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Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria pp 583–603Cite as

Beyond Non-Photochemical Fluorescence Quenching: The Overlapping Antioxidant Functions of Zeaxanthin and Tocopherols

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 40))

Summary

Tocopherols, present in plastids from all lineages of photosynthetic eukaryotes, have long been recognized as key constituents of photoprotective defenses. Membrane-bound tocopherols play an essential antioxidant role by quenching singlet oxygen and preventing the propagation of lipid peroxidation through their radical scavenging activity. However, experiments with tocopherol-deficient plants have shown a surprisingly low impact of high light, and this apparently is the result of a functional overlap of tocopherol with zeaxanthin (Z). Apart from the role of zeaxanthin in the modulation of thermal dissipation (assessed via non-photochemical quenching of chlorophyll fluorescence, NPQ), zeaxanthin molecules dissolved as free pigments in the membrane lipid phase or present at the lipid-protein interfaces may act as direct antioxidants and membrane stabilizers, having a synergistic effect with tocopherol. The existence of pools of unbound zeaxanthin is supported by numerous stress experiments that showed a much higher enhancement of the total pool of violaxanthin-antheraxanthin-zeaxanthin (VAZ) cycle pigments than that of their potential binding sites in antenna proteins. Tocopherol content is also subject to strong environmental modulation by stress factors, and the dynamics of the tocopherol and Z pools are frequently highly correlated. However, a significant proportion of the leaf tocopherol pool accumulates in plastoglobules, instead of thylakoids, where its protective role is not so clearly established. From an evolutionary perspective, there seems to be a trend from a xanthophyll cycle-based photoprotection in algae to a more diversified strategy in terrestrial plants.

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Abbreviations

Dd –:

Diadinoxanthin;

Dd-Dt cycle –:

The xanthophyll cycle involving the carotenoids diadinoxanthin and diatoxanthin;

Dt –:

Diatoxanthin;

ELIPs –:

Early light-induced proteins;

HII Non-lamellar:

hexagonal lipid phase II;

HLIPs –:

High-light-induced proteins;

HOTE –:

Hydroxy-octadecatrienoic acid;

L –:

Lutein;

LCHII –:

Light-harvesting antenna of PS II;

LHCSR –:

Evolutionarily ancient Light Harvesting Complex Stress-Related Protein;

Lx –:

Lutein epoxide;

Lx-L cycle –:

The xanthophyll cycle involving the carotenoids lutein epoxide and lutein;

MGDG –:

Monogalactosyldiacylglycerol;

MYA –:

Million years ago;

NPQ –:

Non-photochemical quenching;

PG –:

Plastoglobule;

PS –:

Photosystem;

PsbS –:

PS II protein PsbS;

ROS –:

Reactive oxygen species;

T –:

Tocopherol or tocotrienol;

Toc –:

α-tocopherol;

V –:

Violaxanthin;

VAZ –:

Violaxanthin + antheraxanthin + zeaxanthin;

VAZ cycle –:

The xanthophyll cycle involving the carotenoids violaxanthin, antheraxanthin, and zeaxanthin;

VDE –:

Violaxanthin de-epoxidase;

Z –:

Zeaxanthin

References

  • Abbasi A, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco (Nicotiana tabacum L.). Plant Physiol 143:1720–1738

    CAS  PubMed Central  PubMed  Google Scholar 

  • Abbasi A, Saur A, Hennig P, Tschiersch H, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2009) Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence. Plant Cell Environ 32:144–157

    CAS  PubMed  Google Scholar 

  • Abreu ME, Munné-Bosch S (2009) Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot 60:1261–1271

    CAS  PubMed Central  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:81–88

    Google Scholar 

  • Artetxe U, García-Plazaola JI, Hernández A, Becerril JM (2002) Low light grown duckweed plants are more protected against the toxicity induced by Zn and Cd. Plant Physiol Biochem 40:859–863

    CAS  Google Scholar 

  • Asensi-Fabado MA, Cela J, Müller M, Arrom L, Chang C, Munné-Bosch S (2012) Enhanced oxidative stress in the ethylene-insensitive (ein3-1) mutant of Arabidopsis thaliana exposed to salt stress. J Plant Physiol 169:360–368

    CAS  PubMed  Google Scholar 

  • Baroli I, Do AD, Yamane T, Niyogi KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15:992–1008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bartoli CG, Simontacchi M, Tambussi J, Montaldi E, Pintarulo S (1999) Drought and watering-dependent oxidative stress effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50:375–383

