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The role of antioxidant enzymes in photoprotection

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Abstract

The enzymatic component of the antioxidant system is discussed as one of the defensive mechanisms providing protection against excessive light absorption in plants. We present an analysis of attempts to improve stress tolerance by means of the creation of transgenic plants with elevated antioxidant enzyme activities and conclude that the effect of such transgenic manipulation strongly depends on the manner in which the stress is imposed. The following factors may diminish the differences in photosynthetic performance between transgenic plants and wild type under field conditions: effective functioning of the thermal dissipation mechanisms providing a primary line of defense against excessive light, long-term adjustments of the antioxidant system and other photoprotective mechanisms, the relatively low level of control over electron transport exerted by the Water–Water cycle, especially under warm conditions, and a decrease in the content of the transgenic product during leaf aging.

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Abbreviations

APX:

ascorbate peroxidase

DCMU:

3–(3′,4′-dichlorophenyl)-1,1-dimethylurea

GR:

glutathione reductase

GSH:

reduced glutathione

MV:

methyl viologen

ROS:

reactive oxygen species

SOD:

superoxide dismutase

References

  • Adams WW, Demmig-Adams B (1994) Carotenoid composition and down regulation of Photosystem II in three conifer species during the winter Physiol Plant 92: 451–458

    CAS  Google Scholar 

  • Adams WW, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants Plant Biol 4: 545–557

    Google Scholar 

  • Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens Bioscience 54: 41–49

    Google Scholar 

  • Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants Plant Physiol 107: 1049–1054

    PubMed  CAS  Google Scholar 

  • Alscher RG and Hess JL (eds) (1993) Antioxidants in Higher Plants, CRC Press, Boca Raton, 174 pp

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

    PubMed  CAS  Google Scholar 

  • Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles Plant Physiol 98: 501–508

    PubMed  CAS  Google Scholar 

  • Andersson B, Barber J (1996) Mechanisms of photodamage and protein degradation during photoinhibition of Photosystem II In: Baker NR, (eds) Photosynthesis and the Environment. Kluwer Academic Publishers, Dordrecht, The Netherlands pp 101–121

    Google Scholar 

  • Aono M, Saji H, Sakamoto A, Tanaka K, Kondo N, Tanaka K (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase Plant Cell Physiol 36:1687–1691

    PubMed  CAS  Google Scholar 

  • Arisi AC, Cornic G, Jouanin L, Foyer CH (1998) Overexpression of iron superoxide dismutase in transformed poplar modifies the regulation of photosynthesis at low CO2 partial pressures or following exposure to the prooxidant herbicide methyl viologen Plant Physiol 117: 565–574

    PubMed  CAS  Google Scholar 

  • Asada K (1996) Radical production and scavenging in chloroplasts In: Baker NR (eds), Photosynthesis and the Environment. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 123–150

    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 

  • Badger MR (1985) Photosynthetoic oxygen exchange Annu Rev Plant Physiol 36: 27–53

    CAS  Google Scholar 

  • Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase Phil Trans Royal Soc Lond, Ser B 355: 1433–1446

    CAS  Google Scholar 

  • Barényi B, Krause GH (1985) Inhibition of photosynthetic reactions by light. A study with isolated spinach chloroplastsPlanta 163: 218–226

    Google Scholar 

  • Baier M, Deitz K-J (2005) Chloroplasts as a 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

    PubMed  CAS  Google Scholar 

  • Barnes D, Mayfield SP (2003) Redox control of posttranscriptional processes in the chloroplast Antioxidants Redox Signal 5: 89–94

    CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance Ann Rev Plant Physiol Plant Mol Biol 43: 83–116

    CAS  Google Scholar 

  • Bradley RL, Long KM, Frasch WD (1991) The involment of Photosystem II generated H2O2 in photoinhibition FEBS Lett 286: 209–213

    PubMed  CAS  Google Scholar 

  • Bratt CE, Arvidsson P-O, Carlsson M, Åkerlund HE (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration Photosynth Res 45: 169–175

