Redox state as a central regulator of plant cell stress responses

Dharmendra K. Gupta José M. Palma Francisco J. Corpas Editors Redox State as a Central Regulator of Plant-Cell Stress Responses Redox State as a Central Regulator of Plant-Cell Stress Responses Dharmendra K Gupta José M Palma Francisco J Corpas • Editors Redox State as a Central Regulator of Plant-Cell Stress Responses 123 Editors Dharmendra K Gupta Institut für Radioökologie und Strahlenschutz (IRS) Gottfried Wilhelm Leibniz Universität Hannover Germany Francisco J Corpas Estación Experimental del Zaidín (EEZ-CSIC) Granada Spain José M Palma Estación Experimental del Zaidín (EEZ-CSIC) Granada Spain ISBN 978-3-319-44080-4 DOI 10.1007/978-3-319-44081-1 ISBN 978-3-319-44081-1 (eBook) Library of Congress Control Number: 2016947790 © Springer International Publishing Switzerland 2016 This work is subject to copyright All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed The use of general descriptive names, registered names, trademarks, service marks, etc in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG Switzerland Preface It is known that reactive oxygen species (ROS) are the by-products of aerobic breakdown and are inescapably formed by a number of metabolic pathways and electron transport chains ROS are partially condensed form of molecular oxygen and normally result from the transfer of electrons to O2 to form, in a succession of univalent reductions, superoxide radical (O2Á−), hydrogen peroxide (H2O2), and hydroxyl radical (•OH), respectively, or through an electron-independent energy transfer till an excited form of oxygen (singlet oxygen) (Gupta et al 2016; Halliwell and Gutteridge 2015) Redox signal transduction is a complete feature of aerobic life enriched through evolution to balance evidence from metabolism and the environment Like all other aerobic creatures, plants maintain most cytosolic thiols in the reduced (−SH) state because of the low thioldisulfide redox potential imposed by millimolar amount of the thiol buffer including glutathione Plants have developed cellular tactics where the endogenous content of antioxidant enzymes deliver them with amplified defense against harmful effects of oxidative stress encouraged by heavy metal and other stress sources (Palma et al 2013) Stress-induced upsurges in ROS level can cause different degree of oxidation of cell components and a gross change in the redox status Plant cells generally cope very well with high rates of generation of superoxide, H2O2, and even singlet oxygen When the increment of ROS in plant cells quickly augments and the scavenging systems of ROS not operate appropriately, a condition of oxidative stress and oxidative injury happens (Gupta et al 2015) In plants, chloroplast is the most important among the organelles in respect of ROS generation as O2 is constantly provided through the water autolysis and freely available inside the organelle (Gupta et al 2015) In plant cells, compartmentalization of ROS production in the different organelles includes chloroplasts, mitochondria, or peroxisomes, and they also have a complex battery of antioxidant enzymes usually close to the site of ROS production (Corpas et al 2015) Plant cells also contain a series of ROS-scavenging non-enzymatic antioxidants such as ascorbic acid, glutathione (GSH), and carotenoids, as well as a set of enzymes such as superoxide dismutase (SOD), catalase, glutathione peroxidase (GPX), peroxiredoxin (Prx), and the v vi Preface ascorbate–glutathione cycle (Corpas et al 2015) The total pool of redox-active complexes which are found in a cell in reduced and oxidized forms generates cellular redox buffers where NAD(P)H/NAD(P)+, ascorbate/dehydroascorbate (AsA/DHA), glutathione/glutathione disulfide (GSH/GSSG), and reduced thioredoxin/oxidized thioredoxin (Trxred/Trxox) are the main pairs AsA and GSH are major constituents of the soluble redox shielding system, and they contribute pointedly to the redox environment of a cell AsA cooperates tightly with GSH (c-Glu-Cys-Gly) in the Foyer–Halliwell–Asada cycle (ascorbate–glutathione cycle), involving three codependent redox couples: AsA/DHA, GSH/GSSG, and NAD(P)H/NAD(P)+ It undertakes subsequent