Skip to main content

Signaling and Integration of Defense Functions of Tocopherol, Ascorbate and Glutathione

  • Chapter
Photoprotection, Photoinhibition, Gene Regulation, and Environment

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 21))

Summary

Ascorbate, glutathione, and tocopherol are the three major low molecular weight antioxidants of plant cells. While tocopherol is hydrophobic and is found only in lipid membranes, ascorbate and glutathione are hydrophilic, accumulating to high concentrations in the chloroplast stroma and other compartments of the plant cell. Ascorbate and glutathione not only limit photo-oxidative damage but can also act independently as signal-transducing molecules regulating defense gene expression. Both metabolites transmit information concerning oxidative load and redoxbuffering capacity. Ascorbate modifies the expression of chloroplast genes. Net glutathione synthesis during stress restores the cellular redox state and allows orchestration of systemic acquired resistance. The degree of redox coupling between these antioxidants has profound implications for regulation, function, and signaling associated with the two major energy-generating systems, i.e. photosynthesis and respiration. Tocopherol fulfills an essential protective function, counter-acting the harmful effects of singlet oxygen production at photosystem II. Ascorbate reduces and thus regenerates oxidized tocopherol, but flux through this reaction is not sufficient to maintain the reduced tocopherol pool under high light stress. This may be because tocopherol regeneration draws on the ascorbate pool of the chloroplast lumen, which may be depleted under stress. Moreover, while glutathione always reduces oxidized ascorbate (dehydroascorbate), the degree of coupling between the ascorbate and glutathione redox couples is variable. The flexibility of coupling between these antioxidant pools is crucial to differential redox signaling, particularly by ascorbate and glutathione.

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 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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76: 343–370

    PubMed  CAS  Google Scholar 

  • Agius F, Gonz’alez-Lamothe R, Caballero JL, Mu˜noz-Blanco J, Botella MA and Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nature Biotechnol 21: 177–181

    CAS  Google Scholar 

  • Allen JF and Hall DO (1973) Superoxide reduction as a mechanism of ascorbate-stimulated oxygen uptake by isolated chloroplasts. Biochem Biophys Res Commun 52: 856–862

    PubMed  CAS  Google Scholar 

  • Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77: 457–64

    CAS  Google Scholar 

  • Alvarez ME, Penell RI, Meijer PJ, Ishikawa A, Dixon RA and Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773–784

    PubMed  CAS  Google Scholar 

  • Amako K, Chen G-X and Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35: 497–504

    CAS  Google Scholar 

  • Anderson JW, Foyer CH and Walker DA (1983a) Lightdependent reduction of hydrogen peroxide by intact spinach chloroplasts. Biochim Biophys Acta 724: 69–74

    CAS  Google Scholar 

  • Anderson JW, Foyer CH and Walker DA (1983b) Lightdependent reduction of dehydroascorbate and uptake of exogenous ascorbate by spinach chloroplasts. Planta 158: 442–450

    CAS  Google Scholar 

  • Angerhofer A (1991) Chlorophyll triplets and radical pairs. In: Scheer H (ed), Chlorophylls, pp 945–992. CRC Press, Boca Raton

    Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochem Biophys Acta 1143: 113–134

    PubMed  CAS  Google Scholar 

  • Arrigoni O and de Tullio MC (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J Plant Physiol 157: 481–488

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Asard H, Kapila J, Verelst W and B’erczi A (2001) Higher-plant plasma membrane cytochrome b561: a protein in search of a function. Protoplasma 217: 77–93

    PubMed  CAS  Google Scholar 

  • Baier M and Dietz KJ (1997) The plant 2-cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J 12: 179–190

    PubMed  CAS  Google Scholar 

  • BaierMand Dietz K-J (1999a) Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts. Trends Plant Sci 4: 166–168

    Google Scholar 

  • Baier M and Dietz K-J (1999b) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119: 1407–1414

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bartling D, Radzio R, Steiner U and Weiler EW (1993) A glutathione-S-transferase with glutathione peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur J Biochem 216: 579–586

    PubMed  CAS  Google Scholar 

  • Bartoli CG, Pastori GM and Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123: 335–343

    PubMed  CAS  Google Scholar 

  • Bartoli CG, Guiamet JJ, Kiddle G, Pastori G, Di Cagno R, Theodoulou FL and Foyer CH (2004) The relationship between L-galactono-1, 4-lactone dehydrogenase (GalLDH) and ascorbate content in leaves under optimal and stress conditions. Plant Cell Environ, In press

    Google Scholar 

  • Berczi A and Møller IM (1998) NADH-monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes. Plant Physiol 116: 1029–1036

    CAS  Google Scholar 

  • Bergmüller E, Porfirova S and Dörmann P (2003) Characterization of an Arapidopsis mutant deficient in γ -tocopherol methyltransferase. Plant Mol Biol 52: 1181–1190

    PubMed  Google Scholar 

  • Beyer RE (1990) The participation of coenzyme Q in free radical production and antioxidation. Free Radic BiolMed8: 545–565

    CAS  Google Scholar 

  • Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA and Leustek T (2001) Regulation of the plant-type 5’-adenylylsulfate reductase by oxidative stress. Biochemistry 40: 9040–9048

