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Regulation and function of xanthophyll cycle-dependent photoprotection in algae

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Abstract

The xanthophyll cycle represents one of the important photoprotection mechanisms in plant cells. In the present review, we summarize current knowledge about the violaxanthin cycle of vascular plants, green and brown algae, and the diadinoxanthin cycle of the algal classes Bacillariophyceae, Xanthophyceae, Haptophyceae, and Dinophyceae. We address the biochemistry of the xanthophyll cycle enzymes with a special focus on protein structure, co-substrate requirements and regulation of enzyme activity. We present recent ideas regarding the structural basis of xanthophyll cycle-dependent photoprotection, including different models for the mechanism of non-photochemical quenching of chlorophyll a fluorescence. In a dedicated chapter, we also describe the unique violaxanthin antheraxanthin cycle of the Prasinophyceae, together with its implication for the mechanism of xanthophyll cycle-dependent heat dissipation. The interaction between the diadinoxanthin cycle and alternative electron flow pathways in the chloroplasts of diatoms is an additional topic of this review, and in the last chapter we cover aspects of the importance of xanthophyll cycle-dependent photoprotection for different algal species in their natural environments.

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Abbreviations

ADP:

Adenosine diphosphate

ATP:

Adenosine triphosphate

Ax:

Antheraxanthin

Chl:

Chlorophyll

DCM:

Deep chlorophyll maximum

DCMU:

3-(3′,4′-dichlorophenyl)-1,1-dimethylurea

DDE:

Diadinoxanthin de-epoxidase

Ddx:

Diadinoxanthin

DEP:

Diatoxanthin epoxidase

DTT:

Dithiothreitol

Dtx:

Diatoxanthin

FAD:

Flavin adenine dinucleotide

FCP:

Fucoxanthin chlorophyll protein

Fd:

Ferredoxin

FNR:

Ferredoxin-NADP-reductase

LHC:

Light-harvesting complex

MGDG:

Monogalactosyldiacylglycerol

NADPH:

Nicotinamide adenine dinucleotide phosphate, reduced form

Ndh:

NAD(P)H dehydrogenase

NPQ:

Non-photochemical quenching of chlorophyll a fluorescence

PQ:

Plastoquinone

PS:

Photosystem

qE:

High-energy-state quenching

qI:

Photoinhibitory quenching

qT:

Quenching related to state transitions

S1:

First singlet excited state

VDE:

Violaxanthin de-epoxidase

Vx:

Violaxanthin

ZEP:

Zeaxanthin epoxidase

Zx:

Zeaxanthin

References

  • Adams WW, Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Envir 18:117–127

    Article  Google Scholar 

  • Aro EM, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in Peas acclimated to different growth irradiances. Plant Physiol 103:835–843

    PubMed  CAS  Google Scholar 

  • Arvidsson P, Bratt CE, Carlsson M, Åkerlund H (1996) Purification and identification of the violaxanthin deepoxidase as a 43 kDa protein. Photosynth Res 49:119–129

    Article  CAS  Google Scholar 

  • Banet G, Pick U, Malkin S, Zamir A (1999) Differential responses to different light spectral ranges of violaxanthin de-epoxidation and accumulation of Cbr, an algal homologue of plant early light inducible proteins, in two strains of Dunaliella. Plant Physiol Biochem 37:875–879

    Article  PubMed  CAS  Google Scholar 

  • Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352–4356

    Article  PubMed  CAS  Google Scholar 

  • Berera R, van Stokkum IH, d’Haene S, Kennis JT, van Grondelle R, Dekker JP (2009) A mechanism of energy dissipation in cyanobacteria. Biophys J 96:2261–2267

    Article  PubMed  CAS  Google Scholar 

  • Bertrand M, Schoefs B, Siffel P, Rohacek K, Molnar I (2001) Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum. FEBS Lett 508:153–156

    Article  PubMed  CAS  Google Scholar 

  • Bilger W, 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

    Article  CAS  Google Scholar 

  • Böhme K, Wilhelm C, Goss R (2002) Light regulation of carotenoid biosynthesis in the prasinophycean alga Mantoniella squamata. Photochem Photobiol Sci 1:619–628