    CAS  Google Scholar 

  • Beatty S, Koh H, Phil M, Henson D, Boulton M (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45:115–134

    CAS  PubMed  Google Scholar 

  • Beisel KG, Jahnke S, Hofmann D, Köppchen S, Schurr U, Matsubara S (2010) Continuous turnover of carotenes and chlorophyll a in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling. Plant Physiol 152:2188–2199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bhosale P, Bernstein PS (2005) Synergistic effects of zeaxanthin and its binding protein in the prevention of lipid membrane oxidation. Biochim Biophys Acta 1740:116–121

    CAS  PubMed  Google Scholar 

  • Bohm F, Edge R, Land EJ, McGarvey DJ, Truscott TG (1997) Carotenoids enhance vitamin E antioxidant efficiency. J Am Chem Soc 119:621–622

    Google Scholar 

  • Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266

    PubMed  Google Scholar 

  • Burton GW, Ingold KU (1981) Autooxidation of biological molecules. I. The antioxidant activity of vitamin E and related chain-breaking phenolic antioxidants in vitro. J Am Chem Soc 103:6472–6477

    CAS  Google Scholar 

  • Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ- rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400

    CAS  PubMed Central  PubMed  Google Scholar 

  • Coesel S, Oborník M, Varela J, Falciatore A, Bowler C (2008) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS One 3:e2896

    PubMed Central  PubMed  Google Scholar 

  • Collakova E, DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol 127:1113–1124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collakova E, DellaPenna D (2003) The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress. Plant Physiol 133:930–940

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collén J, Davison IR (1999) Reactive oxygen metabolism in intertidal Fucus spp. (Phaeophyceae). J Phycol 35:62–69

    Google Scholar 

  • Collin V, Eymery F, Genty B, Rey P, Havaux M (2008) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. Plant Cell Environ 31:244–257

    CAS  PubMed  Google Scholar 

  • Dall’Osto L, Cazzaniga S, Havaux M, Bassi R (2010) Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol Plant 3:576–593

    PubMed  Google Scholar 

  • DellaPenna D, Pogson B (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams RB (2013) Eye nutrition in context: mechanisms, implementation, and future directions. Nutrients 5:2483–2501.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88

    CAS  PubMed  Google Scholar 

  • Desel C, Hubbermann EM, Schawarz K, Krupinska K (2007) Nitration of γ-tocopherol in plant tissues. Planta 226:1311–1322

    CAS  PubMed  Google Scholar 

  • Di Mascio P, Devasagayam TP, Kaiser S, Sies H (1990) Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers. Biochem Soc Trans 18:1054–1056

    PubMed  Google Scholar 

  • Dörmann P (2007) Functional diversity of tocochromanols in plants. Planta 225:269–276

    PubMed  Google Scholar 

  • Douce R, Joyard J (1980) Plant galactolipids. In: Stumpf PK (ed) The Biochemistry of Plants, Volume 4. Academic Press, New York, pp 321–362

    Google Scholar 

  • Duke SO (2010) Herbicide and pharmaceutical relationships. Weed Sci 58:334–339

    CAS  Google Scholar 

  • Durmaz Y, Donato M, Monteiro M, Gouveia L, Nunes ML, Gama Pereira T, Gökpinar S, Bandarra NM (2009) Effect of temperature on α-tocopherol, fatty acid profile and pigments of Diacronema vlkianum (Haptophyceae). Aquac Int 17:391–399

    CAS  Google Scholar 

  • El Kayal W, Keller G, Debayles C, Kumar R, Weier D, Teulieres C, Marque C (2006) Regulation of tocopherol biosynthesis through transcriptional control of tocopherol cyclase during cold hardening in Eucalyptus gunnii. Physiol Plant 126:212–223

    Google Scholar 

  • Esteban R, Olano JM, Castresana J, Fernández-Marín B, Hernández A, Becerril JM, García-Plazaola JI (2009) Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom. Physiol Plant 135:379–389

    CAS  PubMed  Google Scholar 

  • Eugeni Piller L, Abraham M, Dörmann P, Kessler F, Besagni C (2012) Plastid lipid droplets at the crossroads of prenylquinone metabolism. J Exp Bot 63:1609–1618

