<i>S</i>-Nitrosylation Positively Regulates Ascorbate Peroxidase Activity during Plant Stress Responses

Yang, Huanjie; Mu, Jinye; Chen, Lichao; Feng, Jian; Hu, Jiliang; Li, Lei; Zhou, Jian‐Min; Zuo, Jianru

doi:10.1104/pp.114.255216

Cited by 225 publications

(144 citation statements)

References 59 publications

(101 reference statements)

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“…They illustrate that $NO and ROS signaling can underlay synergistic or antagonistic mechanisms or function in parallel. Moreover, the observations by Yang et al (2015) support the notion that $NO-based modifications of antioxidant enzymes play a key role in the regulation of oxidative stress and ROS homeostasis and provide evidence for a molecular mechanism of the sensor-effector relationship between $NO and ROS. Although the $NO research starts to focus on oxidative stress and redox signaling mediated by ROS, we will probably never be able to solve all $NO and ROS interactions, but we should and we can identify critical interfaces, such as the interaction of $NO with ascorbate peroxidase.…”

supporting

confidence: 59%

“…The cycle involves the antioxidant metabolites: ascorbate, glutathione, and NADPH and the enzymes linking these metabolites, among them ascorbate oxidase (Noctor and Foyer, 1998). In this issue, Yang et al (2015) add a new and important aspect to the interplay of $NO and ROS metabolism and control: the regulation of the ROSdegrading enzyme ascorbate peroxidase by nitric oxide. They demonstrated that $NO positively regulates the activity of cytosolic ASCORBATE PEROXIDASE1 by S-nitrosylation of Cys-32.…”

mentioning

confidence: 99%

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Interplay of Reactive Oxygen Species and Nitric Oxide: Nitric Oxide Coordinates Reactive Oxygen Species Homeostasis

Lindermayr

Durner

2015

Plant Physiol.

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Redox reactions are evolutionarily a very old signaling principle, which occur in prokaryotes and eukaryotes. The most important redox molecules are reactive oxygen species (ROS), such as singlet oxygen, hydroxyl radical, superoxide anion, hydrogen peroxide, and nitric oxide ($NO). In plants, they have very important signaling functions and are involved in the regulation of transpiration, gas exchange, plant defense response, cell death, germination, and plant growth and development. The diverse functions may be explained by the fact that ROS and $NO interact rapidly to form a number of reactive nitrogen species, such as ONOO 2 , NO 2 , N 2 O 3 , and other NO x species. Besides the direct interactions of these redox molecules, both molecules can act as oxidizing agents on proteins, and in this way they can modify the activity or function of proteins involved in $NO and ROS signaling as well as metabolism and homeostasis.The first evidence for a physiological interplay between $NO and ROS was provided by Delledonne et al. (2001). They demonstrated that hypersensitive cell death is only triggered by balanced production of $NO and ROS and that interaction of $NO with hydrogen peroxide is required. Additionally, as part of the innate immune response in Arabidopsis (Arabidopsis thaliana), $NO inhibits NADPH oxidase and regulates cell death (Yun et al., 2011). Moreover, in guard cells, $NO and ROS act in concert with abscisic acid during stomatal closure (Bright et al., 2006).Physiologically, ROS and $NO have both beneficial and deleterious effects, depending upon the concentration and exposure time. Plants have developed effective mechanisms to control ROS levels, protecting themselves from oxidative damage on one side, and they also use ROS as signaling molecules on the other side. ROS are detoxified by the glutathione-ascorbate cycle. The cycle involves the antioxidant metabolites: ascorbate, glutathione, and NADPH and the enzymes linking these metabolites, among them ascorbate oxidase (Noctor and Foyer, 1998). In this issue, Yang et al. (2015) add a new and important aspect to the interplay of $NO and ROS metabolism and control: the regulation of the ROSdegrading enzyme ascorbate peroxidase by nitric oxide. They demonstrated that $NO positively regulates the activity of cytosolic ASCORBATE PEROXIDASE1 by S-nitrosylation of Cys-32. S-Nitrosylation of this residue results in an enhanced resistance to oxidative stress and positively affects the immune response. Interestingly, pea (Pisum sativum) cytosolic ASCORBATE PEROXI-DASE1 is regulated by $NO in a dual way. While S-nitrosylation enhances its activity, Tyr nitration results in inhibition (Begara-Morales et al., 2014), demonstrating the complexity of the $NO and ROS interplay.A connection between $NO and ROS has also been demonstrated for other antioxidant enzymes, such as peroxiredoxin II E and superoxide dismutase. S-Nitrosylation of Arabidopsis peroxiredoxin II E inhibits its hydrogen peroxide-reducing and peroxinitrite-detoxifying activities, and in this way, ...

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supporting

confidence: 59%

mentioning

confidence: 99%

Interplay of Reactive Oxygen Species and Nitric Oxide: Nitric Oxide Coordinates Reactive Oxygen Species Homeostasis

Lindermayr

Durner

2015

Plant Physiol.

