Regulation of plant light harvesting by thermal dissipation of excess energy

Biochemical Society Transactions

Volumn 38, Issue 2, 2010, Pages 651-660

  De Bianchi, Silvia ^a   Ballottari, Matteo ^a   Dall'Osto, Luca ^a   Bassi, Roberto ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

Charge transfer quenching; Light harvesting antenna complex protein (LHC protein); Minor antenna protein; Non photochemical quenching (NPQ); Photoprotection; Xanthophyll mutant

Indexed keywords

CAROTENOID; GENE PRODUCT; PIGMENT; PROTEIN LIGHT HARVESTING ANTENNA COMPLEX; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; XANTHOPHYLL;

ARABIDOPSIS; BIOSYNTHESIS; ENERGY RESOURCE; GENETIC ANALYSIS; HARVESTING; HEAT SENSITIVITY; MAIZE; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PH MEASUREMENT; PHENOTYPE; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; REVIEW; SPECTROSCOPY; THERMAL ANALYSIS; BIOLOGICAL MODEL; CELL PROTECTION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; HEAT; LIGHT; LIGHT HARVESTING SYSTEM; MACROMOLECULE; METABOLISM; PHOTOCHEMISTRY; PHOTOTROPHY; PHYSIOLOGY; PLANT; THERMAL DIFFUSION;

EMBRYOPHYTA;

CYTOPROTECTION; ENERGY METABOLISM; GENE EXPRESSION REGULATION, PLANT; HOT TEMPERATURE; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; PHOTOCHEMICAL PROCESSES; PHOTOTROPHIC PROCESSES; PLANTS; THERMAL DIFFUSION; XANTHOPHYLLS;

EID: 77953244521     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0380651     Document Type: Review

References (123)

