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      

Abstract

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.

Glutathione – linking cell proliferation to oxidative stress

“…In its classic function as an antioxidant, GSH serves to remove ROS and hence limit the lifetime of the oxidative signal. However, accumulating molecular genetic evidence suggests that GSH is also important in potentiating ROS signals in plants, particularly through interactions with plant stress hormones such as salicylic acid (SA) and jamonic acid (11)(12)(13).…”

“…The gr1 mutants show enhanced susceptibility to pathogens suggesting that GR1 is essential for redox signalling through the plant hormone-mediated defence pathways (11)(12)(13)76). Characterization of mutants such as the clt mutants that are deficient in the cytosolic GSH (37) and gr1cat2 double mutants that lack both GR1 and the major form of leaf catalase (cat2; 76) have shown that the cytosolic GSH pool per se plays a crucial role in linking ROS signalling to downstream pathogen responses and associated hormone-dependent pathways (11-13, 37).…”

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

“…The photosynthetic electron transport chain generates a number of powerful oxidants, including singlet oxygen in PSII and superoxide and hydrogen peroxide in PSI as a result of electron transfer to oxygen [11]. Singlet oxygen and hydrogen peroxide are important regulators of gene expression that interface with hormone signalling pathways to mediate changes in plant morphology, development and defence [8][9][10][11][12][13][14]. These oxidative signals are considered to function alongside signals arising from changes in the reduction state of the PQ pool to regulate the expression of genes involved in photosynthesis and defence.…”

“…Redox-mediated regulation of chloroplast gene expression is controlled through the phosphorylation of the s-factor called Sig1, which is triggered by oxidization of the PQ pool to regulate expression of the psaA and psaB genes, a process requiring the synergistic activation of thiol signals [25,26,32]. Thiol redox systems involving GSH, thioredoxins, glutaredoxins and peroxiredoxins are widely used as integrators of cellular functions, including electron transport and metabolism, and the linking of photosynthetic functions to gene transcription and translation, protein synthesis and degradation [11][12][13]31]. Peroxiredoxins, which use thioredoxins as a reductant, complement the well-studied glutathione/ascorbate system in peroxide elimination, redox regulation and signalling [11].…”

“…Cross-tolerance occurs because of the synergistic co-activation of non-specific, stress-responsive pathways that cross biotic-abiotic stress boundaries [9,10]. Cross-tolerance phenomena are often associated with the accumulation of reactive oxygen species (ROS) and altered redox and phytohormone signalling, particularly through ethylene (ET), salicylic acid (SA), abscisic acid (ABA) and jasmonate (JA)-mediated pathways [11][12][13][14]. Chloroplasts play an important role in redox signalling events linking light acclimation responses to immunity to pathogens as well as in the synthesis of important plant hormones such as ABA, JA and strigolactones [5][6][7][8][9][10][11][15][16][17].…”