reduction/oxidation reactions catalyzed by ascorbate peroxidase (APX), monodehydroascorbate reductase (MDAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR) that is universally responsible for H2O2 sifting and keeping AsA and GSH in the reduced state at the outflow of NADPH, this cycle being situated in all cellular partitions in which ROS detoxification is required One of the major consequences of stresses in plant cells is the enhanced generation of ROS which usually damage the cellular components such as membranes, nucleic acids, proteins, chloroplast pigments, and alteration in enzymatic and non-enzymatic antioxidants The molecular mechanisms of signal transduction corridors in higher plant cells are vital for processes such as hormone and light sensitivity, growth, development, stress resistance, and nutrient uptake from soil and water (Gupta et al 2013) It is really great achievement for the plant biotechnologists who are working for years to know how redox state handled by plants This edited volume will provide the recent advancements and overview to the plant scientists who are actively involved in redox signaling states and also a key player for cellular tolerance in plant cells under different stresses (biotic and abiotic) Other key features of this book are cellular redox homeostasis as central modulator, redox homeostasis and reactive oxygen species, redox balance in chloroplasts and in mitochondria, and oxidative stress and its role in peroxisome homeostasis Some chapters are also focusing on glutathione-related enzyme system and metabolism under metal(ed) stress Abiotic stress-induced redox changes and programmed cell death are also addressed in the edition In summary, the information compiled in this volume will bring depth knowledge and current achievements in the field of redox state chemistry in plant cell Dr Dharmendra K Gupta, Prof José M Palma, and Dr Francisco J Corpas individually thank all authors for contributing their valuable time, knowledge, and enthusiasm to bring this book into in the current shape Hannover, Germany Granada, Spain Granada, Spain Dharmendra K Gupta José M Palma Francisco J Corpas Preface vii References Corpas FJ, Gupta DK, Palma JM (2015) Production sites of reactive oxygen species (ROS) in plants In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress Springer Publication, Germany, p 1–22 Gupta DK, Corpas FJ, Palma JM (2013) Heavy metal stress in plants Springer-Verlag, Germany Gupta DK, Palma JM, Corpas FJ (2015) Reactive oxygen species and oxidative damage in plants under stress Springer-Verlag, Germany Gupta DK, Peña LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2016) NADPH oxidases differently regulates ROS metabolism and nutrient uptake under cadmium toxicity Plant Cell Environ doi:10.1111/pce.12711 Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine Oxford University Press, Oxford, UK Palma JM, Gupta DK, Corpas FJ (2013) Metalloproteins involved in the metabolism of Reactive Oxygen Species (ROS) and heavy metal stress In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants Springer Publication, Germany, p 1–18 Contents Cellular Redox Homeostasis as Central Modulator in Plant Stress Response C Paciolla, A Paradiso and M.C de Pinto Plant Cell Redox Homeostasis and Reactive Oxygen Species A Trchounian, M Petrosyan and N Sahakyan Redox Balance in Chloroplasts as a Modulator of Environmental Stress Responses: The Role of Ascorbate Peroxidase and Nudix Hydrolase in Arabidopsis T Ishikawa, T Maruta, T Ogawa, K Yoshimura and S Shigeoka 25 51 Physiological Processes Contributing to the Synthesis of Ascorbic Acid in Plants C.G Bartoli, M.E Senn and G.E Gergoff Grozeff 71 Redox State in Plant Mitochondria and its Role in Stress Tolerance N.V Bykova and A.U Igamberdiev 93 Oxidative Stress and its Role in Peroxisome Homeostasis in Plants 117 T Su, Q Shao, P Wang and C Ma Glutathione-Related Enzyme System: Glutathione Reductase (GR), Glutathione Transferases (GSTs) and Glutathione Peroxidases (GPXs) 137 J Csiszár, E Horváth, K Bela and Á Gallé Glutathione Metabolism in Plants Under Metal and Metalloid Stress and its Impact on the Cellular Redox Homoeostasis 159 Luis E Hernández, A González, A Navazas, Á Barón-Sola, F Martínez, A Cuypers and C Ortega-Villasante ix x Contents Glutathione and Related Enzymes in Response to Abiotic Stress 183 I Štolfa, D Špoljarić Maronić, T Žuna Pfeiffer and Z Lončarić 10 The Function of Cellular Redox Homeostasis and Reactive Oxygen Species (ROS) in Plants Tolerance to Abiotic Stresses 213 Qinghua Shi and Biao Gong 11 Abiotic Stress-Induced Redox Changes and Programmed Cell Death in Plants—A Path to Survival or Death? 