    Article  PubMed  CAS  Google Scholar 

  • Bouvier F, d’Harlingue A, Hugueney P, Marin E, Marion-Poll A, Camara B (1996) Xanthophyll biosynthesis: cloning, expression, functional reconstitution, and regulation of β-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). J Biol Biochem 271:28861–28867

    CAS  Google Scholar 

  • Brunet C, Casotti R, Vantrepotte V, Corato F, Conversano F (2006) Picophytoplankton diversity and photoacclimation in the Strait of Sicily (Mediterranean Sea) in summer. I. Mesoscale variations. Aquat Microb Ecol 44:127–141

    Article  Google Scholar 

  • Brunet C, Casotti R, Vantrepotte V, Conversano F (2007) Vertical variability and diel dynamics of picophytoplankton in the Strait of Sicily, Mediterranean Sea, in summer. Mar Ecol Prog Ser 346:15–26

    Article  CAS  Google Scholar 

  • Büch K, Stransky H, Hager A (1995) FAD is a further essential cofactor of the NAD(P)H and O2-dependent zeaxanthin-epoxidase. FEBS Lett 376:45–48

    Article  PubMed  Google Scholar 

  • Büchel C (2003) Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. Biochemistry 42:13027–13034

    Article  PubMed  CAS  Google Scholar 

  • Büchel C, Wilhelm C (1990) Wavelength independent state transitions and light regulated chlororespiration as mechanisms to control the energy status in the chloroplast of Pleurochloris meiringensis. Plant Physiol Biochem 28:307–314

    Google Scholar 

  • Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci USA 93:6320–6325

    Article  PubMed  CAS  Google Scholar 

  • Bugos RC, Hieber D, Yamamoto HY (1998) Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Biochem 273:15321–15324

    CAS  Google Scholar 

  • Burbidge A, Grieve T, Terry C, Corlett J, Thompson A, Taylor I (1997) Structure and expression of a cDNA encoding zeaxanthin epoxidase, isolated from a wilt-related tomato (Lycopersicon esculentum Mill.) library. J Exp Bot 48:1749–1750

    CAS  Google Scholar 

  • Cardol P, Bailleul B, Rappaport F, Derelle E, Béal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H, Finazzi G (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci USA 105:7881–7886

    Article  PubMed  Google Scholar 

  • Carnicas E, Jiménez C, Niell F (1999) Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia. J Photochem Photobiol B 50:149–158

    Article  CAS  Google Scholar 

  • Caron L, Berkaloff C, Duval J, Jupin H (1987) Chlorophyll fluorescence transients from the diatom Phaeodactylum tricornutum: relative rates of cyclic phosphorylation and chlororespiration. Photosynth Res 11:131–139

    Article  CAS  Google Scholar 

  • Casper-Lindley C, Björkman O (1998) Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynth Res 56:277–289

    Article  CAS  Google Scholar 

  • Colombo-Pallotta MF, García-Mendoza E, Ladah LB (2006) Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234

    Article  CAS  Google Scholar 

  • Demers S, Roy S, Gagnon R, Vignault C (1991) Rapid light-induced changes in cell fluorescence and in xanthophyll-cycle pigments of Alexandrium excavatum (Dinophyceae) and Thalassiosira pseudonana (Bacillariophyceae): a photo-protection mechanism. Mar Ecol Prog Ser 76:185–193

    Article  Google Scholar 

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482

    CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW, Heber U, Neimanis S, Winter K, Kruger A, Czygan F, Bilger W, 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

    Article  PubMed  CAS  Google Scholar 

  • Dijkman NA, Kroon BMA (2002) Indications for chlororespiration in relation to light regime in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B 66:179–187

    Article  PubMed  CAS  Google Scholar 

  • Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43:937–947

    Article  CAS  Google Scholar 

  • Dimier C, Brunet C, Geider RJ, Raven JA (2009a) Growth and photoregulation dynamics of the picoeukaryote Pelagomonas calceolata in fluctuating light. Limnol Oceanogr 54:823–836

    CAS  Google Scholar 

  • Dimier C, Giovanni S, Ferdinando T, Brunet C (2009b) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160:397–411

    Article  PubMed  CAS  Google Scholar 

  • Eisenstadt D, Ohad I, Keren N, Kaplan A (2008) Changes in the photosynthetic reaction centre II in the diatom Phaeodactylum tricornutum result in non-photochemical fluorescence quenching. Environ Microbiol 10:1997–2007

