Skip to main content

Regulatory Role of Components of Ascorbate–Glutathione Pathway in Plant Stress Tolerance

  • Chapter
  • First Online:
Ascorbate-Glutathione Pathway and Stress Tolerance in Plants

Abstract

Ascorbate (Asc) and glutathione (GSH) are important molecules functioning in several vital processes in plant cells, including the ascorbate–glutathione cycle. They are involved in basic metabolic reactions normally occurring in plants as well as in those evoked by abiotic or biotic stresses. Asc and GSH are localized in most of cell compartments such as cytoplasm, mitochondria, peroxisomes and chloroplasts, the Asc being additionally also found in the apoplast. These small molecular weight compounds protect cells against oxidative stress and damage by detoxifying reactive oxygen species (ROS) and ROS-generated toxic metabolic products. They do this either directly by scavenging or indirectly through the activation of defense mechanisms. Asc and GSH are engaged in maintaining cellular redox homeostasis, being at the same time involved in redox signaling. They may interact with different molecules and signaling pathways during the resistance responses. Besides the total level of Asc and GSH in the cell the ratio between reduced and oxidized forms of these molecules play an important role in the activation of various defense mechanisms. Furthermore, glutathione is involved in specific functions such as detoxification of heavy metals, transfer and storage of sulfur, regulation of expression of defense-related genes and protein activity, while ascorbate acts as a signal-transducing molecule, cofactor of some enzymes and biosynthetic precursor of oxalic and l-tartaric acids. Moreover all kinds of xanthophylls cycle, considered as the most important photoprotective mechanism in plants, are strongly dependent on the acid form of ascorbate. The biochemical, physiological and genetic aspects of the involvement of ascorbate and glutathione, localized in different cell compartments, in controlling cellular redox state, plant stress tolerance, and defense mechanisms will be discussed.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Institutional subscriptions

References

  • Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie AR, Rothan C, Baldet P (2007) Changes in ascorbate redox state through silencing of L-galactono-1, 4-lactone dehydrogenase (L-GalLDH) affect plant and fruit development in tomato. Plant Physiol 145:1408–1422

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Pfannschmidt T (2000) Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Philos Trans R Soc Lond B Biol Sci 355:1351–1357

    Article  PubMed  CAS  Google Scholar 

  • Almagro L, Ros LVG, Belchi-Navarro S, Bru R, Barceló AR, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390

    Article  PubMed  CAS  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: Relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  PubMed  CAS  Google Scholar 

  • Anderson JV, Davis DG (2004) Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Plant 120:421–433

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal 5:55–67

    Article  PubMed  CAS  Google Scholar 

  • Arsalane W, Rousseau B, Duval J-C (1994) Influence of the pool size of the xanthophyll cycle on the effects of light stress in a diatom: competition between photoprotection and photoinhibition. Photochem Photobiol 60:237–243

    Article  CAS  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  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  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in chloroplasts. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Baier M, Dietz KJ (2005) Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56:1449–1462

    Article  PubMed  CAS  Google Scholar 

  • Baier M, Ströher E, Dietz KJ (2004) The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol 45:997–1006

    Article  PubMed  CAS  Google Scholar 

  • Baier M, Noctor G, Foyer C, Dietz KJ (2000) Antisense suppression of 2-Cys peroxiredoxin in Arabidopsis thaliana specifically enhances the activities and expression of enzymes associated with ascorbate metabolism, but not glutathione metabolism. Plant Physiol 124:823–832

    Article  PubMed  CAS  Google Scholar 

  • Ball L, Accotto G-P, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione synthesis and stress defence gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  CAS  Google Scholar 

  • Banhegyi G, Csala M, Szarka A, Varsanyi M, Benedetti A, Mandl J (2003) Role of ascorbate in oxidative protein folding. Biofactors 17:37–46

    Article  CAS  Google Scholar 

  • Banki K, Hutter E, Colombo E, Gonchoroff NJ, Perl A (1996) Glutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J Biol Chem 271:32994–33001

    Article  CAS  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 del Río LA (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  Google Scholar 

  • Barker JE, Heales SJR, Cassidy A, Bolaños JP, Land JM, Clarka JB (1996) Depletion of brain glutathione results in a decrease of glutathione reductase activity; an enzyme susceptible to oxidative damage. Brain Res 716:118–122

    Article  CAS  Google Scholar 

  • Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-11. Plant Physiol 134:1784–1792

    Article  CAS  Google Scholar 

  • Bartoli CG, Guiamet JJ, Kiddle G, Pastori G, Di Cagno R, Theodoulou FL, Foyer CH (2005) The relationship between L-galactono-1,4-lactone dehydrogenase (GalLDH) and ascorbate content in leaves under optimal and stress conditions. Plant, Cell and Environment 28:1073–1081

    Article  CAS  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer C (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–344

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Yu J, Gómez F, Fernández L, McIntosh L, Foyer CH (2006) Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J Exp Bot 57:1621–1631

    Article  PubMed  CAS  Google Scholar 

  • Bartoli C, Tambussi E, Diego F, Foyer CH (2009) Control of ascorbic acid synthesis and accumulation and glutathione by the incident light red/far red ratio in Phaseolus vulgaris leaves. FEBS Letters 583:118–122

    Article  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Murray RB, Russell LJ (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341

    Article  PubMed  CAS  Google Scholar 

  • Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, Leustek T (2001) Regulation of the plant-type 5´-adenylysulfate reductase by oxidative stress. Biochem 40:9040–9048

    Google Scholar 

  • Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls PNAS 106:12311–12316

    Google Scholar 

  • Bolwell GP, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F, Rowntree EG, Wojtaszek P (1999) Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells. Free Radical Research 31:S137–145

    Google Scholar 

  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a tree-component system. J Exp Bot 53:1367–1376

    Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Bratt CE, Arvidsson PE, Carlsson M, Ǻkerlund HE (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosyth Res 45:165–175

    Google Scholar 

  • Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz K-J, Radke D, Wirtz M, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T (2009) Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21:2715–2732

    Article  PubMed  Google Scholar 

  • Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    Article  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Bungard RA, Ruban AV, Hibberd JM, Press MC, HortonP SJD (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proc Natl Acad Sci USA 96:1135–1139

    Article  PubMed  CAS  Google Scholar 

  • Bulley S, Rassam M, Hoser D, Otto W, Schünemann N, Wright M, MacRae E, Gleave A, Laing W (2009) Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778

    Article  CAS  Google Scholar 

  • Burkey KO, Eason G, Fiscus EL (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiol Plant 117:51–57

    Article  CAS  Google Scholar 

  • Cagnac O, Bourbouloux A, Chakrabarty D, Zhang MY, Delrot S (2004) AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiol 135:1378–1387

    Article  CAS  Google Scholar 

  • Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455

    Article  CAS  Google Scholar 

  • Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Loureiro ME, Fernie AR (2003) Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol 133:1–14

    Article  CAS  Google Scholar 

  • Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environ Exp Bot 28:231–238

    Article  CAS  Google Scholar 

  • Chang CC-C, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499–511

    Article  CAS  Google Scholar 

  • Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Gallie DR (2005) Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol 138:1673–1689

    Article  CAS  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  CAS  Google Scholar 

  • Chen J, Goldsbrough PB (1994) Increased activity of [gamma]-glutamylcysteine synthetase in tomato cells selected for cadmium tolerance. Plant Physiol 106:233–239

    Article  CAS  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SCh, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  CAS  Google Scholar 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. JBC – J Biol Chem 278:46869–46877

