Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions

Jose I. García-Plazaola A , Shizue Matsubara B and C. Barry Osmond C D

A Department of Plant Biology and Ecology, UPV/EHU, Apdo. 644, 48080 Bilbao, Spain.

B Institut Phytosphäre (ICG3), Forschungszentrum Jülich, 52425 Jülich, Germany.

C School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia.

D Corresponding author. Email:

Functional Plant Biology 34(9) 759-773
Submitted: 18 April 2007  Accepted: 8 June 2007   Published: 30 August 2007


Several xanthophyll cycles have been described in photosynthetic organisms. Among them, only two are present in higher plants: the ubiquitous violaxanthin (V) cycle, and the taxonomically restricted lutein epoxide (Lx) cycle, whereas four cycles seem to occur in algae. Although V is synthesised through the β-branch of the carotenoid biosynthetic pathway and Lx is the product of the α-branch; both are co-located in the same sites of the photosynthetic pigment-protein complexes isolated from thylakoids. Both xanthophylls are also de-epoxidised upon light exposure by the same enzyme, violaxanthin de-epoxidase (VDE) leading to the formation of zeaxanthin (Z) and lutein (L) at comparable rates. In contrast with VDE, the reverse reaction presumably catalysed by zeaxanthin epoxidase (ZE), is much slower (or even inactive) with L than with antheraxanthin (A) or Z. Consequently many species lack Lx altogether, and although the presence of Lx shows an irregular taxonomical distribution in unrelated taxa, it has a high fidelity at family level. In those plants which accumulate Lx, variations in ZE activity in vivo mean that a complete Lx-cycle occurs in some (with Lx pools being restored overnight), whereas in others a truncated cycle is observed in which VDE converts Lx into L, but regeneration of Lx by ZE is extremely slow. Accumulation of Lx to high concentrations is found most commonly in old leaves in deeply shaded canopies, and the Lx cycle in these leaves is usually truncated. This seemingly anomalous situation presumably arises because ZE has a low but finite affinity for L, and because deeply shaded leaves are not often exposed to light intensities strong enough to activate VDE. Notably, both in vitro and in vivo studies have recently shown that accumulation of Lx can increase the light harvesting efficiency in the antennae of PSII. We propose a model for the truncated Lx cycle in strong light in which VDE converts Lx to L which then occupies sites L2 and V1 in the light-harvesting antenna complex of PSII (Lhcb), displacing V and Z. There is correlative evidence that this photoconverted L facilitates energy dissipation via non-photochemical quenching and thereby converts a highly efficient light harvesting system to an energy dissipating system with improved capacity to engage photoprotection. Operation of the α- and β-xanthophyll cycles with different L and Z epoxidation kinetics thus allows a combination of rapidly and slowly reversible modulation of light harvesting and photoprotection, with each cycle having distinct effects. Based on the patchy taxonomical distribution of Lx, we propose that the presence of Lx (and the Lx cycle) could be the result of a recurrent mutation in the epoxidase gene that increases its affinity for L, which is conserved whenever it confers an evolutionary advantage.

Additional keywords: antheraxanthin, α-carotene, de-epoxidase, epoxidase, lutein, lutein epoxide, non-photochemical quenching, photoprotection, violaxanthin, xanthophyll cycles, zeaxanthin.


Abadía A Gil E Morales F Montañés L Montserrat G Abadía J 1996 Marcescence and senescence in a submediterranean oak (Quercus subpyrenaica E.H. del Villar): photosynthetic characteristics and nutrient composition. Plant, Cell & Environment 19 685 694 doi:10.1111/j.1365-3040.1996.tb00403.x

Bassi R Caffarri S 2000 Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynthesis Research 64 243 256 doi:10.1023/A:1006409506272

Bishop NI 1996 The β,ε-carotenoid, lutein, is specifically required for the formation of the oligomeric forms of the light harvesting complex in the green alga, Scenedesmus obliquus. Journal of Photochemistry and Photobiology. B, Biology 36 279 283 doi:10.1016/S1011-1344(96)07381-2

Björkman O (1981) Responses to different quantum flux densities. In ‘Encyclopedia of plant physiology. Vol. 12A. Physiological plant ecology I: responses to the physical environment’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 57–107. (Springer-Verlag: New York)