233 S.R Kumar, G Mohanapriya and R Sathishkumar 12 The Role of ROS and Redox Signaling During the Initial Cellular Response to Abiotic Stress 253 Jos H.M Schippers and R Schmidt 13 The Cadmium-Binding Thioredoxin O Acts as an Upstream Regulator of the Redox Plant Homeostasis 275 Moêz Smiri, Sami Boussami, Takwa Missaoui and Amor Hafiane 14 Arsenic Tolerance in Plants: Cellular Maneuvering Through Sulfur Metabolites 297 D Talukdar 15 Regulation of Stomatal Responses to Abiotic and Biotic Stresses by Redox State 331 Y Murata, S Munemasa and I.C Mori 16 The Antioxidant Power of Arginine/Nitric Oxide Attenuates Damage Induced by Methyl Viologen Herbicides in Plant Cells 349 N Correa-Aragunde, P Negri, F Del Castello, N Foresi, J.C Polacco and L Lamattina 17 Protein S-Nitrosylation and S-Glutathionylation as Regulators of Redox Homeostasis During Abiotic Stress Response 365 J.C Begara-Morales, B Sánchez-Calvo, M Chaki, R Valderrama, C Mata-Pérez, F.J Corpas and J.B Barroso About the Editors Dharmendra K Gupta is a senior environmental biotechnology scientist at the Institut für Radioökologie und Strahlenschutz, Gottfried Wilhelm Leibniz Universität Hannover in Germany and has published more than 80 research papers/review articles in peer reviewed journals and has edited nine books His research interests include abiotic stress by heavy metals/radionuclides and xenobiotics in plants; antioxidative system in plants, and environmental pollution (heavy metal/radionuclide) remediation through plants (phytoremediation) José M Palma has more than 30 years experience in plant sciences and related fields He also served as the deputy director and later director of the Estación Experimental del Zaidín (EEZ-CSIC), Granada, Spain He has published more than 100 research papers/review articles in peer reviewed journals and edited five books Francisco J Corpas is a staff member at the Spanish National Research Council (CSIC) and has more than 24 years of research experience in the metabolism of antioxidants and nitric oxide in higher plants under physiological and adverse environmental conditions At present, he is the head of the Department of Biochemistry, Cell and Molecular Biology of Plants at the research institute Estación Experimental del Zaidín-CSIC in Granada, Spain He has published more than 120 research papers/review articles in peer reviewed journals and has edited five books xi 372 J.C Begara-Morales et al plant/tissue/organelles analyzed, NaCl concentration, and extent of the stress generated (Fancy et al 2016) Tanou et al (2009, 2012) identified a pool of S-nitrosylated proteins under NaCl treatment in citrus plants, some of these proteins being related to redox metabolism such as ascorbate peroxidase (APX), iron-containing superoxide dismutase (Fe-SOD), monodehydroascorbate reductase (MDAR), or glutaredoxin However, no effect of this modification on protein activity and/or structure was reported Notably, Fe-SOD and Mn-SOD were also reported to be S-nitrosylated during development or after NaCl treatment, respectively, in pea mitochondria (Camejo et al 2013) However, the treatment of Mn-SOD with GSNO had no impact on protein activity (Camejo et al 2013), this being subsequently corroborated in vitro (Holzmeister et al 2015) Additionally, the peroxiredoxin PRxIIF was identified as a target of S-nitrosylation during salt stress with a negative impact on the protein activity (Camejo et al 2013, 2015) Interestingly, the peroxidase activity of PRxIIE is also inhibited after S-nitrosylation during hypersensitive response, and this inhibits its peroxynitrite reductase activity, promoting tyrosine nitration (Romero-Puertas et al 2007, 2008) Therefore, S-nitrosylation emerges as a crucial mechanism in ONOO− homeostasis