    Article  CAS  Google Scholar 

  • Claquin P, Kromkamp JC, Martin-Jezquel V (2004) Relationship between photosynthetic metabolism and cell cycle in a synchronized culture of the marine alga Cylindrotheca fusiformis (Bacillariophyceae). Eur J Phycol 39:33–41

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) PHYTOCHELATINS AND METALLOTHIONEINS: Roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathionedeficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in c-glutamylcysteine synthetase. Plant J 16:73–78

    Article  PubMed  CAS  Google Scholar 

  • Coesel S, Obornik M, Varela J, Falciatore A, Bowler C (2008) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS ONE 3(8):e2896. doi:10.1371/journal.pone.0002896

    Article  PubMed  CAS  Google Scholar 

  • Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:3857–3868

    Article  CAS  Google Scholar 

  • Conklin PL, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970

    Article  CAS  Google Scholar 

  • Conklin PL, Pallanca JE, Last RL, Smirnoff N (1997) L-ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiol 115:1277–1285

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Williams EH, Last RL (1996) Environmental stress tolerance of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93:9970–9974

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856

    PubMed  CAS  Google Scholar 

  • Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littlechild JA, Smirnoff N (2006) Arabidopsis thaliana VTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 281:15662–15670

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci USA 96:4198–4203

    Article  CAS  Google Scholar 

  • Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856

    Article  CAS  Google Scholar 

  • Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93:9970–9974

    Article  CAS  Google Scholar 

  • Cosio C, Durand Ch (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408

    Article  PubMed  CAS  Google Scholar 

  • Creissen G, Firmin J, Fryer M, Kular B, Leykand N, Reynolds H, Pastori G, Wellburn F, Baker H, Wellburn A (1999) Elevated glutathione biosynthesis causes increased oxidative stress. Plant Cell 11:1277–1291

    Article  CAS  Google Scholar 

  • Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406

    Article  PubMed  CAS  Google Scholar 

  • Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, Rossi R (2008) Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10:445–473

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Darie CC, De Pascalis L, Mutschler B, Haehnel W (2006) Studies of the Ndh complex and photosystem II from mesophyll and bundle sheath chloroplasts of the C4-type plant Zea mays. J Plant Physiol 163:800–808

    Article  PubMed  CAS  Google Scholar 

  • Davey MW, Gilot C, Persiau G, Østergaard J, Han Y, Bauw GC, Van Montagu MC (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 121:535–543

    Article  CAS  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  CAS  Google Scholar 

  • DeBolt S, Cook DR, Ford CM (2006) L-Tartaric acid synthesis from vitamin C in higher plants. PNAS 103:5608–5613

    Article  CAS  Google Scholar 

  • Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WWIII, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trend Plant Sci 1:21–26

    Article  CAS  Google Scholar 

  • Davey MW, Gilot C, Persiau G, Østergaard J, Han Y, Bauw GC, Van Montagu MC (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 121:535–543

    Article  PubMed  CAS  Google Scholar 

  • Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, Neill SJ (2005) A Role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137:831–834

    Article  CAS  Google Scholar 

  • Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic 452 domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191

    Article  CAS  Google Scholar 

  • Deutsch JC (1998) Ascorbic acid oxidation by hydrogen peroxide. Anal Biochem 255:1–7

    Article  PubMed  CAS  Google Scholar 

  • Deutsch JC (2000) Dehydroascorbic acid. J Chromatogr A 881:299–307

    Article  PubMed  CAS  Google Scholar 

  • Dìaz M, Achkor H, Titarenko E, Martínez MC (2003) The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Letters 543:136–139

    Article  CAS  Google Scholar 

  • Díaz-Vivancos P, Barba-Espín G, Clemente-Moreno MJ, Hernández JA (2010) Characterization of the antioxidant system during the vegetative development of pea plants Biol Plant 54:76–82

    Article  CAS  Google Scholar 

  • Diaz-Vivancos P, Rubio M, Mesonero V, Periago PM, Barceló AR, Martínez-Gómez P, Hernández JA (2006) The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 57:3813–3824

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ (1996) Functions and responses of the leaf apoplast under stress. Prog Bot 58:221–254

    Google Scholar 

  • Dietz KJ (2005) Plant thiol enzymes and thiol homeostasis in relation to thiol-dependent redox regulation and oxidative stress. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, Oxford Publishers, pp 25–52

    Google Scholar 

  • Dietz KJ (2003) Redox control, redox signaling, and redox homeostasis in plant cells. Int Rev Cytol 228:141–193

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redoc metabolism. J Exp Bot 57:1697–1709

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ, Stork T, Finkemeier I, Lamkemeyer P, Li WX, El-Tayeb MA, Michel KP, Pistorius E, Baier M (2004) The role of peroxiredoxins in oxygenic photosynthesis of cyanobacteria and higher plants: peroxide detoxification or redox sensing? In: Demmig-Adams B, Adams W, Mattoo A (eds) Photoprotection, photoinhibition, gene regulation, and environment. Kluwer, Dordrecht, The Netherlands

    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  Google Scholar 

  • Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDP-l-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689

    Article  PubMed  CAS  Google Scholar 

  • Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ (1988) Glutathione and fungal elicitor regulation of a plant defense promoter in electroporated protoplasts. Proc Natl Acad Sci USA 85:6738–6742

    Article  CAS  Google Scholar 

  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79:331–348

    Article  CAS  Google Scholar 

  • Drozdowicz YM, Jones RL (1995) Hormonal regulation of organic and phosphoric acid release by barley aleurone layers and scutella. Plant Physiol 108:769–776

    PubMed  CAS  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defence gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  PubMed  CAS  Google Scholar 

  • Dutilleul C, Garnier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1–16

    Article  CAS  Google Scholar 

  • Edreva A (2005) Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31:105–124

    Article  CAS  Google Scholar 

  • Edwards R, Blount JW, Dixon RA (1991) Glutathione and elicitation of the phytoalexin response in legume cell cultures. Planta 184:403–409

    Article  CAS  Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson A, Eskling M, Åkerlund HE (2003) Chemical and mutational modification of histidines in violaxanthin de-epoxidase from Spinacia oleracea. Physiol Plant 84:218–224

    Google Scholar 

  • Escaler M, Aranda MA, Roberts IM, Thomas CL, Maule AJ (2000) A comparison between virus replication and abiotic stress (heat) as modifiers of host gene expression in pea. Mol Plant Pathol 1:159–167

    Article  CAS  Google Scholar 

  • Eskling M, Arvidsson PO, Åkerlund HE (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100:806–816

    Article  CAS  Google Scholar 

  • Esteve JM, Mompo J, De la Asunción JG, Sastre J, Asensi M, Boix J, Vinã JR, Vinã J, Pallardo FV (1999) Oxidative damage to mitochondrial DNA and glutathione oxidation in apoptosis: studiesin vivo and in vitro. FASEB J 13:1055–1064

    Article  CAS  Google Scholar 

  • Fernandez-García N, Martí MC, Jimenez A, Sewilla F, Enrique Olmos E (2009) Sub-cellular distribution of glutathione in an Arabidopsis mutant (vtc1) deficient in ascorbate. J Plant Physiol 166:2004–2012

    Article  PubMed  CAS  Google Scholar 

  • Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu Ch, Cabral A, Parker JE (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17:2601–2613

    Article  CAS  Google Scholar 

  • Ferrer JL, Jez JM, Bowman ME, Dixon RA, Noel JP (1999) Structure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nat Struci Biol 6:775–784

    Article  CAS  Google Scholar 

  • Filkowski J, Kovalchuk O, Kovalchuk I (2004) Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant J 38:60–69

