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Glutathione deficiency of the Arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression, and the hypersensitive response.

Identifieur interne : 001720 ( Main/Exploration ); précédent : 001719; suivant : 001721

Glutathione deficiency of the Arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression, and the hypersensitive response.

Auteurs : Carole Dubreuil-Maurizi [France] ; Jan Vitecek ; Laurent Marty ; Lorelise Branciard ; Patrick Frettinger ; David Wendehenne ; Andreas J. Meyer ; Felix Mauch ; Benoît Poinssot

Source :

RBID : pubmed:22007023

Descripteurs français

English descriptors

Abstract

The Arabidopsis (Arabidopsis thaliana) phytoalexin-deficient mutant pad2-1 displays enhanced susceptibility to a broad range of pathogens and herbivorous insects that correlates with deficiencies in the production of camalexin, indole glucosinolates, and salicylic acid (SA). The pad2-1 mutation is localized in the GLUTAMATE-CYSTEINE LIGASE (GCL) gene encoding the first enzyme of glutathione biosynthesis. While pad2-1 glutathione deficiency is not caused by a decrease in GCL transcripts, analysis of GCL protein level revealed that pad2-1 plants contained only 48% of the wild-type protein amount. In contrast to the wild type, the oxidized form of GCL was dominant in pad2-1, suggesting a distinct redox environment. This finding was corroborated by the expression of GRX1-roGFP2, showing that the cytosolic glutathione redox potential was significantly less negative in pad2-1. Analysis of oxidative stress-related gene expression showed a higher transcript accumulation in pad2-1 of GLUTATHIONE REDUCTASE, GLUTATHIONE-S-TRANSFERASE, and RESPIRATORY BURST OXIDASE HOMOLOG D in response to the oomycete Phytophthora brassicae. Interestingly, oligogalacturonide elicitation in pad2-1 revealed a lower plasma membrane depolarization that was found to act upstream of an impaired hydrogen peroxide production. This impaired hydrogen peroxide production was also observed during pathogen infection and correlated with a reduced hypersensitive response in pad2-1. In addition, a lack of pathogen-triggered expression of the ISOCHORISMATE SYNTHASE1 gene, coding for the SA-biosynthetic enzyme isochorismate synthase, was identified as the cause of the SA deficiency in pad2-1. Together, our results indicate that the pad2-1 mutation is related to a decrease in GCL protein and that the resulting glutathione deficiency negatively affects important processes of disease resistance.

DOI: 10.1104/pp.111.182667
PubMed: 22007023
PubMed Central: PMC3327178


Affiliations:


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<term>Arabidopsis (drug effects)</term>
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (parasitology)</term>
<term>Arabidopsis (physiology)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Arabidopsis Proteins (metabolism)</term>
<term>Cell Membrane (metabolism)</term>
<term>Disease Susceptibility (MeSH)</term>
<term>Gene Expression Regulation, Plant (physiology)</term>
<term>Glutamate-Cysteine Ligase (genetics)</term>
<term>Glutamate-Cysteine Ligase (metabolism)</term>
<term>Glutathione (metabolism)</term>
<term>Host-Pathogen Interactions (MeSH)</term>
<term>Hydrogen Peroxide (metabolism)</term>
<term>Mutation (MeSH)</term>
<term>Nitric Oxide (metabolism)</term>
<term>Oligosaccharides (pharmacology)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Oxidative Stress (MeSH)</term>
<term>Phytophthora (physiology)</term>
<term>Plant Diseases (parasitology)</term>
<term>Plant Leaves (drug effects)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Leaves (parasitology)</term>
<term>Plant Leaves (physiology)</term>
<term>Reactive Oxygen Species (metabolism)</term>
<term>Salicylic Acid (metabolism)</term>
<term>Signal Transduction (MeSH)</term>
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<term>Acide salicylique (métabolisme)</term>
<term>Anti-infectieux (métabolisme)</term>
<term>Arabidopsis (effets des médicaments et des substances chimiques)</term>
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (parasitologie)</term>
<term>Arabidopsis (physiologie)</term>
<term>Espèces réactives de l'oxygène (métabolisme)</term>
<term>Feuilles de plante (effets des médicaments et des substances chimiques)</term>
<term>Feuilles de plante (génétique)</term>
<term>Feuilles de plante (parasitologie)</term>
<term>Feuilles de plante (physiologie)</term>
<term>Glutamate-cysteine ligase (génétique)</term>
<term>Glutamate-cysteine ligase (métabolisme)</term>
<term>Glutathion (métabolisme)</term>
<term>Interactions hôte-pathogène (MeSH)</term>
<term>Maladies des plantes (parasitologie)</term>
<term>Membrane cellulaire (métabolisme)</term>
<term>Monoxyde d'azote (métabolisme)</term>
<term>Mutation (MeSH)</term>
<term>Oligosaccharides (pharmacologie)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Peroxyde d'hydrogène (métabolisme)</term>
<term>Phytophthora (physiologie)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines d'Arabidopsis (métabolisme)</term>
<term>Prédisposition aux maladies (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (physiologie)</term>
<term>Stress oxydatif (MeSH)</term>
<term>Stress physiologique (MeSH)</term>
<term>Transduction du signal (MeSH)</term>
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<term>Glutamate-Cysteine Ligase</term>
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<term>Anti-Infective Agents</term>
<term>Arabidopsis Proteins</term>
<term>Glutamate-Cysteine Ligase</term>
<term>Glutathione</term>
<term>Hydrogen Peroxide</term>
<term>Nitric Oxide</term>
<term>Reactive Oxygen Species</term>
<term>Salicylic Acid</term>
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<term>Glutamate-cysteine ligase</term>
<term>Protéines d'Arabidopsis</term>
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<term>Acide salicylique</term>
<term>Anti-infectieux</term>
<term>Espèces réactives de l'oxygène</term>
<term>Glutamate-cysteine ligase</term>
<term>Glutathion</term>
<term>Membrane cellulaire</term>
<term>Monoxyde d'azote</term>
<term>Peroxyde d'hydrogène</term>
<term>Protéines d'Arabidopsis</term>
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<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
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<term>Oligosaccharides</term>
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<term>Feuilles de plante</term>
<term>Phytophthora</term>
<term>Régulation de l'expression des gènes végétaux</term>
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<term>Arabidopsis</term>
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<term>Mutation</term>
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<term>Mutation</term>
<term>Oxydoréduction</term>
<term>Prédisposition aux maladies</term>
<term>Stress oxydatif</term>
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<div type="abstract" xml:lang="en">The Arabidopsis (Arabidopsis thaliana) phytoalexin-deficient mutant pad2-1 displays enhanced susceptibility to a broad range of pathogens and herbivorous insects that correlates with deficiencies in the production of camalexin, indole glucosinolates, and salicylic acid (SA). The pad2-1 mutation is localized in the GLUTAMATE-CYSTEINE LIGASE (GCL) gene encoding the first enzyme of glutathione biosynthesis. While pad2-1 glutathione deficiency is not caused by a decrease in GCL transcripts, analysis of GCL protein level revealed that pad2-1 plants contained only 48% of the wild-type protein amount. In contrast to the wild type, the oxidized form of GCL was dominant in pad2-1, suggesting a distinct redox environment. This finding was corroborated by the expression of GRX1-roGFP2, showing that the cytosolic glutathione redox potential was significantly less negative in pad2-1. Analysis of oxidative stress-related gene expression showed a higher transcript accumulation in pad2-1 of GLUTATHIONE REDUCTASE, GLUTATHIONE-S-TRANSFERASE, and RESPIRATORY BURST OXIDASE HOMOLOG D in response to the oomycete Phytophthora brassicae. Interestingly, oligogalacturonide elicitation in pad2-1 revealed a lower plasma membrane depolarization that was found to act upstream of an impaired hydrogen peroxide production. This impaired hydrogen peroxide production was also observed during pathogen infection and correlated with a reduced hypersensitive response in pad2-1. In addition, a lack of pathogen-triggered expression of the ISOCHORISMATE SYNTHASE1 gene, coding for the SA-biosynthetic enzyme isochorismate synthase, was identified as the cause of the SA deficiency in pad2-1. Together, our results indicate that the pad2-1 mutation is related to a decrease in GCL protein and that the resulting glutathione deficiency negatively affects important processes of disease resistance.</div>
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<AbstractText>The Arabidopsis (Arabidopsis thaliana) phytoalexin-deficient mutant pad2-1 displays enhanced susceptibility to a broad range of pathogens and herbivorous insects that correlates with deficiencies in the production of camalexin, indole glucosinolates, and salicylic acid (SA). The pad2-1 mutation is localized in the GLUTAMATE-CYSTEINE LIGASE (GCL) gene encoding the first enzyme of glutathione biosynthesis. While pad2-1 glutathione deficiency is not caused by a decrease in GCL transcripts, analysis of GCL protein level revealed that pad2-1 plants contained only 48% of the wild-type protein amount. In contrast to the wild type, the oxidized form of GCL was dominant in pad2-1, suggesting a distinct redox environment. This finding was corroborated by the expression of GRX1-roGFP2, showing that the cytosolic glutathione redox potential was significantly less negative in pad2-1. Analysis of oxidative stress-related gene expression showed a higher transcript accumulation in pad2-1 of GLUTATHIONE REDUCTASE, GLUTATHIONE-S-TRANSFERASE, and RESPIRATORY BURST OXIDASE HOMOLOG D in response to the oomycete Phytophthora brassicae. Interestingly, oligogalacturonide elicitation in pad2-1 revealed a lower plasma membrane depolarization that was found to act upstream of an impaired hydrogen peroxide production. This impaired hydrogen peroxide production was also observed during pathogen infection and correlated with a reduced hypersensitive response in pad2-1. In addition, a lack of pathogen-triggered expression of the ISOCHORISMATE SYNTHASE1 gene, coding for the SA-biosynthetic enzyme isochorismate synthase, was identified as the cause of the SA deficiency in pad2-1. Together, our results indicate that the pad2-1 mutation is related to a decrease in GCL protein and that the resulting glutathione deficiency negatively affects important processes of disease resistance.</AbstractText>
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