1. Ben Shem, A., Frolow, F. and Nelson, N. (2003) Crystal structure of plant Photosystem I. Nature 426, 630-635
2. Caffarri, S., Kouril, R., Kereiche, S., Boekema, E.J. and Croce, R. (2009) Functional architecture of higher plant Photosystem II supercomplexes. EMBO J. 28, 3052-3063
3. Jansson, S. (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim. Biophys. Acta 1184, 1-19
4. Bassi, R., Giuffra, E., Croce, R., Dainese, P. and Bergantino, E. (1996) Biochemistry and molecular biology of pigment binding proteins. In Light as Energy Source and Information Carrier in Plant Photophysiology, (Jennings, R.C., Zucchelli, G., Ghetti, F. and Colombetti, G., eds), pp. 41-63, Plenum Press, New York
5. Jackowski, G. and Jansson, S. (1998) Characterization of Photosystem II antenna complexes separated by non-denaturing isoelectric focusing. Z. Naturforsch. C J. Biosci. 53, 841-848
6. Ballottari, M., Dall'Osto, L., Morosinotto, T. and Bassi, R. (2007) Contrasting behavior of higher plant Photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947-8958
7. Ferreira, K.N., Iverson, T.M., Maghlaoui, K., Barber, J. and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838
8. 6f complexes. Photosynth. Res. 64, 155-166
9. Harrer, R. (2003) Associations between light-harvesting complexes and Photosystem II from Marchantia polymorpha L. determined by two- and three-dimensional electron microscopy. Photosynth. Res. 75, 249-258
10. Amunts, A., Drory, O. and Nelson, N. (2007) The structure of a plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447, 58-63
11. Ben Shem, A., Frolow, F. and Nelson, N. (2004) Light-harvesting features revealed by the structure of plant Photosystem I. Photosynth. Res. 81, 239-250
12. Wise, R.R. and Naylor, A.W. (1987) Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol. 83, 278-282
13. Mehler, A.H. (1951) Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. 33, 65-77
14. Barber, J. and Andersson, B. (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem. Sci. 17, 61-66
15. Aro, E.-M., Virgin, I. and Andersson, B. (1993) Photoinhibition of Photosystem-2: inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134
16. Osmond, C.B. (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In Photoinhibition of Photosynthesis: from Molecular Mechanisms to the Field (Baker, N.R. and Bowyer, J.R., eds), pp. 1-24, Bios Scientific Publishers, Oxford
17. Melis, A. (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage? Trends Plant Sci. 4, 130-135
18. Dall'Osto, L., Fiore, A., Cazzaniga, S., Giuliano, G. and Bassi, R. (2007) Different roles of α- and β-branch xanthophylls in photosystem assembly and photoprotection. J. Biol. Chem. 282, 35056-35068
19. 2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol. 90, 881-886
20. Gilmore, A.M. and Yamamoto, H.Y. (1992) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc. Natl. Acad. Sci. U.S.A. 89, 1899-1903
21. Yamamoto, H.Y. and Kamite, L. (1972) The effects of dithiothreitol on violaxanthin deepoxidation and absorbance changes in the 500 nm region. Biochim. Biophys. Acta 267, 538-543
22. Kagawa, T., Sakai, T., Suetsugu, N., Oikawa, K., Ishiguro, S., Kato, T., Tabata, S., Okada, K. and Wada, M. (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138-2141
23. Escoubas, J.M., Lomas, M., LaRoche, J. and Falkowski, P.G. (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. U.S.A. 92, 10237-10241
24. Maxwell, D.P., Laudenbach, D.E. and Huner, N. (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol. 109, 787-795
25. Montane, M.H., Tardy, F., Kloppstech, K. and Havaux, M. (1998) Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance. Plant Physiol. 118, 227-235
26. Allen, J.F. (1992) Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098, 275-335
27. Allen, J.F. and Forsberg, J. (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci. 6, 317-326
28. Haldrup, A., Jensen, P.E., Lunde, C. and Scheller, H.V. (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci. 6, 301-305
29. Osmond, C.B. and Grace, S.C. (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 46, 1351-1362
30. Niyogi, K.K. (2000) Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3, 455-460
31. Asada, K. (1999) The water - water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639
32. Heber, U. and Walker, D. (1992) Concerning a dual function of coupled cyclic electron-transport in leaves. Plant Physiol. 100, 1621-1626
33. Frank, H.A., Bautista, J.A., Josue, J.S. and Young, A.J. (2000) Mechanism of nonphotochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry 39, 2831-2837
34. Hideg, E. and Schreiber, U. (2007) Parallel assessment of ROS formation and photosynthesis in leaves by fluorescence imaging. Photosynth. Res. 92, 103-108
35. Buschmann, C., Langsdorf, G. and Lichtenthaler, H.K. (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38, 483-491
36. Briantais, J.-M., Vernotte, C., Picaud, M. and Krause, G.H. (1980) Chlorophyll fluorescence as a probe for the determination of the photoinduced proton gradient in isolated chloroplasts. Biochim. Biophys. Acta 591, 198-202
37. Niyogi, K.K. (1999) Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359