Bouvier F d’Harlingue A Hugueney P Marin E Marion-Poll A Camara B 1996 Xanthophyll biosynthesis. Journal of Biological Chemistry 271 28861 28867 doi:10.1074/jbc.271.46.28861

Britton G , Liaaen-Jensen S , Pfander H (2004) ‘Carotenoids handbook.’ (Birkhäuser Verlag: Basel, Switzerland)

Brugnoli E Björkman O 1992 Chloroplast movements: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynthesis Research 32 23 35 doi:10.1007/BF00028795

Bungard RA Ruban AV Hibberd JM Press MC Horton P Scholes JD 1999 Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proceedings of the National Academy of Sciences USA 96 1135 1139 doi:10.1073/pnas.96.3.1135

Caffarri S Croce R Breton J Bassi R 2001 The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. Journal of Biological Chemistry 276 35924 35933 doi:10.1074/jbc.M105199200

Cardini F Pucci S Calamassi R 2006 Quantitative variations of individual carotenoids in relationship with the leaflet development of six species of the genus Ceratozamia (Cycads). Journal of Plant Physiology 163 128 140 doi:10.1016/j.jplph.2005.05.012

Chow WS , Aro E-M (2005) Photoinactivation and mechanisms of recovery. In ‘Photosystem II: the light-driven water/plastoquinone oxidoreductase. Advances in photosynthesis and respiration. Vol. 19’. (Eds T Wydrzynski, K Satoh) pp. 627–648. (Springer-Verlag: Berlin)

Croce R Weiss S Bassi R 1999 Carotenoid-binding sites of the major light-harvesting complex II of higher plants. Journal of Biological Chemistry 274 29613 29623 doi:10.1074/jbc.274.42.29613

Cunningham FX Gantt E 1998 Genes and enzymes of carotenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49 557 583 doi:10.1146/annurev.arplant.49.1.557

Demmig B Winter K Krüger A 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 Physiology 84 218 224

Demmig-Adams B Adams WW III 1992 Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43 599 626

Demmig-Adams B , Adams WW , Ebbert V , Logan BA (1999) Ecophysiology of the xanthophyll cycle. In ‘The Photochemistry of carotenoids’. (Eds HA Frank, AJ Young, G Britton, RJ Cogdell) pp. 245–269. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Edelenbos M Christensen LP Grevsen K 2001 HPLC determination of chlorophyll and carotenoid pigments in processed green pea cultivars (Pisum sativum L.). Journal of Agricultural and Food Chemistry 49 4768 4774 doi:10.1021/jf010569z

Esteban R Jiménez ET Jiménez MS Morales D Hormaetxe K Becerril JM García-Plazaola JI 2007 Dynamics of violaxanthin and lutein epoxide xanthophyll cycles in Lauraceae tree species under field conditions. Tree Physiology 27 1407 1414

Falster DS Westoby M 2003 Leaf size and angle vary widely across species: what consequences for light interception? New Phytologist 158 509 525

Finazzi G Johnson GN Dall’Osto L Joliot P Wollman F-A Bassi R 2004 A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proceedings of the National Academy of Sciences USA 101 12375 12380 doi:10.1073/pnas.0404798101

Firn RD , Jones CG (2004) The evolution of plant biochemistry and the implications for physiology. In ‘The evolution of plant physiology: from whole plants to ecosystems’. (Eds AR Hemsley, I Poole) pp. 67–83. (Elsevier Academic Press: London)

Gandul-Rojas B Cepero MR-L Mínguez-Mosquera MI 1999 Chlorophyll and carotenoid patterns in olive fruits, Olea europaea cv. Arbequina. Journal of Agricultural and Food Chemistry 47 2207 2212 doi:10.1021/jf981158u

García-Plazaola JI Becerril JM 2001 Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Australian Journal of Plant Physiology 28 225 232

García-Plazaola JI Errasti E Hernández A Becerril JM 2002 Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29 1075 1080

García-Plazaola JI Hernández A Olano JM Becerril JM 2003 The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biology 30 319 324 doi:10.1071/FP02224

García-Plazaola JI Hormaetxe K Hernández A Olano JM Becerril JM 2004 The lutein epoxide cycle in vegetative buds of woody plants. Functional Plant Biology 31 815 823 doi:10.1071/FP04054

