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Title: A plant-responsive bacterial-signaling system senses an ethanolamine derivative

Abstract

Certain plant-associated Proteobacteria sense their host environment by detecting an unknown plant signal recognized by a member of a LuxR subfamily of transcription factors. This interkingdom communication is important for both mutualistic and pathogenic interactions. The Populus root endophyte Pseudomonas sp. GM79 possesses such a regulator, named PipR. In a previous study we reported that PipR activates an adjacent gene ( pipA ) coding for a proline iminopeptidase in response to Populus leaf macerates and peptides and that this activation is dependent on a putative ABC-type transporter [Schaefer AL, et al. (2016) mBio 7:e01101-16]. In this study we identify a chemical derived from ethanolamine that induces PipR activity at picomolar concentrations, and we present evidence that this is the active inducer present in plant leaf macerates. First, a screen of more than 750 compounds indicated ethanolamine was a potent inducer for the PipR-sensing system; however, ethanolamine failed to bind to the periplasmic-binding protein (PBP) required for the signal response. This led us to discover that a specific ethanolamine derivative, N -(2-hydroxyethyl)-2-(2-hydroxyethylamino) acetamide (HEHEAA), binds to the PBP and serves as a potent PipR-dependent inducer. We also show that a compound, which coelutes with HEHEAA in HPLC and induces pipA genemore » expression in a PipR-dependent manner, can be found in Populus leaf macerates. This work sheds light on how plant-associated bacteria can sense their environment and on the nature of inducers for a family of plant-responsive LuxR-like transcription factors found in plant-associated bacteria.« less

Authors:
 [1];  [2];  [1]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Washington, Seattle, WA (United States)
  2. Harvard Medical School, Boston, MA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1468883
Alternate Identifier(s):
OSTI ID: 1474576
Grant/Contract Number:  
AC05-00OR22725; AC05-00R227525
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 39; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ethanolamine; LuxR homolog; plant–microbe interactions; transcription activator; quorum sensing

Citation Formats

Coutinho, Bruna G., Mevers, Emily, Schaefer, Amy L., Pelletier, Dale A., Harwood, Caroline S., Clardy, Jon, and Greenberg, E. Peter. A plant-responsive bacterial-signaling system senses an ethanolamine derivative. United States: N. p., 2018. Web. doi:10.1073/pnas.1809611115.
Coutinho, Bruna G., Mevers, Emily, Schaefer, Amy L., Pelletier, Dale A., Harwood, Caroline S., Clardy, Jon, & Greenberg, E. Peter. A plant-responsive bacterial-signaling system senses an ethanolamine derivative. United States. doi:10.1073/pnas.1809611115.
Coutinho, Bruna G., Mevers, Emily, Schaefer, Amy L., Pelletier, Dale A., Harwood, Caroline S., Clardy, Jon, and Greenberg, E. Peter. Thu . "A plant-responsive bacterial-signaling system senses an ethanolamine derivative". United States. doi:10.1073/pnas.1809611115.
@article{osti_1468883,
title = {A plant-responsive bacterial-signaling system senses an ethanolamine derivative},
author = {Coutinho, Bruna G. and Mevers, Emily and Schaefer, Amy L. and Pelletier, Dale A. and Harwood, Caroline S. and Clardy, Jon and Greenberg, E. Peter},
abstractNote = {Certain plant-associated Proteobacteria sense their host environment by detecting an unknown plant signal recognized by a member of a LuxR subfamily of transcription factors. This interkingdom communication is important for both mutualistic and pathogenic interactions. The Populus root endophyte Pseudomonas sp. GM79 possesses such a regulator, named PipR. In a previous study we reported that PipR activates an adjacent gene ( pipA ) coding for a proline iminopeptidase in response to Populus leaf macerates and peptides and that this activation is dependent on a putative ABC-type transporter [Schaefer AL, et al. (2016) mBio 7:e01101-16]. In this study we identify a chemical derived from ethanolamine that induces PipR activity at picomolar concentrations, and we present evidence that this is the active inducer present in plant leaf macerates. First, a screen of more than 750 compounds indicated ethanolamine was a potent inducer for the PipR-sensing system; however, ethanolamine failed to bind to the periplasmic-binding protein (PBP) required for the signal response. This led us to discover that a specific ethanolamine derivative, N -(2-hydroxyethyl)-2-(2-hydroxyethylamino) acetamide (HEHEAA), binds to the PBP and serves as a potent PipR-dependent inducer. We also show that a compound, which coelutes with HEHEAA in HPLC and induces pipA gene expression in a PipR-dependent manner, can be found in Populus leaf macerates. This work sheds light on how plant-associated bacteria can sense their environment and on the nature of inducers for a family of plant-responsive LuxR-like transcription factors found in plant-associated bacteria.},
doi = {10.1073/pnas.1809611115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 39,
volume = 115,
place = {United States},
year = {2018},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1809611115

Citation Metrics:
Cited by: 1 work
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Figures / Tables:

Fig. 1 Fig. 1: The pipR gene region in Pseudomonas GM79 and PipR-dependent ethanolamine activation of PpipA-gfp. (A) The pipR (yellow) genomic region. Genes coding for the predicted ABC-type transporter (blue) and genes coding for the peptidases (red). (B) Activation of gfp expression in strain GM79 containing pPpipA-gfp by ethanolamine. (C) Influencemore » of mutations in ethanolamine (100 μM) activation of gfp expression in strains carrying pPpipA-gfp. AapB, AapB transporter mutant; PipA AapA, PipA, AapA double-peptidase mutant; PipR, PipR mutant; WT, wild type. Data are GFP fluorescence in cells grown without additions (white bars) or cells grownwith 100 μMethanolamine (red bars). B and C showmean relative fluorescence units (RFU) per optical density (OD600) × 10 of four biological replicates, and the bars represent the SDs.« less

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    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.