    PubMed  CAS  Google Scholar 

  • Bishop NI and Wong J (1974) Photochemical characteristics of a vitamin E deficient mutant of Scenedesmus obliquus. Ber dtsch bot Ges 87: 359–371

    Google Scholar 

  • Boveris A, Oshino N and Chance B (1972) The cellular production of hydrogen peroxide. Biochem J 128: 617–630

    PubMed  CAS  Google Scholar 

  • Bramley PM, Elmadf’a I, Kafatos A, Kelly FJ, Manios Y, Roxborough HE, Schuch W, Sheehy PJA and Wagner KH (2000) Vitamin E. J Sci Food Agric 80: 913–938

    CAS  Google Scholar 

  • Booij-James I, Swegle W M, Edelman M and Mattoo A (2002) Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiol 130: 2069–2075

    PubMed  CAS  Google Scholar 

  • Bowsher CG, Hucklesby DP and Emes MJ (1989) Nitrite reduction and carbohydrate metabolism in plastids purified from roots of Pisum sativum L. Planta 177: 359–366

    CAS  Google Scholar 

  • Breitenbach J, ZhuCand Sandmann G(2001) The bleaching herbicice norflurazon inhibits phytoene desaturase by competetion with the cofactors. J Agric Food Chem 49: 5270–5272

    PubMed  CAS  Google Scholar 

  • Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Arch Biochem Biophys 228: 1–9

    Google Scholar 

  • Bunkelmann JR and Trelease RN (1996) Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110: 589–598

    CAS  Google Scholar 

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

    Google Scholar 

  • Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, Van Montagu M, Inze D and Van Camp W (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci USA 95: 5818–5823

    Google Scholar 

  • Chen G and Asada K (1989) Ascorbate peroxidase in tea leaves: Occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30: 987– 998

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cogdell R and Frank HA (1996) Carotenoids in photosynthesis. Photochem Photobiol 63: 257–264

    PubMed  Google Scholar 

  • Collakova E and DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol 127: 1113– 1124

    PubMed  CAS  Google Scholar 

  • Collakova E and DellaPenna D (2003a) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131: 632–642

    CAS  Google Scholar 

  • Collakova E and DellaPenna D (2003b) The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress. Plant Physiol 131: 930–940

    Google Scholar 

  • Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB and Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747–23752

    PubMed  CAS  Google Scholar 

  • Collinson EJ, Wheeler GL, Garrido EO, Avery AM, Avery SV and Grant CM (2002) The yeast glutaredoxins are active as glutathione peroxidases. J Biol Chem 277: 16712–16717

    PubMed  CAS  Google Scholar 

  • Conklin PL and 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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dähnhardt D, Falk J, Appel J, van der Kooij TAW, Schulz- Friedrich R and Krupinska K (2002) The hydroxyphenylpyruvate dioxygenase from Synechocystis sp. PCC 6803 is not required for plastoquinone biosynthesis. FEBS Lett 523: 177– 181

    Google Scholar 

  • Dat J, Vandenabeele S, Vranov’a E, Van Montagu M, Inz’e D and Van Breusegem F (2000) Dual action of AOS during plant stress responses. Cell Mol Life Sci 57: 779–795

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Delauney A, Pflieger D, Barrault MB, Vinh J and Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redoxtransducer in gene activation. Cell 111: 1–11

    Google Scholar 

  • Demmig-Adams B and Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626

    CAS  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54: 93–107

    PubMed  CAS  Google Scholar 

  • Dietz K-J, Stork T, Finkemeier I, Lamkemeyer P, Li W-X, El-Tayeb MA, Michel K-P, Pistorius E and Baier M (2005) The role of peroxiredoxins in oxygenic photosynthesis of cyanobacteria and higher plants: peroxide detoxification or redox sensing? In: Demmig-Adams B, Adams WW III and MattooAK(eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 303–319. Springer, Dordrecht

    Google Scholar 

  • Diner BA and Rappoport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53: 552– 580

    Google Scholar 

  • Dixon DP, Davis BG and Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J BiolChem277: 30859– 30869

    CAS  Google Scholar 

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

    Google Scholar 

  • Du G, Mouithys-Mickalad A and Sluse FE (1998) Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic Biol Med 25: 1066–1074

    PubMed  CAS  Google Scholar 

  • Duke SO, Lydon JM, Becerril TD, Sherman L and Matsumoto H (1991) Protoporphyrinogen oxidase inhibiting herbicides. Weed Sci 39: 465–473

    CAS  Google Scholar 

  • Durrant JB, Giorgi LB, Barber J, Klug DR and Porter G (1990) Characterization of triplet states in isolated photosystem II reaction centers: oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta 1017: 167–175

    CAS  Google Scholar 

  • Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH and Noctor G (2003a) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 313: 264–275

    Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu CD, Ch’etrit P, Foyer CH and De Paepe R (2003b) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15: 1212–1226

    CAS  Google Scholar 

  • Elstner EF, Wagner GA and SchultzW(1998) Activated oxygen in green plants in relation to stress situation. Curr Top Plant Biochem Physiol 7: 159–187

    Google Scholar 

  • Endo T and Asada K (2005) Photosystem I and photoprotection: cyclic electron flow and water-water cycle. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 205–221. Springer, Dordrecht