Gilmore AM 2001 Xanthophyll cycle-dependent nonphotochemical quenching in photosystem II: Mechanistic insight gained from Arabidopsis thaliana L. mutants that lack violaxanthin deepoxidase activity and or lutein. Photosynthesis Research 67 89 101 doi:10.1023/A:1010657000548

Gilmore AM Ball MC 2000 Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences USA 97 11098 11101 doi:10.1073/pnas.150237697

Gilmore AM Yamamoto HY 2001 Time-resolution of the antheraxanthin- and ΔpH-dependent chlorophyll a fluorescence components associated with photosystem II energy dissipation in Mantoniella squamata. Photochemistry and Photobiology 74 291 302 doi:10.1562/0031-8655(2001)074<0291:TROTAA>2.0.CO;2

Goss R 2003 Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217 801 812 doi:10.1007/s00425-003-1044-1

Goss R Böhme K Wilhelm C 1998 The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta 205 613 621 doi:10.1007/s004250050364

Grace SC Logan BA 1996 Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiology 112 1631 1640

Grotz B Molnár P Stransky H Hager A 1999 Substrate specificity and functional aspects of violaxanthin-de-epoxidase, an enzyme of the xanthophyll cycle. Journal of Plant Physiology 154 437 446

Hager A (1980) The reversible light-induced conversions of xanthophylls in the chloroplast. In ‘Pigments in plants’. (Ed. FC Czygan) pp. 57–79. (Fischer: Stuttgart, Germany)

Harker M Hirschberg J 1998 Molecular biology of carotenoid biosynthesis in photosynthetic organisms. Methods in Enzymology 297 244 263

Havaux M Niyogi KK 1999 The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences USA 96 8762 8767

Hieber AD Bugos RC Yamamoto HY 2000 Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochimica et Biophysica Acta 1482 84 91

Hirschberg J 2001 Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4 210 218

Horton P 1983 Relationships between electron transport and carbon assimilation; simultaneous measurement of chlorophyll fluorescence, transthylakoid pH gradient and O2 evolution in isolated chloroplasts. Proceedings of the Royal Society of London. Series B. Biological Sciences 217 405 416

Horton P Hague A 1988 Studies on the induction of chlorophyll fluorescence in barley protoplasts. IV. Resolution of non-photochemical quenching. Biochimica et Biophysica Acta 932 107 115

Horton P Ruban A 2005 Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. Journal of Experimental Botany 56 365 373 doi:10.1093/jxb/eri023

Horton P Ruban AV Walters RG 1996 Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47 655 684 doi:10.1146/annurev.arplant.47.1.655

Horton P Ruban AV Wentworth M 2000 Allosteric regulation of the light-harvesting system of photosystem II. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 355 1361 1370 doi:10.1098/rstb.2000.0698

Horton P Wentworth M Ruban A 2005 Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Letters 579 4201 4206 doi:10.1016/j.febslet.2005.07.003

Jahns P Wehner A Paulsen H Hobe S 2001 De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II. Journal of Biological Chemistry 276 22154 22159 doi:10.1074/jbc.M102147200

Jansson S 1994 The light-harvesting chlorophyll a/b-binding proteins. Biochimica et Biophysica Acta 1184 1 19 doi:10.1016/0005-2728(94)90148-1

Kim J DellaPenna D 2006 Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid β-ring hydroxylase CYP97A3. Proceedings of the National Academy of Sciences USA 103 3474 3479 doi:10.1073/pnas.0511207103

Kirschbaum MUF Pearcy RW 1988 Concurrent measurements of O2 and CO2 exchange during lightflecks in Alocasia macrorrhiza (L.) G. Don. Planta 174 527 533 doi:10.1007/BF00634483

Kolber Z Klimov D Ananyev G Rascher U Berry J Osmond B 2005 Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of PSII in terrestrial vegetation. Photosynthesis Research 84 121 129 doi:10.1007/s11120-005-5092-1

Kramer DM Sacksteder CA Cruz JA 1999 How acidic is the lumen? Photosynthesis Research 60 151 163 doi:10.1023/A:1006212014787

Krause GH Weis E 1991 Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42 313 349 doi:10.1146/annurev.pp.42.060191.001525

Krause GH Koroleva OY Dalling JW Winter K 2001 Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant, Cell & Environment 24 1345 1352 doi:10.1046/j.0016-8025.2001.00786.x