    CAS  PubMed  Google Scholar 

  • Fahrenholtz SR, Doleiden FH, Tozzolo AM, Lamola AA (1974) On the quenching of singlet oxygen by α-tocopherol. Photochem Photobiol 20:505–509

    CAS  PubMed  Google Scholar 

  • Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566

    CAS  PubMed  Google Scholar 

  • Ferreira IC, Barros FR, Abreu RMV (2009) Antioxidants in wild mushrooms. Curr Med Chem 16:1543–1560

    CAS  PubMed  Google Scholar 

  • Förster B, Osmond CB, Pogson BJ (2009) De novo synthesis and degradation of Lx and V cycle pigments during shade and sun acclimation in avocado leaves. Plant Physiol 149:1179–1195

    PubMed Central  PubMed  Google Scholar 

  • Gabrielska J, Gruszecki WI (1996) Zeaxanthin (dihydroxy-β-carotene) but not β-carotene rigidifies lipid membranes: a 1H-NMR study of carotenoid-egg phosphatidylcholine liposomes. Biochim Biophys Acta 1285:167–174

    CAS  PubMed  Google Scholar 

  • Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol 174:799–810

    PubMed  Google Scholar 

  • Galvez-Valdivielso G, Cardenosa R, Vera JM, Pineda M, Aguilar M (2011) Gamma-tocopherol methyltransferase from the green alga Chlamydomonas reinhardtii: functional characterisation and expression analysis. Physiol Plant 143:316–328

    Google Scholar 

  • García-Plazaola JI, Becerril JM, Hernández A, Niinemets Ü, Kollist H (2004) Acclimation of antioxidant pools to the light environment in a natural forest canopy. New Phytol 163:87–97

    Google Scholar 

  • García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773

    Google Scholar 

  • García-Plazaola JI, Esteban R, Hormaetxe K, Fernández-Marín B, Becerril JM (2008) Photoprotective responses of Mediterranean and Atlantic trees to the extreme heat-wave of summer 2003 in southwestern Europe. Trees 22:385–395

    Google Scholar 

  • Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytol 196:763–773

    CAS  PubMed  Google Scholar 

  • González-Pérez S, Gutiérrez J, García-García F, Osuna D, Dopazo J, Lorenzo Ó, Revuelta JL, Arellano JB (2011) Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiol 156:1439–1456

    PubMed Central  PubMed  Google Scholar 

  • Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122

    CAS  PubMed  Google Scholar 

  • Goss R, Lohr M, Latowski D, Grzyb J, Vieler A, Wilhelm C, Strzalka K (2005) Role of hexagonal structure-forming lipids in diadinoxanthin and violaxanthin solubilization and de-epoxidation. Biochemistry 44:4028–4036

    CAS  PubMed  Google Scholar 

  • Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grulke NE, Johnson R, Monschein S, Nikolova P, Tausz M (2003) Variation in morphological and biochemical O3 injury attributes of mature Jeffrey pine within canopies and between microsites. Tree Physiol 23:923–929

    CAS  PubMed  Google Scholar 

  • Gruszecki WI, Strzalka K (1991) Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta 1060:310–314

    CAS  Google Scholar 

  • Hansen U, Schneiderheinze J, Stadelmann S, Rank B (2003) The α-tocopherol content of leaves of pedunculate oak (Quercus robur L.) variation over the growing season and along the vertical light gradient in the canopy. J Plant Physiol 160:91–96

    CAS  PubMed  Google Scholar 

  • Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Google Scholar 

  • Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767

    CAS  PubMed Central  PubMed  Google Scholar 

  • Havaux M, Tardy F, Ravenel J, Chanu D, Parot P (1996) Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell Environ 19:1359–1368

    CAS  Google Scholar 

  • Havaux M, Bonfils J-P, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124:273–284

    CAS  PubMed Central  PubMed  Google Scholar 

  • Havaux M, Guedeney G, He Q, Grossman AR (2003a) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim Biophys Acta 1557:21–33

    CAS  PubMed  Google Scholar 

  • Havaux M, Lütz C, Grimm B (2003b) Chloroplast membrane photostability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol 132:300–310

    CAS  PubMed Central  PubMed  Google Scholar 

  • Havaux M, Dall’Osto L, Cuiné S, Giuliano G, Bassi R (2004) The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J Biol Chem 279:13878–13888

    CAS  PubMed  Google Scholar 

  • Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heddad M, Adamska I (2002) The evolution of light stress proteins of photosynthetic organisms. Comp Funct Genomics 3:504–510

