The role of photochemical quenching and antioxidants in photoprotection of Deschampsia antarctica
Eduardo Pérez-Torres A , Andrea García A , Jorge Dinamarca A , Miren Alberdi B , Ana Gutiérrez C , Manuel Gidekel C , Alexander G. Ivanov D , Norman P. A. Hüner D , Luis J. Corcuera A and León A. Bravo A EA Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile.
B Instituto de Botánica, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile.
C Laboratorio de Fisiología y Biología Molecular Vegetal Facultad de Ciencias Agropecuarias y Forestales, Universidad de La Frontera, Casilla 54-D, Temuco, Chile.
D Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7Canada.
E Corresponding author; email: lebravo@udec.cl
Functional Plant Biology 31(7) 731-741 https://doi.org/10.1071/FP03082
Submitted: 3 May 2003 Accepted: 20 April 2004 Published: 22 July 2004
Abstract
Deschampsia antarctica Desv. (Poaceae) is the only grass that grows in the maritime Antarctic. Constant low temperatures and episodes of high light are typical conditions during the growing season at this latitude. These factors enhance the formation of active oxygen species and may cause photoinhibition. Therefore, an efficient mechanism of energy dissipation and / or scavenging of reactive oxygen species (ROS) would contribute to survival in this harsh environment. In this paper, non-acclimated and cold-acclimated D. antarctica were subjected to high light and / or low temperature for 24 h. The contribution of non-photochemical dissipation of excitation light energy and the activities of detoxifying enzymes in the development of resistance to chilling induced photoinhibition were studied by monitoring PSII fluorescence, total soluble antioxidants, and pigments contents and measuring variations in activity of superoxide dismutase (SOD; EC 1.15.1.1), ascorbate peroxidase (APX; EC 1.11.1.11), and glutathione reductase (GR; EC 1.6.4.2). The photochemical efficiency of PSII, measured as Fv / F m, and the yield of PSII electron transport (ΦPSII) both decreased under high light and low temperatures. In contrast, photochemical quenching (qP) in both non-acclimated and cold-acclimated plants remained relatively constant (approximately 0.8) in high-light-treated plants. Unexpectedly, qP was lower (0.55) in cold-acclimated plants exposed to 4°C and low light intensity. Activity of SOD in cold-acclimated plants treated with high light at low temperature showed a sharp peak 2–4 h after the beginning of the experiment. In cold-acclimated plants APX remained high with all treatments. Activity of GR decreased in cold-acclimated plants. Compared with other plants, D. antarctica exhibited high levels of SOD and APX activity. Pigment analyses show that the xanthophyll cycle is operative in this plant. We propose that photochemical quenching and particularly the high level of antioxidants help D. antarctica to resist photoinhibitory conditions. The relatively high antioxidant capacity of D. antarctica may be a determinant for its survival in the harsh Antarctic environment.
Keywords: Antarctic angiosperms, ascorbate peroxidase, glutathione reductase, low temperature, non-photochemical quenching, photochemical quenching, photoinhibition, reactive oxygen species, superoxide dimutase, xanthophyll cycle.
Acknowledgments
This paper was supported by FONDECYT 1000610, Fundación Andes C-13680/5, GIA-UdeC, 201.111.025–4, INACH 01–03, and DID UACH S200288, and the Natural Science and Engineering Research Council of Canada. We thank Valeria Neira for technical assistance. Eduardo Pérez was supported by a CONICYT fellowship. MECESUP UCO 9906 supported León A. Bravo’s research visit at University of Western Ontario, Canada.
Adams WW,
Demmig-Adams B,
Verhoeven AS, Barker DH
(1995) Photoinhibition during winter stress — involvement of sustained xanthophyll cycle-dependent energy-dissipation. Australian Journal of Plant Physiology 22, 261–276.
Alberdi M,
Bravo LA,
Gutiérrez A,
Gidekel M, Corcuera LJ
(2002) Ecophysiology of antarctic vascular plants. Physiologia Plantarum 115, 479–486.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alscher RG,
Donahue JL, Cramer CL
(1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiologia Plantarum 100, 224–233.
| Crossref | GoogleScholarGoogle Scholar |
Alscher RG,
Erturk N, Heath LS
(2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Anderson JV,
Chevone BI, Hess JL
(1992) Seasonal variation in the antioxidant system of eastern white pine needles. Plant Physiology 98, 501–508.