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  PubMed  CAS  Google Scholar 

  • Finazzi G, Johnson GN, Dallosto L, Joliot P, Wollman F, Bassi R (2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc Natl Acad Sci USA 101:12375–12380

    Article  PubMed  CAS  Google Scholar 

  • Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1–14

    PubMed  CAS  Google Scholar 

  • Flower DR, North ACT, Sansom CE (2000) The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 1482:9–24

    PubMed  CAS  Google Scholar 

  • Frank H, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski M (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41:389–395

    Article  CAS  Google Scholar 

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1996) The lifetimes and energies of the first excited singlet states of diadinoxanthin and diatoxanthin: the role of these molecules in excess energy dissipation in algae. Biochim Biophys Acta 1277:243–252

    Article  PubMed  CAS  Google Scholar 

  • Frommolt R, Goss R, Wilhelm C (2001) The de-epoxidase and epoxidase reactions of Mantoniella squamata (Prasinophyceae) exhibit different substrate-specific reaction kinetics compared to spinach. Planta 213:446–456

    Article  PubMed  CAS  Google Scholar 

  • Frommolt R, Werner S, Paulsen H, Goss R, Wilhelm C, Zauner S, Maier UG, Grossman AR, Bhattacharya D, Lohr M (2008) Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Mol Biol Evol 25:2653–2667

    Article  PubMed  CAS  Google Scholar 

  • García-Mendoza E, Colombo-Pallotta MF (2007) The giant kelp Macrocystis pyrifera presents a different nonphotochemical quenching control than higher plants. New Phytol 173:526–536

    Article  PubMed  CAS  Google Scholar 

  • Geider RJ, MacIntyre HL, Graziano LM, McKay RML (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33:315–332

    Article  Google Scholar 

  • Gentile M, Blanch HW (2001) Physiology and xanthophyll cycle activity of Nannochloropsis gaditana. Biotechnol Bioeng 75:1–12

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt M, Schneider S, Brüggemann W (2009) Physiological acclimation to light in Chara intermedia nodes. Aquat Bot 91:151–156

    Article  CAS  Google Scholar 

  • Gevaert F, Créach A, Davoult D, Migné A, Levavasseur G, Arzel P, Holl A, Lemoine Y (2003) Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar Ecol Prog Ser 247:43–50

    Article  Google Scholar 

  • Gilmore A, Yamamoto H (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

    Article  CAS  Google Scholar 

  • Gilmore AM, Mohanty N, Yamamoto HY (1994) Epoxidation of zeaxanthin and antheraxanthin reverses non-photochemical quenching of photosystem II chlorophyll a fluorescence in the presence of trans-thylakoid delta pH. FEBS Lett 350:271–274

    Article  PubMed  CAS  Google Scholar 

  • Goss R (2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217:801–812

    Article  PubMed  CAS  Google Scholar 

  • Goss R, Garab G (2001) Non-photochemical chlorophyll fluorescence quenching and structural rearrangements induced by low pH in intact cells of Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Photosynth Res 67:185–197

    Article  PubMed  CAS  Google Scholar 

  • Goss R, Richter M, Wild A (1995) Role of ΔpH in the mechanism of zeaxanthin-dependent amplification of qE. J Photochem Photobiol B 27:147–152

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Goss R, Lepetit B, Wilhelm C (2006a) Evidence for a rebinding of antheraxanthin to the light-harvesting complex during the epoxidation reaction of the violaxanthin cycle. J Plant Physiol 163:585–590

    Article  PubMed  CAS  Google Scholar 

  • Goss R, Ann Pinto E, Wilhelm C, Richter M (2006b) The importance of a highly active and ΔpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008–1021

    Article  PubMed  CAS  Google Scholar 

  • Goss R, Latowski D, Grzyb J, Vieler A, Lohr M, Wilhelm C, Strzalka K (2007) Lipid dependence of diadinoxanthin solubilization and de-epoxidation in artificial membrane systems resembling the lipid composition of the natural thylakoid membrane. Biochim Biophys Acta 1768:67–75

    Article  PubMed  CAS  Google Scholar 

  • Grotz B, Molnar P, Stransky H, Hager A (1999) Substrate specificity and functional aspects of violaxanthin-de-epoxidase, an enzyme of the xanthophyll cycle. J Plant Physiol 154:437–446

    CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2006) Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol Plantarum 126:205–211

    Article  CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2008) A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 49:1217–1225

    Article  PubMed  CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2009) The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 1787:929–938

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Grzyb J, Latowski D, Strzalka K (2006) Lipocalins—a family portrait. J Plant Physiol 163:895–915

    Article  PubMed  CAS  Google Scholar 

  • Guglielmi G, Lavaud J, Rousseau B, Etienne A, Houmard J, Ruban AV (2005) The light-harvesting antenna of the diatom Phaeodactylum tricornutum. FEBS J 272:4339–4348

    Article  PubMed  CAS  Google Scholar 

  • Gundermann K, Büchel C (2008) The fluorescence yield of the trimeric fucoxanthin–chlorophyll–protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res 95:229–235

    Article  PubMed  CAS  Google Scholar 

  • Hager A (1967a) Untersuchungen über die lichtinduzierten reversiblen Xanthophyllumwandlungen an Chlorella und Spinacia. Planta 74:148–172

    Article  CAS  Google Scholar 

  • Hager A (1967b) Untersuchungen über die Rückreaktionen im Xanthophyll-Cyclus bei Chlorella, Spinacia und Taxus. Planta 76:138–148

    Article  CAS  Google Scholar 

  • Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung: Beziehungen zur Photophosphorylierung. Planta 89:224–243

    Article  CAS  Google Scholar 

  • Hager A (1975) Die reversiblen, lichtabhängigen Xanthophyllumwandlungen im Chloroplasten. Ber Deutsch Bot Ges 88:27–44

    CAS  Google Scholar 

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

  • Hager A, 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

    Article  CAS  Google Scholar 

  • Harker M, Berkaloff C, Lemoine Y, Britton G, Young AJ, Duval J, Rmikil N, Rousseau B (1999) Effects of high light and desiccation on the operation of the xanthophyll cycle in two marine brown algae. Eur J Phycol 34:35–42

    Article  Google Scholar 

  • Havaux M, 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

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333

    Article  CAS  Google Scholar 

  • Havir E, Tausta S, Peterson R (1997) Purification and properties of violaxanthin de-epoxidase from spinach. Plant Sci 123:57–66

    Article  CAS  Google Scholar 

  • Hendrickson L, Furbank R, Chow W (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81

    Article  PubMed  CAS  Google Scholar 

  • Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482:84–91

    PubMed  CAS  Google Scholar 

  • Holden H, Rypniewski W, Law J, Rayment I (1987) The molecular structure of insecticyanin from the tobacco hornworm Manduca sexta L. at 2.6 A resolution. EMBO J 6:1565–1570

    PubMed  CAS  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li X, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262–267

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375–385

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, 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

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters R (1996) Regulation of light harvesting in green plants. Annu Rev Plant Biol 47:655–684

    Article  CAS  Google Scholar 

  • 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 Lett 579:4201–4206

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079

    Article  PubMed  CAS  Google Scholar 

  • Ihalainen JA, D’Haene S, Yeremenko N, van Roon H, Arteni AA, Boekema EJ, van Grondelle R, Matthijs HCP, Dekker JP (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43) dissipate energy in cyanobacteria. Biochemistry 44:10846–10853

    Article  PubMed  CAS  Google Scholar 

  • Ikeda Y, Komura M, Watanabe M, Minami C, Koike H, Itoh S, Kashino Y, Satoh K (2008) Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1777:351–361

    Article  PubMed  CAS  Google Scholar 

  • Jakob T, Goss R, Wilhelm C (1999) Activation of diadinoxanthin de-epoxidase due to a chlororespiratory proton gradient in the dark in the diatom Phaeodactylum tricornutum. Plant Biol 1:76–82

    Article  CAS  Google Scholar 

  • Jakob T, Goss R, Wilhelm C (2001) Unusual pH-dependence of diadinoxanthin de-epoxidase activation causes chlororespiratory induced accumulation of diatoxanthin in the diatom Phaeodactylum tricornutum. J Plant Physiol 158:383–390

    Article  CAS  Google Scholar 

  • Jakob T, Wagner H, Stehfest K, Wilhelm C (2007) A complete energy balance from photons to new biomass reveals a light- and nutrient-dependent variability in the metabolic costs of carbon assimilation. J Exp Bot 58:2101–2112