Kruk J 2005 Occurrence of chlorophyll precursors in leaves of cabbage heads - the case of natural etiolation. Journal of Photochemistry and Photobiology B: Biology 80 187 194 doi:10.1016/j.jphotobiol.2005.04.003

Külheim C Ågren J Jansson S 2002 Rapid regulation of light harvesting and plant fitness in the field. Science 297 91 93 doi:10.1126/science.1072359

Kull D Pfander H 1995 Isolation and identification of carotenoids from the petals of rape (Brassica napus). Journal of Agricultural and Food Chemistry 43 2854 2857 doi:10.1021/jf00059a016

Latowski D Kostecka A Strzalka K 2000 Effect of monogalactosyldiacylglycerol and other thylakoid lipids on violaxanthin de-epoxidation in liposomes. Biochemical Society Transactions 28 810 812 doi:10.1042/BST0280810

Latowski D Grzyb J Strzalka K 2004 The xanthophyll cycle – molecular mechanism and physiological significance. Acta Physiologiae Plantarum 26 197 212 doi:10.1007/s11738-004-0009-8

Li X-P Björkman O Shih C Grossman AR Rosenquist M Jansson S Niyogi KK 2000 A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 391 395 doi:10.1038/35000131

Li X-P Phippard A Pasari J Niyogi KK 2002 a Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Functional Plant Biology 29 1131 1139 doi:10.1071/FP02065

Li X-P Gilmore AM Niyogi KK 2002 b Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. Journal of Biological Chemistry 277 33590 33597 doi:10.1074/jbc.M204797200

Li X-P Gilmore AM Caffarri S Bassi R Golan T Kramer D Niyogi KK 2004 Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. Journal of Biological Chemistry 279 22866 22874 doi:10.1074/jbc.M402461200

Liu Z Yan H Wang K Kuang T Zhang J Gui L An X Chang W 2004 Crystal structure of spinach major light harvesting complex at 2.72 Å resolution. Nature 428 287 292 doi:10.1038/nature02373

Llorens L Aranda X Abadía A Fleck I 2002 Variations in Quercus ilex chloroplast pigment content during summer stress: involvement in photoprotection according to principal component analysis. Functional Plant Biology 29 81 88 doi:10.1071/PP01080

Lohr M Wilhelm C 1999 Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proceedings of the National Academy of Sciences USA 96 8784 8789 doi:10.1073/pnas.96.15.8784

Lu WH Haynes K Wiley E Clevidence B 2001 Carotenoid content and color in diploid potatoes. Journal of the American Society for Horticultural Science 126 722 726

Ludlow MM Björkman O 1984 Paraheliotropic leaf movements in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions: damage by excessive light and heat. Planta 161 505 518

Matsubara S Gilmore AM Osmond CB 2001 Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii. Australian Journal of Plant Physiology 28 793 800

Matsubara S Gilmore AM Ball MC Anderson JM Osmond CB 2002 Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Functional Plant Biology 29 1157 1169

Matsubara S Morosinotto T Bassi R Christian A-L Fischer-Schliebs E et al 2003 Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217 868 879 doi:10.1007/s00425-003-1059-7

Matsubara S Naumann M Martin R Nichol C Rascher U Morosinotto T Bassi R Osmond B 2005 Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may ‘lock in’ lutein-based photoprotection during acclimation to strong light. Journal of Experimental Botany 56 461 468 doi:10.1093/jxb/eri012

Matsubara S Morosinotto T Osmond B Bassi R 2007 Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144 926 941 doi:10.1104/pp.107.099077

Matus Z Molnár P Szabó LG 1993 Main carotenoids in pressed seeds (Cucurbitae semen) of oil pumkin (Cucurbita pepo convar. pepo var. styriaca). Acta Pharmaceutica Hungarica 63 247 256

Morosinotto T Baronio R Bassi R 2002 Dynamics of chromophore binding to Lhc proteins in vivo and in vitro during operation of the xanthophyll cycle. Journal of Biological Chemistry 277 36913 36920

Morosinotto T Caffarri S Dall’Osto L Bassi R 2003 Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiologia Plantarum 119 347 354 doi:10.1034/j.1399-3054.2003.00213.x

Müller P Li X-P Niyogi KK 2001 Non-photochemical quenching. A response to excess light energy. Plant Physiology 125 1558 1566 doi:10.1104/pp.125.4.1558