via control of PRxIIE (Romero-Puertas et al 2007) As changes in ONOO− levels and tyrosine nitration have been reported in different abiotic stress situations, whether S-nitrosylation of PRxIIE might be involved in plant response to these stress conditions is a major issue to be addressed in the future The regulation of Asa–GSH cycle, a key mechanism to detoxify H2O2, under physiological and stress situations (Asada 1992; Noctor and Foyer 1998; Shigeoka et al 2002) by NO-PTMs is well documented (Begara-Morales et al 2015b) In this regard, although APX at Cys 32 and dehydroascorbate reductase (DHAR) at Cys 20 were identified as endogenously S-nitrosylated in Arabidopsis, they were not differentially S-nitrosylated after a short-term salt treatment (Fares et al 2011) However, after 4d of NaCl treatment, APX and MDAR were reported to be S-nitrosylated in pea leaves with different consequences for their activities While S-nitrosylation of APX at Cys 32 positively regulates its activity, inhibition of MDAR activity was observed after S-nitrosylation (Begara-Morales et al 2014b, 2015a) An increase in APX activity after S-nitrosylation has also been reported in different plant species under different conditions (Keyster et al 2011; Lin et al 2011; Correa-Aragunde et al 2013; Ullah et al 2016) Conversely, S-nitrosylation of APX after programmed cell death (PCD) induced by H2O2 or heat shock in tobacco cells inhibited its activity (de Pinto et al 2013), as previously reported (Clark et al 2000) These discrepancies could be due to a different Cys target of S-nitrosylation in these situations (Begara-Morales et al 2016) Recently, Yang et al (2015), using proteomic and mutagenesis approaches, demonstrated that S-nitrosylation of APX at Cys 32 positively regulates its activity in Arabidopsis and that this Cys plays an essential role in plant response to oxidative stress and plant immunity As a result, S-nitrosylation of Cys 32 appears to be responsible for increasing activity of APX under adverse environmental conditions Notably, pea glutathione reductase (GR) enzyme was found to be S-nitrosylated by GSNO, but 17 Protein S-Nitrosylation and S-Glutathionylation as Regulators … 373 had no significant impact on protein activity (Begara-Morales et al 2015a) In mammal cells, GR activity is inhibited after long exposure to GSNO (Beltrán et al 2000), and human GR is inhibited by S-nitrosylation after GSNO treatment(Becker et al 1995; Francescutti et al 1996), suggesting a different regulation of mammalian and pea GR Strikingly, APX is inhibited by tyrosine nitration, but GR remains unaffected, supporting the idea that pea GR could be crucial for maintaining GSH levels and therefore the redox status under extreme oxidative conditions (Begara-Morales et al 2015a) Collectively, S-nitrosylation can act as a regulator of redox homeostasis in plant cells subjected to salt stress via modulation of the key antioxidant systems However, more information on the residues targets of this NO-PTM and its functional role is needed in future studies 17.4.2 Heat and Cold Stresses Extreme temperatures are among the main factors limiting plant growth High temperature is considered one of the major abiotic stresses that negatively affect both vegetative and reproductive growth (Corpas et al 2011) Heat stress has an impact on the metabolism of RNS (Corpas et al 2008; Abat and Deswal 2009; Ziogas et al 2013), and an NO-mediated activation of some antioxidant enzymes such as SOD, catalase, and APX during heat stress has been reported (Song et al 2006), suggesting an involvement of SNOs in the regulation of redox homeostasis during this stress Under heat acclimation assays, Lee et al (2008) identified an Arabidopsis thermotolerance-defective mutant, hot5 (sensitive to hot temperature 5), with HOT5 encoding GSNOR1 These researchers reported that HOT5/GSNOR1 defective mutants exhibited more nitrate and nitroso species that induced heat sensitivity In addition, heat stress induces an oxidative stress accompanied by an increase in SNOs, which are responsible for intensifying tyrosine nitration in sunflower hypocotyls (Chaki et al 2011b) This greater tyrosine nitration inhibits the activity of the ferredoxin-NADP