    Article  CAS  Google Scholar 

  • Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds) Antioxidants in higher plants. CRC Press, Boca Raton, FL, pp 312–358

    Google Scholar 

  • Foyer C, Lelandais M (1996) A comparision of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mosophyll cells. J Plant Physiol 148:391–398

    Article  CAS  Google Scholar 

  • Fotopoulos V, Sanmartin M, Kanellis AK (2006) Effect of ascorbate oxidase over-expression on ascorbate recycling gene expression in response to agents imposing oxidative stress. J Exp Bot 57:3933–3943

    Article  PubMed  CAS  Google Scholar 

  • Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signaling. J Exp Bot 59:729–737

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Allen JF (2003) Lessons from redox signaling in plants. Antioxid Redox Signal 5:3–5

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Fletcher JM (2001) Plant antioxidants: colour me healthy. Biologist 48:115–120

    Article  CAS  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  Google Scholar 

  • Foyer CH, Lelandais M (1996) A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasma membranes of pea leaf mesophyll cells. J Plant Physiol 148:391–398

    Article  CAS  Google Scholar 

  • Foyer CH, Lopez-Delgrado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005a) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Theodoulou FL, Delrot S (2001) The functions of interand intracellular glutathione transport systems in plants. Trends Plant Sci 6:486–492

    Article  CAS  Google Scholar 

  • Franceschi VR, Nakata PA (2005) CALCIUM OXALATE IN PLANTS: Formation and Function. Annu Rev Plant Biol 56:41–71

    Article  CAS  Google Scholar 

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1996) The lifetimes and energies of the first excited singlet states of diadinoxanthin and diatoxanthin: the role of these molecules in excess energy dissipation in algae. Biochim Biophys Acta 1277:243–252

    Article  PubMed  CAS  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    Article  CAS  Google Scholar 

  • Fridovich I (1986) Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 58:61–97

    PubMed  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    Article  PubMed  CAS  Google Scholar 

  • De Gara (2004) L: Ascorbate and plant growth: from germination to cell death. In Vitamin C Functions and Biochemistry in Animals and Plants. Asard H, May JM, Smirnoff N (eds) Oxford: BIOS Scientific Publishers, vol 1, pp 83–89

    Article  CAS  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  Google Scholar 

  • Gao XH, 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  Google Scholar 

  • Gao Q, Zhang LX (2008) Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana. J Plant Physiol 165:138–148

    Article  CAS  Google Scholar 

  • Garcia-Plazaola JI, Hernandez A, Errasti E, Becerril JM (2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Funct Plant Biol 29:1075–1080

    Article  CAS  Google Scholar 

  • Garcia-Plazaola JI, Hernandez A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Funct Plant Biol 30:319–324

    Article  CAS  Google Scholar 

  • Garcia-Plazaola JI, Matsubara S, Osmond CB (2007) Review: The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773

    Article  CAS  Google Scholar 

  • Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis. Plant J 30:541–553

    Article  CAS  Google Scholar 

  • Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 168:17–20

    Article  PubMed  CAS  Google Scholar 

  • Ghezzi P (2005) Oxidoreduction of protein thiols in redox regulation. Biochem Soc Trans 33:1378–1381

    Article  CAS  Google Scholar 

  • Ghezzi P (2005a) Regulation of protein function by glutathionylation. Free Radic Res 39:573–580

    Article  CAS  Google Scholar 

  • Ghezzi P (2005b) Oxidoreduction of protein thiols in redox regulation. Biochem Soc Trans 33:1378–1381

    Article  CAS  Google Scholar 

  • Ghezzi P, Di Simplicio P (2007) Glutathionylation pathways in drug response. Curr Opin Pharmacol 7:398–403

    Article  CAS  Google Scholar 

  • Giacomelli L, Rudella A, van Wijk KJ (2006) High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiol 141:685–701

    Article  PubMed  CAS  Google Scholar 

  • Gillham DJ, Dodge AD (1986) Hydrogen-peroxide scavenging systems within pea chloroplasts. A quantitative study. Planta 167:246–251

    Article  CAS  Google Scholar 

  • Gillham DJ, Dodge AD (1987) Chloroplast superoxide and hydrogen-peroxide scavenging systems from pea leaves. Seasonal variations. Plant Sci 50:105–109

    Article  CAS  Google Scholar 

  • Giovannoni JJ (2007) Completing a pathway to plant vitamin C synthesis. PNAS 104:9109–9110

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J, Ausubel FM (1994) Isolation of phytoalexindeficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA, 91:8955–8959

    Article  CAS  Google Scholar 

  • Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982

    Article  CAS  Google Scholar 

  • Glazebrook J, Zook M, Merrit F, Kagan I, Rogers EE, Crute IR, Holub EB, Hammerschmidt R, Ausubel FM (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146:381–392

    Article  CAS  Google Scholar 

  • Gomez LD, Vanacker H, Buchner P, Noctor G, Foyer CH (2004a) Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134:1662–1671

    Article  CAS  Google Scholar 

  • Gomez LD, Noctor G, Knight MR, Foyer CH (2004b) Regulation of calcium signalling and gene expression by glutathione. J Exp Bot 55:1851–1859

    Article  CAS  Google Scholar 

  • Gonzalez-Reyes JA, Hidalgo A, Caler JA, Palos R, Navas P (1994) Nutrient-uptake changes in ascorbate free radical-stimulated onion roots. Plant Physiol 104:271–276

    PubMed  CAS  Google Scholar 

  • Goss R, Böhme K, Wilhelm C (1998) The xanthophylls cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta 205:613–621

    Article  CAS  Google Scholar 

  • Goss R (2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217:801–812

    Article  PubMed  CAS  Google Scholar 

  • Grace SC, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylopropanoid pathway. Phil Trans R Soc Lond 355:1499

    Article  PubMed  CAS  Google Scholar 

  • Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signalling in plant disease resistance. Plant Physiol 124:21–29

    Article  PubMed  CAS  Google Scholar 

  • Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433:83–87

    Article  PubMed  CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2006) Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol Plant 126:205–211

    Article  CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2008) A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 49(8):1217–25

    Article  PubMed  CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2009) The regulation of xanthophyll cycle activity ­and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 1787(7):929–938

    Article  PubMed  CAS  Google Scholar 

  • Gruszecki WI, Strzałka K (1991) Does the xanthophyll cycle takes part in the regulation of the fluidity of the thylakoid membrane? Biochim Biophys Acta 1060:310–314

    Article  CAS  Google Scholar 

  • Gukasyan HJ, Lee VHL, Kim KJ, Kannan R (2002) Net glutatione secretion across primary cultured rabbit conjunctival epithelial cell layers. Investigative Ophthalmology Visual Sci 43:1154–1161

    Article  PubMed  CAS  Google Scholar 

  • Gullner G, Kömives T, Rennenberg H (2001) Enhanced tolerance of transgenic poplar plants overexpressing gamma-glutamylcysteine synthetase towards chloroacetanilide herbicides. J Exp Bot 52:971–979

    Google Scholar 

  • Guo Z-J, Lamb Ch, Dixon RA (1998) Potentiation of the oxidative burst and isoflavonoid phytoalex in accumulation by serine protease inhibitors. Plant Physiol 118:1487–1494

    Google Scholar 

  • Gupta AS, Alscher RG, McCune D (1991) Response of photosynthesis and cellular antioxidants to ozone in populus leaves. Plant Physiol 96:650–655

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  PubMed  CAS  Google Scholar 

  • Hancock RD, Viola R (2005) Biosynthesis and catabolism of L-ascorbic acid in plants. Crit Rev Plant Sci 24:167–188

