Skip to main content

Protein S-Nitrosylation and S-Glutathionylation as Regulators of Redox Homeostasis During Abiotic Stress Response

  • Chapter
  • First Online:

Abstract

Abiotic stress, one of the main factors affecting crop yield, is characterized by a rapid burst of redox molecules, especially belonging to reactive oxygen (ROS) and nitrogen (RNS) species. These molecules can act as molecular cues that trigger the defense mechanisms leading to maintaining the cellular redox balance. However, when the stress persists over time, a high concentration of ROS and RNS can overwhelm the capacity of protection of the antioxidant systems, thereby perturbing cellular redox homeostasis. This situation can induce a nitro-oxidative stress that ultimately causes cell damage and compromises plant survival. Therefore, understanding how plants cope with the changing environment can be essential for improving crops. In this regard, cysteine residues appear to be crucial to perceive the environmental signals and to orchestrate plant responses, which are usually mediated by redox posttranslational modifications (PTMs) such as S-nitrosylation and S-glutathionylation. Increasing evidence suggests that these redox PTMs could be key players in maintaining the cellular redox homeostasis by regulating the antioxidant systems. However, although hundreds of proteins, including some main antioxidants, have been reported to be targets of S-nitrosylation and/or S-glutathionylation under physiological and/or abiotic stress, there is still little information on the specific impact of these changes on the protein function and their physiological relevance. In this book chapter, we will explore recent knowledge concerning the involvement of these modifications in response to abiotic stress, with special attention to characterizing these modified proteins at the molecular level.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9:4368–4380

    Article  CAS  PubMed  Google Scholar 

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Del Rio LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant, Cell Environ 35:281–295

    Article  CAS  Google Scholar 

  • Alvarez B, Radi R (2003) Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25:295–311

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radical Res 50:291–303

    Article  CAS  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 13:15193–15208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    Article  CAS  PubMed  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793

    Article  CAS  PubMed  Google Scholar 

  • Becker K, Gui M, Schirmer RH (1995) Inhibition of human glutathione reductase by S-nitrosoglutathione. Eur J Biochem 234:472–478

    Article  CAS  PubMed  Google Scholar 

  • Bedhomme M, Adamo M, Marchand CH, Couturier J, Rouhier N, Lemaire SD, Zaffagnini M, Trost P (2012) Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J 445:337–347

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014a) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014b) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015a) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2015b) Modulation of the Ascorbate-Glutathione cycle antioxidant capacity by posttranslational modifications mediated by nitric oxide in abiotic stress situations. In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Berlin, pp 305–320

    Chapter  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Beltrán B, Orsi A, Clementi E, Moncada S (2000) Oxidative stress and S-nitrosylation of proteins in cells. Brit J Pharmacol 129:953–960

    Article  Google Scholar 

  • Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984

    Article  CAS  PubMed  Google Scholar 

  • Boschi-Muller S, Gand A, Branlant G (2008) The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 474:266–273

    Article  CAS  PubMed  Google Scholar 

  • Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteomics 79:87–99

    Article  CAS  PubMed  Google Scholar 

  • Camejo D, Ortiz-Espín A, Lázaro JJ, Romero-Puertas MC, Lázaro-Payo A, Sevilla F, Jiménez A (2015) Functional and structural changes in plant mitochondrial PrxII F caused by NO. J Proteomics 119:112–125

    Article  CAS  PubMed  Google Scholar 

  • Cha JY, Kim JY, Jung IJ, Kim MR, Melencion A, Alam SS, Yun DJ, Lee SY, Kim MG, Kim WY (2014) NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiol Biochem 80:184–191

    Article  CAS  PubMed  Google Scholar 

  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodíguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011a) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813

    Article  CAS  PubMed  Google Scholar 

  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011b) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant, Cell Environ 34:1803–1818

    Article  CAS  Google Scholar 

  • Chaki M, Carreras A, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Valderrama R, Corpas FJ, Barroso JB (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide 29:30–33

    Article  CAS  PubMed  Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199:633–635

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Chaki M, Fernández-Ocañaa A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Begara-Morales JC, Sánchez-Calvo B, Chaki M, Barroso JB (2015) Nitration and S-nitrosylation: two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) and their role in signalling processes of plant cells. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communication in plants. Springer, Berlin, pp 267–281

    Google Scholar 

  • Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013) Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot 64:3339–3349

    Article  CAS  PubMed  Google Scholar 

  • Couturier J, Chibani K, Jacquot JP, Rouhier N (2013) Cysteine-based redox regulation and signaling in plants. Front Plant Sci 4:105

    Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radical Biol Med 43:883–898

    Article  CAS  Google Scholar 

  • de Pinto MC, Locato V, Sgobba A, del Carmen Romero-Puertas M, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deeb RS, Nuriel T, Cheung C, Summers B, Lamon BD, Gross SS, Hajjar DP (2013) Characterization of a cellular denitrase activity that reverses nitration of cyclooxygenase. Am J Physiol Heart Circ Physiol 305:H687–H698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz-Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione-linking cell proliferation to oxidative stress. Free Radical Biol Med 89:1154–1164

    Article  CAS  Google Scholar 

  • Dietz K-J (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dos Santos CV, Cuiné S, Rouhier N, Rey P (2005) The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiol 138:909–922

    Article  PubMed Central  CAS  Google Scholar 

  • Durner J, Gow AJ, Stamler JS, Glazebrook J (1999) Ancient origins of nitric oxide signaling in biological systems. Proc Nat Acad Sci U S A 96:14206–14207

    Article  CAS  Google Scholar 

  • Eltelib HA, Badejo AA, Fujikawa Y, Esaka M (2011) Gene expression of monodehydroascorbate reductase and dehydroascorbate reductase during fruit ripening and in response to environmental stresses in acerola (Malpighia glabra). J Plant Physiol 168:619–627

    Article  CAS  PubMed  Google Scholar 

  • Espunya MC, Díaz M, Moreno-Romero J, Martínez MC (2006) Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. Plant, Cell Environ 29:1002–1011

    Article  CAS  PubMed  Google Scholar 

  • Fancy NN, Bahlmann AK, Loake GJ (2016) Nitric oxide function in plant abiotic stress. Plant, Cell Environ. doi:10.1111/pce.12707

    Google Scholar 

  • Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336

    Article  CAS  PubMed  Google Scholar 

  • Feechan A, Kwon E, Yun B-W, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Nat Acad Sci U S A 102:8054–8059

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francescutti D, Baldwin J, Lee L, Mutus B (1996) Peroxynitrite modification of glutathione reductase: modeling studies and kinetic evidence suggest the modification of tyrosines at the glutathione disulfide binding site. Protein Eng 9:189–194

    Article  CAS  PubMed  Google Scholar 

  • Gallogly MM, Mieyal JJ (2007) Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr Opin Pharmacol 7:381–391

    Article  CAS  PubMed  Google Scholar 

  • Gao X-H, Bedhomme M, Veyel D, Zaffagnini M, Lemaire SD (2009) Methods for analysis of protein glutathionylation and their application to photosynthetic organisms. Mol Plant 2:218–235

    Article  CAS  PubMed  Google Scholar 

  • Gaston B, Reilly J, Drazen JM, Fackler J, Ramdev P, Arnelle D, Mullins ME, Sugarbaker DJ, Chee C, Singel DJ (1993) Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Nat Acad Sci U S A 90:10957–10961

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Görg B, Qvartskhava N, Voss P, Grune T, Häussinger D, Schliess F (2007) Reversible inhibition of mammalian glutamine synthetase by tyrosine nitration. FEBS Lett 581:84–90

    Article  PubMed  CAS  Google Scholar 

  • Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H (2004) Biological significance of nitric oxide-mediated protein modifications. Am J Physiol Lung Cell Mol Physiol 287:L262–L268

    Article  CAS  PubMed  Google Scholar 

  • Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4

    Google Scholar 

  • Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta 139:9–17

    Article  CAS  PubMed  Google Scholar 

  • Hamilton GA (1991) Chemical and biochemical reactivity of oxygen. In: Pell E, Steffen K (eds) Active oxygen/oxidative stress and plant metabolism. American Society Plant Physiologists, Rockville, pp 6–12

    Google Scholar 

  • Hess DT, Matsumoto A, Kim S-O, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166

    Article  CAS  PubMed  Google Scholar 

  • Holtgrefe S, Gohlke J, Starmann J, Druce S, Klocke S, Altmann B, Wojtera J, Lindermayr C, Scheibe R (2008) Regulation of plant cytosolic glyceraldehyde-3-phosphate dehydrogenase isoforms by thiol modifications. Physiol Planta 133:211–228

    Article  CAS  Google Scholar 

  • Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Huang X, Chen L, Sun X, Lu C, Zhang L, Wang Y, Zuo J (2015) Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167:1731–1746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Iwabuchi M, Ki Ogawa (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol 44:655–660

    Article  CAS  PubMed  Google Scholar 

  • Jaffrey SR, Snyder SH (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 86(11)