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Karimi M, Ghanati F (2011) Responses of growth and antioxidant systems in Carthamus tinctorius L. under water deficit stress. Acta Physiol Plant 33:105–112

    Google Scholar 

  • Hormaetxe K, Esteban R, Becerril JM, García-Plazaola JI (2005) Dynamics of the α-tocopherol pool as affected by external (environmental) and internal (leaf age) factors in Buxus sempervirens leaves. Physiol Plant 125:333–344

    CAS  Google Scholar 

  • Horvath G, Wessjohann L, Bigirimana J, Jansen M, Guisez Y, Caubergs R, Horemans N (2006) Differential distribution of tocopherols and tocotrienols in photosynthetic and non-photosynthetic tissues. Phytochemistry 67:1185–1195

    CAS  PubMed  Google Scholar 

  • Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100:4921–4926

    CAS  PubMed Central  PubMed  Google Scholar 

  • Inoue S, Ejima K, Iwai E, Hayashi H, Appel J, Tyystjärvi E, Murata N, Nishiyama Y (2011) Protection by α-tocopherol of the repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1807:236–241

    CAS  PubMed  Google Scholar 

  • Israelachvili JN, Mitchell DJ (1975) A model for the packing of lipids in bilayer membrane. Biochim Biophys Acta 389:13–19

    CAS  PubMed  Google Scholar 

  • Iturbe-Ormaetxe I, Moran JF, Arrese-Igor C, Gogorcena Y, Klucas RV, Becana M (1995) Activated oxygen and antioxidant defences in iron-deficient pea plants. Plant Cell Environ 18:421–429

    CAS  Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    CAS  PubMed  Google Scholar 

  • Jeffrey SW, Wright SW, Zapata M (2011) Chlorophylls and carotenoids: microalgal classes and their signature pigments. In: Roy S, Llewellyn CA, Egeland ES, Johnse G (eds) Phytoplancton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge University Press, Cambridge, pp 3–77

    Google Scholar 

  • Johnson M, Havaux M, Triantaphylidès C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J Biol Chem 282:22605–22618

    CAS  PubMed  Google Scholar 

  • Kaiser S, Di Mascio P, Murphy ME, Sies H (1990) Physical and chemical scavenging of singlet molecular oxygen by tocopherols. Arch Biochem Biophys 277:101–108

    CAS  PubMed  Google Scholar 

  • Kanwischer M, Porfirova S, Bergmüller E, Dörmann P (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition and oxidative stress. Plant Physiol 137:713–723

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karminska-Rozek E, Pukacki M (2004) Effect of water deficit on oxidative stress degradation of cell membranes in needles of Norway spruce. Acta Physiol Plant 26:431–442

    Google Scholar 

  • Kobayashi N, DellaPenna D (2008) Tocopherol metabolism, oxidation and recycling under high light stress in Arabidopsis. Plant J 55:607–618

    CAS  PubMed  Google Scholar 

  • Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer W (2002) Antioxidants help the resurrection plant Myrothamnus flabellifolia survive desiccation. Plant J 31:13–24

    CAS  PubMed  Google Scholar 

  • Kranner I, Zorn M, Turk B, Wornik S, Beckett RP, Batic F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol 160:167–176

    CAS  Google Scholar 

  • Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What it stress? Concepts, definitions and applications in seed science. New Phytol 188:655–673

    CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A, Trebst A (2006) Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre. J Exp Bot 57:1677–1684

    CAS  PubMed  Google Scholar 

  • Krinsky NI, Landrum JT, Bone RA (2003) Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr 23:171–201

    CAS  PubMed  Google Scholar 

  • Latowski D, Kruk J, Burda K, Skrzynecka-Jaskier M, Kostecka-Gugala A, Strzalka K (2002) Kinetics of violaxanthin de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme, is regulated by membrane fluidity in model lipid bilayers. Eur J Biochem 269:4656–4665

    CAS  PubMed  Google Scholar 

  • Latowski D, Akerlund HE, Strzałka K (2004) Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 43:4417–4420

    CAS  PubMed  Google Scholar 

  • Latowski D, Goss R, Bojko M, Strzałka K (2012) Violaxanthin and diadinoxanthin de-epoxidation in various model lipid systems. Acta Biochim Pol 59:101–103