    Google Scholar 

  • Harada E, Yamaguchia Y, Koizumia N, Hiroshia S (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159:445–448

    Article  PubMed  CAS  Google Scholar 

  • Harms K, Von Ballmoos P, Brunold C, Höfgen R, Hesse H (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J 22:335–343

    Article  PubMed  CAS  Google Scholar 

  • Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplastenkompartiment als Ursache der enzymatischen Violaxanthin- Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta 89:224–243

    Article  CAS  Google Scholar 

  • Hartung W, Radin JW, Hendrix DL (1988) Abscisic-acid movement into the apoplastic solution of water-stressed cotton leaves – role of apoplastic pH. Plant Physiol 86:908–913

    Article  PubMed  CAS  Google Scholar 

  • Havaux M (2003) Spontaneous and thermoinduced photon emission: New methods to detect and quantify oxidative stress in plants. Trends Plant Sci 8:409–413

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Gruszecki WI, Dupont I, Leblanc RM (1991) Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J Photochem Photobiol B Biol 8:361–370

    Article  CAS  Google Scholar 

  • Herbinger K, Tausz M, Wonisch A, Soja G, Sorger A, Grill D (2002) Complex interactive effects of drought and ozone stress on the antioxidant defence systems of two wheat cultivars. Plant Physiol Biochem 40:691–696

    Article  PubMed  CAS  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2 .-/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed  CAS  Google Scholar 

  • Herschbach C, Rennenberg H (1995) Long-distance transport of 35S-sulphur in 3-year-old beech trees (Fagus sylvatica). Physiol Plant 95:379–386

    Article  PubMed  CAS  Google Scholar 

  • Herschbach C, Scheerer U, Ronnenberg H (2009) Redox states of glutathione and ascorbate in root tips of poplar (Populus tremulaxP. alba) depend on Pohlem transport from the shoot to the roots. J Exp Bot 61(4):1–10

    Google Scholar 

  • Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM (2007) Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19:2653–2661

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo A, Gonzalez-Reyes JA, Navas P (1989) Ascorbate free radical enhances vacuolisation in onion root meristems. Plant Cell Environ 12:455–460

    Article  CAS  Google Scholar 

  • Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulphur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulphur nutrition. Plant J 33:651–663

    Article  PubMed  CAS  Google Scholar 

  • Hisabori T, Motohashi K, Hosoya-Matsuda N, Ueoka-Nakanishi H, Romano PGN (2007) Towards a functional dissection of thioredoxin networks in plant cells. Photochem Photobiol 83: 145–151

    Article  PubMed  CAS  Google Scholar 

  • Hofius D, Hajirezaei M-R, Geiger M, Tschiersch H, Melzer M, Sonnewald U (2004) RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiol 135:1256–1268

    Article  PubMed  CAS  Google Scholar 

  • Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5:263–267

    Article  PubMed  CAS  Google Scholar 

  • Horling F, Lamkemeyer P, König J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325

    Article  PubMed  CAS  Google Scholar 

  • Horner HT, Kausch AP, Wagner BL (2000) Ascorbic acid: a precursor of oxalate in crystal idioblasts of Yucca torreyi in liquid root culture. Int J Plant Sci 161:861–868

    Article  PubMed  CAS  Google Scholar 

  • Hothorn M, Wachter A, Gromes R, Stuwe T, Rausch T, Scheffzek K (2006) Structural basis for the redox control of plant glutamate cysteine ligase. J Biol Chem 281:27557–27565

    Google Scholar 

  • Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995) Cadmium sensitive, glutathione deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073

    Article  PubMed  CAS  Google Scholar 

  • Hurd TR, Filipovska A, Costa NJ, Dahm CC, Murphy MP (2005) Disulphide formation on mitochondrial protein thiols. Biochemical Society Transactions 33:1390–1393

    Article  PubMed  CAS  Google Scholar 

  • Hwang C, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257:1496–1502

    Article  PubMed  CAS  Google Scholar 

  • Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, 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  PubMed  CAS  Google Scholar 

  • Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355

    Article  CAS  Google Scholar 

  • Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Iwabuchi M, Ogawa K (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  PubMed  CAS  Google Scholar 

  • Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis Mutant by extracellular superoxide. Science 273:1853–1856

    Article  PubMed  CAS  Google Scholar 

  • Jahns P, Latowski D, Strzałka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  PubMed  CAS  Google Scholar 

  • Jakob T, Goss R, Wilhelm C (2001) Unusual pH-dependence of diadinoxanthin de-epoxidase activation causes chlororespiratory induced accumulation of diatoxanthin in the diatom Phaeodactylum tricornutum. J Plant Physiol 158:383–390

    Article  CAS  Google Scholar 

  • Jez JM, Cahoon RE, Chen S (2004) Arabidopsis thaliana glutamatecysteine ligase. Functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279:33463–33470

    Article  PubMed  CAS  Google Scholar 

  • Jiménez A, Hernández JA, Pastori G, del Río 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  Google Scholar 

  • Jiménez A, Hernández JA, del Río 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  Google Scholar 

  • Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signalling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  PubMed  CAS  Google Scholar 

  • José A, Hernández FMA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O ._2 /H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  Google Scholar 

  • Karpinska B, Wingsle G, Karpinski S (2000) Antagonistic effects of hydrogen peroxide and glutathione on acclimation to excess excitation energy in Arabidopsis. IUBMB Life 50:21–26

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Escobar C, Karprinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    PubMed  CAS  Google Scholar 

  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defense signaling. Curr Opin Plant Biol 6:390–396

    Article  PubMed  CAS  Google Scholar 

  • Karpinska B, Karlsson M, Schinkel H, Streller S, Suss KH, Melzer M, Wingsle G (2001) A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization. Plant Physiol 126:1668–1677

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999a) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  PubMed  CAS  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

    Article  PubMed  CAS  Google Scholar 

  • Keates SE, Tarlyn NM, Loewus FA, Franceschi VR (2000) L-Ascorbic acid and L-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochem 53:433–440

    Article  PubMed  CAS  Google Scholar 

  • Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5:23–32

    Article  PubMed  CAS  Google Scholar 

  • Kingston-Smith AH, Foyer CH (2000) Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures. J Exp Bot 51:123–130

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Brunner M, Riiegsegger A, Stamp P, Brunold Ch (1996) Glutathione synthesis in maize genotypes with different sensitivities to chilling. Planta 198:365–370

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Szalai G, Galiba G (2004a) Effect of osmotic stress on glutathione and hydroxymethylglutathione accumulation in wheat. J Plant Physiol 161:785–794

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Szalai G, Vágújfalvi A, Stéhli L, Orosz G, Galiba G (2000) Genetic study of glutathione accumulation during cold hardening in wheat. Planta 210:295–301

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Kobrehel K, Szalai G, Duviau M-P, Buzás Z, Galiba G (2004b) Abiotic stress-induced changes in glutathione and thioredoxin h levels in maize. Environ Exp Bot 52:101–112

    Article  PubMed  CAS  Google Scholar 

  • Kollist H, Moldau H, Oksanen E, Vapaavuori E (2008) Ascorbate transport from the apoplast to the symplast in intact leaves. Physiol Plant 113:377–383

    Article  Google Scholar 

  • Koprivova A, Kopriva S, Jäger D, Will B, Jouanin L, Rennenberg H (2002) Evaluation of transgenic poplar over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium. Plant Biol 4:664–670

    Google Scholar 

  • Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of sulfate assimilation by salt stress in Arabidopsis roots. Plant Physiol. 146:1408–1420