    CAS  Google Scholar 

  • Bruggemann W, Beyel V, Brodka M, Poth H, Weil M, Stockhaus J (1999) Antioxidants and antioxidative enzymes in wild-type and transgenic Lycopersicon genotypes of different chilling tolerance Plant Sci 140: 145–154

    CAS  Google Scholar 

  • Burkle LA, Logan BA (2003) Seasonal acclimation of photosynthesis in eastern hemlock and partridgeberry growing in different light environmentsNortheastern Naturalist 10: 1–16

    Google Scholar 

  • Canvin DT, Berry JA, Badger MR, Fock H, Osmond CB (1980) Oxygen exchange in leaves in the light Plant Physiol 66: 302–307

    PubMed  CAS  Google Scholar 

  • Charles SA, Halliwell B (1981) Light activation of fructose bisphosphatase in isolated spinach chloroplasts and deactivation by hydrogen peroxidePlanta 151: 242–246

    CAS  Google Scholar 

  • Danna CH, Bartoli CG, Sacco F, Ingala LR, Santa-Maria GE, Guiamet JJ, Ugalde RA (2003) Thylakoid-bound ascorbate peroxidase mutant exhibits impaired electron transport and photosynthetic activityPlant Physiol 132: 2116–2125

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesisTrends Plant Sci 1: 21—26

    Google Scholar 

  • Fey V, Wagner R, Bräutigam K, Pfannschmidt (2005) Photosynthetic redox control of nuclear gene expressionJ Exp Bot 56: 1491–1498

    PubMed  CAS  Google Scholar 

  • Foote CS (1976) Photosensitized oxidation and singlet oxygen: consequences in biological systems In:Pryor WA (eds), Free Radicals in Biology 2.Academic Press New York, United States, pp 8–124

    Google Scholar 

  • Foyer CH (1993) Ascorbic acid In: Alscher RG, Hess JL (eds), Antioxidants in Higher Plants. CRC Press, Boca Raton, United States, pp. 31–58

    Google Scholar 

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

    Google Scholar 

  • Foyer CH and Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH, Mullineaux PM (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, pp 42. CRC Press, Boca Raton, United States

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants Plant Cell Environ 17: 507–523

    CAS  Google Scholar 

  • Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, 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, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling New Phytol 146: 359–388

    CAS  Google Scholar 

  • Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature Plant Physiol 116: 571–580

    PubMed  CAS  Google Scholar 

  • Furbank RT, Badger MR, Osmond CB (1982) Photosynthetic oxygen exchange in isolated cells and chloroplasts of C3 plants Plant Physiol 70: 927–931

    PubMed  CAS  Google Scholar 

  • Gamble PE, Burke JJ (1984) Effect of water stress on the chloroplast antioxidant system. I. Alterations in glutathione reductase activityPlant Physiol 76: 615–621

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves Physiologia Plantarum 99:197–209

    CAS  Google Scholar 

  • Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreensProc Natl Acad Sci, USA 97: 11098–11101

    PubMed  CAS  Google Scholar 

  • Grace S, Pace R, Wydrzynski T (1995) Formation and decay of monodehydroascorbate radicals in illuminated thylakoids as determined by EPR spectroscopyBiochim Biophys Acta 1229: 155–165

    Google Scholar 

  • Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen speciesPlant Physiol 112: 1631–1640

    PubMed  CAS  Google Scholar 

  • Grace SC, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathwayPhil Trans Royal Soc Lond, Ser B 355: 1499–1510

    CAS  Google Scholar 

  • Grace SC, Logan BA, Adams WW (1998) Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repensPlant Cell Environ 21: 513–521

    CAS  Google Scholar 

  • Gupta AS, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutaseProc Natl Acad Sci USA 90: 1629–1633

    PubMed  CAS  Google Scholar 

  • Guy CL, Carter JV (1984) Characterization of partially purified glutathione reductase from cold-hardened and nonhardened spinach leaf tissueCryobiology 21: 454–464