reductase and anhydrase carbonic enzymes, two key proteins in photosynthetic carbon assimilation (Chaki et al 2011b, 2013) Furthermore, some redox-related proteins were reported to be nitrated as a consequence of rising levels of SNOs (Chaki et al 2011b), suggesting a central role of SNOs in redox homeostasis via modulation of the levels of tyrosine nitration during heat stress Low temperature is another environmental stress that affects plant growth, and consequently crop production and quality, in which NO and RNS metabolism are involved (Corpas et al 2008; Airaki et al 2012) Although there is little information about S-nitrosylated-mediated response to this stress, some proteins have been reported to be S-nitrosylated (Abat and Deswal 2009; Sehrawat et al 2013; Puyaubert et al 2014) In this regard, Fe-SOD was identified as an S-nitrosylation target after cold stress in Brassica juncea, positively regulating its enzymatic activity and therefore contributing to the detoxification of superoxide radicals (Sehrawat et al 2013) However, DHAR, a key enzyme involved in regenerating ascorbate in the 374 J.C Begara-Morales et al Asa–GSH cycle, was reported to be inhibited by S-nitrosylation in potato and Arabidopsis plants under physiological conditions (Fares et al 2011; Kato et al 2013; Puyaubert et al 2014), but it is not differentially S-nitrosylated after cold stress (Puyaubert et al 2014), a condition in which DHAR activity is stimulated (Eltelib et al 2011) These results lead to the hypothesis that cold stress could cause DHAR denitrosylation, allowing its activity to increase in response to this stress In summary, since SNOs appear to mediate extreme temperature stress, more information is needed on the identification of S-nitrosylated proteins and their specific role in the response to this stress 17.4.3 Heavy Metal and Ozone Stress The role of NO in response to heavy metals has been proposed to be related to the removal of ROS through activation of the antioxidant systems (Procházková et al 2014) Although a response of the RNS metabolism has been reported under stress conditions such as cadmium stress (Barroso et al 2006; Rodríguez-Serrano et al 2009), there is still scant information about the implication of SNOs under this type of stress Recently, Ortega-Galisteo et al (2012) reported that catalase and glycolate oxidase involved in detoxifying and generating H2O2, respectively, are inactivated by S-nitrosylation in pea peroxisomes These authors also demonstrated that the extent of S-nitrosylation in these proteins is reduced after cadmium stress As a result, the authors suggested that S-nitrosylation might be involved in the regulation of H2O2 levels by modulating both the production and removal of ROS, and therefore contributes to redox homeostasis in peroxisomes On the other hand, recently, an S-nitroso-proteome has been reported in poplar leaves, where 172 proteins were S-nitrosylated under physiological conditions (Vanzo et al 2014) These proteins are related mainly to processes such as photosynthesis and primary metabolism, but also 75 of the identified proteins were related to the redox signaling category It bears noting that, after exposure of acute ozone stress, 32 new proteins were identified as targets of S-nitrosylation, some being proteins with an antioxidant function and therefore involved in redox homeostasis, such as MDAR, APX, and Prx5 (Vanzo et al 2014) Once again, S-nitrosylation could control redox homeostasis by regulating the main antioxidant systems under abiotic stress 17.4.4 Other Types of Stress Although an alteration in NO and its cognate SNO homeostasis has been reported in different plant species under drought, UV radiation, high light intensity, darkness, or wounding (Corpas et al 2008; Abat and Deswal 2009; Chaki et al 2011a), there is no information available on S-nitrosylated proteins identified under these 17 Protein S-Nitrosylation and S-Glutathionylation as Regulators … 375 environmental conditions Therefore, the identification of targets of S-nitrosylation and their potential role in plant response to these abiotic stresses could be a good point for gaining knowledge on S-nitrosylation as a regulator of redox