    CAS  PubMed  Google Scholar 

  • Leipner J, Fracheboud Y, Stamp P (1997) Acclimation by suboptimal growth temperature diminishes photooxidative damage in maize leaves. Plant Cell Environ 20:366–372

    CAS  Google Scholar 

  • Leipner J, Basilidès A, Stamp P, Fracheboud Y (2000) Hardly increased oxidative stress after exposure to low temperature in chilling-acclimated and non-acclimated maize leaves. Plant Biol 2:243–252

    CAS  Google Scholar 

  • Lepetit B, Volke D, Gilbert M, Wilhelm C, Goss R (2010) Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol 154:1905–1920

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Physiol Plant Mol Biol 60:239–260

    CAS  Google Scholar 

  • Li B, Vachali P, Bernstein PS (2010) Human ocular carotenoid-binding proteins. Photochem Photobiol Sci 9:1418–1425

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Z, Keasling JD, Niyogi KK (2012) Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol 158:313–323

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lichtenthaler HK (2007) Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92:163–179

    CAS  PubMed  Google Scholar 

  • Liebler DC, Kaysen KL, Kennedy TA (1989) Redox cycles of vitamin E: hydrolysis and ascorbic acid dependent reduction of 8a(-alkyldioxy)tocopherones. Biochemistry 28:9772–9777

    CAS  PubMed  Google Scholar 

  • Liebler DC, Burr JA, Philips L, Ham AJ (1996) Gas chromatography-mass spectrometry analysis of vitamin E and its oxidation products. Anal Biochem 236:27–34

    CAS  PubMed  Google Scholar 

  • Lim BP, Nagao A, Terao J, Tanaka K, Suzuki T, Takama K (1992) Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. Biochim Biophys Acta 1126:178–184

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z, Jin Z, Chen S, Liu G (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol Lett 30:1275–1280

    CAS  PubMed  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WW III, Grace SC (1998) Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. J Exp Bot 49:1869–1879

    CAS  Google Scholar 

  • Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158:1172–1192

    CAS  PubMed Central  PubMed  Google Scholar 

  • Macko S, Wehner A, Jahns P (2002) Comparison of violaxanthin de-epoxidation from the stroma and lumen sides of isolated thylakoid membranes from Arabidopsis: implications for the mechanism of de-epoxidation. Planta 216:309–314

    CAS  PubMed  Google Scholar 

  • Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2005) Tocopherols protect Synechocystis sp. Strain PCC 6803 from lipid peroxidation. Plant Physiol 138:1422–1435

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18:2710–2732

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malanga G, Calmanovici G, Puntarulo S (1997) Oxidative damage to chloroplasts from Chlorella vulgaris exposed to ultraviolet-B radiation. Physiol Plant 101:455–462

    CAS  Google Scholar 

  • Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80

    CAS  Google Scholar 

  • Matringe M, Ksas B, Rey P, Havaux M (2008) Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol 147:764–778

    CAS  PubMed Central  PubMed  Google Scholar 

  • McNulty HP, Byun J, Lockwood SF, Jacob RF, Mason RP (2007) Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis. Biochim Biophys Acta 1768:167–174

    CAS  PubMed  Google Scholar 

  • Mène-Saffrané L, DellaPenna D (2010) Biosynthesis, regulation and functions of tocochromanols in plants. Plant Physiol Biochem 48:301–309

    PubMed  Google Scholar 

  • Mène-Saffrané L, Dubugnon L, Chételat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284:1702–1708

    PubMed  Google Scholar 

  • Molina-Torres J, Martínez ML (1991) Tocopherols and leaf age in Xanthium strumarium L. New Phytol 118:95–99

    CAS  Google Scholar 

  • Montillet JL, Cacas J-L, Garnier L, Montané M-H, Douki T, Bessoule J-J, Polkowska-Kowalczyk L, Maciejewska U, Agnel J-P, Vial A, Triantaphylidès C (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J 40:439–451

    CAS  PubMed  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352

    CAS  Google Scholar 

  • Morosinotto T, Bassi R (2012) Assembly of light harvesting pigment-protein complexes in photosynthetic eukaryotes. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation. Advances in Photosynthesis and Respiration, Volume 34. Springer, Dordrecht, pp 113–126

    Google Scholar 

  • Mueller MJ, Mène-Saffrané L, Grun C, Karg K, Farmer EE (2006) Oxylipin analysis methods. Plant J 45:472–489