    Google Scholar 

  • Kopriva S, Wiedemann G, Reski R (2007) Sulfate assimilation in basal land plants – what does genomic sequencing tell us? Plant Biol 9:556–564

    Google Scholar 

  • Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842

    Google Scholar 

  • Kostman TA, Tarlyn NM, Loewus FA, Franceschi VR (2001) Biosynthesis of L-Ascorbic Acid and conversion of carbons 1 and 2 of L-Ascorbic Acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. Plant Physiol 125:634–640

    Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinasecascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Birtić S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: universal stress marker and modulator of programmed cell death? Free Radic Biol Med 40:2155–2165

    Article  PubMed  CAS  Google Scholar 

  • Kristensen BK, Askerlund P, Bykova NV, Egsgaard H, Moller IM (2004) Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatographytandem mass spectrometry. Phytochemistry 65:1839–1851

    Article  PubMed  CAS  Google Scholar 

  • Kurganova LN, Veselov AP, Sinitsina YV, Elikova EA, Kulaeva ON (1999) Lipid peroxidation products as possible mediators of heat stress response in plants. Russ J Plant Physiol 46:181–185

    Article  PubMed  CAS  Google Scholar 

  • Kuźniak E, Niewiadomska E, Miszalski Z, Karpinski S (2009) The role of chloroplasts and redox status in holistic regulation of stress responses in plants. In: Maksymiec W (ed) Compartmentation of responses to stresses in higher plants, true or false. Transworld Research Network (ISBN: 978-81-7895-422-6), pp 163–192

    Article  PubMed  CAS  Google Scholar 

  • Kuźniak E, Skłodowska M (2005) Compartment-specific role of the ascorbate–glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. J Exp Bot 56:921–933

    Article  PubMed  CAS  Google Scholar 

  • Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content. PNAS, USA 104:9534–9539

    Article  CAS  Google Scholar 

  • Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schottler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A, Weis E, Miginiac-Maslow M, Dietz KJ (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981

    Article  PubMed  CAS  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    Article  PubMed  CAS  Google Scholar 

  • Lee SK, Kader AA (2000) Preharvest and postharvest factors influencing vitamin C content of horticultural crops. Post Harv Biol Technol 20:207–220

    Article  CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  CAS  Google Scholar 

  • Lin LS, Varner JE (1991) Expression of ascorbate oxidase in zucchini squash (Cucurbita pepo L.). Plant Physiol 96:159–165

    Article  PubMed  CAS  Google Scholar 

  • Linster CL, Gomez TA, Christensen KC, Adler LN, Young BD, Brenner C, Clarke SG (2007) Arabidopsis VTC2 encodes a GDP-L-galactose phosphorylase, the last unknown enzyme in the Smirnoff–Wheeler pathway to ascorbic acid in plants. J Biol Chem 282: 18879–18885

    Article  PubMed  CAS  Google Scholar 

  • Linster CL, Clarke SG (2008) L-Ascorbate biosynthesis in higher plants: the rope of VTC2. Trends Plant Sci 13:567–573

    Article  PubMed  CAS  Google Scholar 

  • Logan BA, Barker DH, Demmig-Adamas B, Adams WW III (1996) Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest. Plant Cell Environ 19:1083–1090

    Article  CAS  Google Scholar 

  • Van Loon LC, Pierpoint WS, Boller T, Conejero V (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12:254–264

    Article  CAS  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  CAS  Google Scholar 

  • López-Carbonell M, Munné-Bosch S, Alegre L (2006) The ascorbate-deficient vtc-1 Arabidopsis mutant shows altered ABA accumulation in leaves and chloroplasts. J Plant Growth Regul 25:137–144

    Article  CAS  Google Scholar 

  • Lyons T, Ollerenshaw J, Barnes JD (1999) Impacts of ozone on Plantago major: apoplastic and symplastic antioxidant status. New Phytol 141:253–263

    Article  CAS  Google Scholar 

  • Madamanchi NR, Alscher RG (1991) Metabolic bases for differences in sensitivity of two Pea cultivars to sulfur dioxide. Plant Physiol 97:88–93

    Article  CAS  Google Scholar 

  • Mahalingam R, Fedoroff NV (2003) Stress response, cell death and signaling: the many faces of ROS. Physiol Plant 119:56–68

    Article  CAS  Google Scholar 

  • Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4:R20. Epub 2003

    Article  CAS  Google Scholar 

  • Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and coresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15:2331–2342

    PubMed  CAS  Google Scholar 

  • Marrè MT, Albergoni FG, Moroni A, Marrè E (1989) Light-induced activation of electrogenic HR extrusion and KR uptake in Elodea densa depends on photosynthesis and is mediated by the plasma membrane ATPase. J Exp Bot 40:343–352

    Article  Google Scholar 

  • Maruta T, Yonemitsu M, Kabuta Y, Tamoi M, Ishikawa T, Shigeoka S (2008) Arabidopsis phosphomannose isomerase 1, but not phosphomannose isomerase 2, is essential for ascorbic acid biosynthesis. J Biol Chem 283:28842–28851

    Article  PubMed  CAS  Google Scholar 

  • Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807

    Article  PubMed  CAS  Google Scholar 

  • Matsubara S, Gilmore AM, Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii. Aust J Plant Physiol 28:792–800

    Google Scholar 

  • Matsubara S, Morosinotto T, Bassi R, Christian AL, Fischer-Schliebs E, Luttge U, Orthen B, Franco AC, Scarano FR, Forster B, Pogson BJ, Osmond CB (2003) Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217:868–879

    Article  PubMed  CAS  Google Scholar 

  • Matsubara S, Naumann M, Martin R, Nichol C, Rascher U, Morosinotto T, Bassi R, Osmond B (2005) Slowly reversible de-epoxidation of luteinepoxide in deep shade leaves of a tropical tree legume may ‘lock in’ lutein-based photoprotection during acclimation to strong light. J Exp Bot 56:461–468

    Article  PubMed  CAS  Google Scholar 

  • May MJ, Leaver CJ (1994) Arabidopsis thaliana c-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs. Proc Natl Acad Sci USA 91:10,059–10,063

    Article  PubMed  CAS  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    Article  PubMed  CAS  Google Scholar 

  • Mehlhorn H, Lelandais M, Korth HG, Foyer CH (1996) Ascorbate is the natural substrate for plant peroxidases? FEBS Lett 378:203–206

    Article  PubMed  CAS  Google Scholar 

  • Melhorn H (1990) Ethylene-promoted ascorbate peroxidase activity protects plants against hydrogen peroxide, ozone and paraquat. Plant Cell Environ 13:971–976

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulphur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671

    Article  PubMed  CAS  Google Scholar 

  • Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403

    Article  PubMed  CAS  Google Scholar 

  • Meyer AJ, Hell R (2005) Glutathione homeostasis and redoxregulation by sulfhydryl groups. Photosynth Res 86:435–457

    Article  PubMed  CAS  Google Scholar 

  • Michelet L, Zaffagnini M, Massot V, Keryer E, Vanacke H, Miginiac-Maslow M, Issakidis-Bourguet E, Lemaire SD (2006) Thioredoxins, glutaredoxins, and glutathionylation: new crosstalks to explore. Photosynth Res 89:225–245

    Article  PubMed  CAS  Google Scholar 

  • Mieda T, Kabuta Y, Rapolu M, Motoki T, Takeda T, Yoshimura K, Ishikawa T, Shigeoka S (2004) Feedback inhibition of spinach L-galactose dehydrogenase by L-ascorbate. Plant Cell Physiol 45:1271–1279

