Crystallisation, structure and function of plant light-harvesting Complex II

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 6, 2009, Pages 753-772

  Barros, Tiago ^a   Kühlbrandt, Werner ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Crystallisation; Electron microscopy; Light harvesting; Membrane protein; Non photochemical quenching; Photosynthesis

Indexed keywords

CAROTENOID; MEMBRANE PROTEIN; XANTHOPHYLL;

BINDING SITE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON MICROSCOPY; ENERGY METABOLISM; ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; BINDING SITES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; FREEZE FRACTURING; LIGHT-HARVESTING PROTEIN COMPLEXES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOTOCHEMICAL PROCESSES; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 66449120007     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.03.012     Document Type: Review

References (174)

1. Thornber J.P. Thirty years of fun with antenna pigment-proteins and photochemical reaction centers: a tribute to the people who have influenced my career. Photosynth. Res. 44 (1995) 3-22
2. Ogawa T., Obata F., and Shibata K. Two pigment proteins in spinach chloroplasts. Biochim. Biophys. Acta 112 (1966) 223-234
3. Thornber J.P., Gregory R.P., Smith C.A., and Bailey J.L. Studies on the nature of the chloroplast lamella. I. Preparation and some properties of two chlorophyll-protein complexes. Biochemistry 6 (1967) 391-396
4. Thornber J.P., and Highkin H.R. Composition of the photosynthetic apparatus of normal barley leaves and a mutant lacking chlorophyll b. Eur. J. Biochem. 41 (1974) 109-116
5. Peter G.F., and Thornber J.P. Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J. Biol. Chem. 266 (1991) 16745-16754
6. Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4 (1999) 236-240
7. Camm E.L., and Green B.R. How the chlorophyll-proteins got their names. Photosynth Res. 80 (2004) 189-196
8. Jansson S., Pichersky E., Bassi R., Green B., Ikeuchi M., Melis A., Simpson D., Spangfort M., Staehelin L., and Thornber J. A nomenclature for the genes encoding the chlorophyll a/b-binding proteins of higher plants. Plant Mol. Biol. Reporter 10 (1992) 242-253
9. Meyer G., and Kloppstech K. A rapidly light-induced chloroplast protein with a high turnover coded for by pea nuclear DNA. Eur. J. Biochem. 138 (1984) 201-207
10. Adamska I. ELIPs - light-induced stress proteins. Physiologia. Plantarum. 100 (1997) 794-805
11. Wedel N., Klein R., Ljungberg U., Andersson B., and Herrmann R.G. The single-copy gene psbS codes for a phylogenetically intriguing 22 kDa polypeptide of photosystem II. FEBS Lett. 314 (1992) 61-66
12. Kim S., Sandusky P., Bowlby N.R., Aebersold R., Green B.R., Vlahakis S., Yocum C.F., and Pichersky E. Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett. 314 (1992) 67-71
13. Kung S.D., Thornber J.P., and Wildman S.G. Nuclear DNA codes for the photosystem II chlorophyll-protein of chloroplast membranes. FEBS Lett. 24 (1972) 185-188
14. Broglie R., Bellemare G., Bartlett S.G., Chua N.H., and Cashmore A.R. Cloned DNA sequences complementary to mRNAs encoding precursors to the small subunit of ribulose-1,5-bisphosphate carboxylase and a chlorophyll a/b binding polypeptide. Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 7304-7308
15. Coruzzi G., Broglie R., Cashmore A., and Chua N.H. Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose 1,5-bisphosphate carboxylase and the major chlorophyll a/b-binding thylakoid polypeptide. J. Biol. Chem. 258 (1983) 1399-1402
16. Straus N.A. Iron deprivation: physiology and gene regulation. In: Bryant D.A. (Ed). The Molecular Biology of Cyanobacteria (1994), Kluwer Academic Publishers 731-750
17. Bricker T. The structure and function of CPa-1 and CPa-2 in photosystem II. Photosynth. Res. 24 (1990) 1-13
18. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438 (2005) 1040-1044
19. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., and Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 303 (2004) 1831-1838
20. Murray J.W., Duncan J., and Barber J. CP43-like chlorophyll binding proteins: structural and evolutionary implications. Trends Plant Sci. 11 (2006) 152-158
21. McDermott G., Prince S.M., Freer A.A., Hawthornthwaite-Lawless A.M., Papiz M.Z., Cogdell R.J., and Isaacs N.W. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374 (1995) 517-521
22. Cogdell R.J., Gall A., and Kohler J. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q. Rev. Biophys. 39 (2006) 227-324
23. Brunisholz R.A., and Zuber H. Structure, function and organization of antenna polypeptides and antenna complexes from the three families of Rhodospirillaneae. J. Photochem. Photobiol. B. 15 (1992) 113-140