Munné-Bosch S Peñuelas J Asensio D Llusià J 2004 Airborne ethylene may alter antioxidant protection and reduced tolerance of Holm oak to heat and drought stress. Plant Physiology 136 2937 2947 doi:10.1104/pp.104.050005

Niinemets Ü Bilger W Kull O Tennhunen JD 1998 Acclimation to high irradiance in temperate trees in the field: changes in xanthophyll pool size and photosynthetic capacity along a canopy light gradient. Plant, Cell & Environment 21 1205 1218 doi:10.1046/j.1365-3040.1998.00364.x

Niinemets Ü Kollist H García-Plazaola JI Hernández A Becerril JM 2003 Do the capacity and kinetics for modification of xanthophyll cycle pool size depend on growth irradiance in temperate tress? Plant, Cell & Environment 26 1787 1801 doi:10.1046/j.1365-3040.2003.01096.x

Niyogi KK 1999 Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50 333 359 doi:10.1146/annurev.arplant.50.1.333

Niyogi KK Björkman O Grossman AR 1997 The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences USA 94 14162 14167 doi:10.1073/pnas.94.25.14162

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 doi:10.1105/tpc.10.7.1121

Orset S Young AJ 1999 Low-temperature-induced synthesis of a-carotene in the microalga Dunaliella salina (Chlorophyta). Journal of Phycology 35 520 527 doi:10.1046/j.1529-8817.1999.3530520.x

Osmond CB , Anderson JM , Ball MC , Egerton JJG (1999) Compromising efficiency: the molecular ecology of light resource utilisation in terrestrial plants. In ‘Advances in physiological plant ecology’. (Eds MC Press, JC Scholes, MG Barker) pp. 1–24. (Blackwell: Oxford)

Pearcy RW 1988 Photosynthetic utilization of lightflecks by understory plants. Australian Journal of Plant Physiology 15 223 238

Pearcy RW 1990 Sunflecks and photosynthesis in plant canopies. Annual Review of Plant Physiology and Plant Molecular Biology 41 421 453

Peng C-L Lin Z-F Su Y-Z Lin G-Z Dou H-Y Zhao C-X 2006 The antioxidative functions of lutein: electron spin resonance studies and chemical detection. Functional Plant Biology 33 839 846 doi:10.1071/FP06013

Pfündel E Renganathan M Gilmore AM Yamamoto HY Dilley RA 1994 Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin de-epoxidation. Plant Physiology 106 1647 1658

Pogson B McDonald KA Truong M Britton G DellaPenna D 1996 Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. The Plant Cell 8 1627 1639

Pogson BJ Rissler HM 2000 Genetic manipulation of carotenoid biosynthesis and photoprotection. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences. 355 1395 1403 doi:10.1098/rstb.2000.0701

Pogson BJ Niyogi KK Björkman O DellaPenna D 1998 Altered xanthophyll composition adversely affect chlorophyll accumulation and non-photochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences USA 95 13324 13329 doi:10.1073/pnas.95.22.13324

Rabinowitch HD Budowski P Kedar N 1975 Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122 91 97 doi:10.1007/BF00385408

Raniello R Lorenti M Brunet C Buia MC 2006 Photoacclimation of the invasive alga Caulerpa racemosa var. Cylindracea to depth and daylight patterns and a putative new role for siphonaxanthin. Marine Ecology 27 20 30 doi:10.1111/j.1439-0485.2006.00080.x

Razungles AJ Babic I Sapisd JC Bayonove CL 1996 Particular behaviour of epoxy xanthophylls during veraison and maturation of grape. Journal of Agricultural and Food Chemistry 44 3821 3825 doi:10.1021/jf960260t

Rmiki NE Brunet C Cabioch J Lemoine Y 1996 Xanthophyll-cycle and photosynthetic adaptation to environment in macro- and microalgae. Hydrobiologia 326–327 407 413 doi:10.1007/BF00047839

Robinson SA Lovelock CE Osmond CB 1993 Wax as a mechanism for protection against photoinhibition – a study of Cotyledon orbiculata. Botanica Acta 106 307 312

Ruban AV Horton P 1995 An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiology 108 721 726

