichia coli AaeAB Efflux Pump: a Metabolic Relief Valve?
journal, October 2004

Inactivation of Efflux Pumps Abolishes Bacterial Biofilm Formation
journal, October 2008

Biosynthesis of the repeating units of the exopolysaccharides amylovoran from Erwinia amylovora and stewartan from Pantoea stewartii
journal, April 2011

Some chemical and physiological properties of 3-indolylpyruvic acid
journal, September 1956

Contribution of Indole-3-Acetic Acid Production to the Epiphytic Fitness of Erwinia herbicola
journal, September 1998

Differential Involvement of Indole-3-Acetic Acid Biosynthetic Pathways in Pathogenicity and Epiphytic Fitness of Erwinia herbicola pv. gypsophilae
journal, July 1998

Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation
journal, March 2007

Isolation and Identification of Indole-3-Ethanol (Tryptophol) from Cucumber Seedlings
journal, April 1967

Indole-3-ethanol Oxidase: Kinetics, Inhibition, and Regulation by Auxins
journal, April 1973

Syntheses of the plant auxin conjugate 2- O -(indole-3-acetyl)- myo -inositol IAInos
journal, January 2018

Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants
journal, June 2018