24. Fenna R.E., and Matthews B.W. Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature 258 (1975) 573-577
25. Samsonoff W.A., and MacColl R. Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Arch. Microbiol. 176 (2001) 400-405
26. Palacios M.A., Standfuss J., Vengris M., van Oort B.F., van Stokkum I.H., Kühlbrandt W., van Amerongen H., and van Grondelle R. A comparison of the three isoforms of the light-harvesting complex II using transient absorption and time-resolved fluorescence measurements. Photosynth. Res. (2006)
27. La Roche J., van der Staay G.W., Partensky F., Ducret A., Aebersold R., Li R., Golden S.S., Hiller R.G., Wrench P.M., Larkum A.W., and Green B.R. Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 15244-15248
28. Schuenemann D., Gupta S., Persello-Cartieaux F., Klimyuk V.I., Jones J.D., Nussaume L., and Hoffman N.E. A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 10312-10316
29. Stengel K.F., Holdermann I., Cain P., Robinson C., Wild K., and Sinning I. Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43. Science 321 (2008) 253-256
30. Plumley F.G., and Schmidt G.W. Reconstitution of chlorophyll a/b light-harvesting complexes: xanthophyll-dependent assembly and energy transfer. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 146-150
31. Paulsen H., Rümler U., and Rüdiger W. Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia coli. Planta 181 (1990) 204-211
32. Giuffra E., Cugini D., Croce R., and Bassi R. Reconstitution and pigment-binding properties of recombinant CP29. Eur. J. Biochem. 238 (1996) 112-120
33. Ros F., Bassi R., and Paulsen H. Pigment-binding properties of the recombinant photosystem II subunit CP26 reconstituted in vitro. Eur. J. Biochem. 253 (1998) 653-658
34. Pagano A., Cinque G., and Bassi R. In vitro reconstitution of the recombinant photosystem II light-harvesting complex CP24 and its spectroscopic characterization. J. Biol. Chem. 273 (1998) 17154-17165
35. Standfuss J., and Kühlbrandt W. The three isoforms of the light-harvesting complex II: spectroscopic features, trimer formation, and functional roles. J. Biol. Chem. 279 (2004) 36884-36891
36. Storf S., Jansson S., and Schmid V.H. Pigment binding, fluorescence properties, and oligomerization behavior of Lhca5, a novel light-harvesting protein. J. Biol. Chem. 280 (2005) 5163-5168
37. Castelletti S., Morosinotto T., Robert B., Caffarri S., Bassi R., and Croce R. Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42 (2003) 4226-4234
38. Schmid V.H., Cammarata K.V., Bruns B.U., and Schmidt G.W. In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: heterodimerization is required for antenna pigment organization. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 7667-7672
39. Kühlbrandt W., Wang D.N., and Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367 (1994) 614-621
40. Rogl H., and Kühlbrandt W. Mutant trimers of light-harvesting complex II exhibit altered pigment content and spectroscopic features. Biochemistry 38 (1999) 16214-16222
41. Remelli R., Varotto C., Sandona D., Croce R., and Bassi R. Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residues. J. Biol. Chem. 274 (1999) 33510-33521
42. Bassi R., Croce R., Cugini D., and Sandona D. Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10056-10061
43. Morosinotto T., Castelletti S., Breton J., Bassi R., and Croce R. Mutation analysis of Lhca1 antenna complex. Low energy absorption forms originate from pigment-pigment interactions. J. Biol. Chem. 277 (2002) 36253-36261
44. Croce R., Morosinotto T., Ihalainen J.A., Chojnicka A., Breton J., Dekker J.P., van Grondelle R., and Bassi R. Origin of the 701-nm fluorescence emission of the Lhca2 subunit of higher plant photosystem I. J. Biol. Chem. 279 (2004) 48543-48549
45. Mozzo M., Morosinotto T., Bassi R., and Croce R. Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta 1757 (2006) 1607-1613
46. Corbet D., Schweikardt T., Paulsen H., and Schmid V.H. Amino acids in the second transmembrane helix of the Lhca4 subunit are important for formation of stable heterodimeric light-harvesting complex LHCI-730. J. Mol. Biol. 370 (2007) 170-182
47. Booth P.J., and Paulsen H. Assembly of light-harvesting chlorophyll a/b complex in vitro. Time-resolved fluorescence measurements. Biochemistry 35 (1996) 5103-5108
48. Horn R., Grundmann G., and Paulsen H. Consecutive binding of chlorophylls a and b during the assembly in vitro of light-harvesting chlorophyll-a/b protein (LHCIIb). J. Mol. Biol. 366 (2007) 1045-1054
49. Schmid V. Light-harvesting complexes of vascular plants. Cell. Mol. Life Sci. 65 (2008) 3619-3639
50. Hobe S., Forster R., Klingler J., and Paulsen H. N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34 (1995) 10224-10228