38. Horton, P. (1996) Nonphotochemical quenching of chlorophyll fluorescence. In Light as Energy Source and Information Carrier in Plant Photophysiology (Jennings, R.C., Zucchelli, G., Ghetti, F. and Colombetti, G., eds), pp 99-111, Plenum Press, New York
39. Horton, P., Ruban, A.V. and Walters, R.G. (1996) Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655-684
40. Dall'Osto, L., Caffarri, S. and Bassi, R. (2005) A mechanism of nonphotochemical energy dissipation, independent from Psbs, revealed by a conformational change in the antenna protein CP26. Plant Cell 17, 1217-1232
41. Rintamaki, E., Salonen, M., Suoranta, U.M., Carlberg, I., Andersson, B. and Aro, E.M. (1997) Phosphorylation of light-harvesting complex II and Photosystem II core proteins shows different irradiance-dependent regulation in vivo: application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J. Biol. Chem. 272, 30476-30482
42. Ganeteg, U., Kulheim, C., Andersson, J. and Jansson, S. (2004) Is each light-harvesting complex protein important for plant fitness? Plant Physiol. 134, 502-509
43. Kulheim, C., Agren, J. and Jansson, S. (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91-93
44. Ruban, A.V. and Horton, P. (1995) An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiol. 108, 721-726
45. Joliot, P. and Joliot, A. (2002) Cyclic electron transfer in plant leaf. Proc. Natl. Acad. Sci. U.S.A. 99, 10209-10214
46. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K. and Yokota, A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around Photosystem I. Proc. Natl. Acad. Sci. U.S.A. 95, 9705-9709
47. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M. and Shikanai, T. (2002) PGR5 is involved in cyclic electron flow around Photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361-371
48. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Nemann, D.S., Finazzi, G., Joliot, P., Barbato, R. and Leister, D. (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132, 273-285
49. Munekage, Y.N., Genty, B. and Peltier, G. (2008) Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol. 49, 1688-1698
50. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S. and Niyogi, K.K. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395
51. Li, X.P., Gilmore, A.M. and Niyogi, K.K. (2002) Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in Photosystem II. J. Biol. Chem. 277, 33590-33597
52. Dominici, P., Caffarri, S., Armenante, F., Ceoldo, S., Crimi, M. and Bassi, R. (2002) Biochemical properties of the PsbS subunit of Photosystem II either purified from chloroplast or recombinant. J. Biol. Chem. 277, 22750-22758
53. Jahns, P., Polle, A. and Junge, W. (1988) The photosynthetic water oxidase: its proton pumping activity is short-circuited within the protein by DCCD. EMBO J. 7, 589-594
54. Li, X.P., Gilmore, A.M., Caffarri, S., Bassi, R., Golan, T., Kramer, D. and Niyogi, K.K. (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279, 22866-22874
55. Niyogi, K.K., Grossman, A.R. and 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
56. Betterle, N., Ballottari, M., Zorzan, S., de Bianchi, S., Cazzaniga, S., Dall'Osto, L., Morosinotto, T. and Bassi, R. (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284, 15255-15266
57. Morosinotto, T., Baronio, R. and Bassi, R. (2002) Dynamics of chromophore binding to Lhc proteins in vivo and in vitro during operation of the xanthophyll cycle. J. Biol. Chem. 277, 36913-36920
58. Jahns, P., Wehner, A., Paulsen, H. and Hobe, S. (2001) De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II. J. Biol. Chem. 276, 22154-22159
59. Walters, R.G. and Horton, P. (1999) Structural and functional heterogeneity in the major light- harvesting complexes of higher plants. Photosynth. Res. 61, 77-89
60. Caffarri, S., Croce, R., Breton, J. and Bassi, R. (2001) The major antenna complex of Photosystem II has a xanthophyll binding site not involved in light harvesting. J. Biol. Chem. 276, 35924-35933
61. Demmig-Adams, B. (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1-24
62. Johnson, G.N., Young, A.J. and Horton, P. (1994) Activation of non-photochemical quenching in thylakoids and leaves. Planta 194, 550-556
63. Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.C., Niyogi, K.K., Bassi, R. and Fleming, G.R. (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320, 794-797
64. Niyogi, K.K., Shih, C., Soon, C.W., Pogson, B.J., Dellapenna, D. and Bjorkman, O. (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth. Res. 67, 139-145
65. Pogson, B.J., Niyogi, K.K., Björkman, O. and DellaPenna, D. (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc. Natl. Acad. Sci. U.S.A. 95, 13324-13329
66. Dall'Osto, L., Lico, C., Alric, J., Giuliano, G., Havaux, M. and Bassi, R. (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol. 6, 32
67. Lokstein, H., Tian, L., Polle, J.E. and DellaPenna, D. (2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in Photosystem II antenna size and stability. Biochim. Biophys. Acta 1553, 309-319
68. Kalituho, L., Rech, J. and Jahns, P. (2007) The roles of specific xanthophylls in light utilization. Planta 225, 423-439
