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Modulation of the Ascorbate–Glutathione Cycle Antioxidant Capacity by Posttranslational Modifications Mediated by Nitric Oxide in Abiotic Stress Situations

  • Chapter
Reactive Oxygen Species and Oxidative Damage in Plants Under Stress

Abstract

Environmental stresses cause a rapid burst of second messengers belonging to reactive oxygen (ROS) and nitrogen (RNS) species, mainly hydrogen peroxide (H2O2) and nitric oxide (NO), respectively. H2O2 can act as a signal molecule or become toxic at high levels. Plants have developed different antioxidant tools, such as the ascorbate–glutathione (Asa–GSH) cycle, a key antioxidant system involved in the finely tuned regulation of H2O2 in cells, in order to control H2O2 overproduction. In recent years, a growing body of evidence points to the existence of a link between NO and physiological and stress responses in plants. NO activity is mainly conveyed through posttranslational modifications (PTMs) such as S-nitrosylation and/or tyrosine nitration. Over the last 10 years, the number of S-nitrosylated and nitrated proteins subjected to physiological and a stress condition has been observed to increase significantly in higher plants, suggesting that NO-PTMs are involved in plant physiology. Emerging evidence shows that ROS and NO interact during plant responses to (a)biotic stress, and proteins linked to ROS metabolism have been reported to be regulated by NO-related PTMs. Furthermore, using proteomic analytical techniques, enzymes involved in the Asa–GSH cycle have been identified as NO targets. However, little information exists on the specific impact of NO-PTMs on the structure and activity of these antioxidant enzymes. In this chapter, we will discuss recent findings concerning the regulation of the Asa–GSH cycle antioxidant capacity by NO-PTMs, particularly in relation to the role played by the NO target residues identified under stress conditions.

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References

  • Abello N, Kerstjens HAM, Postma DS, Bischoff R (2009) Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J Proteome Res 8:3222–3238

    Article  CAS  PubMed  Google Scholar 

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2011a) 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  PubMed  CAS  Google Scholar 

  • Airaki M, Sánchez-Moreno L, Leterrier M, Barroso JB, Palma JM, Corpas FJ (2011b) Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. Plant Cell Physiol 52:2006–2015

    Article  CAS  PubMed  Google Scholar 

  • Álvarez C, Lozano-Juste J, Romero LC, García I, Gotor C, León J (2011) Inhibition of Arabidopsis O-acetylserine (thiol) lyase A1 by tyrosine nitration. J Biol Chem 286:578–586

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase – a hydrogen peroxide-scavenging enzyme in plants. Physiol Planta 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  PubMed Central  CAS  PubMed  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 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6, e20714

    Article  PubMed Central  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 

  • Begara-Morales JC, Chaki M, Sanchez-Calvo B, Mata-Parez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013a) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64:1121–1134

    Article  PubMed Central  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 (2013b) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Begara-Morales JC, Sanchez-Calvo B, Chaki M, Mata-Perez C, Valderrama R, Padilla MN, Lopez-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot. doi:10.1093/jxb/erv306

    PubMed  Google Scholar 

  • Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inza D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358

    Article  CAS  PubMed  Google Scholar 

  • Bowdicht ML, Donaldson RP (1990) Ascorbate free-radical reduction by glyoxysomal membranes. Plant Physiol 94:531–537

    Article  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 

  • 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, Chaki M, Fernández-Ocaña 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, Leterrier M, Begara-Morales JC, Valderrama R, Chaki M, López-Jaramillo J, Luque F, Palma JM, Padilla MN, Sánchez-Calvo B (2013a) Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochim Biophys Acta 1830:4981–4989

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Palma JM, Luis A, Barroso JB (2013b) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 4:29

    PubMed Central  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, Germany

    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 

  • Creissen G, Edwards EA, Enard C, Wellburn A, Mullineaux P (1992) Molecular characterization of glutathione reductase cDNAs from pea (Pisum sativum L.). Plant J 2:129–131

    CAS  PubMed  Google Scholar 

  • Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodíguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009a) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol 50:265–279

    Article  CAS  PubMed  Google Scholar 

  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, López-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B (2009b) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60:4221–4234

    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 (2011a) 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  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 (2011b) 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  PubMed Central  CAS  PubMed  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 

  • Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CP, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules. Plant Physiol 102:481–489

    PubMed Central  CAS  PubMed  Google Scholar 

  • de Pinto MC, Locato V, Sgobba A, Romero-Puertas MC, 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 Central  PubMed  CAS  Google Scholar 

  • del Río LA, Javier Corpas F, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Hernández JA, Burgos L (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotechnol J 11:976–985

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284

    Article  CAS  PubMed  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 

  • 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 BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci U S A 102:8054–8059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  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 

  • 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 Natl Acad Sci USA 90:10957–10961

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gechev T, Willekens H, Van Montagu M, Inzo D, Van Camp W, Toneva V, Minkov I (2003) Different responses of tobacco antioxidant enzymes to light and chilling stress. J Plant Physiol 160:509–515

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212

    Article  CAS  PubMed  Google Scholar 

  • Gomez JM, Jimenez A, Olmos E, Sevilla F (2004) Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. J Exp Bot 55:119–130

    Article  CAS  PubMed  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 

  • Groβ F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419

    Google Scholar 

  • Groden D, Beck E (1979) H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim Biophys Acta 546:426–435

    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 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  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  Google Scholar 

  • Jespersen H, Kjrd I, Stergaard L, Welinder K (1997) From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem J 326:305–310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jimenez A, Hernandez JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335

    Article  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  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  PubMed  Google Scholar 

  • Kubo A, Aono M, Nakajima N, Saji H, Tanaka K, Kondo N (1999) Differential responses in activity of antioxidant enzymes to different environmental stresses in Arabidopsis thaliana. J Plant Res 112:279–290

    Article  CAS  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 

  • 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 

  • Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, Luis A (2005) Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leterrier M, Barroso JB, Valderrama R, Palma JM, Corpas FJ (2012) NADP-dependent isocitrate dehydrogenase from Arabidopsis roots contributes in the mechanism of defence against the nitro-oxidative stress induced by salinity. Sci World J. ID: 694740.

