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The carotenoid zeaxanthin and ‘high-energy-state quenching’ of chlorophyll fluorescence

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Abstract

The possibility that zeaxanthin mediates the dissipation of an excess of excitation energy in the antenna chlorophyll of the photochemical apparatus has been tested through the use of an inhibitor of violaxanthin de-epoxidation, dithiothreitol (DTT), as well as through the comparison of two closely related organisms (green and blue-green algal lichens), one of which (blue-green algal lichen) naturally lacks the xanthophyll cycle. In spinach leaves, DTT inhibited a major component of the rapidly relaxing high-energy-state quenching' of chlorophyll fluorescence, which was associated with a quenching of the level of initial fluorescence (F′0) and exhibited a close correlation with the zeaxanthin content of leaves when fluorescence quenching was expressed as the rate constant for radiationless energy dissipation in the antenna chlorophyll. Green algal lichens, which possess the xanthophyll cycle, exhibited the same type of fluorescence quenching as that observed in leaves. Two groups of blue-green algal lichens were used for a comparison with these green algal lichens. A group of zeaxanthin-free blue-green algal lichens did not exhibit the type of chlorophyll fluorescence quenching indicative of energy dissipation in the pigment bed. In contrast, a group of blue-green algal lichens which had formed zeaxanthin slowly through reactions other than the xanthophyll cycle, did show a very similar response to that of leaves and green algal lichens. Fluorescence quenching indicative of radiationless energy dissipation in the antenna chlorophyll was the predominant component of ‘high-energy-state quenching’ in spinach leaves under conditions allowing for high rates of steady-state photosynthesis. A second, but distinctly different type of ‘high-energy-state quenching’ of chlorophyll fluorescence, which was not inhibited by DTT (i.e., it was zeaxanthin independent) and which is possibly associated with the photosystem II reaction center, occurred in addition to that associated with zeaxanthin in leaves under a range of conditions which were less favorable for linear photosynthetic electron flow. In intact chloroplasts isolated from (zeaxanthin-free) spinach leaves a combination of these two types of rapidly reversible fluorescence quenching occurred under all conditions examined.

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Abbreviations

DTT:

dithiothreitol

F0 (or F′0):

yield of instantaneous fluorescence at open PS II reaction centers in the dark (or during actinic illumination)

FM (or F′M):

yield of maximum fluorescence induced by a saturation pulse of light in the dark (or during actinic illumination)

FV (or F′V):

yield of variable fluorescence induced by a saturating pulse of light in the dark (or during actinic illumination)

k D :

rate constant for radiationless energy dissipation in the antenna chlorophyll

SV:

Stern-Volmer equation

PFD:

photon flux density

PS I:

photosystem I

PS II:

photosystem II

QA :

acceptor of photosystem II

qN :

coefficient of nonphotochemical chlorophyll fluorescence quenching

qP :

coefficient of photochemical chlorophyll fluorescence quenching

References

  • Adams WW III, Díaz M and Winter K (1989) Diurnal changes in photochemical efficiency, the reduction state of Q, radiationless energy dissipation, and non-photochemical fluorescence quenching in cacti exposed to natural sunlight in northern Venezuela. Oecologia 80: 553–561

    Google Scholar 

  • Adams WW III, Demmig-Adams B and Winter K (1990) Relative contributions 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

    Google Scholar 

  • 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 of Hedera canariensis. Photosynth Res 25: 173–185

    Google Scholar 

  • 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

    Google Scholar 

  • Björkman O and Powles SB (1984) Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161: 490–504

    Article  Google Scholar 

  • Briantais JM, Vernotte C, Picaud M and Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548: 128–138

    PubMed  Google Scholar 

  • Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Ann Rev Plant Physiol 29: 345–378

    Article  Google Scholar 

  • Butler WL and Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376: 116–125

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Demmig B, Winter K, Krüger A and Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218–224

    Google Scholar 

  • Demmig B, Winter K, Krüger A and Czygan F-C (1988) Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. Plant Physiol 87: 17–24

    Google Scholar 

  • Demmig-Adams B (1991) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta, Reviews on Bioenergetics, in press