    Google Scholar 

  • Eshdat Y, Holland D, Faltin Z and Ben-Hayyim G (1997) Plant glutathione peroxidases. Physiol Plant 100: 234–240

    CAS  Google Scholar 

  • Eskling M and Âkerlund HE (1998) Changes in the quantities of violaxanthin de-epoxidase, xanthophylls and ascorbate in spinach upon shift from low to high light. Photosynth Res 57: 41–50

    CAS  Google Scholar 

  • Falk J, Krauβ N, Dähnhardt D and Krupinska K (2002) The senescence associated gene of barley encoding 4-hydroxyphenylpyruvate dioxygenase is expressed during oxidative stress. J Plant Physiol 159: 1245–1253

    Google Scholar 

  • Fath A, Bethke PC and Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126: 156–166

    PubMed  CAS  Google Scholar 

  • Feierabend J and Dehne S (1996) Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction center protein D1 in mature rye leaves. Planta 198: 413–422

    CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the Photosynthetic Oxygen-Evolving Center Science 303: 1831–1838.

    Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM and Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442–446

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Foyer CH and Harbinson J (1999) Relationships between antioxidant metabolism and carotenoids in the regulation of photosynthesis. In: Frank HA, Young AJ, Britton G and Cogdell RJ (eds) The Photochemistry of Carotenoids, pp 305–325. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Foyer CH, Rowell J and Walker D (1983) Measurements of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157: 239–244

    CAS  Google Scholar 

  • Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C and Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109: 1047–1057

    PubMed  CAS  Google Scholar 

  • Foyer CH, GomezLDand van Heerden PDR. (2005) Glutathione. In: Smirnoff N (ed) Antioxidants and Reactive Species in Plants, pp 000–000. Blackwell Publishing, London

    Google Scholar 

  • Fryer MJ (1992) The antioxidant effect of thylakoid vitamin E (α-tocopherol). Plant Cell Environ 15: 381–392

    CAS  Google Scholar 

  • Fufezan C, Rutherford AW and Krieger-Liszkay A(2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532: 407–410

    PubMed  CAS  Google Scholar 

  • Genova ML, Ventura B, Giuliano G, Bovina C, Formiggini G, Castelli GP and Lenaz G (2001) The site of production of superoxide radical in mitochondrial Complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett 505: 364–368

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Gomez L, Vanacker H, Buchner P, NoctorGand Foyer CH (2004) Regulation of glutathione metabolism during the short-term chilling response of maize leaves. Plant Physiol 134: 1662– 1671

    PubMed  CAS  Google Scholar 

  • Graβes T, Grimm B, Koroleva O and Jahns P (2001) Loss of α-tocopherol in tobacco plants with decreased geranylgeranyl reductase activity does not modify photosynthesis in optimal growth conditions but increases sensitivity to high-light stress. Planta 213: 620–628

    Google Scholar 

  • Green R and Fluhr R (1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell: 203–212

    Google Scholar 

  • Gressel J (2002) Molecular Biology of Weed Control. Taylor & Francis, London

    Google Scholar 

  • Groden D and Beck E (1979) H2O2 destruction by ascorbatedependent systems from chloroplasts. Biochim Biophys Acta 546: 426–435

    PubMed  CAS  Google Scholar 

  • Han D, Canali R, Rettori D and Cadenas E (2001) Production of superoxide into the intermembrane space and cytoplasm by heart mitochondria. Free Radic Biol Med 31: 45

    Google Scholar 

  • Hancock JT, Desikan R and Neill SJ (2001) Does the redox status of cytochrome C act as a fail-safe mechanism in the regulation of programmed cell death? Free Rad Biol Medic 31: 697– 703

    CAS  Google Scholar 

  • Havaux M, Lütz C and Grimm B (2003) Chloroplast membrane photostability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol 132: 300–310

    PubMed  CAS  Google Scholar 

  • Heazlewood JL, Howell KA and Millar AH (2003) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim Biophys Acta 1604: 159–169

    PubMed  CAS  Google Scholar 

  • Herbette S, Lenne C, Leblanc N, Julien JL, Drevet JR and Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 269: 2414–2420

    PubMed  CAS  Google Scholar 

  • Hideg E, Spetea C and Vass I (1994) Singlet oxygen production in thylakoid membranes during photoinhibition as detected by ESR spectroscopy. Photosynth Res 39: 191–199

    CAS  Google Scholar 

  • Hideg E, Kalai T, Hideg K and Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37: 11405–11411

    PubMed  CAS  Google Scholar 

  • Hideg E, Barta C, Kalai T, Vass I, Hideg K and Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43: 1154–1164

    PubMed  CAS  Google Scholar 

  • Hofius D and Sonnewald U (2003) Vitamin E biosynthesis: biochemistry meets cell biology. Trends Plant Sci 8: 6–8

    PubMed  CAS  Google Scholar 

  • Horemans N, Asard H, Van Gestelen P and Caubergs RJ (1998) Faciliated diffusion drives transport of oxidized molecules into purified plasma membrane vesicles of Phaseolus vulgaris. Physiol Plant 104: 783–789

    CAS  Google Scholar 

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

    Google Scholar 

  • Horling F, Lamkemeyer P, Konig J, Finkemeier I, Kandlbinder A, Baier M and 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