Asada K
(1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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. Philosophical Transactions Royal Society London Biology 355, 1433–1446.
| Crossref | GoogleScholarGoogle Scholar |
Bendall DS, Manasse RS
(1995) Cyclic photophosphorylation and electron transport. Biochimica et Biophysica Acta 1229, 23–38.
| Crossref | GoogleScholarGoogle Scholar |
Björkman O, Demmig-Adams B
(1995) Regulation of photosynthetic light energy capture, conversion and dissipation in leaves of higher plants. ‘Ecophysiology of photosynthesis’. (Eds E-D Schulze, MM Caldwell)
pp. 17–47. (Springer-Verlag: Berlin, Germany)
Bowler C, Fluhr R
(2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends in Plant Science 5, 241–246.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bowler C,
van Montagu M, Inzé D
(1992) Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43, 83–116.
| Crossref | GoogleScholarGoogle Scholar |
Bravo LA,
Ulloa N,
Zúñiga GE,
Casanova A,
Corcuera LJ, Alberdi M
(2001) Cold resistance in Antarctic angiosperms. Physiologia Plantarum 111, 55–65.
| Crossref | GoogleScholarGoogle Scholar |
Cogdell RJ, Frank HA
(1987) How carotenoids function in photosynthetic bacteria. Biochimica et Biophysica Acta 895, 63–79.
| PubMed |
Demmig-Adams B, Adams WW
(1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
| Crossref | GoogleScholarGoogle Scholar |
Diaz M,
Ball E, Luttge U
(1990) Stress-induced accumulation of the xanthophyll rhodoxanthin in leaves of Aloe vera.
Plant Physiology and Biochemistry 28, 679–682.
Donahue JL,
Okpodu CM,
Cramer CL,
Grabau EA, Alscher RG
(1997) Responses of antioxidants to paraquat in pea leaves. Plant Physiology 113, 249–257.
| PubMed |
Fink RC, Scandalios JG
(2002) Molecular evolution and structure–function relationships of the superoxide dismutase gene families in Angiosperms and their relationship to other eucaryotic and prokaryotic superoxide dismutases. Archives of Biochemistry and Biophysics 399, 19–36.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foyer CH, Halliwell B
(1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.
Foyer CH,
Lelandais M, Kunert KJ
(1994) Photooxidative stress in plants. Physiologia Plantarum 92, 696–717.
| Crossref | GoogleScholarGoogle Scholar |
Gilmore AM
(1997) Mechanistic role of xanthophyll-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99, 197–209.
| Crossref | GoogleScholarGoogle Scholar |
Gould KS,
McKelvie J, Marckham KR
(2002) Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant, Cell and Environment 25, 1261–1269.
| Crossref | GoogleScholarGoogle Scholar |
Grant JJ, Loake GJ
(2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology 124, 21–29.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grasses T,
Pesaresi P,
Schiavon F,
Varotto C,
Salamini F,
Jahns P, Leister D
(2002) The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana.
Plant Physiology and Biochemistry 40, 41–49.
| Crossref | GoogleScholarGoogle Scholar |
Hüner NPA,
Öquist G,
Hurry VM,
Krol M,
Falk S, Griffith M
(1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynthesis Research 37, 19–39.
Hüner NPA, Ivanov AG, Wilson KE, Miskiewicz E, Krol M, Öquist G
(2002) Energy sensing and photostasis in photoautotrophs. ‘Sensing, signaling and cell adaptation’. (Eds KB Storey, JM Storey)
pp. 243–255. (Elsevier Science BV: Amsterdam, The Netherlands)
Hurry V,
Anderson JM,
Chow WS, Osmond CB
(1997) Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo.
Plant Physiology 113, 639–648.
| PubMed |
Inzé D, Van Montagu M
(1995) Oxidative stress in plants. Current Opinion in Biotechnology 6, 153–158.
| Crossref | GoogleScholarGoogle Scholar |
Ivanov AG,
Krol M,
Maxwell D, Huner NPA
(1995) Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle. FEBS Letters 371, 61–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kimura M,
Yoshizumi T,
Manabe K,
Yamamoto YY, Matsui M
(2001)
Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and -independent pathways. Genes to Cells 6, 607–617.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kornyeyev D,
Logan BA,
Payton PR,
Allen RD, Holaday AS
(2003) Elevated chloroplastic glutathione reductase activities decreased chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton. Functional Plant Biology 30, 101–110.