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free Radicals in Biology and Medicine.3 Oxford University Press, Oxford, p. 936

    Google Scholar 

  • Havaux M, Niyogi K (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanismProc Natl Acad Sci USA.96 8762–8767

    PubMed  CAS  Google Scholar 

  • Hirotsu N, Makino A, Ushio A, Mae T (2004) Changes in the thermal dissipation and the electron flow in the water/water cycle in rice grown under conditions of physiologically low temperaturePlant Cell Physiol 45: 635–644

    PubMed  CAS  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting Science 307: 433–436

    PubMed  CAS  Google Scholar 

  • Hossain HA, Asada K (1984) Purification of dehyrdroascorbate reductase from spinach and its characterisation as a thiol enzyme Plant Cell Physiol 25: 85–95

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Jablonski PP, Anderson JW (1982) Light-dependent reduction of hydrogen peroxide by ruptured pea chloroplastPlant Physiol 69: 1407–1413

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Korneyeyev D, Holaday A and Logan BA (2004) Minimization of the light energy absorbed by ȁ8closedȁ9 reaction centers of photosystem II as a photoprotective strategy in higher plants. Photosynthetica 42: 377–386

    CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Payton P, Allen RD, Holaday AS (2001) Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of Photosystem II in cotton overexpressing genes encoding chloroplast-targeted antioxidant enzymes Physiol Plant 113: 323–331

    PubMed  CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Allen RD, Holaday AS (2003a) Effect of chloroplastic overproduction of ascorbate peroxidase on photosynthesis and photoprotection in cotton leaves subjected to low temperature photoinhibition Plant Sci 165: 1033–1041

    CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Payton PR, Allen RD, Holaday AS (2003b) Elevated chloroplastic glutathione reductase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cottonFunct Plant Biol 30: 101–110

    CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Allen RD, Holaday AS (2005) Field-grown cotton plants with elevated activity of chloroplastic glutathione reductase exhibit no significant alteration of diurnal and seasonal patterns of excitation energy partitioning and CO2 fixation Field Crops Res 94: 165–175

    Google Scholar 

  • Kouril R, Lazar D, Lee H, Jo J, Naus J (2003) Moderately elevated temperature eliminates resistance of rice plants with enhanced expression of glutathione reductase to intensive photooxidative stress Photosynthetica 41: 571–578

    CAS  Google Scholar 

  • Kurepa J, Hérouart D, Van Montagu M, Inzé D (1997) Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress and hormonal treatments Plant Cell Physiol 38: 463–470

    PubMed  CAS  Google Scholar 

  • Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene J Plant Physiol 160: 347–353

    PubMed  CAS  Google Scholar 

  • Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerance of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress Plant Cell Environ 25: 873–882

    Google Scholar 

  • Li X-P, Phippard A, Pasari J, Niyogi KK (2002) Structure-function analysis of Photosystem II subunit S (PsbS) in vivo Funct Plant Biol 29: 1131–1139

    Google Scholar 

  • Link G (2003) Redox regulation of chloroplast transcription Antioxidants Redox Signal 5: 79–87

    CAS  Google Scholar 

  • Lohrmann N, Logan B, Johnson A 2004. Seasonal acclimatization of antioxidants and photosynthesis in Chondrus crispus and Mastocarpus stellatus, two co-occurring red algae with differing stress tolerancesBiol Bull 207: 225–232

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Logan BA, Barker DH, Demmig-Adams B, Adams WW (1997) The response of xanthophyll cycle-dependent energy dissipation in Alocasia brisbanensis to sunflecks in a subtropical rainforest Aust J Plant Physiol 24: 27–33

    Article  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW III, Grace SC (1998a) Antioxidation and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo and Vinca major acclimated to four growth irradiances in the field J Exp Bot 49: 1869–1879

