Abstract
This paper discusses biochemical and regulatory aspects of the violaxanthin cycle as well as its possible role in photoprotection. The violaxanthin cycle responds to environmental conditions in the short-term and long-term by adjusting rates of pigment conversions and pool sizes of cycle pigments, respectively. Experimental evidence indicating a relationship between zeaxanthin formation and non-photochemical energy dissipation is reviewed. Zeaxanthin-associated energy dissipation appears to be dependent on transthylakoid ΔpH. The involvement of light-harvesting complex II in this quenching process is indicated by several studies. The current hypotheses on the underlying mechanism of zeaxanthin-dependent quenching are alterations of membrane properties, including conformational changes of the light-harvesting complex II, and singlet-singlet energy transfer from chlorophyll to zeaxanthin
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Abbreviations
- chl:
-
chlorophyll
- DBMIB:
-
2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone
- DCMU:
-
3,3-(3′,4′-dichlorophenyl)-1,1-dimethylurea
- DTT:
-
dithiothreitol
- Fo :
-
minimum fluorescence yield with all PS II reaction centers open
- LHC:
-
light-harvesting complex
- PS:
-
photosystem
- PQ:
-
plastoquinone
- qE-quenching:
-
pN-quenching dependent on thylakoid lumen acidification
- qN-quenching:
-
non-photochemical quenching
- UV-B:
-
ultraviolet radiation in the range from 280 to 320 nm
References
AdamsIII WW, Demmig-Adams B and Winter K (1990) Relative contribution of zeaxanthin-related and zeaxanthin-unrelated types of ‘high-energy-state’ quenching of chlorophyll fluorescence in spinach leaves exposed to various environmental conditions. Plant Physiol 92: 302–309
AdamsIII WW and Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186: 390–398
AdamsIII WW, Demmig-Adams B and Lange OL (1993) Carotenoid composition and metabolism in green and blue-green algal lichens in the field. Oecologia 94: 576–584
Arsalane W, Rousseau B and Duval J-C (1994) Influence of the pool size of the xanthophyll cycle on the effects of a light stress in a diatom: Competition between photoprotection and photoinhibition. Photochem Photobiol 60: 237–243
Avron M and Schreiber U (1977) Proton gradients as possible intermediary energy transducers during ATP-driven reverse electron flow in chloroplasts. FEBS Lett 77: 1–6
Barry P, Young AJ and Britton G (1991) Accumulation of pigments during the greening of etiolated seedlings ofHordeum vulgare L. J Exp Bot 42: 229–234
Bassi R, Pineau B, Dainese P and Marquardt J (1993) Carotenoid-binding proteins of Photosystem II. Eur J Biochem 212: 297–303
Beddard GS, Davidson RS and Trethewey KR (1977) Quenching of chlorophyll fluorescence by β-carotene. Nature 26: 373–374
Bidigare RR, Schofield O and Prézelin BB (1989) Influence of zeaxanthin on quantum yield ofSynechococcus clone WH7803 (DC2). Mar Ecol Prog Ser 56: 177–188
Bilger W and Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves ofHedera canariensis. Photosynth Res 25: 173–185
Bilger W and Björkman O (1991) Temperature dependence of violaxanthin deepoxidation and non-photochemical fluorescence quenching in intact leaves ofGossypium hirsutum L. andMalva parviflora L. Planta 184: 226–234
Bilger W and Björkman O (1994) Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193: 238–246
Bilger W, Björkman O and Thayer SS (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol 91: 542–551
Bilger W, Heber U and Schreiber U (1988) Kinetic relationship between energy-dependent fluorescence quenching, light scattering, chlorophyll luminescence and proton pumping in intact leaves. Z Naturforsch 43c: 877–887
Björkman O (1987) High-irradiance stress in higher plants and interaction with other stress factors. In: Biggins L (ed) Progress in Photosynthesis Research, Vol 4, pp 11–18. Martinus Nijhoff Publishers, Dordrecht, The Netherlands
Björkman O and Demmig-Adams B (1994) Regulation of photosynthetic light energy capture conversion, and dissipation in leaves of higher plants. In: Schulze E-D and Caldwell MM (eds) Ecophysiology of Photosynthesis, pp 17–47. Springer, Berlin
Briantais J-M, Vernotte C, Picaud M and Krause GH (1979). A quantitative study of the slow decline of chlorophyll fluorescence in isolated chloroplasts. Biochim Biophys Acta 548: 128–138
Brugnoli E and Björkman O (1992a) Growth of cotton under continuous salinity stress: Influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. Planta 187: 335–347
Brugnoli E and Björkman O (1992b) Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth Res 32: 23–35