    CAS  PubMed  Google Scholar 

  • Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2000) The significance of β-carotene, α-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Aust J Plant Physiol 27:139–146

    Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Google Scholar 

  • Munné-Bosch S, Müller M, Schwarz K, Alegre L (2001a) Diterpenes and antioxidative protection in drought-stressed Salvia officinalis plants. J Plant Physiol 158:1431–1437

    Google Scholar 

  • Munné-Bosch S, Schwarz K, Alegre L (2001b) Water deficit in combination with high solar radiation leads to midday depression of α-tocopherol in field-grown lavender (Lavandula stoechas) plants. Aust J Plant Physiol 28:315–321

    Google Scholar 

  • Munné-Bosch S, Peñuelas J, Asensio D, Llusià J (2004) Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. Plant Physiol 136:2937–2947

    PubMed Central  PubMed  Google Scholar 

  • 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 trees? Plant Cell Environ 26:1787–1801

    CAS  Google 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. Plant Cell 10:1121–1134

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nussberger S, Dorr K, Wang DN, Kuhlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234:347–356

    CAS  PubMed  Google Scholar 

  • Peñuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10:166–169

    PubMed  Google Scholar 

  • Peñuelas J, Munné-Bosch S, Llusiá J, Filella I (2004) Leaf reflectance and photon and antioxidant protection in field-grown summer-stressed Phyllirea angustifolia. Optical signs of oxidative stress? New Phytol 162:115–124

    Google Scholar 

  • Porfirova S, Bergmuller E, Tropf S, Lemke R, Dörmann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci USA 99:12495–12500

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat JL, Havaux M (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158:1267–1278

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rise M, Cojocaru M, Gottlieb HE, Goldschmidt EE (1989) Accumulation of α-tocopherol in senescing organs as related to chlorophyll degradation. Plant Physiol 89:1028–1030

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruggeri BA, Gray RJH, Watkins TR, Tomlins RI (1985) Effects of low temperature acclimation and oxygen stress on tocopherol production in Euglena gracilis Z. Appl Environ Microbiol 50:1404–1408

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16:1419–1432

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schaller S, Latowski D, Jemioła-Rzemińska M, Wilhelm C, Strzałka K, Goss R (2010) The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim Biophys Acta 1797:414–424

    CAS  PubMed  Google Scholar 

  • Schumann A, Goss R, Jakob T, Wilhelm C (2007) Investigation of the quenching efficiency of diatoxanthin in cells of Phaedactylum tricornutum (Bacillariophycea) with different pool sizes of xanthophyll cycle pigments. Phycologia 46:113–117

    Google Scholar 

  • Sircelj H, Tausz M, Grill D, Batic F (2005) Biochemical responses in leaves of two apple tree cultivars subjected to progressing drought. J Plant Physiol 162:1308–1318

    CAS  PubMed  Google Scholar 

  • Stillwell W, Ehringer W, Wassall SR (1992) Interaction of alpha-tocopherol with fatty acids in membranes and ethanol. Biochim Biophys Acta 1105:237–244

    CAS  PubMed  Google Scholar 

  • Stratton SP, Liebler DC (1997) Determination of singlet oxygen-specific versus radical-mediated lipid peroxidation in photosensitized oxidation of lipid bilayers: effect of β-carotene and α-tocopherol. Biochemistry 36:12911–12920

    CAS  PubMed  Google Scholar 

  • Sujak A, Gabrielska J, Grudzinski W, Borc R, Mazurek P, Gruszecki WI (1999) Lutein and zeaxanthin as protectors of lipid membranes against oxidative damage: the structural aspects. Arch Biochem Biophys 371:301–307

    CAS  PubMed  Google Scholar 

  • Sussmann RAC, Angeli CB, Peres VJ, Kimura EA, Katzin AM (2011) Intraerythrocytic stages of Plasmodium falciparum biosynthesize vitamin E. FEBS Lett 585:3985–3991

    CAS  PubMed  Google Scholar 

  • Szilagyi A, Selstam E, Åkerlund HE (2008) Laurdan fluorescence spectroscopy in the thylakoid bilayer: the effect of violaxanthin to zeaxanthin conversion on the galactolipid dominated lipid environment. Biochim Biophys Acta 1778:348–355

    CAS  PubMed  Google Scholar 

  • Tardy F, Havaux M (1997) Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta 1330:179–193