  • Demmig-Adams B, Adams WW III, Winter K, Meyer A, Schreiber U, Pereira JS, Krüger A, Czygan F-C and Lange OL (1989a) Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the ‘midday depression’ of net CO2 uptake in Arbutus unedo growing in Portugal. Planta 177: 377–387

    Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989) Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol 90: 881–886

    Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989c) 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

    Google Scholar 

  • Demmig-Adams B, Adams WW III, Czygan F-C, Schreiber U and Lange OL (1990a) Differences in the capacity for radiationless energy dissipation in green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180: 582–589

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW III, Green TGA, Czygan F-C and Lange OL (1990b) Differences in the susceptibility to light stress in two closely related organisms, one possessing and one lacking the xanthophyll cycle. Oecologia, in press

  • Demmig-Adams B, Adams WW III, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W and Björkman O (1990c) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92: 293–301

    Google Scholar 

  • Demmig-Adams B, Björkman O, Bilger W, Adams WW III, Thayer SS and Shih C (1990d) Diurnal changes in zeaxanthin content and radiationless energy dissipation in leaves of field-grown cotton (Gossypium hirsutum L.). Physiol Plant, in press

  • Demmig-Adams B, Máguas C, Adams WW III, Meyer A, Kilian E and Lange OL (1990e) Effect of high light on the effeciency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta 180: 400–409

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Horton P and Hague A (1988) Studies on the induction of chlorophyll fluorescence quenching in isolated barley chloroplasts. IV. Resolution of nonphotochemical quenching. Biochim Biophys Acta 932: 107–115

    Google Scholar 

  • Horton P and Lee P (1983) Stimulation of cyclic electron-transfer pathway around photosystem II by phosphorylation of chloroplast thylakoid proteins. FEBS Lett 162: 81–84

    Article  Google Scholar 

  • Kitajima M and Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105–115

    PubMed  Google Scholar 

  • Krause GH, Briantais JM and Vernotte C (1983) Characterization of chlorophyll fluorescence quenching in chloroplasts by fluorescence spectroscopy at 77 K. I. ΔpH-dependent quenching. Biochim Biophys Acta 723: 169–175

    Google Scholar 

  • Krause GH, Vernotte C and Briantais JM (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochim Biophys Acta 679: 116–124

    Google Scholar 

  • Oxborough K and Horton P (1987) Characterisation 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

    Google Scholar 

  • Schäfer C and Björkman O (1989) Relationship between efficiency of photosynthetic energy conversion and chlorophyll fluorescence quenching in Upland cotton (Gossypium hirsutum L.). Planta 178: 367–376

    Google Scholar 

  • Schreiber U and Bilger W (1987) Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. In: Tenhunen JD, Catarino FM, Lange OL and Oechel WC (eds) Plant Response to Stress — Functional Analysis in Mediterranean Ecosystems, pp 27–53. Berlin: Springer-Verlag

    Google Scholar 

  • Schreiber U and Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c: 1255–1264

    Google Scholar 

  • 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. Berlin: Springer-Verlag

    Google Scholar 

  • Siefermann D and Yamamoto HY (1975) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. IV. The effect of electron transport conditions on violaxanthin availability. Biochim Biophys Acta 387: 149–158

    PubMed  Google Scholar 

  • Stransky H and Hager A (1970) Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyllcyclus in verschiedenen Algenklassen. IV. Cyanophyceae und Rhodophyceae. Arch Mikrobiol 72: 84–96

    PubMed  Google Scholar 

  • Weis E and Berry JA (1987) Quantum efficiency of photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198–208

    Google Scholar 

  • Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51: 639–648

    Google Scholar 

  • 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

    PubMed  Google Scholar 

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  1. Department of Environmental, Population, and Organismic Biology, University of Colorado, Campus Box 334, 80309, Boulder, Colorado, USA

    Barbara Demmig-Adams & William W. Adams III

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  1. Barbara Demmig-Adams
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  2. William W. Adams III
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Demmig-Adams, B., Adams, W.W. The carotenoid zeaxanthin and ‘high-energy-state quenching’ of chlorophyll fluorescence. Photosynth Res 25, 187–197 (1990). https://doi.org/10.1007/BF00033160

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