    Article  PubMed  CAS  Google Scholar 

  • Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Merquiol E, Hallk HE, Rachmilevitch S, Kaplan A, Cohen M (2001) Living under a “dormant” canopy: a molecular acclimation mechanism of the desert plant Retama raetam. Plant J 25:407–416

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Mittova V, Guy G, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    Article  PubMed  CAS  Google Scholar 

  • Møller IM, Kristensen BK (2004) Protein oxidation in plant mitochondria as a stress indicator. Phytochem Photobiol Sci 3:730–735

    Article  CAS  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTS). Plant Hormones 72:155–202

    Article  CAS  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113–935

    Article  CAS  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  CAS  Google Scholar 

  • Müller-Moulé P, Conklin PL, Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128:970–977

    Article  CAS  Google Scholar 

  • Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48

    Article  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141:346–350

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Alegre L (2003) Drought-induced changes in the redox state of α-tocopherol, ascorbate, and the diterpene carnosic acid in chloroplasts of Labiatae Species differing in carnosic acid contents. Plant Physiol 131:1816–1825

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Falk J (2004) New insights into the function of tocopherols in plants. Planta 218:323–326

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Weiler EW, Alegre L, Müller M, Düchting P, Falk J (2007) a-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta 225:681–691

    Article  PubMed  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2R channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    PubMed  CAS  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  Google Scholar 

  • Müller-Moulé P, Conklin PL, Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128:970–977

    Article  PubMed  CAS  Google Scholar 

  • Müller-Moulé P, Golan T, Niyogi KK (2004) Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol 134:1163–1172

    Article  PubMed  CAS  Google Scholar 

  • Müller-Moulé P, Havaux M, Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133:748–760

    Article  PubMed  CAS  Google Scholar 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot J-P, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    Article  PubMed  CAS  Google Scholar 

  • Neubauer C, Yamamoto HY (1994) Membrane barriers and Mehler-peroxidase reaction limit the ascorbate availability for violaxanthin de-epoxidase activity in intact chloroplasts. Photosynth Res 39:137–147

    Article  PubMed  CAS  Google Scholar 

  • Nieto-Sotclo J, Ho T-HD (1986) ElTect of heal shock on the metabolism of glutathione in maize roots. Plant Physiol 82:1031–1015

    Article  PubMed  CAS  Google Scholar 

  • Niewiadomska E, Borland AM (2008) Crassulacean acid metabolism: a cause or consequence of oxidative stress in planta? In: Lüttge UE, Beyschlag W, Murata J (eds): Progress in botany 69. Springer-Verlag, Berlin, Heidelberg 247 (ISBN: 978-3-540-72953-2)

    Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Current Opinion Plant Biol 3:455–460

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Björkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67:139–145.

    Article  PubMed  CAS  Google Scholar 

  • Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Queval G, Gakiere B (2006) NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. J Exp Bot 57:1603–1620

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50:1093–1106

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137:611–622

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Sweetlove LJ, Fernie AR (2007) The influence of the tricarboxylic acid cycle on photosynthetic metabolism of the illuminated leaf. Physiol Plant 129:45–56

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Sulpice R, Gibon Y, Fernie AR (2008) The enigmatic contribution of mitochondrial function in Photosynthesis. J Exp Bot 59:1675–1684

    Article  PubMed  CAS  Google Scholar 

  • Ohashi Y, Matsuoka M (1987) Induction and secretion of pathogenesis-related proteins by salicylate or plant hormones in tobacco suspension cultures. Plant Cell Physiol 28:573–580

    CAS  Google Scholar 

  • Olaizola M, La Roche J, Kolber Z, Falkowski P (1994) Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41:357–370

    Article  CAS  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Packer JE, Slater TF, Willson RL (1979) Direct observation of a free radical interaction between vitamin E and vitamin C Nature (London) 278:737–738

    Article  PubMed  CAS  Google Scholar 

  • Padh H (1990) Cellular functions of ascorbic acid Biochem Cell Biol 68:1166–1173

    Article  PubMed  CAS  Google Scholar 

  • Pallanca JE, Smirnoff N (2000) The control of ascorbic acid synthesis and turnover in pea seedlings. J Exp Bot 51:669–674

    Article  PubMed  CAS  Google Scholar 

  • Panchuk II, Volkov RA, Schöffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  PubMed  CAS  Google Scholar 

  • Papadakis AK, Paschalidis KA, Roubelakis-Angelakis KA (2005a) Biosynthesis profile and endogenous titers of polyamines differ in totipotent and recalcitrant plant protoplasts. Physiol Plant 125:10–20

    Article  CAS  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (2005b) Polyamines inhibit NADPH oxidase-mediated superoxides generation and putrescine prevents programmed cell death syndrome induced by the polyamine oxidase generated hydrogen peroxide. Planta 220:826–837

    Article  PubMed  CAS  Google Scholar 

  • Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a -glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172

    Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005a) Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant: correlations with age, cell division/expansion, and differentiation. Plant Physiol 138:142–152

    Article  PubMed  CAS  Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005b) Sites and regulation of polyamine catabolism in the tobacco plant: Correlations with cell division/expansion, cell-cycle progression, and vascular development. Plant Physiol 138:2174–2184

    Article  PubMed  CAS  Google Scholar 

  • Pasqualini S, Batini P, Ederli L, Porceddu A, Piccioni C, De Marchis F, Antonielli M (2001) Effects of short-term ozone fumigation on tobacco plants: response of the scavenging system and expression of the glutathione reductase. Plant Cell Environ 24:245–252

    Article  PubMed  CAS  Google Scholar 

  • Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks and pathways of cross tolerance to stress. The central role of ‘redox’ and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes controlling development through hormone signaling. Plant Cell 15:1212–1226

    Article  CAS  Google Scholar 

  • Pastori GM, Mullineaux PM, Foyer CH (2000) Posttranscriptional regulation prevents accumulation of glutathione reductase protein and activity in the bundle sheath cells of maize. Plant Physiol 122:667–675

    Article  PubMed  CAS  Google Scholar 

  • Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400

    Article  PubMed  CAS  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  PubMed  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Allen JF, Oelmuller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112:1–9

    Article  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Liege K (2005) Redox regulation and modification of proteins controlling chloroplast gene expression. Antioxid Redox Signal 7:607–618

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Bräutigam K, Wagner R, Dietzel L, Schröter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103:599–607

    Article  PubMed  CAS  Google Scholar 

  • Pfanz H, Dietz KJ (1987) A fluorescence method for the determination of the apoplastic proton concentration in intact leaf tissues. J Plant Physiol 129:41–48

    Article  CAS  Google Scholar 

  • Pifanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MOL modulator of defense and cell death is responsive to biotic and abiotic stimuli. Plant Physiol 120:1076–1085

    Article  CAS  Google Scholar 

  • Pignocchi C, Fletcher JM, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase (AO) in tobacco (Nicotiana tabacum L.). Plant Physiol 132:1631–1641

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6:379–389

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Kiddle G, Hernández I, Asensi A, Taybi T, Barnes JD, Foyer CH (2006) Apoplast redox state modulates gene transcription leading to modified hormone signalling and defence in tobacco. Plant Physiol 141:423–435

    Article  PubMed  CAS  Google Scholar 

  • Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25:142–152

    Article  PubMed  CAS  Google Scholar 

  • Pineau B, Layoune O, Danon A, De Paepe R (2008) L-galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 283: 32500–32505

    Article  PubMed  CAS  Google Scholar 

  • de Pinto MC, De Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55:2559–2569

    Article  PubMed  CAS  Google Scholar 

  • de Pinto MC, Francis D, De Gara L (1999) The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209:90–97