    CAS  PubMed  Google Scholar 

  • Tardy F, Créach A, Havaux M (1998) Photosynthetic pigment concentration, organization and interconversions in a pale green Syrian landrace of barley (Hordeum vulgare L. Tadmor) adapted to harsh climatic conditions. Plant Cell Environ 21:479–489

    CAS  Google Scholar 

  • Tausz M, Hietz P, Briones O (2001) The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of a Mexican cloud forest. Aust J Plant Physiol 28:775–783

    CAS  Google Scholar 

  • Tramontano WA, Ganci D, Pennino M, Dierenfeld ES (1992) Age dependent α-tocopherol concentrations in leaves of soybean and pinto beans. Phytochemistry 31:3349–3351

    CAS  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

    PubMed  Google Scholar 

  • Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968

    PubMed Central  PubMed  Google Scholar 

  • Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dörmann P, Kessler F, Bréhélin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234

    CAS  PubMed  Google Scholar 

  • Volkova L, Tausz M, Bennet LT, Dreyer E (2009) Interactive effects of high irradiance and moderate heat on photosynthesis, pigments, and tocopherol in the tree-fern Dicksonia antarctica. Funct Plant Biol 36:1046–1056

    CAS  Google Scholar 

  • Wingsle G, Hällgren JE (1993) Influence of SO2 and NO2 exposure on glutathione, superoxide dismutase and glutathione reductase activities in scots pine needles. J Exp Bot 259:463–470

    Google Scholar 

  • Woodall AA, Bitton G, Jackson MJ (1997) Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: relationship between carotenoid structure and protective ability. Biochim Biophys Acta 1336:575–586

    CAS  PubMed  Google Scholar 

  • Wrona M, Rozanowska M, Sarna T (2004) Zeaxanthin in combination with ascorbic acid or α-tocopherol protects ARPE-19 cells against photosensitized peroxidation of lipids. Free Radic Biol Med 36:1094–1101

    CAS  PubMed  Google Scholar 

  • Yamamoto HY, Bugos RC, Hieber AD (1999) Biochemistry and molecular biology of the xanthophyll cycle. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The Photochemistry of Carotenoids, Advances in Photosynthesis, Volume 8. Kluwer, Dordrecht, pp 293–303

    Google Scholar 

  • Yokoyama A, Sandmann G, Hoshino T, Adachi K, Sakai M, Shizuri Y (1995) Thermozeaxanthins, new carotenoid-glycoside-esters from thermophilic Eubacterium Thermus thermophilus. Tetrahedron Lett 36:4901–4904

    CAS  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    CAS  PubMed  Google Scholar 

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Acknowledgments

JIGP thanks the research grants BFU 2010-15021 and UPV/EHU-GV IT-624-13 for support of research related to this chapter. MH would like to thank the Marie Curie International Training Network HARVEST for financial support of the research performed on zeaxanthin and NPQ in his laboratory. JIGP also thanks Unai Artetxe and the technical and human support provided by SGIker (UPV/EHU, MICINN, GV/EJ, ESF) for the micrograph in Fig. 26.4 and Sergio Seoane for helpful comments on the manuscript.

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Authors and Affiliations

  1. Department of IBEB, CEA, DSV, Laboratoire d’Ecophysiologie Moléculaire des Plantes, Saint-Paul-lez-Durance, F-13108, France

    Michel Havaux

  2. CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Saint-Paul-lez-Durance, F-13108, France

    Michel Havaux

  3. Aix-Marseille Université, Saint-Paul-lez-Durance, F-13108, France

    Michel Havaux

  4. Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Bilbao, 48080, Spain

    José Ignacio García-Plazaola

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  1. Michel Havaux
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Correspondence to Michel Havaux .

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  1. Ecology and Evolutionary Biology, University of Colorado, Boulder, Boulder, Colorado, USA

    Barbara Demmig-Adams

  2. Laboratory of Photosynthetic Membranes Biological Research Center, Institute of Plant Biology Hungarian Academy of Sciences, Szeged, Hungary

    Gyozo Garab

  3. Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA

    William Adams III

  4. Department of Plant Biology 265 Morrill Hall, MC-116, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

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Havaux, M., García-Plazaola, J.I. (2014). Beyond Non-Photochemical Fluorescence Quenching: The Overlapping Antioxidant Functions of Zeaxanthin and Tocopherols. In: Demmig-Adams, B., Garab, G., Adams III, W., Govindjee, . (eds) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9032-1_26

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