    Article  PubMed  CAS  Google Scholar 

  • Jans F, Mignolet E, Houyoux P, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105:20546–20551

    Article  PubMed  Google Scholar 

  • Josue JS, Frank HA (2002) Direct determination of the S1 excited-state energies of xanthophylls by low-temperature fluorescence spectroscopy. J Phys Chem US 106:4815–4824

    Article  CAS  Google Scholar 

  • Kalituho L, Beran KC, Jahns P (2007) The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol 143:1861–1870

    Article  PubMed  CAS  Google Scholar 

  • Küster A, Schaible R, Schubert H (2004) Light acclimation of photosynthesis in three charophyte species. Aquat Bot 79:111–124

    Article  CAS  Google Scholar 

  • Kuwabara T, Hasegawa M, Kawano M, Takaichi S (1999) Characterization of violaxanthin de-epoxidase purified in the presence of Tween 20: effects of Dithiothreitol and Pepstatin A. Plant Cell Physiol 40:1119–1126

    PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Lavaud J, Kroth PG (2006) In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. Plant Cell Physiol 47:1010–1016

    Article  PubMed  CAS  Google Scholar 

  • Lavaud J, Rousseau B, van Gorkom HJ, Etienne A (2002a) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406

    Article  PubMed  CAS  Google Scholar 

  • Lavaud J, Rousseau B, Etienne A (2002b) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523:163–166

    Article  PubMed  CAS  Google Scholar 

  • Lavaud J, Rousseau B, Etienne A (2003) Enrichment of the light-harvesting complex in diadinoxanthin and implications for the nonphotochemical fluorescence quenching in diatoms. Biochemistry 42:5802–5808

    Article  PubMed  CAS  Google Scholar 

  • Lavaud J, Rousseau B, Etienne A (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137

    Google Scholar 

  • Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194

    Article  CAS  Google Scholar 

  • Lepetit B, Volke D, Szabo M, Hoffmann R, Garab G, Wilhelm C, Goss R (2007) Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry 46:9813–9822

    Article  PubMed  CAS  Google Scholar 

  • Lepetit B, Volke D, Szabo M, Hoffmann R, Garab G, Wilhelm C, Goss R (2008) The oligomeric antenna of the diatom P. tricornutum—localization of diadinoxanthin cycle pigments. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 277–280

    Google Scholar 

  • Li X, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi K (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  PubMed  CAS  Google Scholar 

  • Li X, Müller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227

    Article  PubMed  CAS  Google Scholar 

  • Litchman E, Klausmeier CA (2001) Competition of phytoplankton under fluctuating light. Am Nat 157:170–187

    Article  PubMed  CAS  Google Scholar 

  • Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784–8789

    Article  PubMed  CAS  Google Scholar 

  • Lohr M, Wilhelm C (2001) Xanthophyll synthesis in diatoms: quantification of putative intermediates and comparison of pigment conversion kinetics with rate constants derived from a model. Planta 212:382–391

    Article  PubMed  CAS  Google Scholar 

  • MacIntyre HL, Geider RJ (1996) Regulation of Rubisco activity and its potential effect on photosynthesis during mixing in a turbid estuary. Mar Ecol Prog Ser 144:247–267

    Article  CAS  Google Scholar 

  • MacIntyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17

    Article  PubMed  CAS  Google Scholar 

  • Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15:2331–2342

    PubMed  CAS  Google Scholar 

  • Marquardt J, Hanelt D (2004) Carotenoid composition of Delesseria lancifolia and other marine red algae from polar and temperate habitats. Eur J Phycol 39:285–292

    Article  CAS  Google Scholar 

  • Masojídek J, Kopecká J, Koblízek M, Torzillo G (2004) The xanthophyll cycle in green algae (Chlorophyta): its role in the photosynthetic apparatus. Plant Biol 6:342–349

    Article  PubMed  CAS  Google Scholar 

  • Mewes H, Richter M (2002) Supplementary ultraviolet-B radiation induces a rapid reversal of the diadinoxanthin cycle in the strong light-exposed diatom Phaeodactylum tricornutum. Plant Physiol 130:1527–1535

    Article  PubMed  CAS  Google Scholar 

  • Meyer AA, Tackx M, Daro N (2000) Xanthophyll cycling in Phaeocystis globosa and Thalassiosira sp.: a possible mechanism for species succession. J Sea Res 43:373–384