Büchel C and Wilhelm C (1993) In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: Progress, problems and perspectives. Photochem Photobiol 58: 137–148
Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29: 345–378
Cammarata KV and Schmidt GW (1992) In vitro reconstitution of a light-harvesting gene product: Deletion mutagenesis and analysis of pigment binding. Biochemistry 31: 2779–2789
Caron L, Duval J-C and Arsalane W (1992) Comparative efficiency of the violaxanthin-zeaxanthin and diadino-diatoxanthin cycles in PS II photoprotective processes. FESPP workshop on the environmental factors affecting Photosystem II, Szeged, Hungary
Costes C (1968) Caroténoïdes et photosynthèse: variations induites de la teneur en pigments dans des folioles excisées de tomate. Ann Physiol Vég 10: 171–197
Costes C, Burghoffer C, Joyard J, Block M and Douce R (1979) Occurrence and biosynthesis of violaxanthin in isolated spinach chloroplast envelope. FEBS Lett 103: 17–21
Dainese P, Marquardt J, Pineau B and Bassi R (1992) Identification of violaxanthin and zeaxanthin binding proteins in maize Photosystem II. In: Murata N (ed) Research in Photosynthesis, Vol 1, pp 287–290. Kluwer Academic Publishers, Dordrecht, The Netherlands
DeCoster B, Christensen RL, Gebhard R, Lugtenburg J, Farhoosh R and Frank HA (1992) Low-lying electronic states of carotenoids. Biochim Biophys Acta 1102: 107–114
Demmig B and Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184
Demmig B and Winter K (1988) Characterisation of three components of non-photochemical fluorescence quenching and their response to photoinhibition. Aust J Plant Physiol 15: 163–177
Demmig B, Winter K, Krüger A and Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. Plant Physiol 84: 218–224
Demmig-Adams B (1990a) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24
Demmig-Adams (1990b) Zeaxanthin-associated energy dissipation and the susceptibility of various organisms to light stress. In: Baltscheffsky M (ed) Current research in Photosynthesis, Vol 2, pp 357–364. Kluwer Academic Publishers, Dordrecht, The Netherlands
Demmig-Adams B and AdamsIII WW (1990) The carotenoid zeaxanthin and ‘high-energy-state quenching’ of chlorophyll fluorescence. Photosynth Res 25: 187–197
Demmig-Adams B and AdamsIII WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626
Demmig-Adams B and AdamsIII WW (1993a) The xanthophyll cycle, protein turnover, and the high light tolerance of sunacclimated leaves. Plant Physiol 103: 1413–1420
Demmig-Adams B and AdamsIII WW (1993b) The xanthophyll cycle. In: Alscher RG and Hess JL (eds) Antioxidants in Higher Plants, pp 91–110. CRC Press, Boca Raton, FL
Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989a) Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol 90: 881–886
Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989b) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol 90: 887–893
Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989c) Zeaxanthin synthesis, energy dissipation, and photoprotection of Photosystem II at chilling temperatures. Plant Physiol 90: 894–898
Demmig-Adams B, AdamsIII WW, Czygan F-C, Schreiber U and Lange OL (1990a) Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in the carotenoid composition. Planta 180: 582–589
Demmig-Adams B, AdamsIII WW, Heber U, Neimanis S, Winter K, Krüger A Czygan F-C, Bilger W and Björkman O (1990b) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92: 293–301
Dexter DL (1953) A theory of sensitized luminescence in solids. J Chem Phys 21: 836–850
Dilley RA (1991) Energy coupling in chloroplasts: A calcium-gated switch controls proton fluxes between localized and delocalized proton gradients. Curr Topics Bioenerg 16: 265–318
Dilley RA, Theg SM and Beard WA (1987) Membrane-proton interactions in chloroplast bioenergetics: Localized proton domains. Ann Rev Plant Physiol 38: 347–389
Douce R and Joyard J (1979) Structure and function of the plastid envelope. In: Woolhouse HW (ed) Advances in Botanical Research, Vol 7, pp 1–116. Academic Press, London
Duval J-C, Harker M, Rousseau B, Young AJ, Britton G and Lemoine Y (1992) Photoinhibition and zeaxanthin formation in the brown algaeLaminaria saccharina andPelvetia canaliculata. In: Murata N (ed) Research in Photosynthesis, Vol 4, pp 581–584. Kluwer Academic Publishers, Dordrecht, The Netherlands
Eickmeier WG, Casper C and Osmond CB (1993) Chlorophyll fluorescence in the resurrection plantSelaginella lepidophylla (Hook. & Grev.) Spring during high-light and desiccation stress, and evidence for zeaxanthin-associated photoprotection. Planta 189: 30–38
Foyer CH and Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH and Mullineaux PM (eds) Causes of Photooxidative Stress and Amelioration of Defence Systems in Plants, pp 1–42. CRC Press, Boca Raton, FL
