ROS-Mediated Inhibition of S-nitrosoglutathione Reductase Contributes to the Activation of Anti-oxidative Mechanisms

Kovács, Izabella; Holzmeister, Christian; Wirtz, Markus; Geerlof, Arie; Fröhlich, Thomas; Römling, Gaby; Kuruthukulangarakoola, Gitto Thomas; Linster, Eric; Hell, Rüdiger; Arnold, Georg J.; Durner, Joerg; Lindermayr, Christian

doi:10.3389/fpls.2016.01669

Cited by 57 publications

(44 citation statements)

References 81 publications

(93 reference statements)

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“…This low H 2 O 2 level may be associated with the significantly (3-fold) increased total glutathione content of this line ( Fig 6B). Kovács et al (2016) also observed increased glutathione content in gsnor1-3 compared to the WT, but using 3,3'-diaminobenzidine staining similar H 2 O 2 levels were detected in gsnor1-3 and the WT. It is also interesting that Zn did not modify glutathione levels in the WT and 35S::FLAG-GSNOR1 plants, but significantly decreased the relatively high glutathione content in gsnor1-3.…”

Section: Zn-induced H 2 O 2 Is Directly Involved In Gsnor Inactivationsupporting

confidence: 52%

“…Regarding its protein structure, GSNOR is rich in Cys residues and contains two Zn ions per subunit, one of which has catalytic whereas the other, a structural role (Lindermayr 2018). A direct interaction between H 2 O 2 and GSNOR was revealed when the H 2 O 2 inducer (paraquat) triggered oxidative modification of Cys residues in the active site (Cys177, Cys47), causing release of Zn 2+ from the catalytic site of the enzyme leading to its inactivation (Kovács et al 2016). Additional Cys residues (e.g.…”

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confidence: 99%

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S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

Kolbert

Feigl

et al. 2019

Plant and Cell Physiology

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Accumulation of heavy metals such as zinc (Zn) disturbs the metabolism of reactive oxygen (e.g. hydrogen peroxide, H2O2) and nitrogen species (e.g. nitric oxide, NO; S-nitrosoglutathione, GSNO) in plant cells; however, their signal interactions are not well understood. Therefore, this study examines the interplay between H2O2 metabolism and GSNO signaling in Arabidopsis. Comparing the Zn tolerance of the wild type (WT), GSNO reductase (GSNOR) overexpressor 35S::FLAG-GSNOR1 and GSNOR-deficient gsnor1-3, we observed relative Zn tolerance of gsnor1-3, which was not accompanied by altered Zn accumulation capacity. Moreover, in gsnor1-3 plants Zn did not induce NO/S-nitrosothiol (SNO) signaling, possibly due to the enhanced activity of NADPH-dependent thioredoxin reductase. In WT and 35S::FLAG-GSNOR1, GSNOR was inactivated by Zn, and Zn-induced H2O2 is directly involved in the GSNOR activity loss. In WT seedlings, Zn resulted in a slight intensification of protein nitration detected by Western blot and protein S-nitrosation observed by resin-assisted capture of SNO proteins (RSNO-RAC). LC-MS/MS analyses indicate that Zn induces the S-nitrosation of ascorbate peroxidase 1. Our data collectively show that Zn-induced H2O2 may influence its own level, which involves GSNOR inactivation-triggered SNO signaling. These data provide new evidence for the interplay between H2O2 and SNO signaling in Arabidopsis plants affected by metal stress.

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Section: Zn-induced H 2 O 2 Is Directly Involved In Gsnor Inactivationsupporting

confidence: 52%

mentioning

confidence: 99%

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

Kolbert

Feigl

et al. 2019

Plant and Cell Physiology

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“…Our data underscore the complexity of redox regulation in the biochemically intricate environment of the plant cell. They add to studies implicating changes of GSNOR activities in response to stress conditions such as MV, exogenous H 2 O 2 , nitrogen stress, and hypoxia, conditions in which redox‐based modification of the protein has previously been described (Chen et al, ; Frungillo et al, ; Kovacs et al, ; Tichá et al, ; Zhan et al, ). Although we note in previous reports that GSNOR1 activity may be inhibited by H 2 O 2 in vitro (Kovacs et al, ; Tichá et al, ), such effects may be counteracted in cat2 by up‐regulation of the amount of GSNOR1 protein (Figure ) or simply not operative because H 2 O 2 accumulation inside the cell is restricted to localized subcellular areas, transient in nature, and unlikely to greatly exceed values of about 10 μM (Han et al, ; Mhamdi et al, ; Rahantaniaina et al, ; Tuzet et al, ; Xu, Guerra, Lee, & Vierling, ).…”