    Article  CAS  Google Scholar 

  • Miloslavina Y, Grouneva I, Lambrev PH, Lepetit B, Goss R, Wilhelm C, Holzwarth AR (2009) Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim Biophys Acta 1787:1189–1197

    Article  PubMed  CAS  Google Scholar 

  • Murphy AM, Cowles TJ (1997) Effects of darkness on multi-excitation in vivo fluorescence and survival in a marine diatom. Limnol Oceanogr 42:1444–1453

    Article  CAS  Google Scholar 

  • Newcomer M, Jones T, Aqvist J, Sundelin J, Eriksson U, Rask L, Peterson P (1984) The three-dimensional structure of retinol-binding protein. EMBO J 3:1451–1454

    PubMed  CAS  Google Scholar 

  • Niyogi K (1999) Photoprotection revisited: genetic and Molecular Approaches. Annu Rev Plant Phys 50:333–359

    Article  CAS  Google Scholar 

  • Nultsch W, Pfau J, Rüffer U (1981) Do correlations exist between chromatophore arrangement and photosynthetic activity in seaweeds? Marine Biol 62:111–117

    Article  Google Scholar 

  • Olaizola M, Roche J, Kolber Z, Falkowski PG (1994) Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41:357–370

    Article  CAS  Google Scholar 

  • Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137

    Article  PubMed  CAS  Google Scholar 

  • Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521

    Article  PubMed  CAS  Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550

    Article  PubMed  CAS  Google Scholar 

  • Peltier G, Ravenel J, Verméglio A (1987) Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: evidence for a chlororespiration. Biochim Biophys Acta 893:83–90

    Article  CAS  Google Scholar 

  • Pfündel EE, Renganathan M, Gilmore AM, Yamamoto HY, Dilley RA (1994) Intrathylakoid pH in isolated Pea chloroplasts as probed by violaxanthin deepoxidation. Plant Physiol 106:1647–1658

    PubMed  Google Scholar 

  • Polívka T, Herek JL, Zigmantas D, Åkerlund H, Sundström V (1999) Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 96:4914–4917

    Article  PubMed  Google Scholar 

  • Richter M, Goss R, Wagner B, Holzwarth AR (1999) Characterization of the fast and slow reversible components of non-photochemical quenching in isolated Pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis. Biochemistry 38:12718–12726

    Article  PubMed  CAS  Google Scholar 

  • Rockholm DC, Yamamoto HY (1996) Violaxanthin de-epoxidase (purification of a 43-kilodalton lumenal protein from lettuce by lipid-affinity precipitation with Monogalactosyldiacylglyceride). Plant Physiol 110:697–703

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues MA, Santos CPD, Yoneshigue-Valentin Y, Strbac D, Hall DO (2000) Photosynthetic light response curves and photoinhibition of the deep water Laminaria abyssalis and the intertidal Laminaria digitata (Phaeophyceae). J Phycol 36:97–106

    Article  CAS  Google Scholar 

  • Rodrigues MA, Santos CPD, Young AJ, Strbac D, Hall DO (2002) A smaller and impaired xanthophyll cycle makes the deep sea macroalgae Laminaria abyssalis (Phaeophyceae) highly sensitive to daylight when compared with shallow water Laminaria digitata. J Phycol 38:939–947

    Article  Google Scholar 

  • Ruban AV, Phillip D, Young AJ, Horton P (1997) Carotenoid-dependent oligomerization of the major chlorophyll a/b light harvesting complex of photosystem II of plants. Biochemistry 36:7855–7859

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne A-L (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    Article  PubMed  CAS  Google Scholar 

  • Sampath-Wiley P, Neefus CD, Jahnke LS (2008) Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). J Exp Mar Bot Ecol 361:83–91

    Article  CAS  Google Scholar 

  • Sarry JE, Montillet JL, Sauvaire Y, Havaux M (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 353:147–150

    Article  PubMed  CAS  Google Scholar 

  • Sarthou G, Timmermans KR, Blain S, Tréguer P (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42

    Article  CAS  Google Scholar 

  • Sazanov LA, Burrows PA, Nixon PJ (1998) The plastid ndh genes code for an NADH-specific dehydrogenase: Isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95:1319–1324