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
Foyer CH, Dujardyn M and Lemoine Y (1989) Responses of photosynthesis and the xanthophyll and ascorbate-glutathione cycles to changes in irradiance, photoinhibition and recovery. Plant Physiol Biochem 27: 751–760
Foyer CH, Furbank R, Harbinson J and Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25: 83–100
Frank HA, Farhoosh R, Aldema ML, DeCoster B, Christensen RL, Gebhard R and Lugtenburg J (1993) Carotenoid-to-bacteriochlorophyll singlet energy transfer in carotenoid-incorporated B850 light-harvesting complexes ofRhodobacter sphaeroides R-26.1. Photochem Photobiol 57: 49–55
Frank HA, Cua A, Chynwat V, Young A, Gosztola D and Wasielewski PMR (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41: 389–395
Franklin LA, Levavasseur G, Osmond CB, Henley WJ and Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186: 399–408
Genty B, Harbinson J, Briantais JM and Baker NR (1990) The relationship between the relative quantum efficiencies of photosystems in leaves. Efficiency of PS2 in relation to non-photochemical fluorescence quenching. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 4, pp 365–368. Kluwer Academic Publishers, Dordrecht, The Netherlands
Gerbling KP, Kelly GJ, Fisher KH and Latzko E (1984) Partial purification and properties of soluble ascorbate peroxidase from tea leaves. J Plant Physiol 115: 59–67
Giersch C and Krause GH (1991) A simple model relating photoinhibitory fluorescence quenching in chloroplasts to a population of altered Photosystem II reaction centers. Photosynth Res 30: 115–121
Gillbro T, Andersson PO, Liu RSH, Asato AE, Takaishi S and Cogdell RJ (1993). Location of the carotenoid 2Ag-state and its role in photosynthesis. Photochem Photobiol 57: 44–48
Gillham DJ and Dodge AD (1986) Hydrogen-scavenging systems within pea chloroplasts: A quantitative study. Planta 167: 246–251
Gilmore AM and Björkman O (1994a) Adenine nucleotides and the xanthophyll cycle in leaves. I. Effects of CO2- and temperature-limited photosynthesis on adenylate energy charge and violaxanthin de-epoxidation. Planta 192: 526–536
Gilmore AM and Björkman O (1994b) Adenine nucleotides and the xanthophyll cycle in leaves. II. Comparison of the effects of CO2- and temperature-limited photosynthesis on Photosystem II fluorescence quenching, the adenylate energy charge and violaxanthin de-epoxidation in cotton. Planta 192: 537–544
Gilmore AM and Yamamoto HY (1990) Zeaxanthin formation in qE-inhibited chloroplasts. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 2, pp 495–498. Kluwer Academic Publishers, Dordrecht, The Netherlands
Gilmore AM and Yamamoto HY (1991) Zeaxanthin formation and energy dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and and cyclic electron transport. Plant Physiol 96: 635–643
Gilmore AM and Yamamoto HY (1992a) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc Natl Acad Sci USA 89: 1899–1903
Gilmore AM and Yamamoto HY (1992b) Zeaxanthin-dependent quenching of the variable fluorescence arising from ATP-induced reverse electron flow. In: Murata M (ed) Research in Photosynthesis, Vol 1, pp 255–258. Kluwer Academic Publishers, Dordrecht, The Netherlands
Gilmore AM and Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67–78
Green BR, Durnford D, Aebersold R and Pichersky E (1992) Evolution of structure and function in the chla/b and chla/c antennae protein family. In: Murata M (ed) Research in Photosynthesis, Vol 1, pp 195–202. Kluwer Academic Publishers, Dordrecht, The Netherlands
Grumbach K (1984) New aspects about the xanthophyll cycle of higher plants. In: Siegenthaler P-A and Eichenberger W (eds) Structure, Function and Metabolism of Plant Lipids, pp 259–262. Elsevier Science Publishers, Amsterdam
Gruszecki WI and Krupa Z (1993a) LHC II preparation exhibits properties of a zeaxanthin epoxidase. J Photochem Photobiol B: Biol 17: 291–292
Gruszecki WI and Krupa Z (1993b) LHC II, the major light-harvesting pigment-protein complex is a zeaxanthin epoxidase. Biochim Biophys Acta 1144: 97–101
Gruszecki WI and Strzalka K (1991) Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta 1060: 310–314
Gust D and Moore TA (1991) Mimicking photosynthetic electron transport and energy transfer. In: Volman D, Hammond G and Neckers D (eds) Advances in Photochemistry, pp 1–65. John Wiley & Sons, New York
Hager A (1966) Die Zusammenhänge zwischen lichtinduzierten Xanthophyll-Umwandlungen und Hill-Reaktion. Ber Deutsch Bot Ges 79: 94–107
Hager A (1967a) Untersuchungen über die lichtinduzierten reversiblen Xanthophyllumwandlungen an Chlorella und Spinacia. Planta 74: 148–172
