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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

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:
 [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4];  [1];  [2]; ORCiD logo [1]; ORCiD logo [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. 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)
  4. Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
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.
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
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.
@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 = {2018},
month = {2}
}

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Figures / Tables:

Figure 1 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 » and red lines with exes indicating the absence of genes encoding candidate enzymes for the pathway.« less

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