    PubMed  CAS  Google Scholar 

  • Hossain MA and Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25: 1285–1295

    CAS  Google Scholar 

  • Hou WC, Chen HJ and Lin YH (1999) Dioscorins, the major tuber storage proteins of yam (Dioscorea batatas Decne), with dehydroascorbate reductase and monodehydroascorbate reductase activities. Plant Sci 149: 151–156

    CAS  Google Scholar 

  • Imai T, Karita S, Shiratori G, Hattori M, Nunome T, Oba K and Hirai M (1998) L-galactono-γ -lactone dehydrogenase from sweet potato: Purification and cDNA sequence analysis. Plant Cell Physiol 39: 1350–1358

    PubMed  CAS  Google Scholar 

  • Ito H, Iwabuchi M and 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

    PubMed  CAS  Google Scholar 

  • Jiménez A, Hernández JA, del Río L and 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 BH, Bae YS and Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. 126: 1055–1060

    CAS  Google Scholar 

  • Jung BG, Lee KO, Lee SS, Chi YH, Jang HH, Kang SS, Lee K, Lim D, Yoon SC, Yun DJ, Inoue Y, Cho MJ and Lee SY (2002) A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidases. J Biol Chem 277: 12572–12578

    PubMed  CAS  Google Scholar 

  • Kaiser S, DiMascio P, Murphy ME and Sies H (1990), Physical and chemical scavenging of singlet molecular oxygen by tocopherols. Arch Biochem Biophys 277: 101–108

    PubMed  CAS  Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygenevolving photosystem II from Thermosynechoccus vulcanus at 3.7 A resolution. Proc Natl Acad Sci USA 100: 98–103

    PubMed  CAS  Google Scholar 

  • Kanwischer M, Porfirova S, Bergmüller E andDörmann P (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arapidosis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol 137: 713–723.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kelly GJ and Latzko E (1979) Soluble ascorbate peroxidase. Naturwissenschaften 66: 377–382

    Google Scholar 

  • Keren N, Gong. H and Ohad I (1995) Oscillations of reaction center II-D1 protein degradation in vivo induced by repetitive light flashes. J Biol Chem 270: 806–814

    PubMed  CAS  Google Scholar 

  • Keren N, Berg A, van Kann PJM, Levanon H and Ohad I (1997) Mechanism of photosystem II inactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 94: 1579–1584

    PubMed  CAS  Google Scholar 

  • Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ and Foyer CH (2003) Effects of ascorbate signaling on defense and photosynthesis genes. Antioxidant Redox Signaling 5: 23–32

    CAS  Google Scholar 

  • Kimura M., Yoshizumi T, Manabe K, Yamamoto YY and Matsui M (2001) Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and -independent pathways. Genes Cells 6: 607–617

    PubMed  CAS  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K and Matsui M (2003) Identification of Arabidopsis genes regulated by light stress using cDNA microarray. Photochem. Photobiol 77: 226–233

    PubMed  CAS  Google Scholar 

  • Kinkema M, Fan WH and Dong XN (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339–2350

    PubMed  CAS  Google Scholar 

  • Klatt P and Lamas S (2000) Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267: 4928–4944

    PubMed  CAS  Google Scholar 

  • Köhler B and Blatt MR (2002) Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant J 32: 185–194

    PubMed  Google Scholar 

  • Köhler B, Hills A and Blatt MR (2003) Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol 131: 385–388

    PubMed  Google Scholar 

  • Kovalchuk I, Bojko V, Kovalchuk O, Gloeckler V, Filkowski J, Heinlein M and Hohn B (2003) Pathogen induced systemic plant signal triggers genome instability. Nature 423: 760– 762

    PubMed  CAS  Google Scholar 

  • Krieger A, Rutherford AW, Vass I and Hideg E (1998) Relationship between activity, D1 loss, and Mn binding in photoinhibition of photosystem II. Biochemistry 37: 16262–16269

    PubMed  CAS  Google Scholar 

  • Kruk J and Strzalka K (1995) Occurrence and function of alphatocopherol quinone in plants. J Plant Physiol 145: 405–409

    CAS  Google Scholar 

  • Kuge S, Jones N and Nomoto A (1997) Regulation of YAP-1 nuclear localization in response to oxidative stress. EMBO J 16: 1710–1720

    PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD and Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623–2633

    PubMed  CAS  Google Scholar 

  • Lamb C and Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275

    PubMed  CAS  Google Scholar 

  • Lee DL, PrisbyllaMP, McLean ProvanW, Frase T and Mutter LC (1997) The discovery and structural requirements of inhibitors of p-hydroxyphenylpyruvate dioxygenase. Weed Sci 45: 601– 609

    Google Scholar 

  • LeeKP, Kim C, LeeDWand Apel K (2003) TIGRINAd, required for regulating the biosynthesis of tetrapyrroles in barley, is an ortholog of the FLU gene of Arabidopsis thaliana. FEBS Lett 553: 119–124

    PubMed  CAS  Google Scholar 

  • Lemaire SD (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res 79: 305–318

    PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (1968) Plastoglobuli and the fine structure of plastids. Endeavour XXVII: 144–149