Hager A (1967b) Untersuchungen über die Rückreaktionen im Xanthophyll-Cyclus bei Chlorella, Spinacia und Taxus. Planta 76: 138–148
Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin- → Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta 89: 224–243
Hager A (1975) Die reversiblen, lichtabhängigen Xanthophyll-umwandlungen im Chloroplasten. Ber Deutsch Bot Ges 88: 27–44
Hager A (1980) The reversible light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in Plants, pp 57–79. Fischer, Stuttgart
Hager A and Holocher K (1994) Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 192: 581–589
Hager A and Perz H (1970) Veränderung der Lichtabsorption eines Carotinoids im Enzym(De-epoxidase)-Substrat(violaxanthin)-komplex. Planta 93: 314–322
Havaux M and Gruszecki WI (1993) Heat- and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin: Indications of a regulatory effect of zeaxanthin on thylakoid membrane fluidity. Photochem Photobiol 58: 607–614
Havaux M, Strasser RS and Greppin H (1990) In vivo photoregulation of photochemical and nonphotochemical deactivation of Photosystem II in intact plants. Plant Physiol Biochem 28(6). 735–746
Havaux M, Gruszecki WI, Dupont I and Leblanc RM (1991) Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J Photochem Photobiol B 8: 361–370
Heber U (1969) Conformational changes of chloroplasts induced by illumination of leaves in vivo. Biochim Biophys Acta 180: 302–319
Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I and Heldt HW (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95: 1131–1137
Holzwarth AR (1991) Excited-state kinetics in chlorophyll systems and its relationship to the functional organization of the photosystems. In: Scheer H (ed) The Chlorophylls, pp 1125–1151. CRC Press, Boca Raton, FL
Horton P and Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochim Biophys Acta 932: 107–115
Horton P and Ruban AV (1992) Regulation of Photosystem II. Photosynth Res 34: 375–385
Horton P and Ruban AV (1993) ΔpH-dependent quenching of the Fo level of chlorophyll fluorescence in spinach leaves. Biochim Biophys Acta 1142: 203–206
Horton P and Ruban AV (1994) The role of light-harvesting complex II in energy quenching. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 111–128. Bios Scientific Publishers, Oxford
Horton P, Ruban AV, Rees D, Pascal AA, Noctor G and Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett 292: 1–4
Huner NPA, Öquist G, Hurry VM, Krol M, Falk S and Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19–39
Irrgang K-D, Geiken B, Lange B and Renger G (1992) Disulfide bridge modifiers and sulfhydryl group blockers are inactivating the oxygen evolving enzyme of PS II from spinach. In: Murata N (ed) Research in Photosynthesis, Vol 2, pp 417–420. Kluwer Academic Publishers, Dordrecht, The Netherlands
Jahns P and Krause GH (1994) Xanthophyll cycle and energy-dependent fluorescence quenching in leaves from pea plants grown under intermittent light. Planta 192: 176–182
Jansson S (1994) The light-harvesting chlorophylla/b-binding proteins. Biochim Biophys Acta 1184: 1–19
Johnson GN, Scholes JD, Horton P and Young AJ (1993a) Relationships between carotenoid composition and growth habit in British plant species. Plant, Cell and Environment 16: 681–686
Johnson GN, Young AJ, Scholes JD and Horton P (1993b) The dissipation of excess excitation energy in British plant species. Plant, Cell and Environment 16: 673–679
Joyard J and Douce R (1976) Préparation et activités enzymatiques de l'enveloppe des chloroplastes d'Épinard. Physiol Vég 14: 31–48
Junesch V and Gräber P (1985) The rate of ATP synthesis as a function of ΔpH in normal and dithiothreitol-modified chloroplasts. Biochim Biophys Acta 809: 429–434
Junesch V and Gräber P (1987) Influence of the redox state and the activation of the chloroplast ATP synthase on proton transport-coupled ATP synthesis/hydrolysis. Biochim Biophys Acta 893: 275–288
Krause GH (1973) The high-energy state of the thylakoid system as indicated by chlorophyll fluorescence and chloroplast shrinkage. Biochim Biophys Acta 292: 715–728
Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 331–348. Bios Scientific Publishers, Oxford
Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Mol Biol 42: 313–349
Krause GH, Laasch H and Weis E (1988) Regulation of thermal dissipation of absorbed light energy in chloroplasts indicated by energy-dependent fluorescence quenching. Plant Physiol Biochem 26(4): 445–452
Krieger A and Weis E (1992) Energy-dependent quenching of chlorophyll-a-fluorescence: The involvement of proton-calcium exchange at Photosystem 2. Photosynthetica 27: 89–98