    Article  PubMed  CAS  Google Scholar 

  • Schubert H, Forster RM (1997) Sources of variability in the factors used for modelling primary productivity in eutrophic waters. Hydrobiologia 349:75–85

    Article  CAS  Google Scholar 

  • Schubert H, Sagert S, Forster RM (2001) Evaluation of the different levels of variability in the underwater light field of a shallow estuary. Helgoland Mar Res 55:12–22

    Article  Google Scholar 

  • Schubert N, García-Mendoza E, Pacheco-Ruiz I (2006a) Carotenoid composition of marine red algae. J Phycol 42:1208–1216

    Article  CAS  Google Scholar 

  • Schubert H, Andersson M, Snoeijs P (2006b) Relationship between photosynthesis and non-photochemical quenching of chlorophyll fluorescence in two red algae with different carotenoid compositions. Marine Biol 149:1003–1013

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Serôdio J, Cruz S, Vieira S, Brotas V (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. J Exp Mar Bot Ecol 326:157–169

    Article  CAS  Google Scholar 

  • Siefermann D, Yamamoto H (1975) NADPH and oxygen-dependent epoxidation of zeaxanthin in isolated chloroplasts. Biochem Bioph Res Co 62:456–461

    Article  CAS  Google Scholar 

  • Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. Plant Cell 15:2152–2164

    Article  PubMed  CAS  Google Scholar 

  • Sinha R, Klisch M, Gröniger A, Häder D (1998) Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B 47:83–94

    Article  CAS  Google Scholar 

  • Six C, Finkel ZV, Rodriguez F, Marie D, Partensky F, Campbell DA (2008) Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter Ostreococcus. Limnol Oceanogr 53:255–265

    CAS  Google Scholar 

  • Six C, Sherrard R, Lionard M, Roy S, Campbell DA (2009) Photosystem II and pigment dynamics among ecotypes of the green alga Ostreococcus. Plant Physiol 151:379–390

    Article  PubMed  CAS  Google Scholar 

  • Stransky H, Hager A (1970) Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyllcyclus in verschiedenen Algenklassen. Arch Microbiol 71:164–190

    CAS  Google Scholar 

  • Štroch M, Špunda V, Kurasová I (2004) Non-radiative dissipation of absorbed excitation energy within photosynthetic apparatus of higher plants. Photosynthetica 42:323–337

    Article  Google Scholar 

  • Ting CS, Owens TG (1993) Photochemical and nonphotochemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol 101:1323–1330

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ursi S, Pedersén M, Plastino E, Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Marine Biol 142:997–1007

    CAS  Google Scholar 

  • van der Weij-de Wit CD, Ihalainen JA, van de Vijver E, D’Haene S, Matthijs HC, van Grondelle R, Dekker JP (2007) Fluorescence quenching of IsiA in early stage of iron deficiency and at cryogenic temperatures. Biochim Biophys Acta 1767:1393–1400

    Article  PubMed  CAS  Google Scholar 

  • Wagner B, Goss R, Richter M, Wild A, Holzwarth AR (1996) Picosecond time-resolved study on the nature of high-energy-state quenching in isolated pea thylakoids different localization of zeaxanthin dependent and independent quenching mechanisms. J Photochem Photobiol B 36:339–350

    Article  CAS  Google Scholar 

  • Walters RG, Ruban AV, Horton P (1994) Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by Dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur J Biochem 226:1063–1069

    Article  PubMed  CAS  Google Scholar 

  • Wilhelm C, Duval J (1990) Fluorescence induction kinetics as a tool to detect a chlororespiratory activity in the prasinophycean alga, Mantoniella squamata. Biochim Biophys Acta 1016:197–202

    Article  CAS  Google Scholar 

  • Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, LaRoche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz J, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul J, Kerfeld CA, van Grondelle R, Robert B, Kennis JTM, Kirilovsky D (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci USA 105:12075–12080

    Article  PubMed  Google Scholar 

  • Yamamoto H, Higashi R (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190:514–522

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto HY, 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

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Nakayama T, Chichester C (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97:168–173

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Financial support from the Deutsche Forschungsgemeinschaft (Go 818/6-1) is gratefully acknowledged. We thank Prof. Dr. C. Wilhelm for the discussion and correction of the manuscript.

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Goss, R., Jakob, T. Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106, 103–122 (2010). https://doi.org/10.1007/s11120-010-9536-x

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