    CAS  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW III (1998b) Antioxidation and xanthophyll cycle dependent energy dissipation in Cucurbita pepo and Vinca major during a transfer from low to high irradiance in the field J Exp Bot 49: 1881–1888

    CAS  Google Scholar 

  • Logan BA, Grace SC, Adams WW III, Demmig-Adams B (1998c) Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environmentsOecologia 116: 9–17

    Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW III (1999a) Acclimation of photosynthesis to the environment In: Singhal GS, Renger G, Sopory SK, Irrgang KD, Govindjee (eds), Concepts in Photobiology: Photosynthesis and Photomorphogenesis. Narosa Publishing House, New Dehli, India, pp 477–512

    Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW III, Rosenstiel TN (1999b) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics Planta 209: 213–220

    CAS  Google Scholar 

  • Logan BA, Monteiro G, Kornyeyev D, Payton P, Allen R, Holaday A (2003) Transgenic overproduction of glutathione reductase does not protect cotton, Gossypium hirsutum (Malvaceae), from photoinhibtion during growth under chilling conditions Am J Bot 90: 1400–1403

    Google Scholar 

  • Lovelock CE, Winter K (1996) Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical tree species Planta 198: 580–587

    CAS  Google Scholar 

  • Makino A, Miyake C, Yokota A (2002) Physiological functions of the Water–Water cycle (Mehler reaction) and the cyclic electron flow around PS I in rice leaves Plant Cell Physiol 43: 1017—1026

    PubMed  CAS  Google Scholar 

  • Matsubara S, Gilmore AM, Ball MC, Anderson JM, Osmond CB (2002) Sustained downregulation of Photosystem II in mistletoes during winter depression of photosynthesis Func Plant Biol 29: 1157–1169

    CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erthyrocuprein (hemocuprein)J Biol Chem 244: 6049–6055

    PubMed  CAS  Google Scholar 

  • McKersie BD, Murnaghan J, Jones KS, Bowley SR (2000) Iron-superoxide dismutase expression in transgenic alfalfa increases winter survival without a detectable increase in photosynthetic oxidative stress tolerance Plant Physiol 122: 1427–1438

    PubMed  CAS  Google Scholar 

  • Mehler AH (1951) Studies on the reaction of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagentsArch Biochem Biophys 33: 65–77

    CAS  Google Scholar 

  • Mehler AH, Brown AH (1952) Studies on the reactions of illuminated chloroplasts. III. Simultaneous photoproduction and consumption of oxygen studied with oxygen isotopesArch Biochem Biophys 38: 365–370

    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 

  • Mishra NP, Mishra RK, Singhal GS (1993) Changes in the activities of antioxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of different protein synthesis inhibitorsPlant Physiol 102: 867–880

    Google Scholar 

  • Mishra NP, Fatma T, Singhal GS (1995) Development of antioxidative defense system of wheat seedlings in response to high light Physiol Plant 95: 77–82

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from droughtPlant J 5: 397–405

    PubMed  CAS  Google Scholar 

  • Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoidsPlant Cell Physiol 33: 541–553

    CAS  Google Scholar 

  • Miyake C, Yokota A (2000) Determination of the rate of photoreduction of O2 in the Water–Water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesisPlant Cell Physiol 41: 335–343

    PubMed  CAS  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants Planta 194: 346–352

    CAS  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell deathPlant J 38: 940–953

    PubMed  CAS  Google Scholar 

  • Neubauer C, Yamamoto HY (1992) Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts Plant Physiol 99: 1354–1361

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches Annu Rev Plant Physiol Plant Mol Biol 50: 333–359

    PubMed  CAS  Google Scholar 

  • Noctor G, Veljovic-Jovanovic, Foyer CH (2000) Peroxide processing in photosynthesis: antioxidant coupling and redox signaling Phil Trans Royal Soc Lond, Ser B 355: 1465–1475