Krieger A and Weis E (1993) The role of calcium in the pH-dependent control of Photosystem II. Photosynth Res 37: 117–130
Krieger A, Moya I and Weis E (1992) Energy-dependent quenching of chlorophylla fluorescence: Effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem II preparations. Biochim Biophys Acta 1102: 167–176
Krinsky NJ (1966) The role of carotenoid pigments as protective agents against photosensitized oxidations in chloroplasts. In: Goodwin TW (ed) Biochemistry of Chloroplasts, Vol 1, pp 423–430. Academic Press, New York
Laisk A, Oja V, Kiirats O, Raschke K and Heber U (1989) The state of the photosynthetic apparatus in leaves as analyzed by rapid gas exchange and optical methods: The pH of the chloroplast stroma and activation of enzymes in vivo. Planta 177: 350–358
Leisner JMR, Bilger W, Czygan F-C and Lange OL (1993) Lipophilous carotenoids of cyanobacterial lichens from different habitats, including an extreme desert site. Crypt Bot 4: 74–82
Leisner JMR, Bilger W, Czygan F-C and Lange OL (1994) Light exposure and carotenoids in lichens. J Plant Physiol 143: 514–519
Leverenz JW, Öquist G and Wingsle G (1992) Photosynthesis and photoinhibition in leaves of chlorophyllb-less barley in relation to absorbed light. Physiol Plant 85: 495–502
Lichtenthaler HK and Schindler C (1992) Studies on the photoprotective function of zeaxanthin at high-light conditions. In: Murata N (ed) Research in Photosynthesis, Vol 4, pp 517–520. Kluwer Academic Publishers, Dordrecht, The Netherlands
Liu L-X, Chow WS and Anderson JM (1993) Light quality during growth ofTradescantia albiflora regulates photosystem stoichiometry, photosynthetic function and susceptibility to photoinhibition. Physiol Plant 89: 854–860
Lokstein H, Härtel H, Hoffmann P and Renger G (1993) Comparison of chlorophyll fluorescence quenching in leaves of wild-type with a chlorophyll-b-less mutant of barley (Hordeum vulgare L.). J Photochem Photobiol B: Biol 19: 217–225
Lovelock CE and Clough BF (1992) Influence of solar radiation and leaf angle on leaf xanthophyll concentrations in mangroves. Oecologia 91: 518–525
Machold O (1981) Chlorophylla/b-proteins and light-harvesting complex ofVicia faba andHordeum vulgare. Biochem Physiol Pflanzen 176: 805–827
Mimuro M (1990) Studies on excitation energy flow in the photosynthetic pigment system; structure and energy transfer mechanism. Bot Mag Tokyo 103: 233–253
Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41, 445–502
Morales F, Abadia A and Abadia J (1990) Characterization of the xanthophyll cycle and other photosynthetic pigment changes induced by iron deficiency in sugar beet (Beta vulgaris L.). Plant Physiol 94: 607–613
Mullineaux CW, Pascal AA, Horton P and Holzwarth AR (1993) Excitation-energy quenching in aggregates of LHC II chlorophyll-protein complex: A time-resolved fluorescence study. Biochim Biophys Acta 1141: 23–28
Neubauer C (1993) Multiple effects of DTT on non-photochemical fluorescence quenching in intact chloroplasts: Influence on violaxanthin de-epoxidase activity and ascorbate peroxidase activity. Plant Physiol 103: 575–583
Neubauer C and Yamamoto HY (1992) Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts. Plant Physiol 99: 1354–1361
Neubauer C and Yamamoto HY (1994) Membrane barriers and Mehler-peroxidase reaction limit the ascorbate available for deepoxidase activity in intact chloroplasts. Photosynth Res 39: 137–147
Noctor G, Rees D, Young A and Horton P (1991) The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts. Biochim Biophys Acta 1057: 320–330
Noctor G, Ruban AV and Horton P (1993) Modulation of ΔpH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach leaves. Biochim Biophys Acta 1183: 339–344
Oberhuber W and Bauer H (1991) Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees. Planta 185: 545–553
Ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184: 538–544
Omata T and Murata N (1984) Isolation and characterization of three types of membranes from the cyanobacterium (blue-green algae)Synechocystis PCC 6714. Arch Microbiol 139: 113–116
Öquist G, Anderson JM, McCaffery S and Chow WS (1992a) Mechanistic differences in photoinhibition of sun and shade leaves. Planta 188: 422–431
Öquist G, Chow WS and Anderson JM (1992b) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of Photosystem II. Planta 186: 450–460
Owens TG (1994) Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 95–107. Bios Scientific Publishers, Oxford
Owens TG, Shreve AP and Albrecht AC (1992) Dynamics and mechanism of singlet energy transfer between carotenoids and chlorophylls: light harvesting and non-photochemical fluorescence quenching. In: Murata N (ed) Research in Photosynthesis, Vol 1, pp 171–178. Kluwer Academic Publishers, Dordrecht, The Netherlands
