Regulation and function of xanthophyll cycle-dependent photoprotection in algae

Photosynthesis Research

Volumn 106, Issue 1-2, 2010, Pages 103-122

  Goss, Reimund ^a   Jakob, Torsten ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Algae; Chlororespiration; NPQ; Photoprotection; Xanthophyll cycle

Indexed keywords

ALGAE; BACILLARIOPHYCEAE; BACILLARIOPHYTA; DINOPHYCEAE; HAPTOPHYCEAE; PHAEOPHYCEAE; PRASINOPHYCEAE; TRACHEOPHYTA; XANTHOPHYCEAE;

DIADINOXANTHIN; VIOLAXANTHIN; XANTHOPHYLL;

BROWN ALGA; ENVIRONMENT; EUKARYOTE; GREEN ALGA; LIGHT; METABOLISM; RADIATION EXPOSURE; REVIEW;

CHLOROPHYTA; ENVIRONMENT; EUKARYOTA; LIGHT; PHAEOPHYTA; XANTHOPHYLLS;

EID: 78650231192     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-010-9536-x     Document Type: Review

References (164)

1. 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
2. Aro EM, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in Peas acclimated to different growth irradiances. Plant Physiol 103:835-843
3. 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
4. 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
5. Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352-4356
6. 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
7. 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
8. 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
9. Böhme K, Wilhelm C, Goss R (2002) Light regulation of carotenoid biosynthesis in the prasinophycean alga Mantoniella squamata. Photochem Photobiol Sci 1:619-628
10. 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
11. 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
12. 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
13. 2-dependent zeaxanthin-epoxidase. FEBS Lett 376:45-48
14. Büchel C (2003) Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. Biochemistry 42:13027-13034
15. 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
16. 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
17. 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
18. 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 (Pubitemid 27452983)
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474-482
26. Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11-21
27. 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
28. 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
29. Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43:937-947
30. 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
31. Dimier C, Giovanni S, Ferdinando T, Brunet C (2009b) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160:397-411
32. 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
33. 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
34. 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
35. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1-14
36. Flower DR, North ACT, Sansom CE (2000) The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 1482:9-24
37. 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
38. 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
39. 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 (Pubitemid 32682631)
40. 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
41. 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
42. 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
43. Gentile M, Blanch HW (2001) Physiology and xanthophyll cycle activity of Nannochloropsis gaditana. Biotechnol Bioeng 75:1-12
44. Gerhardt M, Schneider S, Brüggemann W (2009) Physiological acclimation to light in Chara intermedia nodes. Aquat Bot 91:151-156
45. 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
46. 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
47. 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
48. Goss R (2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217:801-812
49. 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
50. Goss R, Richter M, Wild A (1995) Role of DpH in the mechanism of zeaxanthin-dependent amplification of qE. J Photochem Photobiol B 27:147-152
51. 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
52. 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 (Pubitemid 40358055)
53. 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
54. Goss R, Ann Pinto E, Wilhelm C, Richter M (2006b) The importance of a highly active and DpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008-1021
55. 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
56. 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
57. 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
58. 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
59. 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
60. 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
61. Grzyb J, Latowski D, Strzalka K (2006) Lipocalins - a family portrait. J Plant Physiol 163:895-915
62. 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
63. Gundermann K, Büchel C (2008) The fluorescence yield of thetrimeric fucoxanthin-chlorophyll-protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res 95:229-235
64. Hager A (1967a) Untersuchungen über die lichtinduzierten reversiblen Xanthophyllumwandlungen an Chlorella und Spinacia. Planta 74:148-172
65. Hager A (1967b) Untersuchungen über die Rückreaktionen im Xanthophyll-Cyclus bei Chlorella, Spinacia und Taxus. Planta 76:138-148
66. Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin- Zeaxanthin-Umwandlung:Beziehungen zur Photophosphorylierung. Planta 89:224-243
67. Hager A (1975) Die reversiblen, lichtabhängigen Xanthophyllumwandlungen im Chloroplasten. Ber Deutsch Bot Ges 88:27-44
68. 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
69. 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
70. 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
71. 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
72. 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
73. 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
74. Havir E, Tausta S, Peterson R (1997) Purification and properties of violaxanthin de-epoxidase from spinach. Plant Sci 123:57-66
75. 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
76. Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482:84-91
77. 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
78. 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
79. 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
80. Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375-385
81. 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
82. Horton P, Ruban AV, Walters R (1996) Regulation of light harvesting in green plants. Annu Rev Plant Biol 47:655-684
83. Horton P, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCIIaggregation model for non-photochemical quenching. FEBS Lett 579:4201-4206
84. Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macroorganisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069-1079
85. 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
86. 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
87. Jakob T, Goss R, Wilhelm C (1999) Activation of diadinoxanthin deepoxidase due to a chlororespiratory proton gradient in the dark in the diatom Phaeodactylum tricornutum. Plant Biol 1:76-82
88. 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