    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

    PubMed  CAS  Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46: 1351–1362

    CAS  Google Scholar 

  • Payton P, Allen RD, Trolinder N, Holaday AS (1997) Overexpression of chloroplast-targeted Mn superoxide dismutase in cotton (Gossypium hirsutum L., cv. Coker 312) does not alter the reduction of photosynthesis after short exposures to low temperature and high light intensityPhotosynth Res 52: 233–244

    CAS  Google Scholar 

  • Payton P, Webb R, Kornyeyev D, Allen R, Holaday S (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activityJ Exp Bot 52: 2345–2354

    PubMed  CAS  Google Scholar 

  • Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Soderberg L, Roepstorff P, von Heijne G, van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction Plant Cell 14: 211–236

    PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Liere K (2005) redox regulation and modification of proteins controlling chloroplast gene expressionAntioxidants Redox Signal 7: 607–618

    CAS  Google Scholar 

  • Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BM (1991) Overproduction of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco Plant Physiol 97: 452–455

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Prasil O, Adir N, Ohad I (1992) Dynamics of Photosystem II: mechanisms of photoinhibition and recovery processes In: Barber J, (eds), Topics in Photosynthesis, Vol. 11, The Photosystems: Structure, Function and Molecular Biology. Elsevier Science Publishers, Amsterdam, pp 295–348

    Google Scholar 

  • Richter M, Rühle W, Wild A (1990) Studies on of Photosystem II photoinhibition. II. The involvement of toxic oxygen speciesPhotosynth Res 24: 237–243

    CAS  Google Scholar 

  • Rubio MC, Gonzalez EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (1997) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutase Physiol Plant 115: 531–540

    Google Scholar 

  • Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000a) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of rubisco: little evidence for significant Mehler reaction J Exp Bot 51: 357–368

    CAS  Google Scholar 

  • Ruuska SA, von Caemmerer S, Badger MR, Andrews TJ, Price GD, Robinson SA (2000b) Xanthophyll cycle, light energy dissipation and electron transport in transgenic tobacco with reduced carbon assimilation capacity Aust J Plant Physiol 27: 289–300

    Article  CAS  Google Scholar 

  • Schöner S, Krause GH (1990) Protective systems against active oxygen species in spinach: response to cold acclimation in excess lightPlanta 180: 383–389

    Google Scholar 

  • Schwanz P, Polle A (2001) Differential stress responses on antioxidative systems to drought in pendunculate oak (Quercus robur) and maritime pine (Pinus pinaster) grown under high CO2 concentrationsJ Exp Bot 52: 133–143

    PubMed  CAS  Google Scholar 

  • Sen Gupta A, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993a) Increased tolerance to oxidative stress in transgenic plants that overexpress chloroplastic Cu Zn superoxide dismutase Proc Natl Acad Sci USA 90: 1629–1633

    CAS  Google Scholar 

  • Sen Gupta A, Webb PR, Holaday AS, Allen RD (1993b) Overexpression of superoxide dismutase protects plants from oxidative stress: induction of ascorbate peroxidase in superoxide dismutase-overproducing plants Plant Physiol 103: 1067–1073

    CAS  Google Scholar 

  • Slooten L, Capiau K, Van Camp W, Van Montagu M, Sybesma C, Inze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts Plant Physiol 107: 737–750

    PubMed  CAS  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1989) Properties and functions of glutathione reductase in plantsPhysiol Plant 77: 449–456

    CAS  Google Scholar 

  • Stevens RG, Creissen GP, Mullineaux PM (2000) Characterisation of pea cytosolic glutathione reductase expressed in transgenic tobacco Planta 211: 537–545

    PubMed  CAS  Google Scholar 

  • Strohm M, Eiblmeier M, Langebartels C, Jouanin L, Polle A, Sandermann H, Rennenberg H (1999) Responses of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase or glutathione reductase to acute ozone stress: visible injury and leaf gas exchangeJ Exp Bot 50: 363–372

    Google Scholar 

  • Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated level of chloroplastic SOD are not more resistant to superoxide toxicity Plant Mol Biol 14: 501–510

