Abstract
Zeaxanthin has been correlated with high-energy non-photochemical fluorescence quenching but whether antheraxanthin, the intermediate in the pathway from violaxanthin to zeaxanthin, also relates to quenching is unknown. The relationships of zeaxanthin, antheraxanthin and ΔpH to fluorescence quenching were examined in chloroplasts ofPisum sativum L. cv. Oregon andLactuca sativa L. cv. Romaine. Data matrices as five levels of violaxanthin de-epoxidation against five levels of light-induced lumen-proton concentrations were obtained for both species. The matrices included high levels of antheraxanthin as well as lumen-proton concentrations induced by subsaturating to saturation light levels. Analyses of the matrices by simple linear and multiple regression showed that quenching is predicted by models where the major independent variable is the product of lumen acidity and de-epoxidized xanthophylls, the latter as the sum of zeaxanthin and antheraxanthin. The interactions of lumen acidity and xanthophyll concentration are shown in three-dimensional plots of the best-fit multiple regression models. Antheraxanthin apparently contributes to quenching as effectively as zeaxanthin and explains quenching previously not accounted for by zeaxanthin. Hence, we propose that all high-energy dependent quenching is xanthophyll dependent. Quenching requires a threshold lumen pH that varies with xanthophyll composition. After the threshold, quenching is linear with lumen acidity or xanthophyll composition.
Similar content being viewed by others
Abbreviations
- FM :
-
fluorescence intensity with PS II traps closed under non-energized, dark-adapted conditions
- F′M :
-
fluorescence intensity with PS II traps closed in energized state
- F0 :
-
fluorescence intensity with PS II reaction centers open in non-energized conditions
- NPQ:
-
non-photochemical quenching
- PFD:
-
photon flux density
- SVN :
-
Stern Volmer non-photochemical quenching
- SVE :
-
Stern Volmer energy-dependent non-photochemical quenching
- qE :
-
coefficient of energy-dependent quenching
- kD :
-
rate constant for non-radiative energy dissipation
- V:
-
violaxanthin
- A:
-
antheraxanthin
- Z:
-
zeaxanthin
References
Adams WWIII, Demmig-Adams B and Winter K (1990) Relative contributions of zeaxanthin-related and zeaxanthin-unrelated types of ‘high-energy’ quenching of chlorophyll fluorescence of spinach leaves exposed to various environmental conditions. Plant Physiol 92: 302–309
Baker NR (1991) A possible role for Photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81: 563–570
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 Willd. Photosynth Res 25: 173–185
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
Björkman O (1987) Low-temperature chlorophyll fluorescence in leaves and its relationship to photon yield of photosynthesis in photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ(eds) Photoinhibition, pp 123–144. Elsevier Science Publishers, Dordrecht
Bradbury M and Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of Photosystem II electron acceptors and fluorescence emission from Photosystems I and II. Biochim Biophys Acta 635: 542–551
Briantais J-M, Vernotte C, Picaud M and Krause GH (1979) A quantitative study of the slow decline of chlorophylla fluorescence in isolated chloroplasts. Biochim Biophys Acta 548: 128–138
Briantais J-M, Vernotte C, Picaud M and Krause GH (1980) Chlorophyll fluorescence as a probe for the determination of the photo-induced proton gradient in isolated chloroplasts. Biochim Biophys Acta 591: 198–202
Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24
Demmig-Adams B, Adams WWIII, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W and Björkman O (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92: 293–301
Gilmore AM and Yamamoto HY (1991a) Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol 96: 635–643
Gilmore AM and Yamamoto HY (1991b) Resolution of lutein and zeaxanthin using a nonendcapped, lightly carbon-loaded C-18 high-performance liquid chromatographic column. J Chromatogr 543: 137–145
Gilmore AM and Yamamoto HY (1991c) Zeaxanthin-dependent and independent nonphotochemical quenching are quantitatively related to ΔpH. Plant Physiol 96: 41
Gilmore AM and Yamamoto HY (1992) Dark induction of zeaxanthin-dependent non-photochemical quenching mediated by ATP. Proc Natl Acad Sci USA 89: 1899–1903
Horton P and Lee P (1985) Stimulation of a cyclic electrontransfer pathway around Photosystem II by phosphorylation of chloroplast thylakoid proteins. FEBS Lett 162: 81–84
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 LHC II chlorophyll-protein complex. FEBS Lett 292: 1–4
Junge W, Schönknecht G and Förster V (1986) Neutral red as an indicator of pH transients in the lumen of thylakoidssome answers to criticism. Biochim Biophys Acta 852: 93–99
Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Ann Rev Plant Physiol Plant Mol Biol 42: 313–349
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
Rees D, Young A, Noctor G, Britton G and Horton P (1989) Enhancement of the ΔpH-dependent dissipation of excitation energy in spinach chloroplasts by light activation: Correlation with the synthesis of zeaxanthin. FEBS Lett 256: 85–90
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
Schreiber U and Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the photosystem donor side and possible ways of interpretation. Z Naturforsch 42c: 1255–1264
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
Siefermann-Harms D (1978) The accumulation of neutral red in illuminated thylakoids. Biochim Biophys Acta 504: 265–227
Thayer SS and Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23: 331–343
vanKooten O and Snel JFH (1990) The use of fluorescence nomenclature in plant stress physiology. Photosynth Res 25: 147–150
Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure and Appl Chem 51: 639–648
Yamamoto HY and Higashi RM (1978) Violaxanthin deepoxidase, 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, Kamite L and Wang YY (1972) An ascorbate-induced absorbance change in chloroplasts from violaxanthin de-epoxidation. Plant Physiol 49: 224–228
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gilmore, A.M., Yamamoto, H.Y. Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35, 67–78 (1993). https://doi.org/10.1007/BF02185412
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02185412