homeostasis under these circumstances 17.5 S-Glutathionylation is Involved in Signaling Mechanisms in Plants Although S-glutathionylation has been traditionally considered to be a protective mechanism against oxidative stress, the emerging evidence implies that this redox PTM could be involved in signaling processes modulating the function of the target proteins (Dixon et al 2005; Dalle-Donne et al 2007; Zaffagnini et al 2007, 2012c) In this regard, as part of a signaling mechanism related to redox regulation, the signal generated after this Cys-PTM has to be transient Thus, glutaredoxin (Grx) enzymes have emerged as the major deglutathionylating agent controlling the extent of protein S-glutathionylation (Fig 17.2), and consequently, they could have an important role in redox signaling pathways (Zaffagnini et al 2012b, c) Fig 17.2 Mechanisms of S-glutathionylation/deglutathionylation There are different mechanisms giving rise to S-glutathionylation in vitro For instance, a thiol group on a protein (P-SH) can be S-glutathionylated by the action of GSSG or GSH (1) GSH can be also S-nitrosylated leading to GSNO that, in addition to its role as S-nitrosylating agent, can also mediate protein S-glutathionylation (2) The generation of sulfenic acid (3) or S-nitrosothiols (4) by the action of ROS and RNS can be a previous step for protein S-glutathionylation The deglutathionylation process is mainly mediated by GRX (5) generating GSSG, which in turn is reduced again by GR (6) P protein, P-SH thiol group of the protein, P-SSG glutathionylated protein, P-SOH thiol group that has been oxidized into sulfenic acid, P-SNO S-nitrosylated protein, GRX glutaredoxin, GR glutathione reductase 376 J.C Begara-Morales et al This Cys-PTM consists of the formation of a mixed disulfide bridge between a reactive Cys on a protein and GSH Different mechanisms leading to S-glutathionylation in vitro have been reported, including the involvement of thiol–disulfide exchange, sulfenic acids, or S-nitrosothiols, among others (Gallogly and Mieyal 2007; Zaffagnini et al 2012c) (Fig 17.2) However, the exact mechanism and the physiological relevance of protein S-glutathionylation in vivo in plants remains unclear (Zaffagnini et al 2012c; Zagorchev et al 2013) The increase in the oxidative state inside the cell leading to a decrease in the GSH/GSSG ratio can promote protein S-glutathionylation (Dalle-Donne et al 2007) This alteration of the GSH/GSSG ratio commonly occurs under different types of abiotic stress, and consequently, it is reasonable to consider that S-glutathionylation may be involved in signaling mechanisms in plant response to these adverse situations Several studies that identify protein targets of S-glutathionylation have used oxidant molecules to strengthen this PTM, thereby boosting the likelihood of success in the identification (Ito et al 2003; Dixon et al 2005; Michelet et al 2008) This strategy has enabled the identification of glutathionylated proteins in vitro and in vivo (Dixon et al 2005; Michelet et al 2008; Zaffagnini et al 2012a), emerging a possible function of these Cys-PTMs in signaling processes in chloroplasts, organelles subjected continuously to oxidative stress (Zaffagnini et al 2012b) Precisely, one of the best characterized glutathionylated proteins in plants is glyceraldehyde-3-phosphate dehydrogenase (GAPDH), involved in the Calvin cycle, which is inhibited after this modification (Zaffagnini et al 2007; Holtgrefe et al 2008; Bedhomme et al 2012) In this regard, S-glutathionylation of chloroplastic GAPDH from Arabidopsis at Cys 149 inhibits its enzymatic activity and at the same time could protect against the irreversible oxidation caused by H2O2 (Zaffagnini et al 2007) Likewise, cytoplasmic GAPDH activity is also reversibly inhibited by S-nitrosylation at Cys 149 (Zaffagnini et al 2013) This highlights the idea that a reactive Cys involved in the catalytic mechanism can be altered by several Cys-PTMs in different oxidation states Albeit hundreds of proteins have been identified as being glutathionylated, there is still a meager information on the role of this PTM under physiological conditions or in plant response to abiotic stress (Zagorchev et al 2013) Most