Arabidopsis GLUTATHIONE REDUCTASE1 Plays a Crucial Role in Leaf Responses to Intracellular Hydrogen Peroxide and in Ensuring Appropriate Gene Expression through Both Salicylic Acid and Jasmonic Acid Signaling Pathways

• Published in: Plant physiology (Bethesda) 2010-07, Vol.153 (3), p.1144-1160
• Main Authors: Mhamdi, Amna, Hager, Jutta, Chaouch, Sejir, Queval, Guillaume, Han, Yi, Taconnat, Ludivine, Saindrenan, Patrick, Gouia, Houda, Issakidis-Bourguet, Emmanuelle, Renou, Jean-Pierre, Noctor, Graham
• Format: Article
• Language: English
• Subjects: Antioxidants - metabolism; Arabidopsis - drug effects; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - microbiology; Ascorbic Acid - metabolism; Biological and medical sciences; Cyclopentanes - pharmacology; DNA, Bacterial - genetics; ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS; Enzymes; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Profiling; Gene Expression Regulation, Plant - drug effects; Genes; Genetic mutation; Glutathione - metabolism; Glutathione Reductase - genetics; Glutathione Reductase - metabolism; Hydrogen Peroxide - metabolism; Intracellular Space - drug effects; Intracellular Space - enzymology; Mutagenesis, Insertional - drug effects; Mutagenesis, Insertional - genetics; Mutation - genetics; Oligonucleotide Array Sequence Analysis; Oxidative stress; Oxidative Stress - drug effects; Oxidative Stress - genetics; Oxylipins - pharmacology; Phenotypes; Photoperiod; Plant cells; Plant growth; Plant Leaves - cytology; Plant Leaves - drug effects; Plant Leaves - enzymology; Plant Leaves - genetics; Plant physiology and development; Plants; RNA, Messenger - genetics; RNA, Messenger - metabolism; Salicylic Acid - pharmacology; Signal Transduction - drug effects; Signal Transduction - genetics
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.110.153767

Glutathione is a major cellular thiol that is maintained in the reduced state by glutathione reductase (GR), which is encoded by two genes in Arabidopsis (Arabidopsis thaliana; GR1 and GR2). This study addressed the role of GR1 in hydrogen peroxide (H₂O₂) responses through a combined genetic, transcriptomic, and redox profiling approach. To identify the potential role of changes in glutathione status in H₂O₂ signaling, gr1 mutants, which show a constitutive increase in oxidized glutathione (GSSG), were compared with a catalase-deficient background (cat2), in which GSSG accumulation is conditionally driven by H₂O₂. Parallel transcriptomics analysis of gr1 and cat2 identified overlapping gene expression profiles that in both lines were dependent on growth daylength. Overlapping genes included phytohormone-associated genes, in particular implicating glutathione oxidation state in the regulation of jasmonic acid signaling. Direct analysis of H₂O₂-glutathione interactions in cat2 gr1 double mutants established that GR1-dependent glutathione status is required for multiple responses to increased H₂O₂ availability, including limitation of lesion formation, accumulation of salicylic acid, induction of pathogenesis-related genes, and signaling through jasmonic acid pathways. Modulation of these responses in cat2 gr1 was linked to dramatic GSSG accumulation and modified expression of specific glutaredoxins and glutathione S-transferases, but there is little or no evidence of generalized oxidative stress or changes in thioredoxin-associated gene expression. We conclude that GR1 plays a crucial role in daylength-dependent redox signaling and that this function cannot be replaced by the second Arabidopsis GR gene or by thiol systems such as the thioredoxin system.