GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000

The nonprotein amino acid γ-aminobutyric acid (GABA) is the most abundant amino acid in the tomato (Solanum lycopersicum) leaf apoplast and is synthesized by Arabidopsis thaliana in response to infection by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000). High...

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Main Authors: S. L. McCraw, D. H. Park, R. Jones, M. A. Bentley, A. Rico, R. G. Ratcliffe, N. J. Kruger, A. Collmer, G. M. Preston
Format: Article
Language:English
Published: The American Phytopathological Society 2016-12-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-16-0172-R
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author S. L. McCraw
D. H. Park
R. Jones
M. A. Bentley
A. Rico
R. G. Ratcliffe
N. J. Kruger
A. Collmer
G. M. Preston
author_facet S. L. McCraw
D. H. Park
R. Jones
M. A. Bentley
A. Rico
R. G. Ratcliffe
N. J. Kruger
A. Collmer
G. M. Preston
author_sort S. L. McCraw
collection DOAJ
description The nonprotein amino acid γ-aminobutyric acid (GABA) is the most abundant amino acid in the tomato (Solanum lycopersicum) leaf apoplast and is synthesized by Arabidopsis thaliana in response to infection by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000). High levels of exogenous GABA have previously been shown to repress the expression of the type III secretion system (T3SS) in DC3000, resulting in reduced elicitation of the hypersensitive response (HR) in the nonhost plant tobacco (Nicotiana tabacum). This study demonstrates that the GABA permease GabP provides the primary mechanism for GABA uptake by DC3000 and that the gabP deletion mutant ΔgabP is insensitive to GABA-mediated repression of T3SS expression. ΔgabP displayed an enhanced ability to elicit the HR in young tobacco leaves and in tobacco plants engineered to produce increased levels of GABA, which supports the hypothesis that GABA uptake via GabP acts to regulate T3SS expression in planta. The observation that P. syringae can be rendered insensitive to GABA through loss of gabP but that gabP is retained by this bacterium suggests that GabP is important for DC3000 in a natural setting, either for nutrition or as a mechanism for regulating gene expression.[Graphic: see text] Copyright © 2016 The Author(s). This is an open access article distributed under the CC BY Attribution 4.0 International license.
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spelling doaj.art-37fe1b6036e84bd28f61fb613050871b2022-12-22T03:10:31ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062016-12-01291293894910.1094/MPMI-08-16-0172-RGABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000S. L. McCraw0D. H. Park1R. Jones2M. A. Bentley3A. Rico4R. G. Ratcliffe5N. J. Kruger6A. Collmer7G. M. Preston8Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;Department of Applied Biology, College of Agriculture and Life Sciences, Kangwon National University, Chuncheon 200-701, Republic of Korea;Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;Departamento de Didáctica de la 9 Matemática y de las Ciencias Experimentales, Faculty of Education and Sport, University of the Basque Country UPV/EHU, Juan Ibañez de Sto. Domingo 1, 01006 Vitoria-Gasteiz, Spain; andDepartment of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;School of Integrative Plant Science, Section of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853, U.S.A.Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.;The nonprotein amino acid γ-aminobutyric acid (GABA) is the most abundant amino acid in the tomato (Solanum lycopersicum) leaf apoplast and is synthesized by Arabidopsis thaliana in response to infection by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000). High levels of exogenous GABA have previously been shown to repress the expression of the type III secretion system (T3SS) in DC3000, resulting in reduced elicitation of the hypersensitive response (HR) in the nonhost plant tobacco (Nicotiana tabacum). This study demonstrates that the GABA permease GabP provides the primary mechanism for GABA uptake by DC3000 and that the gabP deletion mutant ΔgabP is insensitive to GABA-mediated repression of T3SS expression. ΔgabP displayed an enhanced ability to elicit the HR in young tobacco leaves and in tobacco plants engineered to produce increased levels of GABA, which supports the hypothesis that GABA uptake via GabP acts to regulate T3SS expression in planta. The observation that P. syringae can be rendered insensitive to GABA through loss of gabP but that gabP is retained by this bacterium suggests that GabP is important for DC3000 in a natural setting, either for nutrition or as a mechanism for regulating gene expression.[Graphic: see text] Copyright © 2016 The Author(s). This is an open access article distributed under the CC BY Attribution 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-16-0172-R
spellingShingle S. L. McCraw
D. H. Park
R. Jones
M. A. Bentley
A. Rico
R. G. Ratcliffe
N. J. Kruger
A. Collmer
G. M. Preston
GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
Molecular Plant-Microbe Interactions
title GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
title_full GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
title_fullStr GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
title_full_unstemmed GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
title_short GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000
title_sort gaba γ aminobutyric acid uptake via the gaba permease gabp represses virulence gene expression in pseudomonas syringae pv tomato dc3000
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-16-0172-R
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