51. Green R.R., and Pichersky E. Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosynth. Res. 39 (1994) 149-162
52. Hobe S., Prytulla S., Kühlbrandt W., and Paulsen H. Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J. 13 (1994) 3423-3429
53. Ruban A.V., Wentworth M., Yakushevska A.E., Andersson J., Lee P.J., Keegstra W., Dekker J.P., Boekema E.J., Jansson S., and Horton P. Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421 (2003) 648-652
54. Jansson S., Stefansson H., Nyström U., Gustafsson P., and Albertsson P.-Å. Antenna protein composition of PS I and PS II in thylakoid sub-domains. Biochim. Biophys. Acta 1320 (1997) 297-309
55. Boekema E.J., Hankamer B., Bald D., Kruip J., Nield J., Boonstra A.F., Barber J., and Rogner M. Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 175-179
56. Boekema E.J., van Roon H., Calkoen F., Bassi R., and Dekker J.P. Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38 (1999) 2233-2239
57. van Amerongen H., and van Grondelle R. Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants. J. Phys. Chem. B. 105 (2001) 604-617
58. Polivka T., and Sundstrom V. Ultrafast dynamics of carotenoid excited states and #x2212; from solution to natural and artificial systems. Chem. Rev. 104 (2004) 2021-2072
59. Novoderezhkin V.I., Palacios M.A., van Amerongen H., and van Grondelle R. Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure. J. Phys. Chem. B. 109 (2005) 10493-10504
60. Barzda V., Gulbinas V., Kananavicius R., Cervinskas V., van Amerongen H., van Grondelle R., and Valkunas L. Singlet-singlet annihilation kinetics in aggregates and trimers of LHCII. Biophys. J. 80 (2001) 2409-2421
61. van Grondelle R., and Novoderezhkin V.I. Energy transfer in photosynthesis: experimental insights and quantitative models. Phys. Chem. Chem. Phys. 8 (2006) 793-807
62. Bennett J. Phosphorylation of chloroplast membrane polypeptides. Nature 269 (1977) 344-346
63. Bennett J. Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett. 103 (1979) 342-344
64. Mullet J.E. The amino acid sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts. J. Biol. Chem. 258 (1983) 9941-9948
65. Bennett J., Steinback K.E., and Arntzen C.J. Chloroplast phosphoproteins: regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 5253-5257
66. Allen J.F. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098 (1992) 275-335
67. Allen J.F., and Forsberg J. Molecular recognition in thylakoid structure and function. Trends Plant. Sci. 6 (2001) 317-326
68. Wollman F.A. State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20 (2001) 3623-3630
69. Allen J.F., Bennett J., Steinback K.E., and Arntzen C.J. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291 (1981) 25-29
70. Jansson S. The light-harvesting chlorophyll a/b-binding proteins. Biochim. Biophys. Acta 1184 (1994) 1-19
71. Bellafiore S., Barneche F., Peltier G., and Rochaix J.D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433 (2005) 892-895
72. Andersson J., Wentworth M., Walters R.G., Howard C.A., Ruban A.V., Horton P., and Jansson S. 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 (2003) 350-361
73. Ryrie I.J., and Fuad N. Membrane adhesion in reconstituted proteoliposomes containing the light-harvesting chlorophyll a/b-protein complex: the role of charged surface groups. Arch. Biochem. Biophys. 214 (1982) 475-488
74. Barber J. Membrane surface charges and potentials in relation to photosynthesis. Biochim. Biophys. Acta 594 (1980) 253-308
75. McDonnel A., and Staehelin L.A. Adhesion between liposomes mediated by the chlorophyll a/b light-harvesting complex isolated from chloroplast membranes. J. Cell. Biol. 84 (1980) 40-56
76. Mullet J.E., and Arntzen C.J. Simulation of grana stacking in a model membrane system. Mediation by a purified light-harvesting pigment-protein complex from chloroplasts. Biochim. Biophys. Acta 589 (1980) 100-117
77. Li J., and Hollingshead C. Formation of crystalline arrays of chlorophyll a/b - light-harvesting protein by membrane reconstitution. Biophys. J. 37 (1982) 363-370
78. Kühlbrandt W., Thaler T., and Wehrli E. The structure of membrane crystals of the light-harvesting chlorophyll a/b protein complex. J. Cell. Biol. 96 (1983) 1414-1424
79. Lyon M.K., and Miller K.R. Crystallization of the light-harvesting chlorophyll a/b complex within thylakoid membranes. J. Cell. Biol. 100 (1985) 1139-1147
80. Kühlbrandt W. Three-dimensional structure of the light-harvesting chlorophyll a/b-protein complex. Nature 307 (1984) 478-480
81. Butler P.J., and Kühlbrandt W. Determination of the aggregate size in detergent solution of the light-harvesting chlorophyll a/b-protein complex from chloroplast membranes. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 3797-3801