    Google Scholar 

  • Lichtenthaler HK (1998) The plants 1-deoxy-d-xylulose-5- phosphate pathway for biosynthesis of isoprenoids. Fett Lipid 100: 128–138

    CAS  Google Scholar 

  • Liere K and Link G (1997) Chloroplast endoribonuclease p54 involved in RNA 3’-end processing is regulated by phosphorylation and redox state. Nucleic Acids Res 25: 2403–2408

    PubMed  CAS  Google Scholar 

  • Liu YB, Fiskum G and Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80: 780–787

    PubMed  CAS  Google Scholar 

  • Logan BA, Barker DH, Demmig-Adams B and 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

    CAS  Google Scholar 

  • Macpherson AN, Telfer A, Barber J and Truscott TG (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochim Biophys Acta 1143: 301–309

    CAS  Google Scholar 

  • Maddison J, Lyons TM, Plöchl M and Barnes JD (2002) Hydroponically-cultivated radish fed L-galactono-1, 4-lactone exhibit increased tolerance to ozone. Planta 214: 383–391

    PubMed  CAS  Google Scholar 

  • Mathis P, Butler WL and Satoh K (1979) Carotenoid triplet state and chlorophyll fluorescence quenching in chloroplasts and subchloroplast particles. Photochem Photobiol 30: 603–614

    CAS  Google Scholar 

  • Matsumoto H, Mizutani M, Yamaguchi T and Kadotani J (2002) Herbicide pyrazolate causes cessation of carotenoids synthesis in early watergrass by inhibiting 4-hydroxyphenylpyruvate dioxygenase. Weed Biol Manag 2: 39–45

    CAS  Google Scholar 

  • Mattoo AK, Marder JB and EdelmanM(1989) Dynamics of the photosystem II reaction center. Cell 56: 241–246

    Google Scholar 

  • MayMJ,VernouxT, Leaver C, Van MontaguMand Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49: 649–667

    Google Scholar 

  • Mayer M, Beyer P and Kleinig H (1990) Quinone compounds are able to replace molecular oxygen as terminal electron acceptor in phytoene desaturation in chromoplasts of Narcissus pseudonarcissus L. Eur J Biochem 191: 359–363

    PubMed  CAS  Google Scholar 

  • Melis A (1999) Photosystem II damage and repair cycle in chloroplasts:what modulates the rate of photodamage in vivo? Trends Plant Sci 4: 130–135

    PubMed  Google Scholar 

  • Meskauskine R, Nater M, Goslings D, Kessler F, op den Camp R and Apel K (2001) FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826–12831

    Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mittler R and Zilinskas BA (1992) Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J Biol Chem 267: 21802–21807

    PubMed  CAS  Google Scholar 

  • Mittova V, Kiddle G, Theodoulou FL, Gomez L, Volokita M, Tal M, Foyer CH and Guy M (2003) Co-ordinate induction of glutathione biosynthesis and glutathione-metabolising enzymes is correlated with salt tolerance in tomato. FEBS Lett 554: 417–421

    PubMed  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C and Kangasjärvi J (2002) Ethylene sunthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130: 1918–1926

    PubMed  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561–591

    PubMed  Google Scholar 

  • Morimura Y, Iwamoto K, Ohya T, Igarashi T, Nakamura Y, Kubo A, Tanaka K and Ikawa T (1999) Light-enhanced induction of ascorbate peroxidase in Japanese radish roots during postgerminative growth. Plant Sci 142: 123–132

    CAS  Google Scholar 

  • Mou Z, Fan WH and Dong XN (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935–944

    PubMed  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S, Jimenez A, Cleary SP, Robinson C and Creissen GP (1998) Identification of cDNAS encoding plastid-targeted glutathione peroxidases. Plant J 13: 375– 379

    PubMed  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S and Creissen GP (2005) Integration of signaling in antioxidant defenses. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 223–239. Springer, Dordrecht

    Google Scholar 

  • Munné-Bosch S and Alegre L (2002a) Plant aging increases oxidative stress in chloroplasts. Planta 214: 608–615

    Google Scholar 

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

    Google Scholar 

  • Munné-Bosch S and Falk J (2003) New insights into the function of tocopherols in plants. Planta 218: 323–326

    PubMed  Google Scholar 

  • MurataY, Pei ZM, Mori IC and Schroeder JI (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolicNAD(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

    Google Scholar 

  • Neely WC, Martin JM and Barker SA (1988) Products and relative reaction rates of the oxidation of tocopherols with singlet molecular oxygen. Photochem Photobiol 48: 423–428

    PubMed  CAS  Google Scholar 

  • Nishizawa AN and Buchanan BB (1981) Enzyme regulation in C4 photosynthesis. Purification and properties of thioredoxinlinked fructose bisphosphatase and sedoheptulose bisphosphatase from corn leaves. J Biol Chem 256: 6119–6126

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S and Foyer CH (2000) Peroxide processing in photosynthesis: antixoxidant coupling and redox signalling. Proc Roy Soc Lond B 355: 1465–1475

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Noctor G, Veljovic-Jovanovic SD, Driscoll S, Novitskaya L and Foyer CH (2002b) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89: 841–850