Oxborough K and Horton P (1987) Characterization of the effects of antimycin A upon high energy state quenching of chlorophyll fluorescence (qE) in spinach and pea chloroplasts. Photosynth Res 12: 119–128
Paulsen H, Rümler U and Rüdiger W (1990) Reconstitution of pigment-containing complexes from light-harvesting chlorophylla/b-binding protein overexpressed inEscherichia coli. Planta 181: 204–211
Peter GF and Thornber JP (1991) Biochemical composition and organization of higher plant Photosystem II light-harvesting pigment-proteins. J Biol Chem 266: 16745–16754
Pfündel E (1993) Is zeaxanthin capable of energy transfer to chlorophyll a in partially greened leaves? A study of fluorescence excitation spectra during violaxanthin deepoxidation. Photochem Photobiol 57: 356–361
Pfündel E and Baake E (1990) A quantitative description of fluorescence excitation spectra in intact bean leaves greened under intermittent light. Photosynth Res 26: 19–28
Pfündel E and Dilley RA (1993) The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts. Plant Physiol 101: 65–71
Pfündel E and Strasser RJ (1988) Violaxanthin de-epoxidase in etiolated leaves. Photosynth Res 15: 67–73
Pfündel E, Pan R-S and Dilley RA (1992) Inhibition of violaxanthin deepoxidation by ultraviolet-B radiation in isolated chloroplasts and intact leaves. Plant Physiol 98: 1372–1380
Pfündel E, Renganathan M, Gilmore AM, Yamamoto HY and Dilley RA (1994) Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin deepoxidation. Plant Physiol (in press)
Plumley FG and Schmidt GW (1987) Reconstitution of chlorophylla/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci USA 84: 146–150
Quick WP and Horton P (1984) Studies on the induction of chlorophyll fluorescence quenching by redox state and transthylakoid pH gradient. Proc R Soc Lond Ser B 220: 371–382
Quick WP and Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim Biophys Acta 977: 287–296
Quiñones MA and Zeiger E (1994) A putative role of the xanthophyll, zeaxanthin, in blue light photoreception of corn coleoptiles. Science 264: 558–561
Ramm D and Hansen U-P (1993) Can charge recombination as caused by pH-dependent donor-side limitation in PS2 account for high-energy state quenching? Photosynth Res 35: 97–100
Rees D, Young A, Noctor G, Britton G and Horton P (1989) Enhancement of the ΔpH-dependent dissipation of excitation energy in spinach chloroplast by light-activation: Correlation with the synthesis of zeaxanthin. FEBS Lett 256: 85–90
Rees D, Noctor GD and Horton P (1990) The effect of high-energystate quenching on maximum and dark level fluorescence yield. Photosynth Res 25: 199–211
Rees D, Noctor G, Ruban AV, Crofts J, Young A and Horton P (1992) pH Dependent chlorophyll fluorescence quenching in spinach thylakoids from light treated or dark adapted leaves. Photosynth Res 31: 11–19
Renganathan M, Pfündel E, Dilley RA (1993) Thylakoid lumenal pH determination using a fluorescent dye: Correlation of lumen pH and gating between localized and delocalized energy coupling. Biochim Biophys Acta 1142: 277–292
Richter M, Goss R, Böthin B and Wild A (1994) Zeaxanthin dependent and zeaxanthin independent changes in nonphotochemical energy dissipation. J Plant Physiol 143: 495–499
Rock CD and Zeevaart (1991) The aba mutant ofArabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA: 7496–7499
Rock CD, Bowlby NR, Hoffmann-Benning S and Zeevaart JAD (1992) The aba mutant ofArabidopsis thaliana (L.) Heynh. has reduced chlorophyll fluorescence yields and reduced thylakoid stacking. Plant Physiol 100: 1796–1801
Rockholm DC and Yamamoto HY (1993) Purification of violaxanthin de-epoxidase by lipid affinity precipitation. In: Yamamoto HY and Smith CM (eds) Photosynthetic Responses to the Environment, p 237. American Soc Plant Phys, Rockwell, MD
Ruban AV, Rees D, Noctor GD, Young A and Horton P (1991) Long-wavelength chlorophyll species are associated with amplification of high-energy-state excitation quenching in higher plants. Biochim Biophys Acta 1059: 355–360
Ruban AV, Rees D, Pascal AA and Horton P (1992) Mechanisms of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. II. The relationship between LHCII aggregation in vitro and qE in isolated thylakoids. Biochim Biophys Acta 1102: 39–44
Ruban AV, Horton P and Young AJ (1993a) Aggregation of higher plant xanthophylls: Differences in absorption spectra and in the dependency on solvent polarity. J Photochem Photobiol B: Biol 21: 229–234
Ruban AV, Young AJ and Horton P (1993b) Induction of nonphotochemical energy dissipation and absorbance changes in leaves. Plant Physiol 102: 741–750