89. 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
90. 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
91. Josue JS, Frank HA (2002) Direct determination of the S1 excitedstate energies of xanthophylls by low-temperature fluorescence spectroscopy. J Phys Chem US 106:4815-4824
92. 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
93. Küster A, Schaible R, Schubert H (2004) Light acclimation of photosynthesis in three charophyte species. Aquat Bot 79:111-124
94. 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
95. 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
96. 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
97. 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
98. Lavaud J, Rousseau B, Etienne A (2002b) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a nonphotochemical fluorescence quenching. FEBS Lett 523:163-166
99. Lavaud J, Rousseau B, Etienne A (2003) Enrichment of the lightharvesting complex in diadinoxanthin and implications for the nonphotochemical fluorescence quenching in diatoms. Biochemistry 42:5802-5808
100. Lavaud J, Rousseau B, Etienne A (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130-137
101. 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
102. 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
103. 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
104. 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
105. Li X, Müller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbSdependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222-15227
106. Litchman E, Klausmeier CA (2001) Competition of phytoplankton under fluctuating light. Am Nat 157:170-187
107. Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784-8789
108. 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
109. 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
110. 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
111. 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
112. 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
113. 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
114. 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
115. 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
116. 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
117. Murphy AM, Cowles TJ (1997) Effects of darkness on multiexcitation in vivo fluorescence and survival in a marine diatom. Limnol Oceanogr 42:1444-1453
118. Newcomer M, Jones T, Aqvist J, Sundelin J, Eriksson U, Rask L, Peterson P (1984) The three-dimensional structure of retinolbinding protein. EMBO J 3:1451-1454
119. Niyogi K (1999) Photoprotection revisited: genetic and Molecular Approaches. Annu Rev Plant Phys 50:333-359 (Pubitemid 129491966)
120. Nultsch W, Pfau J, Rüffer U (1981) Do correlations exist between chromatophore arrangement and photosynthetic activity in seaweeds? Marine Biol 62:111-117
121. Olaizola M, Roche J, Kolber Z, Falkowski PG (1994) Nonphotochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41:357-370
122. 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 (Pubitemid 40966199)
123. 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
124. Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523-550
125. 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
126. 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
127. Polívka T, Herek JL, Zigmantas D, Å kerlund H, Sundström V (1999) Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 96:4914-4917
128. Richter M, Goss R, Wagner B, Holzwarth AR (1999) Characterization of the fast and slow reversible components of nonphotochemical quenching in isolated Pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis. Biochemistry 38:12718-12726
129. 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
130. 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
131. 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
132. Ruban AV, Phillip D, Young AJ, Horton P (1997) Carotenoiddependent oligomerization of the major chlorophyll a/b light harvesting complex of photosystem II of plants. Biochemistry 36:7855-7859
133. Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne AL (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165-175
134. 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
135. 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
136. Sarry JE, Montillet JL, Sauvaire Y, Havaux M (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 353:147-150
137. 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
138. 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
139. Schubert H, Forster RM (1997) Sources of variability in the factors used for modelling primary productivity in eutrophic waters. Hydrobiologia 349:75-85
140. 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
141. Schubert N, García-Mendoza E, Pacheco-Ruiz I (2006a) Carotenoid composition of marine red algae. J Phycol 42:1208-1216
142. 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
143. 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
144. 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
145. Siefermann D, Yamamoto H (1975) NADPH and oxygen-dependent epoxidation of zeaxanthin in isolated chloroplasts. Biochem Bioph Res Co 62:456-461
146. 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
147. Sinha R, Klisch M, Gröniger A, Häder D (1998) Ultravioletabsorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B 47:83-94
148. 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
149. 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
150. Stransky H, Hager A (1970) Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyllcyclus in verschiedenen Algenklassen. Arch Microbiol 71:164-190
151. Štroch M, Špunda V, Kurasová I (2004) Non-radiative dissipation of absorbed excitation energy within photosynthetic apparatus of higher plants. Photosynthetica 42:323-337
152. Ting CS, Owens TG (1993) Photochemical and nonphotochemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol 101:1323-1330
153. Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219-228
154. 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
155. 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
156. Wagner B, Goss R, Richter M, Wild A, Holzwarth AR (1996) Picosecond time-resolved study on the nature of high-energystate quenching in isolated pea thylakoids different localization of zeaxanthin dependent and independent quenching mechanisms. J Photochem Photobiol B 36:339-350
157. Walters RG, Ruban AV, Horton P (1994) Higher plant lightharvesting complexes LHCIIa and LHCIIc are bound by Dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur J Biochem 226:1063-1069
158. 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
159. 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
160. Wilson A, Ajlani G, Verbavatz J, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisomerelated energy dissipation in cyanobacteria. Plant Cell 18:992-1007
161. 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
162. Yamamoto H, Higashi R (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190:514-522
163. 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
164. Yamamoto H, Nakayama T, Chichester C (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97:168-173