    CAS  Google Scholar 

  • Noctor G, Dutilleul C, De Paepe R and Foyer CH (2004) The use of mitochondrial mutants to evaluate the effects of redox state on photosynthesis, stress tolerance, and the integration of carbon and nitrogen metabolism. J Exp Bot 55: 49–57

    PubMed  CAS  Google Scholar 

  • Norris SR, Barette TR and DellaPenna D (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7: 2139–2148

    PubMed  CAS  Google Scholar 

  • Oba K, Ishikawa S, Nishikawa M, Mizuno H and Yamamoto T (1995) Purification and properties of L-galactono-γ -lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. J Biochem 117: 120–124

    PubMed  CAS  Google Scholar 

  • Ogawa K, Hatano-Iwasaki A, Yanagida M and Iwabuchi M (2004) Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: Mechanism of strong interaction of light intensity with flowering. Plant Cell Physiol 45: 1–8

    PubMed  CAS  Google Scholar 

  • Op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M and Apel K(2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320–2332

    PubMed  CAS  Google Scholar 

  • Orozco-Cardenas ML, Narvaez-Vazquez J and Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response towounding, systemin, and methyl jasmonate. Plant Cell 13: 179–191

    PubMed  CAS  Google Scholar 

  • Ostergaard J, Persiau G, DaveyMW, BauwGandVanMontaguM (1997) Isolation of a cDNA coding for L-galactono-γ -lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. Purification, characterization, cDNA cloning, and expression in yeast. J Biol Chem 272: 30009– 30016

    PubMed  CAS  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field, pp 1–24. Bios Scientific Publishers, Oxford, UK

    Google Scholar 

  • Osmond CB and Förster B (2005) Photoinhibition: then and now. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 11–22. Springer, Dordrecht

    Google Scholar 

  • Pallanca JE and Smirnoff N (1999) Ascorbic acid metabolism in pea seedlings. A comparison of D-glucosone, L-sorbosone, and L-galactono-1, 4-lactone as ascorbate precursors. Plant Physiol 120: 453–461

    PubMed  CAS  Google Scholar 

  • Pallett K (2000) The mode of action of isoxaflutole: a case study of an emerging target site. In: Cobb AH and Kirkwood RC (eds) Herbicides and Their Mechanism of Action, pp 215– 238. CRC Press, Boca Raton, FL

    Google Scholar 

  • Pallett KE, Little JP, Sheekey M and Veeasekaran P (1998) The mode of action of isoxaflutole. Pestic Biochem Physiol 62: 113–124

    CAS  Google Scholar 

  • Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D and Fehér A (2002) The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129: 1807–1819

    PubMed  CAS  Google Scholar 

  • Pastori GM and Foyer CH (2002) Common components, pathways and networks of cross tolerance to stress: the central role of “redox” and hormone-mediated controls. Plant Physiol 129: 460–468

    PubMed  CAS  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S,Veljovic-Jovanovic S, Verrier PJ, Noctor G and Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes controlling development through hormone signaling. Plant Cell 15: 939–951

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pignocchi C (2000) Establishing the functional significance of ascorbate oxidase in Planta. PhD Thesis. University of Newcastle, U.K.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Polle A (2001) Dissecting the superoxide-dismutase-ascorbateglutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126: 445–462

    CAS  Google Scholar 

  • Porfirova S, Bergmüller E, Tropf S, Lemke R and Dörmann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci USA 99: 12495–12500

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Potters G, De Gara L, AsardHand HoremansN(2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40: 537–548

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ and Knight M (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6: 1301–1310

    PubMed  CAS  Google Scholar 

  • Puntarulo S, Sanchez RA and Boveris A (1988) Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol 86: 626–630

    PubMed  CAS  Google Scholar 

  • Puntarulo S, Galleano M, Sanchez RA and Boveris A (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochim Biophys Acta 1074: 277–283

    PubMed  CAS  Google Scholar 

  • Raha S and Robinson BH (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25: 502– 508

    PubMed  CAS  Google Scholar 

  • Rennenberg H (1997) Molecular approaches to glutathione biosynthesis. In: Cram WJ, DeKok LJ, Stulem I, Brunnold C and Rennenberg H (eds) Sulphur Metabolism in Higher Plants, pp 59–70. Backhuys Publishers, Leiden, The Netherlands

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rodermel S (2001) Pathways of plastid-to-nucleus signalling. Trends Plant Sci 6: 471–478

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rouhier N, Gelhaye E and Jacquot JP (2002) Glutaredoxindependent peroxiredoxin from poplar. Protein-protein interaction and catalytic mechanism. J Biol Chem 277: 13609–13614

    PubMed  CAS  Google Scholar 

  • Rutherford AW and Krieger-Liszkay A (2001) Herbicideinduced oxidative stress in photosystem II. Trends Biochem Sci 26: 648–653

    PubMed  CAS  Google Scholar 

  • Sandermann H (2001) Active oxygen species as mediators of plant immunity: three case studies. Biol. Chem 381: 649– 653

    Google Scholar 

  • Sanmartin M, Drogouti PD, Lyons T, Barnes J and Kanellis AK (2003) Overexpression 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 

  • Satoh K and Mathis P (1981) Photosystem II chlorophyll α- protein complex: a study by flash absorption spectroscopy. Photobiochem Photobiophys 2: 189–198