    Google Scholar 

  • Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464

    Article  PubMed Central  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 (2009) S-nitrosylation in plants: pattern and function. J Proteomics 73:1–9

    Article  CAS  PubMed  Google Scholar 

  • Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Bao H, Cai J, Han J, Zhou L (2014) A novel thylakoid ascorbate peroxidase from Jatrophacurcas enhances salt tolerance in transgenic tobacco. Int J Mol Sci 15:171–185

    Article  PubMed Central  CAS  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 

  • Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malik SI, Hussain A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181:540–544

    Article  CAS  PubMed  Google Scholar 

  • Mandelman D, Jamal J, Poulos TL (1998) Identification of two electron-transfer sites in ascorbate peroxidase using chemical modification, enzyme kinetics, and crystallography. Biochemistry 37:17610–17617

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Ruiz A, Lamas S (2007) Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences. Cardiovasc Res 75:220–228

    Article  PubMed  CAS  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    Article  CAS  PubMed  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 

  • Oidaira H, Sano S, Koshiba T, Ushimaru T (2000) Enhancement of antioxidative enzyme activities in chilled rice seedlings. J Plant Physiol 156:811–813

    Article  CAS  Google Scholar 

  • Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmino 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río LA (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57:1747–1758

    Article  CAS  PubMed  Google Scholar 

  • Patterson WR, Poulos TL (1995) Crystal structure of recombinant pea cytosolic ascorbate peroxidase. Biochemistry 34:4331–4341

    Article  CAS  PubMed  Google Scholar 

  • Procházková D, Sumaira J, Wilhelmová Na, Pavlíková D, Száková J (2014) Reactive nitrogen species and the role of NO in abiotic stress. In: Ahmad P, Rasool S (ed) Emerging Technologies and Managment of Crops Stress Tolerance. Elsevier.

    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 Natl Acad Sci USA 101:4003–4008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Radi R (2013) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46:550–559

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Luder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19:3170–3193

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reumann S, Corpas FJ (2010) The peroxisomal ascorbate-glutathione pathway: molecular identification and insights into its essential role under environmental stress conditions. In: Anjum NA, Chan MT, Umar S (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Germany

    Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodríguez-Serrano M, Del Río LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Laxa M, Matte 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Campostrini N, Matte 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 

  • Rusterucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282–1292

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Savvides SN, Scheiwein M, Bohme CC, Arteel GE, Karplus PA, Becker K, Schirmer RH (2002) Crystal structure of the antioxidant enzyme glutathione reductase inactivated by peroxynitrite. J Biol Chem 277:2779–2784

    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. doi:10.1007/s00709-015-0756-y

  • Shapiro AD (2005) Nitric oxide signaling in plants. Vitam Horm 72:339–398

    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 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455

    Article  CAS  PubMed  Google Scholar 

  • Souza JM, Peluffo G, Radi R (2008) Protein tyrosine nitration-functional alteration or just a biomarker? Free Radic Biol Med 45:357–366

    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 Int Plant Biol 57:550–561

    Article  CAS  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

    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 

  • Turko IV, Murad F (2002) Protein nitration in cardiovascular diseases. Pharmacol Rev 54:619–634

    Article  CAS  PubMed  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 

  • 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 Int 22:3489–3497

    Article  CAS  PubMed  Google Scholar 

  • Wu TM, Lin WR, Kao YT, Hsu YT, Yeh CH, Hong CY, Kao CH (2013) Identification and characterization of a novel chloroplast/mitochondria co-localized glutathione reductase 3 involved in salt stress response in rice. Plant Mol Biol 83:379–390

    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  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Feechan A, Yin M, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Quan G, Wang J, Han H, Chen S, Guo S, Yin H (2015) Functional validation of Phragmites communis glutathione reductase (PhaGR) as an essential enzyme in salt tolerance. Appl Biochem Biotechnol 175:3418–3430

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qiu Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS One 8:e57472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by an ERDF grant co-financed by the Ministry of Economy and Competitiveness (projects BIO2012-33904 and RECUPERA2020) and the Junta de Andalucía (groups BIO286 and BIO192) in Spain. J. Begara-Morales would like to thank the Ministry of Science and Innovation for funding the Ph.D. fellowship (F.P.U.). LC/MS/MS analyses were carried out at the Laboratorio de Proteómica LP-CSIC/UAB, a member of ProteoRed network.

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Correspondence to J. B. Barroso .

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Begara-Morales, J.C. et al. (2015). Modulation of the Ascorbate–Glutathione Cycle Antioxidant Capacity by Posttranslational Modifications Mediated by Nitric Oxide in Abiotic Stress Situations. In: Gupta, D., Palma, J., Corpas, F. (eds) Reactive Oxygen Species and Oxidative Damage in Plants Under Stress. Springer, Cham. https://doi.org/10.1007/978-3-319-20421-5_12

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