Ruban AV, Young AJ, Pascal AA and Horton P (1994) The effects of illumination on the xanthophyll composition of the Photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol 104: 227–234
Rumberg B and Siggel U (1969) pH changes in the inner phase of the thylakoids during photosynthesis. Naturwissenschaften 56: 130–132
Sapozhnikov DI and Bazhanova NV (1958) A description of the light reaction in isolated chloroplasts. Dokl Akad Nauk 120: 1141–1143
Sapozhnikov DI, Krasovskaya TA and Mayevskaya AN (1957) Changes observed in the relation between the main carotenoids in the plastids of green leaves exposed to light. Dokl Akad Nauk 113: 456–467
Satoh K and Fork DC (1983) A new mechanism for adaptation to changes in light intensity and quality in the red algaPorphyra perforata. III. Fluorescence transients in the presence of 3-(3,3-dichlorophenyl)-1,1-dimethylurea. Plant Physiol 71: 673–676
Schäfer C and Schmidt E (1991) Light acclimation potential and xanthophyll cycle pigments in photoautotrophic suspension cells ofChenopodium rubrum. Physiol Plant 82: 440–448
Schäfer C, Schmid V and Ross M (1994) Characterization of high-light-induced increases in xanthophyll cycle pigment and lutein contents in photoautotrophic cell cultures. J Photochem Photobiol B: Biol 22: 67–75
Schatz GH, Brock H and Holzwarth AR (1988) Kinetic and energetic model for the primary processes in PhotosystemII. Biophys J 54: 397–405
Schindler C, Reith P and Lichtenthaler HK (1994) Differential levels of carotenoids and decrease of zeaxanthin cycle performance during leaf development in a green and an aurea variety of tobacco. J Plant Physiol 143: 500–507
Schöner S and Krause GH (1990) Protective systems against active oxygen species in spinach: Response to cold acclimation in excess light. Planta 180: 383–389
Schreiber U and Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Progress in Botany 54: 151–173
Schreiber U and Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illuminanation: II. Partial control by the Photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c: 1255–1264
Schreiber U and Neubauer C (1990) O2-dependent electron flow, membrane energetization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25: 279–293
Schreiber U, Schliwa U and Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51–62
Schubert H, Kroon BMA and Matthijs HCP (1994) In vivo manipulation of the xanthophyll cycle and the role of zeaxanthin in the protection against photodamage in the green algaChlorella pyrenoidosa. J Biol Chem 269: 7267–7272
Sharma PK and Hall DO (1992) Changes in carotenoid composition and photosynthesis in sorghum under high light and salt stress. J Plant Physiol 140: 661–666
Siefermann D and Yamamoto HY (1974a) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. III. Reaction kinetics and effect of light intensity on de-epoxidase activity and substrate availability. Biochim Biophys Acta 357: 144–150
Siefermann D and Yamamoto HY (1974b) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. V. Dehydroascorbate, a link between photosynthetic electron transport and de-epoxidation. In: Avron M (ed) Proceedings of the 3rd International Congress on Photosynthesis, pp 1991–1998. Elsevier Science Publishers, Amsterdam
Siefermann D and Yamamoto HY (1975a) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. IV. The effects of electron-transport conditions on violaxanthin availability. Biochim Biophys Acta 387: 149–158
Siefermann D and Yamamoto HY (1975b) Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts. Arch Biochem Biophys 171: 70–77
Siefermann D and Yamamoto HY (1975c) NADPH and oxygen-dependent epoxidation of zeaxanthin in isolated chloroplasts. Biochem Biophys Res Commun 62: 456–461
Siefermann D and Yamamoto HY (1976) Deepoxidation in grana and in stroma lamellae. Plant Physiol 57: 939–940
Siefermann-Harms D (1977) The xanthophyll cycle in higher plants. In: Tevini M and Lichtenthaler HK (eds) Lipids and lipid polymers in Higher Plants, pp 218–230, Springer, Berlin
Siefermann-Harms D (1984) Evidence for a heterogeneous organization of violaxanthin in thylakoid membranes. Photochem Photobiol 40: 507–512
Siefermann-Harms D (1984) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochim Biophys Acta 811: 325–355
Siefermann-Harms D (1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol Plant 69: 561–568
Siefermann-Harms D (1992) The yellowing of spruce in polluted atmospheres. Photosynthetica 27: 323–341
Siefermann-Harms D, Joyard J and Douce R (1978) Light-induced changes of the carotenoid levels in chloroplast envelopes. Plant Physiol 61: 530–533