| Crossref | GoogleScholarGoogle Scholar |
Krinsky NI
(1989) Antioxidant functions of carotenoids. Free Radical Biology and Medicine 7, 617–635.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lewis-Smith RI
(2003) The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica. ‘Antarctic biology in a global context’. (Eds AHL Huiskes, WWC Gieskes, J Rozema, RML Schorno, SM vander Vies, WJ Wolff)
pp. 234–239. (Backhuys Publishers: Leiden, The Netherlands)
Li X-P,
Björkman O,
Shih C,
Grossman AR,
Rosenquist M,
Jansson S, Niyogi K
(2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395.
| Crossref | GoogleScholarGoogle Scholar |
McCord JM, Fridovich I
(1969) Superoxide dismutase. An enzymic function for erythrocuprin (hemocuprin). The Journal of Biological Chemistry 224, 6049–6055.
Mittler R
(2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Müller P,
Li X-P, Niyogi K
(2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Crossref | GoogleScholarGoogle Scholar |
Neill SO,
Gould KS,
Kilmartin PA,
Mitchell KA, Markham KR
(2002) Antioxidant capacities of green and cyanic leaves in the sun species, Quintinia serrata.
Functional Plant Biology 29, 1437–1443.
| Crossref | GoogleScholarGoogle Scholar |
Niyogi KK,
Grossman AR, Björkman O
(1998)
Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niyogi KK
(1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333–359.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niyogi KK
(2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niyogi KK,
Shih C,
Chow WS,
Pogson BJ,
DellaPenna D, Björkman O
(2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis.
Photosynthesis Research 67, 139–145.
| Crossref | GoogleScholarGoogle Scholar |
Omran RG
(1980) Peroxide levels and the activities of catalase, peroxidase and indoleacetic acid oxidase during and after chilling cucumber seedlings. Plant Physiology 65, 407–408.
Palozza P, Krinsky NI
(1992) Antioxidant effects of carotenoids in vivo and in vitro: an overview. Methods in Enzymology 213, 403–420.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Prasad TK,
Anderson MD,
Martin BA, Stewart CR
(1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. The Plant Cell 6, 65–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Raison JK, Lyons JM
(1970) Oxidative activity of mitochondria isolated from plant tissues sensitive and resistant to chilling injury. Plant Physiology 45, 386–389.
| PubMed |
Rajguru S,
Banks S,
Gossett D, Lucas MC
(1999) Antioxidant response to salt stress during fiber development in cotton ovules. Journal of Cotton Science 3, 11–18.
Rao MV,
Gopinadhan P, Ormrod DP
(1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana.
Plant Physiology 110, 125–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ruban AV,
Pascal AA,
Robert B, Horton P
(2002) Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. Journal of Biological Chemistry 277, 7785–7789.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schöner S, Krause GH
(1990) Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta 180, 383–389.
Schreiber U,
Schliwa W, Bilger W
(1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosynthesis Research 10, 51–62.
Stajner D,
Milic N,
Lazic B, Mimica-Dukié N
(1998) Study on antioxidant enzymes in Allium cepa L. and Allium fistulosum L. Phytotherapy Research 12, s15–s17.
| Crossref | GoogleScholarGoogle Scholar |
Un-Haing C, Jung OP
(2000) Mercury-induced oxidative stress in tomato seedlings. Plant Science 156, 1–9.
| Crossref |
van Kooten O, Snel JFH
(1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25, 147–150.
Xiong FS,
Ruhland CT, Day TA
(1999) Photosynthetic temperature response of the Antarctic vascular plants Colobanthus quitensis and Deschampsia antarctica.
Physiologia Plantarum 106, 276–286.
| Crossref | GoogleScholarGoogle Scholar |
Xiong FS,
Mueller EC, Day TA
(2000) Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. American Journal of Botany 87, 700–710.
| PubMed |
Xu C-C,
Li L, Kuang T
(2000) Photoprotection in chilling-sensitive and -resistant plants illuminated at chilling temperature: role of the xanthophyll cycle in the protection against lumen acidification. Australian Journal of Plant Physiology 27, 669–675.
| Crossref | GoogleScholarGoogle Scholar |
Yu Q, Rengel Z
(1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Annals of Botany 83, 175–182.
| Crossref | GoogleScholarGoogle Scholar |