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“…S-nitrosylation of SABP3 suppresses its binding with salicylic acid and the enzymatic activity during the hypersensitive response, whereas S-nitrosylation of FBA6 negatively regulates its enzymatic activity van der Linde et al, 2011). S-Nitrosylation of APX1 enhances its enzymatic activity in response to oxidative stresses (Yang et al, 2015).…”

Section: Resultsmentioning

confidence: 99%

Site-Specific Nitrosoproteomic Identification of EndogenouslyS-Nitrosylated Proteins in Arabidopsis

et al. 2015

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Nitric oxide (NO) regulates multiple developmental events and stress responses in plants. A major biologically active species of NO is S-nitrosoglutathione (GSNO), which is irreversibly degraded by GSNO reductase (GSNOR). The major physiological effect of NO is protein S-nitrosylation, a redox-based posttranslational modification mechanism by covalently linking an NO molecule to a cysteine thiol. However, little is known about the mechanisms of S-nitrosylation-regulated signaling, partly due to limited S-nitrosylated proteins being identified. In this study, we identified 1,195 endogenously S-nitrosylated peptides in 926 proteins from the Arabidopsis (Arabidopsis thaliana) by a site-specific nitrosoproteomic approach, which, to date, is the largest data set of S-nitrosylated proteins among all organisms. Consensus sequence analysis of these peptides identified several motifs that contain acidic, but not basic, amino acid residues flanking the S-nitrosylated cysteine residues. These S-nitrosylated proteins are involved in a wide range of biological processes and are significantly enriched in chlorophyll metabolism, photosynthesis, carbohydrate metabolism, and stress responses. Consistently, the gsnor1-3 mutant shows the decreased chlorophyll content and altered photosynthetic properties, suggesting that S-nitrosylation is an important regulatory mechanism in these processes. These results have provided valuable resources and new clues to the studies on S-nitrosylation-regulated signaling in plants.

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“…6F). Transgenic plants with reduced protein levels or activities of CAT and APX revealed accumulations of H 2 O 2 , an early event in PCD (Dat et al, 2003), and cytosolic APX was found to be S-nitrosylated at the onset of PCD (de Pinto et al, 2013;Lindermayr and Durner, 2015;Yang et al, 2015). The enhanced S-nitrosylation of CAT and APX in the NE genotype upon ozone fumigation may analogically lead to increased H 2 O 2 levels compared with the IE genotype.…”

Section: Target Sites Of No Action In Ie and Ne Gray Poplarmentioning

confidence: 95%

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

et al. 2016

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ORCID IDs: 0000-0002-3422-4083 (J.M.-P.); 0000-0001-8410-5624 (J.B.); 0000-0002-9825-867X (J.-P.S.).Researchers have been examining the biological function(s) of isoprene in isoprene-emitting (IE) species for two decades. There is overwhelming evidence that leaf-internal isoprene increases the thermotolerance of plants and protects them against oxidative stress, thus mitigating a wide range of abiotic stresses. However, the mechanisms of abiotic stress mitigation by isoprene are still under debate. Here, we assessed the impact of isoprene on the emission of nitric oxide (NO) and the S-nitroso-proteome of IE and non-isoprene-emitting (NE) gray poplar (Populus 3 canescens) after acute ozone fumigation. The short-term oxidative stress induced a rapid and strong emission of NO in NE compared with IE genotypes. Whereas IE and NE plants exhibited under nonstressful conditions only slight differences in their S-nitrosylation pattern, the in vivo S-nitroso-proteome of the NE genotype was more susceptible to ozone-induced changes compared with the IE plants. The results suggest that the nitrosative pressure (NO burst) is higher in NE plants, underlining the proposed molecular dialogue between isoprene and the free radical NO. Proteins belonging to the photosynthetic light and dark reactions, the tricarboxylic acid cycle, protein metabolism, and redox regulation exhibited increased S-nitrosylation in NE samples compared with IE plants upon oxidative stress. Because the posttranslational modification of proteins via S-nitrosylation often impacts enzymatic activities, our data suggest that isoprene indirectly regulates the production of reactive oxygen species (ROS) via the control of the S-nitrosylation level of ROS-metabolizing enzymes, thus modulating the extent and velocity at which the ROS and NO signaling molecules are generated within a plant cell.It has been demonstrated that isoprene protects plants against a plethora of abiotic stresses (Singsaas et al., 1997;Behnke et al., 2007;Velikova et al., 2008;Vickers et al., 2009b). Since the discovery of the positive influence of isoprene emission on plants' photosynthetic processes in the early 1990s (Sharkey and Singsaas, 1995), many efforts have been made to explain the primary mechanism of isoprene functioning. Most attention was given to the hypothesis that isoprene improves the thermotolerance of the photosynthetic machinery by stabilizing chloroplast (thylakoid) membranes during short, high-temperature episodes (Sharkey and Singsaas, 1995;Loreto and Schnitzler, 2010). Successive studies underlined that isoprene helps maintain high rates of chloroplastic electron transport and CO 2 assimilation during heat stress and accelerates recovery from stress (Singsaas and Sharkey, 2000;Velikova et al., 2006;Behnke et al., 2010b;Way et al., 2011).One mechanistic explanation is that isoprene molecules are dissolved in thylakoid membrane and prevent membrane lipid denaturation following oxidative stress (Sharkey and Yeh, 2001). It was suggested that isoprene acts directly to st...

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S-Nitrosylation Positively Regulates Ascorbate Peroxidase Activity during Plant Stress Responses

Cited by 225 publications

References 59 publications

Interplay of Reactive Oxygen Species and Nitric Oxide: Nitric Oxide Coordinates Reactive Oxygen Species Homeostasis

Interplay of Reactive Oxygen Species and Nitric Oxide: Nitric Oxide Coordinates Reactive Oxygen Species Homeostasis

Site-Specific Nitrosoproteomic Identification of EndogenouslyS-Nitrosylated Proteins in Arabidopsis

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

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