Siefermann-Harms D, Michel J-M and Collard F (1980) Carotenoid transformation underlying the blue absorbance change in flashed bean leaves during the induction of oxygen evolution. Biochim Biophys Acta 589: 315–323
Sielewiesiuk J and Gruszecki WI (1991) A simple model describing the kinetics of the xanthophyll cycle. Biophys Chem 41: 125–129
Stransky H and Hager A (1970) Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyllcyclus in verschiedenen Algenklassen. Arch Mikrobiol 73: 315–323
Strasser RJ (1973) Induction phenomena in green plants when the photosynthetic apparatus starts to work. Arch Int Physiol Biochim 81: 935–955
Strasser RJ and Butler WL (1976) Correlation of absorbance changes and thylakoid fusion with the induction of oxygen evolution in bean leaves greened by brief flashes. Plant Physiol 58: 371–376
Thayer SS and Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23: 331–343
Thayer SS and Björkman O (1992) Carotenoid distribution and deep-oxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth Res 33: 213–225
Thiele A and Krause GH (1994) Xanthophyll cycle and thermal energy dissipation in Photosystem II: Relationship between zeaxanthin formation, energy-dependent fluorescence quenching and photoinhibition. J Plant Physiol (in press)
Veljovic-Jovanovic S, Bilger W and Heber U (1993) Inhibition of photosynthesis, acidification and stimulation of zeaxanthin formation in leaves by sulfur dioxide and reversal of these effects. Planta 191: 365–376
Walters RG and Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27: 121–133
Walters RG and Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PS II fluorescence in barley leaves. Photosynth Res 36: 119–139
Weedon BCL (1971) Stereochemistry. In: Isler O (ed) Carotenoids, pp 267–323. Birkhäuser Verlag, Stuttgart
Weis E and Berry JA (1987) Quantum efficiency of photosystem 2 in relation to ‘energy’ dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198–208
Werdan KW, Heldt HW and Milovancev M (1975) The role of pH in the regulation of carbon fixation in the chloroplast stroma. Studies on CO2 fixation in the light and dark. Biochim Biophys Acta 396: 276–292
Westerhoff N (1974) Beziehungen zwischen den lichtbedingten Xanthophyll-Umwandlungen und dem photosynthetischen Elek-tronentransport bzw. der Photophosphorylierung. Ber Deutsch Bot Ges 87: 545–551
Wihelm C (1990) The biochemistry and physiology of light-harvesting processes in chlorophyllb- and chlorophyllc- containing algae. Plant Physiol Biochem 28 (2): 293–306
Willemoës M and Monas E (1991) Relationship between growth irradiance and the xanthophyll cycle pool in the diatomNitzschia palea. Physiol Plant 83: 449–456
Winter K and Königer M (1989) Dithiothreitol, an inhibitor of violaxanthin de-epoxidation increases the susceptibility of leaves ofNerium oleander L. to photoinhibition of photosynthesis. Planta 180: 24–31
Wolfe GR, Cunningham FX, Durnford D, Green BR and Gantt E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568
Xu DQ, Chen XM, Zhang LX, Wang RF and Hesketh JD (1993) Leaf photosynthesis and chlorophyll fluorescence in a chlorophyll-deficient soybean mutant. Photosynthetica 29: 103–112
Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51: 639–648
Yamamoto HY and Chichester CO (1965) Dark incorporation of18O2 into antheraxanthin by bean leaves. Biochim Biophys Acta 109: 303–305
Yamamoto HY and Higashi RM (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190: 514–522
Yamamoto HY and Kamite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500 nm region. Biochim Biophys Acta 267: 538–543
Yamamoto HY and Takeguchi CA (1972) Concepts on the role of epoxy carotenoids in plants. In: Forti G, Avron M and Melandri A (eds) Proceedings of the 2nd International Congress on Photosynthesis Research, pp 621–627. Junk, The Hague, The Netherlands
Yamamoto HY, Nakayama TOM and Chichester CO (1962) Studies of the light interconversions of the leaf xanthophylls. Arch Biochem Biophys 97: 168–173
Yamamoto HY, Kamite L and Wang YY (1972) An ascorbate-induced absorbance change in chloroplasts from violaxanthin de-epoxidation. Plant Physiol 49: 224–228
Yamamoto HY, Chenchin EE and Yamada DK (1975) Effect of chloroplast lipids on violaxanthin de-epoxidase activity. In: Avron M (ed) Proceedings of the Third International Congress on Photosynthesis, 1999–2006. Elsevier Science Publishers, Amsterdam
Young AJ (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83: 702–708
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Pfündel, E., Bilger, W. Regulation and possible function of the violaxanthin cycle. Photosynth Res 42, 89–109 (1994). https://doi.org/10.1007/BF02187121
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DOI: https://doi.org/10.1007/BF02187121