69. Li, Z., Ahn, T.K., Avenson, T.J., Ballottari, M., Cruz, J.A., Kramer, D.M., Bassi, R., Fleming, G.R., Keasling, J.D. and Niyogi, K.K. (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21, 1798-1812
70. Gilmore, A.M. and Yamamoto, H.Y. (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
71. Rock, C.D. and Zeevaart, J.A. (1991) The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 88, 7496-7499
72. Dall'Osto, L., Cazzaniga, S., North, H., Marion-Poll, A. and Bassi, R. (2007) The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photoxidative stress. Plant Cell 19, 1048-1064
73. Havaux, M., Dall'Osto, L., Cuine, S., Giuliano, G. and 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
74. Li, X.P., Muller-Moule, P., Gilmore, A.M. and Niyogi, K.K. (2002) PsbS-dependent enhancement of feedback de-excitation protects Photosystem II from photoinhibition. Proc. Natl. Acad. Sci. U.S.A. 99, 15222-15227
75. Bonente, G., Howes, B.D., Caffarri, S., Smulevich, G. and Bassi, R. (2008) Interactions between the Photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J. Biol. Chem. 283, 8434-8445
76. Funk, C., Schröder, W.P., Napiwotzki, A., Tjus, S.E., Renger, G. and Andersson, B. (1995) The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34, 11133-11141
77. Aspinall-O'Dea, M., Wentworth, M., Pascal, A., Robert, B., Ruban, A.V. and Horton, P. (2002) In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc. Natl. Acad. Sci. U.S.A. 99, 16331-16335
78. Havaux, M., Dall'Osto, L. and 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
79. Finazzi, G., Johnson, G.N., Dall'Osto, L., Joliot, P., Wollman, F.A. and Bassi, R. (2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the Photosystem II core complex. Proc. Natl. Acad. Sci. U.S.A. 101, 12375-12380
80. Croce, R., Weiss, S. and Bassi, R. (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274, 29613-29623
81. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X. and Chang, W. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287-292
82. Bassi, R. and Dainese, P. (1992) A supramolecular light-harvesting complex from chloroplast Photosystem-II membranes. Eur. J. Biochem. 204, 317-326
83. Croce, R., Cinque, G., Holzwarth, A.R. and Bassi, R. (2000) The Soret absorption properties of carotenoids and chlorophylls in antenna complexes of higher plants. Photosynth. Res. 64, 221-231
84. Jahns, P., Latowski, D. and Strzalka, K. (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 1787, 3-14
85. Morosinotto, T., Caffarri, S., Dall'Osto, L. and Bassi, R. (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol. Plant. 119, 347-354
86. Wehner, A., Storf, S., Jahns, P. and Schmid, V.H. (2004) De-epoxidation of violaxanthin in light-harvesting complex I proteins. J. Biol. Chem. 279, 26823-26829
87. Moya, I., Silvestri, M., Vallon, O., Cinque, G. and Bassi, R. (2001) Time-resolved fluorescence analysis of the Photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40, 12552-12561
88. Gastaldelli, M., Canino, G., Croce, R. and Bassi, R. (2003) Xanthophyll binding sites of the CP29 (Lhcb4) subunit of higher plant Photosystem II investigated by domain swapping and mutation analysis. J. Biol. Chem. 278, 19190-19198
89. Croce, R., Canino, G., Ros, F. and Bassi, R. (2002) Chromophore organization in the higher-plant Photosystem II antenna protein CP26. Biochemistry 41, 7334-7343
90. Johnson, M.P., Perez-Bueno, M.L., Zia, A., Horton, P. and Ruban, A.V. (2009) The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotochemical quenching involve common conformational changes within the Photosystem II antenna in Arabidopsis. Plant Physiol. 149, 1061-1075
91. Andersson, J., Wentworth, M., Walters, R.G., Howard, C.A., Ruban, A.V., Horton, P. and Jansson, S. (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of Photosystem II: effects on photosynthesis, grana stacking and fitness. Plant J. 35, 350-361
92. Damkjaer, J.T., Kereiche, S., Johnson, M.P., Kovacs, L., Kiss, A.Z., Boekema, E.J., Ruban, A.V., Horton, P. and Jansson, S. (2009) The Photosystem II light-harvesting protein Lhcb3 affects the macrostructure of Photosystem II and the rate of state transitions in Arabidopsis. Plant Cell 21, 3245-3256
93. Andersson, J., Walters, R.G., Horton, P. and Jansson, S. (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13, 1193-1204
94. de Bianchi, S., Dall'Osto, L., Tognon, G., Morosinotto, T. and Bassi, R. (2008) Minor antenna proteins CP24 and CP26 affect the interactions between Photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20, 1012-1028
95. Kovacs, L., Damkjaer, J., Kereiche, S., Ilioaia, C., Ruban, A.V., Boekema, E.J., Jansson, S. and Horton, P. (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18, 3106-3120
96. Berera, R., van Stokkum, I.H., Kodis, G., Keirstead, A.E., Pillai, S., Herrero, C., Palacios, R.E., Vengris, M., van Grondelle, R., Gust, D. et al. (2007) Energy transfer, excited-state deactivation, and exciplex formation in artificial caroteno-phthalocyanine light-harvesting antennas. J. Phys. Chem. B 111, 6868-6877
97. Pascal, A.A., Liu, Z., Broess, K., van Oort, B., Van Amerongen, H., Wang, C., Horton, P., Robert, B., Chang, W. and Ruban, A. (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436, 134-137 (Pubitemid 40966199)
98. Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H., Kennis, J.T., Pascal, A.A., Van Amerongen, H., Robert, B., Horton, P. and van Grondelle, R. (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575-578
99. Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.P., Niyogi, K.K. and Fleming, G.R. (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433-436
100. Avenson, T.J., Ahn, T.K., Zigmantas, D., Niyogi, K.K., Li, Z., Ballottari, M., Bassi, R. and Fleming, G.R. (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283, 3550-3558
101. Barros, T. and Kuhlbrandt, W. (2009) Crystallisation, structure and function of plant light-harvesting complex II. Biochim. Biophys. Acta 1787, 753-772
102. Barros, T., Royant, A., Standfuss, J., Dreuw, A. and Kuhlbrandt, W. (2009) Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J. 28, 298-306
103. Horton, P., Ruban, A.V., Rees, D., Pascal, A.A., Noctor, G. and Young, A.J. (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll - protein complex. FEBS Lett. 292, 1-4
104. Ruban, A.V., Young, A.J. and Horton, P. (1996) Dynamic properties of the minor chlorophyll a/b binding proteins of Photosystem II, an in vitro model for photoprotective energy dissipation in the photosynthetic membrane of green plants. Biochemistry 35, 674-678
105. Horton, P., Ruban, A.V. and Wentworth, M. (2000) Allosteric regulation of the light-harvesting system of Photosystem II. Philos. Trans. R. Soc. London Ser. B 355, 1361-1370
106. Berera, R., Herrero, C., van Stokkum, L.H.M., Vengris, M., Kodis, G., Palacios, R.E., van Amerongen, H., van Grondelle, R., Gust, D., Moore, T.A. et al. (2006) A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis. Proc. Natl. Acad. Sci. U.S.A. 103, 5343-5348
107. van Stokkum, I.H.M., Larsen, D.S. and van Grondelle, R. (2004) Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82-104
108. Miloslavina, Y., Wehner, A., Lambrev, P.H., Wientjes, E., Reus, M., Garab, G., Croce, R. and Holzwarth, A.R. (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett. 582, 3625-3631
109. Horton, P. and Ruban, A. (2005) Molecular design of the Photosystem II light-harvesting antenna: photosynthesis and photoprotection. J. Exp. Bot. 56, 365-373
110. Ilioaia, C., Johnson, M.P., Horton, P. and Ruban, A.V. (2008) Induction of efficient energy dissipation in the isolated light-harvesting complex of Photosystem II in the absence of protein aggregation. J. Biol. Chem. 283, 29505-29512
111. Bode, S., Quentmeier, C.C., Liao, P.N., Hafi, N., Barros, T., Wilk, L., Bittner, F. and Walla, P.J. (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl. Acad. Sci. U.S.A. 106, 12311-12316
112. Mozzo, M., Passarini, F., Bassi, R., van Amerongen, H. and Croce, R. (2008) Photoprotection in higher plants: the putative quenching site is conserved in all outer light-harvesting complexes of Photosystem II. Biochim. Biophys. Acta 1777, 1263-1267
113. Schiffer, R., Neis, M., Holler, D., Rodriguez, F., Geier, A., Gartung, C., Lammert, F., Dreuw, A., Zwadlo-Klarwasser, G., Merk, H. et al. (2003) Active influx transport is mediated by members of the organic anion transporting polypeptide family in human epidermal keratinocytes. J. Invest. Dermatol. 120, 285-291
114. Amarie, S., Standfuss, J., Barros, T., Kuhlbrandt, W., Dreuw, A. and Wachtveitl, J. (2007) Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis. J. Phys. Chem. B 111, 3481-3487
115. Avenson, T.J., Ahn, T.K., Niyogi, K.K., Ballottari, M., Bassi, R. and Fleming, G.R. (2009) Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex. J. Biol. Chem. 284, 2830-2835
116. Amarie, S., Wilk, L., Barros, T., Kuhlbrandt, W., Dreuw, A. and Wachtveitl, J. (2009) Properties of zeaxanthin and its radical cation bound to the minor light-harvesting complexes CP24, CP26 and CP29. Biochim. Biophys. Acta 1787, 747-752
117. Teardo, E., De Laureto, P.P., Bergantino, E., Dalla, V.F., Rigoni, F., Szabo, I. and Giacometti, G.M. (2007) Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochim. Biophys. Acta 1767, 703-711
118. Arnoux, P., Morosinotto, T., Saga, G., Bassi, R. and Pignol, D. (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21, 2036-2044
119. Yamamoto, H.Y., Chang, J.L. and Aihara, M.S. (1967) Light-induced interconversion of violaxanthin and zeaxanthin in New Zealand spinach-leaf segments. Biochim. Biophys. Acta 141, 342-347
120. Ruban, A.V., Pascal, A.A. and Robert, B. (2000) Xanthophylls of the major photosynthetic light-harvesting complex of plants: identification, conformation and dynamics. FEBS Lett. 477, 181-185
121. Cheng, Y.C., Ahn, T.K., Avenson, T.J., Zigmantas, D., Niyogi, K.K., Ballottari, M., Bassi, R. and Fleming, G.R. (2008) Kinetic modeling of charge-transfer quenching in the CP29 minor complex. J. Phys. Chem. B 112, 13418-13423
122. Kiss, A.Z., Ruban, A.V. and Horton, P. (2008) The PsbS protein controls the organization of the Photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem. 283, 3972-3978
123. Bergantino, E., Segalla, A., Brunetta, A., Teardo, E., Rigoni, F., Giacometti, G.M. and Szabo, I. (2003) Light- and pH-dependent structural changes in the PsbS subunit of Photosystem II. Proc. Natl. Acad. Sci. U.S.A. 100, 15265-15270