    Article  PubMed  Google Scholar 

  • de Pinto MC, Tommasi F, De Gara L (2000) Enzymes of the ascorbate biosynthesis and ascorbate–glutathione cycle in cultured cells of tobacco Bright Yellow 2. Plant Physiol Biochem 38:541–550

    Article  Google Scholar 

  • Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:59–198

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Horemans N, Bellone S, Caubergs J, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Horemans N, Caubergs RJ, Asard H (2000) Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension. Plant Physiol 124:17–20

    Article  PubMed  CAS  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    Article  PubMed  CAS  Google Scholar 

  • Preger V, Scagliarini S, Pupillo P, Trost P (2005) Identification of an ascorbate-dependent ­cytochrome b of the tonoplast membrane sharing biochemical features with members of the cytochrome b561 family. Planta 220:365–375

    Article  PubMed  CAS  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–16

    Article  PubMed  CAS  Google Scholar 

  • Queval G, Hager J, Gakière B, Noctor G (2008) Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts. J Exp Bot 59:135–146

    Article  PubMed  CAS  Google Scholar 

  • Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakière B, Vanacker H, Miginiac-Maslow M, Van Breusegem F, Noctor G (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J 52:640–657

    Article  PubMed  CAS  Google Scholar 

  • Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakiere B, Noctor G (2009) H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol Plant 2:344–356

    Article  PubMed  CAS  Google Scholar 

  • Quinones MA, Zeiger E (1994) A putative role of the xanthophyll, zeaxanthin, in blue light photoreception of corn coleoptiles. Science 264:558–561

    Article  CAS  Google Scholar 

  • Rabinowitch HD, Budowski P, Kedar N (1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122:91–97

    Article  PubMed  CAS  Google Scholar 

  • Rautenkranz AAF, Li L, Machler F, Martinoia E, Oertli JJ (1994) Transport of ascorbic and dehydroascorbic acid across protoplasts and vacuole membranes isolated from barley (Hordeum vulgare L. cv. Gerbel) leaves. Plant Physiol 106:187–193

    Article  PubMed  CAS  Google Scholar 

  • Rausch T, Gromes R, Liedschulle V, Müller I, Bogs J, Galovic V, Wachter A (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol 9:565–572

    Article  PubMed  CAS  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    Article  PubMed  CAS  Google Scholar 

  • Rennenberg H (1980) Glutathione metabolism and possible biological roles in higher plants. Phytochemistry 21:2771–2781

    Article  Google Scholar 

  • Rennenberg H, Herschbach C, Haberer K, Kopriva S (2007) Sulfur metabolism in plants: are trees different? Plant Biol 9:620–637

    Article  PubMed  CAS  Google Scholar 

  • Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479

    Article  PubMed  CAS  Google Scholar 

  • Retsky KL, Freeman MW, Frei B (1993) Ascorbic acid oxidation product(s) protect human low density lipoprotein against atherogenic modification. J Biol Chem 268:1304–1309

    PubMed  CAS  Google Scholar 

  • del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272

    Article  PubMed  Google Scholar 

  • Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inzé D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342

    Article  PubMed  CAS  Google Scholar 

  • Robinson JM, Bunce JA (2000) Influence of drought-induced water stress on soybean and spinach leaf ascorbate-dehydroascorbate level and redox status. Int J Plant Sci 161:271–279

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez AA, Grunberg KA, Taleisnik EL (2002) Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol 129:1627–1632

    Article  PubMed  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  CAS  Google Scholar 

  • Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ 29:269–281

    Article  PubMed  CAS  Google Scholar 

  • Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  PubMed  CAS  Google Scholar 

  • Ruiz JM, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969

    Article  PubMed  CAS  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism, the long and smelling road. Plant Physiol 136:2443–2450

    Article  PubMed  CAS  Google Scholar 

  • Sakuta M (2000) Transcriptional control of chalcone synthase by environmental stimuli. J Plant Res 113:327–333

    Article  PubMed  CAS  Google Scholar 

  • Sanmartin M, Drogouti PD, Lyons T, Barnes J, Kanellis AK (2003) Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216:918–928

    PubMed  CAS  Google Scholar 

  • Sandermann H Jr, Ernst D, Heller W, Langebartels C (1998) Ozone: an abiotic elicitor of plant defense reactions. Trends Plant Sci 3:47–50

    Article  Google Scholar 

  • Sapozhnikov DI, Krasovskaya TA, Maevskaya AN (1957) Change in the interrelationship of the basic carotenoids of the plastids of green leaves under the action of light. Dokl Akad Nauk USSR 113:465–467

    CAS  Google Scholar 

  • Sarry JE, Montillet JL, Sauvaire Y, Havaux M (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 353:147–150

    Article  PubMed  CAS  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  PubMed  CAS  Google Scholar 

  • Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167–192

    Article  CAS  Google Scholar 

  • Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  PubMed  CAS  Google Scholar 

  • Schäfer HJ, Haag-Kerwer A, Rausch T (1998) cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy metal accumulator Brassica juncea L: evidence for Cd induction of a putative mitochondrial -glutamylcysteine synthetase isoform. Plant Mol Biol 37:87–97

    Article  PubMed  CAS  Google Scholar 

  • Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489

    Article  PubMed  CAS  Google Scholar 

  • Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J 55:774–786

    Article  PubMed  CAS  Google Scholar 

  • Scheerer U, Haensch R, Mendel RR, Kopriva S, Rennenberg H, Herschbach C (2010) Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5’-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing g-ECS, SO, or APR. J Exp Bot 61:609–622

    Article  PubMed  CAS  Google Scholar 

  • Schopfer P, Liszkai A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    Article  PubMed  CAS  Google Scholar 

  • Schöner S, Krause GH (1990) Protective systems against active oxygen species in spinach. Response to cold-acclimation in excess light. Planta 180:383–389

    Article  Google Scholar 

  • Schupp R, Rennenberg H (1988) Diurnal changes in the glutathione concentration of spruceneedles (Picea abies L.). Plant Sci 57:113–117

    Article  CAS  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  Google Scholar 

  • Sen CK (2000) Cellular thiols and redox-regulated signal transduction. Curr Top Cell Regul 36:1–30

    Article  PubMed  CAS  Google Scholar 

  • Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211

    Article  PubMed  CAS  Google Scholar 

  • Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14

    Article  PubMed  CAS  Google Scholar 

  • Siefermann-Harms D (1985) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochim Biophys Acta 811:325–335

    Article  CAS  Google Scholar 

  • Singla-Pareek SL, Reddy MK, Sopory SK (2003) Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc Natl Acad Sci USA 100:14672–14677

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    Article  CAS  Google Scholar 

  • Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235

    PubMed  CAS  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Dowdle J, Ishikawa T (2007) The role of VTC2 in vitamin C biosynthesis in Arabidopsis thaliana. Comp Biochem Physiol A 146:S250

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Running JA, Gatzek S (2004) Ascorbate biosynthesis: a diversity of pathways. In: Asard H, May JM, Smirnoff N (eds) Vitamin C. Functions and biochemistry in animals and plants. BIOS Scientific Publishers, Oxford, pp 7–29

    Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314

    Article  PubMed  CAS  Google Scholar 

  • Smith IK, Pole A, Rennenberg H (1990) Glutathione. In: Alscher RG, Cumming J (eds) Stress responses in plants: adaptation and acclimation mechanisms. Wiley-Liss, New York,pp 201–217

    Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  PubMed  CAS  Google Scholar 

  • Srivastava A, Zeiger E (1995) The inhibitor of zeaxanthin formation, dithiothreitol, inhibits blue-light stimulated stomatal opening in Vicia faba. Planta 196:445–449