    PubMed  CAS  Google Scholar 

  • Terashima I, Noguchi K, Itoh-Nemoto T, Park Y-M, Kubo A, Tanaka K (1998) The cause of PS I photoinhibition at low temperatures in leaves of Cucumis sativus, a chilling sensitive plant Physiol Plant 103: 295–303

    CAS  Google Scholar 

  • Tschiersch H, Ohmann E (1993) Photoinhibition in Euglena gracilis: involment of reactive oxygen species Planta 191: 316–323

    CAS  Google Scholar 

  • Torsethaugen G, Pitcher LH, Zilinskas BA, Pell EJ (1997) Overproduction of ascorbate peroxidase in the tobacco chloroplast does not provide protection against ozone Plant Physiol 114:529–537

    PubMed  CAS  Google Scholar 

  • Tyystjärvi E, Riikonen M, Arisi A-CM, Kettunen R, Jouanin L, Foyer CH (1999) Photoinhibition of Photosystem II in tobacco plants overexpressing glutathione reductase and poplars overexpressing superoxide dismutase Physiol Plant 105: 409–416

    Google Scholar 

  • Van Camp W, Capiau K, Van Montagu M, Inze D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts Plant Physiol 112: 1703–1714

    PubMed  Google Scholar 

  • Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress Plant Cell Physiol 40: 725–732

    PubMed  CAS  Google Scholar 

  • Wang Y, Wisniewski M, Meilan R, Cui M, Webb R, Fuchigami L (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress J Am Soc Hort Sci 130: 167–173

    CAS  Google Scholar 

  • Winkler BS, Orselli SM, Rex TS (1994) The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective Free Radicals Biol Med 17: 333–349

    CAS  Google Scholar 

  • Wise RR (1995) Chilling-enhanced photooxidation. The production, action and study of reactive oxygen species produced during chilling in the lightPhotosynth Res 45: 79–97

    CAS  Google Scholar 

  • Wu J, Neimanis S, Heber U (1991) Photorespiration is more effective than the Mehler reaction in protecting the photosynthetic apparatus against photoinhibition Bot Acta 104: 283–291

    CAS  Google Scholar 

  • Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress Plant J 32: 915–925

    PubMed  CAS  Google Scholar 

  • Yan J, Wang J, Tissue D, Holaday AS, Allen R, Zhang H (2003) Photosynthesis and seed production under water-deficit conditions in transgenic tobacco plants that overexpress an Arabidopsis ascorbate peroxidase gene Crop Sci 43: 1477–1483

    Article  CAS  Google Scholar 

  • Yamasaki H, Grace SC (1998) EPR detection of phytophenoxyl radicals stabilized by zinc ions: evidence for the redox-coupling of plant phenolics with ascorbate in the H2O2-peroxidase systemFEBS Lett 422: 377–380

    PubMed  CAS  Google Scholar 

  • Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stressesPlant Physiol 123: 223–233

    PubMed  CAS  Google Scholar 

  • Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species Plant Cell Physiol 35: 785–791

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Bowdoin College, 6500 College Station, Brunswick, ME, 04011, USA

    Barry A. Logan & Justin Hardison

  2. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409, USA

    Dmytro Kornyeyev & A. Scott Holaday

  3. Institute of Plant Physiology and Genetics, Vasylkivska St. 31/17, 03022, Kyiv, Ukraine

    Dmytro Kornyeyev

Authors
  1. Barry A. Logan
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  2. Dmytro Kornyeyev
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  3. Justin Hardison
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  4. A. Scott Holaday
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Correspondence to Barry A. Logan.

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Logan, B.A., Kornyeyev, D., Hardison, J. et al. The role of antioxidant enzymes in photoprotection. Photosynth Res 88, 119–132 (2006). https://doi.org/10.1007/s11120-006-9043-2

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  • DOI: https://doi.org/10.1007/s11120-006-9043-2

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