Schiefthaler U Russell AW Bolhàr-Nordenkampf HR Critchley C 1999 Photoregulation and photodamage in Schefflera arboricola leaves adapted to different light environments. Australian Journal of Plant Physiology 26 485 494

Snyder AM Clark BM Robert B Ruban AV Bungard RA 2004 Carotenoid specificity of light-harvesting complex II binding sites; occurrence of 9-cis-viloaxanthin in the neoxanthin-binding site in the parasitic angiosperm Cuscuta reflexa. Journal of Biological Chemistry 279 5162 5168

Snyder AM Clark BM Bungard RA 2005 Light-dependent conversion of carotenoids in the parasitic angiosperm Cuscuta reflexa L. Plant, Cell & Environment 28 1326 1333 doi:10.1111/j.1365-3040.2005.01379.x

Strand A Kvernberg K Karlsen AM Liaaen-Jensen S 2000 Geometrical E/Z isomers of (6R)- and (7S)- neoxanthin and biological implications. Biochemical Systematics and Ecology 28 443 455 doi:10.1016/S0305-1978(99)00078-2

Stransky H Hager A 1970 The carotenoid pattern and the occurrence of the light-induced xanthophyll cycle in various classes of algae. VI. Chemosystematic study. Archiv fur Mikrobiologie 73 315 323 doi:10.1007/BF00412298

Tai CY Chen BH 2000 Analysis and stability of carotenoids in the flowers of daylily (Hemerocallis disticha) as affected by various treatments. Journal of Agricultural and Food Chemistry 48 5962 5968 doi:10.1021/jf000956t

Thayer SS Björkman O 1990 Leaf xanthophylls content and composition in sun and shade determined by HPLC. Photosynthesis Research 23 331 343 doi:10.1007/BF00034864

Thiele A Krause GH Winter K 1998 In situ study of photoinhibition of photosynthesis and xanthophyll cycle activity in plants growing in natural gaps of the tropical forest. Australian Journal of Plant Physiology 25 185 195

Verhoeven AS Adams WW III Demmig-Adams B Croce R Bassi R 1999 Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca minor. Plant Physiology 120 727 737

Watanabe K Takahashi B 1996 Chlorophyll and carotenoid pigments in green- and yellow-fleshed kiwifruit during fruit development and storage. Journal of the Japanese Society for Horticultural Science 68 1038 1043

Watling JR Robinson SA Woodrow IE Osmond CB 1997 Responses of rainforest understorey plants to excess light during sunflecks. Australian Journal of Plant Physiology 24 17 25

Watson TL Close DC Davidson NJ Davies NW 2004 Pigment dynamics during cold-induced photoinhibition of Acacia melanoxylon. Functional Plant Biology 31 481 489

Wehner A Storf S Jahns P Schmid VHR 2004 De-epoxidation of violaxanthin in light-harvesting complex I proteins. Journal of Biological Chemistry 279 26823 26829 doi:10.1074/jbc.M402399200

Weis E Berry JA 1987 Quantum efficiency of photosystem II in relation to energy dependent quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 894 198 208 doi:10.1016/0005-2728(87)90190-3

Wingerath T Stahl W Kirsch D Kaufmann R Sies H 1996 Fruit juice carotenol fatty acid esters and carotenoids as identified by matrix-assisted laser desorption ionization (MALDI) mass spectrometry. Journal of Agricultural and Food Chemistry 44 2006 2013 doi:10.1021/jf960057y

Yamamoto HY Kamite L 1972 The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochimica et Biophysica Acta 267 538 543 doi:10.1016/0005-2728(72)90182-X

Yamamoto HY Higashi RM 1978 Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Archives of Biochemistry and Biophysics 190 514 522 doi:10.1016/0003-9861(78)90305-3

Yamamoto HY Nakayama TOM Chichetser CO 1962 Studies on the light and dark interconversions of leaf xanthophylls. Archives of Biochemistry and Biophysics 97 168 173 doi:10.1016/0003-9861(62)90060-7

Yen WJ Chen BH 1995 Isolation of xanthophylls from Taiwanese orange peels and their effects on the oxidation stability of soybean oil. Food Chemistry 53 417 425 doi:10.1016/0308-8146(95)99837-P

Zhu XG Ort DR Whitmarsh J Long SP 2004 The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. Journal of Experimental Botany 55 1167 1175 doi:10.1093/jxb/erh141

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