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  PubMed  CAS  Google Scholar 

  • Sweetlove L, Fait A, Nunes-Nesi A, Williams T, Fernie A (2007) The Mitochondrion: An Integration Point of Cellular Metabolism and Signalling Critical Reviews in Plant Sciences 26:17–43

    Article  PubMed  CAS  Google Scholar 

  • Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904

    Article  PubMed  CAS  Google Scholar 

  • Szalai G, Kellös T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80

    Article  PubMed  CAS  Google Scholar 

  • Ślesak I, Karpinska B, Surówka E, Miszalski Z, Karpinski S (2003) Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L. Plant Cell Physiol 44:573–581

    Article  PubMed  Google Scholar 

  • Ślesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z (2007) The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim Pol 54:39–50

    PubMed  Google Scholar 

  • Tabata K, Takaoka T, Esaka M (2002) Gene expression of ascorbic acid related enzymes in tobacco. Phytochem 61:631–635

    Article  PubMed  CAS  Google Scholar 

  • Takahama U (1993) Redox state of ascorbic acid in the apoplast of stems of Kalanchoë daigremontiana. Physiol Plant 89:791–798

    Article  CAS  Google Scholar 

  • Takahama U (1994) Changes induced by abscisic acid and light in the redox state of ascorbate in the apoplast of epicotyls of Vigna angularis. Plant Cell Physiol 35:975–978

    CAS  Google Scholar 

  • Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, Aono M, Saji H (2003) Light-controlled expression of a gene encoding l-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana. Plant Sci 164:1111–1117

    Article  PubMed  CAS  Google Scholar 

  • Tambussi EA, Bartoli CG, Beltrano J, Guiamet JJ, Araus JL (2000) Oxidative damage to thylakoid proteins in water-stressed leaves of wheat (Triticum aestivum). Physiol Plant 108:398–404

    Article  PubMed  CAS  Google Scholar 

  • Tardy F, Havaux M (1997) Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta 1330:179–193

    Article  PubMed  CAS  Google Scholar 

  • Tausz M, Bytnerowicz A, Arbaugh MJ, Wonisch A, Grill D (2001) Multivariate patterns of biochemical responses of Pinus ponderosa trees at field plots in the San Bernardino Mountains, southern California. Tree Physiol 21:329–336

    Article  PubMed  CAS  Google Scholar 

  • Tausz M, Šircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Townsend DM (2007) S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol Interv 7:313–324

    Article  PubMed  CAS  Google Scholar 

  • Turcsányi E, Lyons T, Plöchl M, Barnes J (2000) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? Testing the concept using broad bean (Vicia faba L.). J Exp Bot 51:901–910

    Article  PubMed  Google Scholar 

  • Ullmann P, Gondet L, Potier S, Bach TJ (1996) Cloning of Arabidopsis thaliana glutathione synthetase (GSH2) by functional complementation of a yeast gsh2 mutant. Eur J Biochem 236: 662–669

    Article  PubMed  CAS  Google Scholar 

  • Urbańczyk-Wochniak E, Usadel B, Thimm O, Munes-Nesi A, Carrari F, Davy M, Blasing O, Kowalczyk M, Weicht D, Polinceusz A, Meyer S, Stitt M, Fernie AR (2006) Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol Biol 60:773–792

    Article  PubMed  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley–powdery mildew interaction. Plant Physiol 123:1289–1300

    Article  PubMed  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  PubMed  CAS  Google Scholar 

  • Vanacker H, Harbinson J, Ruisch J, Carver TLW, Foyer CH (1998b) Antioxidant defences of the apoplast. Protoplasma 205:129–140

    Article  CAS  Google Scholar 

  • Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127:426–435

    Article  PubMed  CAS  Google Scholar 

  • Venis MA, Napier RM (1997) Auxin perception and signal transduction. In: Basel AP (ed) Signal transduction in plants. Birkhäuser Verlag Basel, Switzerland, pp 45–63

    Chapter  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110

    Article  PubMed  CAS  Google Scholar 

  • Vieira Dos Santos C, Laugier E, Tarrago L, Massot V, Issakidis-Bourguet E, Rouhier N, Rey P (2007) Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett 581:4371–4376

    Article  PubMed  CAS  Google Scholar 

  • Vieira Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:329–334

    Article  PubMed  CAS  Google Scholar 

  • Wachter A, Rausch T (2005) Regulation of glutathione (GSH) synthesis in plants: Novel insight from Arabidopsis. FAL Agricultural Research 283:149–155

    Article  PubMed  CAS  Google Scholar 

  • Wachter A, Wolf S, Steininger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiations: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15–30

    Article  PubMed  CAS  Google Scholar 

  • Wagner GJ (1981) Vacuolar deposition of ascorbate-derived oxalic acid in barley. Plant Physiol 67:591–593

    Article  PubMed  CAS  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    Article  PubMed  CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  PubMed  CAS  Google Scholar 

  • Wingate VPM, Lawton MA, Lamb ChJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210

    Article  PubMed  CAS  Google Scholar 

  • Wingsle G, Karpinski S, Hällgren JE (1999) Low temperature, high light stress and antioxidant defence mechanisms in higher plants. Phyton 39:253–268

    CAS  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen. Biochem J 322:681–692

    PubMed  CAS  Google Scholar 

  • Wolucka BA, Van Montagu M (2007) The VTC2 cycle and de novo biosynthesis pathways for vitamin C in plants: an opinion. Phytochemistry 68:2602–2613

    Article  PubMed  CAS  Google Scholar 

  • Wormuth D, Heiber I, Shaikali J, Kandlbinder A, Baier M, Dietz KJ (2007) Redox regulation and antioxidative defence in Arabidopsis leaves viewed from a systems biology perspective. J Biotechnol 129:229–248

    Article  PubMed  CAS  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  CAS  Google Scholar 

  • Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J Exp Bot 58:2661–2671

    Article  PubMed  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23:51–68

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto HY (1979) Biochemistry of the Violaxanthin Cycle in Higher-Plants. Pure Appl Chem 51:639–648

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto A, Bhuiyan MNH, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Takabe T (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J Exp Bot 56:1785–1796

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto HY, Higashi RM (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190:514–522

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki H, Takahashi S, Heshiki R (1999) The tropical fig Ficus microcarpa L. f. cv. golden leaves lacks heat-stable dehydroascorbate reductase activity. Plant Cell Physiol 40:640–646

    Article  CAS  Google Scholar 

  • Yen TCH, King KL, Lee HCH, Yen SH, Wei YK (1994) Age dependent increase of mitochondrial DNA deletions together with lipid peroxides and superoxide dismutase in human liver mitochondria. Free Radical Biol Med 16:207–214

    Article  PubMed  CAS  Google Scholar 

  • Yu O, Jez JM (2008) Nature’s assembly line: biosynthesis of simple phenylpropanoids and polyketides. Plant J 54:750–762

    Article  PubMed  CAS  Google Scholar 

  • Zechmann B, Zellnig G, Müller M (2006) Immunocytochemical localization of glutathione precursors in plant cells. J Electron Microsc 55:173–181

    Article  CAS  Google Scholar 

  • Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by the Polish Ministry of Science and Higher Education (project No. 50/N-DFG/2007/0).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazimierz Strzałka .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Latowski, D., Surówka, E., Strzałka, K. (2010). Regulatory Role of Components of Ascorbate–Glutathione Pathway in Plant Stress Tolerance. In: Anjum, N., Chan, MT., Umar, S. (eds) Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9404-9_1

Download citation

Publish with us

Policies and ethics