    CAS  Google Scholar 

  • Sattler SE, Cahoon EB, Coughlan SJ and DellaPenna D (2003) Characterisation of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol 132: 2184–2195

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Schledz M, Seidler A, Beyer P and Neuhaus G (2001) A novel phytyltransferase from Synechocystis sp. PCC 6803 involved in tocopherol biosynthesis. FEBS Lett 499: 15–20

    PubMed  CAS  Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: Implications for the control of elongation growth. Plant J 28: 679–688

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM and Waner D (2001a) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52: 627–658

    CAS  Google Scholar 

  • Schroeder JI,Kwak JM and Allen GJ (2001b) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410: 327–330

    Google Scholar 

  • Schulz A, Ot O, Beyer P and Kleinig H (1993) SC-0051, a benzoyl-cyclohexane-1, 3-dione bleaching herbicide, is a potent inhibitor of the enzyme p-hydroxyphenylpyruvate dioxygenase. FEBS Lett 318: 162–166

    PubMed  CAS  Google Scholar 

  • Schupp R and Rennenberg H (1990) Diurnal changes in the thiol composition of spruce needles. In: Rennenberg H, Brunold CH, de Kok LJ and Stulen I (eds) Sulfur Nutrition and Sulfur Assimilation in Higher Plants, pp 249–254. SPB Acad Publ, The Hague, Netherlands

    Google Scholar 

  • Schürmann P and Jacquot J-P (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371–400

    PubMed  Google Scholar 

  • Scott JW, Cort WM, Harley H, Parrish DR and Saucy G (1974) 6-Hydroxychroman-2-carboxylic acid: Novel antioxidants. J Am Oil Chem Soc 51: 200–203

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Shimaoka T, Yokota A and Miyake C (2000) Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant Cell Physiol 41: 1110–1118

    PubMed  CAS  Google Scholar 

  • Siendones E, Gonzalez-Reyes JA, Santos-Ocana C, Navas P and Cordoba F (1999) Biosynthesis of ascorbic acid in kidney bean. L-galactono-γ -lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane. Plant Physiol 120: 907–912

    Article  PubMed  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 and Pallanca JE (1996) Ascorbate metabolism in relation to oxidative stress. Biochem Soc Trans 24: 472–478

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Smirnoff N, Running JA and Gatzek S (2004) Ascorbate metabolism in relation to oxidative stress. In: Asrad H, MayJ M and Smirnoff N (eds) Vitamin C Functions and Biochemistry in Animals and Plants, pp 1–30. Bios Scientific Publishers. London, UK

    Google Scholar 

  • Smith IK, Kendall AC, Keys AJ, Turner JC and Lea PJ (1984) Increased levels of glutathione in a catalase-deficient mutant of barley (Hordeum vulgare L.). Plant Sci Lett 37: 29–33

    CAS  Google Scholar 

  • Soll J, Schultz G, Joyard J, Douce R and BlockMA(1985) Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Arch Biochem Biophys 238: 290–299

    PubMed  CAS  Google Scholar 

  • StarkeDW, ChockPBand Mieyal JJ (2003) Glutathione thiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase). Potential role in redox signal transduction. J Biol Chem 278: 14607–14613

    Google Scholar 

  • Sticher L, MauchMani B and Metraux JP (1997) Systemic acquired resistance. Annu Rev Phytopath 35: 235–270

    CAS  Google Scholar 

  • Streb P, Aubert S, Gout E and Bligny R (2003) Cold- and lightinduced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum. Physiol Plant 118: 96–104

    PubMed  CAS  Google Scholar 

  • Strand A, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421: 79–83

    PubMed  CAS  Google Scholar 

  • Sweetlove L and Foyer CH (2004). Roles for reactive oxygen species and antioxidants in plant mitochondria. In: Day DA, Millar AH and Whelan J (eds) Plant Mitochondria: From Genome to Function. Advances in Photosynthesis and Respiration, Vol 17, pp 307–320. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Tabata K, Oba K, Suzuki K and Esaka M (2001) Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for L-galactono-1, 4-lactone dehydrogenase. Plant J 27: 139–148

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, AonoMand 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

    CAS  Google Scholar 

  • Telfer A (2002) What is β-carotene doing in the photosystem II reaction centre? Phil Trans Roy Soc Lond 357: 1431–1440

    CAS  Google Scholar 

  • Telfer A and Barber J (1995) Role of carotenoid bound to the photosystem II reaction centre. In: Mathis P (ed) Photosynthesis: from Light to Biosphere, Vol IV, pp 15–20. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Telfer A, Bishop SM, Philipps D and Barber J (1994a) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269: 13244–13253

    CAS  Google Scholar 

  • Telfer A, Dhami S, Bishop SM, Phillips D and Barber J (1994b) β-carotene quenches singlet oxygen formed in isolated photosystem II reaction center. Biochemistry 33: 14469– 14474

    CAS  Google Scholar 

  • TeviniMand Lichtenthaler HK (1970) Untersuchungen über die Pigment- und Lipochinonausstattung der zwei photosynthetischen Pigmentsysteme. Z Pflanzenphysiol 62: 17–32

    Google Scholar 

  • Trebst A (1999) Singlet oxygen in photosynthesis. In: Denke A and Dornisch K (eds) Different Pathways through Life, pp 125–142. Lincom Europe, München, Germany

