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.
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 (H(2)O(2)) responses through a combined genetic, transcriptomic, and redox profiling approach. To identify the potential role of changes in glutathione status in H(2)O(2) 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 H(2)O(2). 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 H(2)O(2)-glutathione interactions in cat2 gr1 double mutants established that GR1-dependent glutathione status is required for multiple responses to increased H(2)O(2) 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.
Mhamdi
Amna
A
Institut de Biologie des Plantes, UMR8618 CNRS, Université de Paris Sud, 91405 Orsay cedex, France.
Hager
Jutta
J
Chaouch
Sejir
S
Queval
Guillaume
G
Han
Yi
Y
Taconnat
Ludivine
L
Saindrenan
Patrick
P
Gouia
Houda
H
Issakidis-Bourguet
Emmanuelle
E
Renou
Jean-Pierre
JP
Noctor
Graham
G
D000975:Antioxidants / Q000378:metabolism; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics / Q000382:microbiology; D001205:Ascorbic Acid / Q000378:metabolism; D003517:Cyclopentanes / Q000494:pharmacology*; D004269:DNA, Bacterial / Q000235:genetics; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects*; D005978:Glutathione / Q000378:metabolism; D005980:Glutathione Reductase / Q000235:genetics / Q000378:metabolism*; D006861:Hydrogen Peroxide / Q000378:metabolism*; D042541:Intracellular Space / Q000187:drug effects / Q000201:enzymology; D016254:Mutagenesis, Insertional / Q000187:drug effects / Q000235:genetics; D009154:Mutation / Q000235:genetics; D020411:Oligonucleotide Array Sequence Analysis; D018384:Oxidative Stress / Q000187:drug effects / Q000235:genetics; D054883:Oxylipins / Q000494:pharmacology*; D018515:Plant Leaves / Q000166:cytology / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D020156:Salicylic Acid / Q000494:pharmacology*; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics
D000975:Antioxidants; D003517:Cyclopentanes; D004269:DNA, Bacterial; D054883:Oxylipins; D012333:RNA, Messenger; C036483:T-DNA; C011006:jasmonic acid; D006861:Hydrogen Peroxide; D005980:Glutathione Reductase; D005978:Glutathione; D020156:Salicylic Acid; D001205:Ascorbic Acid