    Google Scholar 

  • Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • John GS, Brot N, Ruan J, Erdjument-Bromage H, Tempst P, Weissbach H, Nathan C (2001) Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Nat Acad Sci U S A 98:9901–9906

    Article  Google Scholar 

  • Kapoor D, Sharma R, Handa N, Kaur H, Rattan A, Yadav P, Gautam V, Kaur R, Bhardwaj R (2015) Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:13

    Article  Google Scholar 

  • Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Planta 148:371–386

    Article  CAS  Google Scholar 

  • Keyster M, Klein A, Egbich I, Jacobs A, Ludidi N (2011) Nitric oxide increases the enzymatic activity of three ascorbate peroxidase isoforms in soybean root nodules. Plant Signal Behav 6:956–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitajima S, Kurioka M, Yoshimoto T, Shindo M, Kanaori K, Tajima K, Oda K (2008) A cysteine residue near the propionate side chain of heme is the radical site in ascorbate peroxidase. FEBS J 275:470–480

    Article  CAS  Google Scholar 

  • Klotz LO (2002) Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol Chem 383:443–456

    Article  CAS  PubMed  Google Scholar 

  • Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162

    Article  CAS  PubMed  Google Scholar 

  • Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol 208:860–872

    Article  CAS  PubMed  Google Scholar 

  • Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  CAS  PubMed  Google Scholar 

  • Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20:786–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458

    Article  CAS  PubMed  Google Scholar 

  • Li CW, Lee SH, Chieh PS, Lin CS, Wang YC, Chan MT (2012) Arabidopsis root-abundant cytosolic methionine sulfoxide reductase B genes MsrB7 and MsrB8 are involved in tolerance to oxidative stress. Plant Cell Physiol 53:1707–1719

    Article  CAS  PubMed  Google Scholar 

  • Lin CC, Jih PJ, Lin HH, Lin JS, Chang LL, Shen YH, Jeng ST (2011) Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol Biol 77:235–249

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr C, Durner J (2015) Interplay of reactive oxygen species and nitric oxide: nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol 167:1209–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494

    Article  CAS  PubMed  Google Scholar 

  • Lounifi I, Arc E, Molassiotis A, Job D, Rajjou L, Tanou G (2013) Interplay between protein carbonylation and nitrosylation in plants. Proteomics 13:568–578

    Article  CAS  PubMed  Google Scholar 

  • Manai J, Gouia H, Corpas FJ (2014) Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J Plant Physiol 171:1028–1035

    Article  CAS  PubMed  Google Scholar 

  • McKersie BD, Lesheim Y (2013) Stress and stress coping in cultivated plants. Springer, Berlin

    Google Scholar 

  • Meng T-C, Fukada T, Tonks NK (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9:387–399

    Article  CAS  PubMed  Google Scholar 

  • Michelet L, Zaffagnini M, Vanacker H, Le Maréchal P, Marchand C, Schroda M, Lemaire SD, Decottignies P (2008) In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J Biol Chem 283:21571–21578

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230

    PubMed  PubMed Central  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Procházková D, Sumaira J, Na Wilhelmová, Pavlíková D, Száková J (2014) Reactive nitrogen species and the role of NO in abiotic stress. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crops stress tolerance. Elsevier, Amsterdam

    Google Scholar 

  • Puyaubert J, Fares A, Rézé N, Peltier JB, Baudouin E (2014) Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci 215:150–156

    Article  PubMed  CAS  Google Scholar 

  • Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Nat Acad Sci U S A 101:4003–4008

    Article  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romero-Puertas MC, Laxa M, Matté A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Dos Santos CV, Tarrago L, Rey P (2006) Plant methionine sulfoxide reductase A and B multigenic families. Photosynth Res 89:247–262

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sehrawat A, Abat JK, Deswal R (2013) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Front Plant Sci 4:342

    Article  PubMed  PubMed Central  Google Scholar 

  • Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66:2945–2955

    Article  CAS  PubMed  Google Scholar 

  • Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Sobrino-Plata J, Carrasco-Gil S, Abadía J, Escobar C, Álvarez-Fernández A, Hernández LE (2014) The role of glutathione in mercury tolerance resembles its function under cadmium stress in Arabidopsis. Metallomics 6:356–366

    Article  CAS  PubMed  Google Scholar 

  • Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171:449–458

    Article  CAS  PubMed  Google Scholar 

  • Spadaro D, Yun BW, Spoel SH, Chu C, Wang YQ, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Planta 138:360–371