    Google Scholar 

  • Trebst A (2003) Function of β-carotene and tocopherol in photosystem II. Z Naturforsch 58c: 609–620

    Google Scholar 

  • Trebst A and Depka B (1997) Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii. FEBS Lett 400: 359–362

    PubMed  CAS  Google Scholar 

  • Trebst A, Depka B and Holländer-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 516: 156–160

    PubMed  CAS  Google Scholar 

  • Trebst A, Depka B, Jäger J and Oettmeier W (2004) Reversal of the inhibition of photosynthesis by herbicides affecting hydroxyphenylpyruvate dioxygenase by plastoquinone- and tocopheryl-derivatives in Chlamydomonas reinhardtii. Pest Manag Sci publication 60: 669–674.

    CAS  Google Scholar 

  • Trumper S, Follmann H and Haberlein I (1994) A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Lett 352: 159–162

    PubMed  CAS  Google Scholar 

  • Trumpower BL (1990) The protomotive Q cycle. Energy transduction by coupling of proton translocation to electron transfer by the cytochrome bc1 complex. J Biol Chem 265: 11409– 11412

    PubMed  CAS  Google Scholar 

  • Tsegaye Y, Shintani DK and DellaPenna D (2002) Overexpression of the enzyme p-hydroxyphenolpyruvate dioxygenase in Arabidopsis and its relation to tocopherol biosynthesis. Plant Physiol Biochem 40: 913–920.

    CAS  Google Scholar 

  • Tsukaguchi H, Tokui T, Mackenzie B, Berger UV, Chen XZ, Wang Y, Brubaker RF and Hediger MA (1999) A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 399: 70–75

    PubMed  CAS  Google Scholar 

  • Urano J, Nakagawa T, Maki Y, Masumura T, Tanaka K, Murata N and Ushimaru T (2000) Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Lett 466: 107–111

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vanlerberghe G C and Ordog SH (2002) Alternative oxidase: integrating carbon metabolism and electron transport in plant respiration. In: Foyer CH and Noctor G (eds) Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism, Advances in Photosynthesis and Respiration, Vol 12, pp 173–191. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Van Gorkom HJ and Schelvi JPM (1993) Kok’s oxygen clock: what makes it tick? The structure of P680 and consequences of its oxidizing power. Photosynth Res 38: 297–301

    Google Scholar 

  • Veljovic-Jovanovic SD, Pignocchi C, Noctor G and 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

    PubMed  CAS  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 and Sung ZR (2000) The ROOTMERISTEMLESS1/ CADMIUM SENSITIVE2 gene defines a glutathionedependent pathway involved in initiation and maintenance of cell division during post-embryonic root development. Plant Cell 12: 97–100

    PubMed  CAS  Google Scholar 

  • Vranova E, Inze D and Van Breusegem F (2002a) Signal transduction during oxidative stress. J Exp Bot 53: 1227–1236

    CAS  Google Scholar 

  • Vranova E, Atichartpongkul S, Villarroel R., Van Montagu M., Inzé D and Van Camp W (2002b) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc Natl Acad Sci USA 99: 10870–10875

    CAS  Google Scholar 

  • Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee K P,Wursch M, Laloi C, Nater M, Higeg E and Apel K (2004) The genetic basis of singlet oxygen-induced stress reactions of Arabidopsis thaliana. Science 306: 1183–1185.

    Google Scholar 

  • Wells WW, Xu DP, Yang Y and Rocque PA (1990) Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J Biol Chem 265: 15361–15364

    PubMed  CAS  Google Scholar 

  • Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Groner F, Hebbeker U and Flugge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787–802

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Winkler BS (1992) Unequivocal evidence in support of the nonenzymatic redox coupling between glutathione/glutathione disulfide and ascorbic acid/dehydroascorbic acid. Biochim Biophys Acta 1117: 287–290

    PubMed  CAS  Google Scholar 

  • Witt HT (1996) Photosynthesis. Ber Bunsenge Phys Chem 100: 1923–1927

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yabuta Y, Yoshimura K, Takeda T and Shigeoka S (2000) Molecular characterization of tobacco mitochondrial L-galactono-γ -lactone dehydrogenase and its expression in Escherichia coli. Plant Cell Physiol. 41: 666–675

    PubMed  CAS  Google Scholar 

  • Yamaguchi K, Mori H and Nishimura M(1995) A novel isozyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36: 1157–1162

    PubMed  CAS  Google Scholar 

  • Yoshimura K, Ishikawa T, NakamuraY, Tamoi M, Takeda T, Tada T, Nishimura K and Shigeoka S (1998) Comparative study on recombinant chloroplastic and cytosolic ascorbate peroxidase isozymes of spinach. Arch Biochem Biophys 353: 55–63

    Google Scholar 

  • Zhang W, Zhang L, Dong F, Gao J, Galbraith DW and Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126: 1438–1448

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Foyer, C.H., Trebst, A., Noctor, G. (2008). Signaling and Integration of Defense Functions of Tocopherol, Ascorbate and Glutathione. In: Demmig-Adams, B., Adams, W.W., Mattoo, A.K. (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, vol 21. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3579-9_16

Download citation

Publish with us

Policies and ethics