of the proteins identified are related to redox processes, including some peroxiredoxins, glutathione transferase, or heat-shock proteins (Michelet et al 2008; Gao et al 2009; Zaffagnini et al 2012a) However, little information is available in relation to the impact of this Cys-PTM on protein structure/function Here, we will discuss some examples of proteins that have been detected as glutathionylated and are involved mainly in plant response to abiotic stress situations, suggesting a potential role of this PTM as a regulator of redox signaling under adverse environmental conditions Dixon et al (2005) identified a set of glutathionylated proteins in Arabidopsis plants subjected to oxidative stress They identified only eight proteins that undergo this modification using in vivo approaches However, the number of glutathionylated proteins increased after in vitro experiments, with 132 protein targets of S-glutathionylation being detected Among these, two components of the Asa–GSH cycle were identified, i.e., MDAR and DHAR1, suggesting that the functioning of 17 Protein S-Nitrosylation and S-Glutathionylation as Regulators … 377 this antioxidant system could be regulated by S-glutathionylation However, verification of this requires that the effect of this modification on the activity/structure of these proteins to be determined No information of this type is available on MDAR However, a reversible inactivation of DHAR1 activity as a consequence of S-glutathionylation at the catalytic Cys 20 has been reported (Dixon et al 2002) Therefore, regeneration of reduced ascorbate in the Asa–GSH cycle could be compromised, and consequently, it could have a negative impact on the functioning of this antioxidant system In addition, it has been reported that APX can also be glutathionylated in vitro (Kitajima et al 2008) The authors suggested that this alteration may be a protective mechanism to avoid the irreversible oxidation and inactivation of the enzyme under oxidative conditions However, there is no clear information about the impact of S-glutathionylation on APX activity As a whole, the Asa–GSH cycle appears to be regulated by S-glutathionylation, as previously described in the case of S-nitrosylation (Begara-Morales et al 2014b, 2015a), and therefore, this key antioxidant system could be regulated by both Cys-PTMs in response to environmental insults However, further studies are needed to determine the effect of S-glutathionylation on the functioning of the cycle, in order to identify the Cys targets of S-glutathionylation in vivo and to establish the physiological relevance of this Cys-PTM in response to abiotic conditions NADP-malic enzyme (ME), which is part of the NADPH-generating systems, has also been identified as target of S-glutathionylation under induced oxidative stress (Dixon et al 2005) NADPH is an indispensable cofactor in cellular redox homeostasis since it is an essential electron donor in numerous enzymatic reactions For instance, it is needed for the regeneration of GSH by glutathione reductase (Halliwell and Foyer 1978) as a component of the Asa–GSH cycle and for the activity of the NADPH-dependent thioredoxin system (Cha et al 2014), two important cell antioxidant systems against oxidative damage Similarly, NADPH is also necessary for the generation of ðO2 ÁÀ Þ by NADPH oxidase (Sagi and Fluhr 2006) Furthermore, the NADPH-generating systems could be involved in plant response to oxidative stress induced by adverse environmental conditions (Valderrama et al 2006; Wang et al 2008), where the balance in the NADPH/NADP+ ratio is also crucial for maintaining the redox state (Kapoor et al 2015) Therefore, it is important to determine the effect of S-glutathionylation on NADP-ME activity under abiotic stress since it could have an impact on redox homeostasis Methionine oxidation by ROS or RNS (John et al 2001; Alvarez and Radi 2003) leads to the formation of methionine sulfoxide (MetSO) (Boschi-Muller et al 2008), which could alter both the activity and the conformation of many proteins (Dos Santos et al 2005; Rouhier et al 2006; Li et al 2012) However, this oxidative damage is reversible because methionine sulfoxide reductase (MSR) enzymes catalyze