    Article  CAS  Google Scholar 

  • Spoel SH, Loake GJ (2011) Redox-based protein modifications: the missing link in plant immune signalling. Curr Opin Plant Biol 14:358–364

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2014) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol 57:550–561

    Article  PubMed  CAS  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    Article  CAS  PubMed  Google Scholar 

  • Tamura M, Saito M, Yamamoto K, Takeuchi T, Ohtake K, Tateno H, Hirabayashi J, Kobayashi J, Arata Y (2015) S-nitrosylation of mouse galectin-2 prevents oxidative inactivation by hydrogen peroxide. Biochem Biophys Res Commun 457:712–717

    Google Scholar 

  • Tanou G, Job C, Lc Rajjou, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804

    Article  CAS  PubMed  Google Scholar 

  • Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599

    Article  CAS  PubMed  Google Scholar 

  • Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Maréchal P, Rouhier N, Lemaire SD, Rey P (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284:18963–18971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullah S, Kolo Z, Egbichi I, Keyster M, Ludidi N (2016) Nitric oxide influences glycine betaine content and ascorbate peroxidase activity in maize. S Afr J Bot 105:218–225

    Article  CAS  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A, Gómez-Rodríguez MV, Chaki M, Pedrajas JR, Fernández-Ocaña AM, del Río LA, Barroso JB (2006) The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant, Cell Environ 29:1449–1459

    Article  CAS  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, Luis A, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461

    Article  CAS  PubMed  Google Scholar 

  • Vanzo E, Ghirardo A, Merl-Pham J, Lindermayr C, Heller W, Hauck SM, Durner J, Schnitzler JP (2014) S-nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS ONE 9:e106886

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang XM, Ma YY, Huang CH, Li JS, Wan Q, Bi YR (2008) Involvement of glucose-6-phosphate dehydrogenase in reduced glutathione maintenance and hydrogen peroxide signal under salt stress. Plant Signal Behav 3:394–395

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A, Taylor P, Xue P, Yang FQ, Xie ZS, Pallas JA (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284:2131–2137

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Liu Y, Tan X, Liu H, Zeng G, Hu X, Jian H, Gu Y (2015) Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress. Environ Sci Pollut Res 22:3489–3497

    Article  CAS  Google Scholar 

  • Woo HA, Jeong W, Chang TS, Park KJ, Park SJ, Yang JS, Rhee SG (2005) Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins. J Biol Chem 280:3125–3128

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu BP (1994) Cellular defenses against damage from reactive oxygen species. Physiol Rev 74:139–162

    CAS  PubMed  Google Scholar 

  • Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: aredox cue in deconvolution. New Phytol 202:1142–1156

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Spoel SH, Loake GJ (2011) Synthesis of and signalling by small, redox active molecules in the plant immune response. Biochim BiophyS Acta (BBA)-General Subjects 1820:770–776

    Google Scholar 

  • Zaffagnini M, Michelet L, Marchand C, Sparla F, Decottignies P, Le Maréchal P, Miginiac-Maslow M, Noctor G, Trost P, Lemaire SD (2007) The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS Lett 274:212–226

    Article  CAS  Google Scholar 

  • Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero B, Cassier-Chauvat C, Decottignies P, Lemaire SD (2012a) Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol Cell Proteom 11(M111):014142

    PubMed  Google Scholar 

  • Zaffagnini M, Bedhomme M, Lemaire SD, Trost P (2012b) The emerging roles of protein glutathionylation in chloroplasts. Plant Sci 185–86:86–96

    Article  CAS  Google Scholar 

  • Zaffagnini M, Bedhomme M, Marchand CH, Morisse S, Trost P, Lemaire SD (2012c) Redox regulation in photosynthetic organisms: focus on glutathionylation. Antioxid Redox Signal 16:567–586

    Article  CAS  PubMed  Google Scholar 

  • Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288:22777–22789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Biochem 68:118–126

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

JC Begara-Morales would like to thank the Alfonso Martin Escudero Foundation for funding his postdoctoral fellowship. This study was supported by an ERDF grant cofinanced by the Ministry of Economy and Competitiveness (project BIO2015-66390-P; MINECO/FEDER) and the Junta de Andalucía (groups BIO286 and BIO192) in Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. B. Barroso .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Begara-Morales, J.C. et al. (2016). Protein S-Nitrosylation and S-Glutathionylation as Regulators of Redox Homeostasis During Abiotic Stress Response. In: Gupta, D., Palma, J., Corpas, F. (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer, Cham. https://doi.org/10.1007/978-3-319-44081-1_17

Download citation

Publish with us

Policies and ethics