Section: Discussionmentioning

confidence: 93%

Glutathione‐dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H₂O₂

Zhang

Chen

et al. 2020

Plant Cell & Environment

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Photorespiratory hydrogen peroxide (H2O2) plays key roles in pathogenesis responses by triggering the salicylic acid (SA) pathway in Arabidopsis. However, factors linking intracellular H2O2 to activation of the SA pathway remain elusive. In this work, the catalase‐deficient Arabidopsis mutant, cat2, was exploited to elucidate the impact of S‐nitrosoglutathione reductase 1 (GSNOR1) on H2O2‐dependent signalling pathways. Introducing the gsnor1‐3 mutation into the cat2 background increased S‐nitrosothiol levels and abolished cat2‐triggered cell death, SA accumulation, and associated gene expression but had little additional effect on the major components of the ascorbate‐glutathione system or glycolate oxidase activities. Differential transcriptome profiles between gsnor1‐3 and cat2 gsnor1‐3 together with damped ROS‐triggered gene expression in cat2 gsnor1‐3 further indicated that GSNOR1 acts to mediate the SA pathway downstream of H2O2. Up‐regulation of GSNOR activity was compromised in cat2 cad2 and cat2 pad2 mutants in which glutathione accumulation was genetically prevented. Experiments with purified recombinant GSNOR revealed that the enzyme is posttranslationally regulated by direct denitrosation in a glutathione‐dependent manner. Together, our findings identify GSNOR1‐controlled nitrosation as a key factor in activation of the SA pathway by H2O2 and reveal that glutathione is required to maintain this biological function.

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“…Cysteines are also modified by gluthionylation and S ‐nitrosylation. These modifications interact with H 2 O 2 signalling (Kovacs et al ., ).…”

Section: H2o2 Signallingmentioning

confidence: 97%

Hydrogen peroxide metabolism and functions in plants

2018

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1 I. Introduction 2 II. Measurement and imaging of H O 2 III. H O and O toxicity 3 IV. Production of H O : enzymes and subcellular locations 4 V. H O transport 9 VI. Control of H O concentration: how and where? 9 VII. Metabolic functions of H O 11 VIII. H O signalling 11 IX. Where next? 13 Acknowledgements 13 References 13 SUMMARY: Hydrogen peroxide (H O ) is produced, via superoxide and superoxide dismutase, by electron transport in chloroplasts and mitochondria, plasma membrane NADPH oxidases, peroxisomal oxidases, type III peroxidases and other apoplastic oxidases. Intracellular transport is facilitated by aquaporins and H O is removed by catalase, peroxiredoxin, glutathione peroxidase-like enzymes and ascorbate peroxidase, all of which have cell compartment-specific isoforms. Apoplastic H O influences cell expansion, development and defence by its involvement in type III peroxidase-mediated polymer cross-linking, lignification and, possibly, cell expansion via H O -derived hydroxyl radicals. Excess H O triggers chloroplast and peroxisome autophagy and programmed cell death. The role of H O in signalling, for example during acclimation to stress and pathogen defence, has received much attention, but the signal transduction mechanisms are poorly defined. H O oxidizes specific cysteine residues of target proteins to the sulfenic acid form and, similar to other organisms, this modification could initiate thiol-based redox relays and modify target enzymes, receptor kinases and transcription factors. Quantification of the sources and sinks of H O is being improved by the spatial and temporal resolution of genetically encoded H O sensors, such as HyPer and roGFP2-Orp1. These H O sensors, combined with the detection of specific proteins modified by H O , will allow a deeper understanding of its signalling roles.

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ROS-Mediated Inhibition of S-nitrosoglutathione Reductase Contributes to the Activation of Anti-oxidative Mechanisms

Cited by 57 publications

References 81 publications

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

Glutathione‐dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H₂O₂

Hydrogen peroxide metabolism and functions in plants

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ROS-Mediated Inhibition of S-nitrosoglutathione Reductase Contributes to the Activation of Anti-oxidative Mechanisms

Cited by 57 publications

References 81 publications

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

Glutathione‐dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H2O2

Hydrogen peroxide metabolism and functions in plants

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Glutathione‐dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H₂O₂