the reduction of MetSO back to methionine, and consequently, MSR enzymes are repair systems that protect against methionine oxidation Arabidopsis methionine sulfoxide reductase B1 (MSRB1) has also been reported to be glutathionylated in vitro at catalytic Cys 186 (Tarrago et al 2009) Notably, it has been reported that the expression level of MSRB1 and MSRB2, 378 J.C Begara-Morales et al among other MSRBs, is similarly down-regulated after the treatment of Arabidopsis plants with GSH (Begara-Morales et al 2014a), suggesting a similar transcriptional response of both proteins However, MSRB1, but not MSRB2, is glutathionylated (Tarrago et al 2009), suggesting that these proteins can have a different posttranslational regulation Some MSRs have been related to plant responses to oxidative stress (Li et al 2012), and consequently, these proteins may have a key role in plant response to abiotic stress In this regard, the S-glutathionylation of MSRB could have an impact on regeneration of reduced methionine and therefore in abiotic stress response To confirm this, further studies are needed in order to determine the physiological role of this modification of MSRB1 in response to abiotic stress Collectively, the emerging data suggest that S-glutathionylation could be a key player in the regulation of redox homeostasis during abiotic stress via control of the main antioxidant systems 17.6 Conclusion and Future Perspective In recent years, S-nitrosylation and S-glutathionylation have emerged as key redox PTMs involved in signaling mechanisms in plants However, while the metabolism of S-nitrosothiols has been demonstrated to be involved in plant response to a wide range of abiotic stress conditions, the information on the role of S-glutathionylation is still in its infancy In this sense, most of the glutathionylated proteins have been identified after treatment with oxidant molecules, so that future studies addressed to identify protein targets of S-glutathionylation under different abiotic stresses such as salinity, extreme temperature, or drought constitute a good point to move forward In addition, although an increasing number of proteins have been shown to be S-nitrosylated and/or S-glutathionylated, a molecular characterization of these PTMs and their physiological relevance in response to abiotic stress remains to be established In this regard, not only the detection of protein targets of these redox PTMs in response to environmental insults in vivo are required, but also the identification of one or more modified cysteine residues, especially in the antioxidant systems and proteins associated with redox balance This could clarify the involvement of these PTMs as regulators of redox homeostasis during plant acclimation In this sense, the Asa–GSH cycle has been the best characterized, since it has been reported that S-nitrosylation modulates the components of the cycle with different effects on their functions (Begara-Morales et al 2014b, 2015a) Consequently, S-nitrosylation of APX at Cys 32 has emerged as crucial in plants’ response to oxidative stress, especially during salinity (Begara-Morales et al 2014b; Yang et al 2015) Furthermore, different components of the cycle have been identified as targets of S-glutathionylation For instance, S-glutathionylation at Cys 20 induces the reversible inactivation of DHAR (Dixon et al 2002), but a role of this change under stress conditions has not been specified It bears noting that 17 Protein S-Nitrosylation and S-Glutathionylation as Regulators … 379 enzymes of Asa–GSH cycle, and other proteins such as GAPDH, are targets of both PTMs, suggesting a cross-link between the two signaling pathways In conclusion, future studies to identify S-nitrosylated and S-glutathionylated proteins under stress conditions and the impact of these redox PTMs on protein structure and in plant responses to stress are needed in order to gain knowledge related to plant acclimation and ultimately to design strategies to develop crops that cope more efficiently with environmental insults Acknowledgments JC Begara-Morales would like to thank the Alfonso Martin Escudero Foundation for funding his 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