82. Wang D.N., and Kühlbrandt W. Three-dimensional electron diffraction of plant light-harvesting complex. Biophys. J. 61 (1992) 287-297
83. Grigorieff N., Ceska T.A., Downing K.H., Baldwin J.M., and Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259 (1996) 393-421
84. Henderson R., Baldwin J.M., Downing K.H., Lepault J., and Zemlin F. Structure of purple membrane from halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy 19 (1986) 147-178
85. Michel H., and Oesterhelt D. Three-dimensional crystals of membrane proteins: bacteriorhodopsin. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 1283-1285
86. Michel H. Three-dimensional crystals of a membrane protein complex. The photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol. 158 (1982) 567-572
87. Garavito R.M., and Rosenbusch J.P. Three-dimensional crystals of an integral membrane protein: an initial X-ray analysis. J. Cell. Biol. 86 (1980) 327-329
88. Kühlbrandt W. Three-dimensional crystals of the light-harvesting chlorophyll a/b protein complex from pea chloroplasts. J. Mol. Biol. 194 (1987) 757-762
89. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., and Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428 (2004) 287-292
90. Dekker J.P., van Roon H., and Boekema E.J. Heptameric association of light-harvesting complex II trimers in partially solubilized photosystem II membranes. FEBS Lett. 449 (1999) 211-214
91. Standfuss J., Terwisscha van Scheltinga A.C., Lamborghini M., and Kühlbrandt W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24 (2005) 919-928
92. Michel H. Crystallization of membrane proteins. Trends Biochem. Sci. 8 (1983) 56-59
93. Kühlbrandt W., and Wang D.N. Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350 (1991) 130-134
94. Hoffman N.E., Pichersky E., Malik V.S., Castresana C., Ko K., Darr S.C., and Cashmore A.R. A cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophyll a/b-binding polypeptides. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 8844-8848
95. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., and Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 407 (2000) 599-605
96. Yamashita A., Singh S.K., Kawate T., Jin Y., and Gouaux E. Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437 (2005) 215-223
97. Faham S., Watanabe A., Besserer G.M., Cascio D., Specht A., Hirayama B.A., Wright E.M., and Abramson J. The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321 (2008) 810-814
98. Green B.R., and Kühlbrandt W. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth. Res. 44 (1995) 139-148
99. Kuttkat A., Hartmann A., Hobe S., and Paulsen H. The C-terminal domain of light-harvesting chlorophyll-a/b-binding protein is involved in the stabilisation of trimeric light-harvesting complex. Eur. J. Biochem. 242 (1996) 288-292
100. Tanford C. Contribution of hydrophobic interactions to the stability of the globular conformation of proteins. J. Am. Chem. Soc. 84 (1962) 4240-4247
101. Day D.A., Ryrie I.J., and Fuad N. Investigations of the role of the main light-harvesting chlorophyll-protein complex in thylakoid membranes. Reconstitution of depleted membranes from intermittent-light-grown plants with the isolated complex. J. Cell. Biol. 98 (1984) 163-172
102. Croce R., Canino G., Ros F., and Bassi R. Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41 (2002) 7334-7343
103. Paulsen H., Finkenzeller B., and Kuhlein N. Pigments induce folding of light-harvesting chlorophyll a/b-binding protein. Eur. J. Biochem. 215 (1993) 809-816
104. Strand A., Kvernberg K., M.K.A., and Liaaen-Jensen S. Geometrical E/Z isomers of (6R)- and (6S)-neoxanthin and biological implications. Biochem. Syst. Ecol. 28 (2000) 443-455
105. Takaichi S., and Mirauro M. Distribution and geometric isomerism of neoxanthin in oxygenic phototrophs: 9′-cis, a sole molecular form. Plant. Cell. Physiol. 39 (1998) 968-977
106. Dall'Osto L., Cazzaniga S., North H., Marion-Poll A., and Bassi R. The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant. Cell. 19 (2007) 1048-1064
107. Ruban A.V., Lee P.J., Wentworth M., Young A.J., and Horton P. Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J. Biol. Chem. 274 (1999) 10458-10465
108. Porra R.J., Thompson W.A., and Kriedemann P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975 (1989) 384-394
109. Barros T., Royant A., Standfuss J., Dreuw A., and Kuhlbrandt W. Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J. 28 (2009) 298-306
110. Yan H., Zhang P., Wang C., Liu Z., and Chang W. Two lutein molecules in LHCII have different conformations and functions: insights into the molecular mechanism of thermal dissipation in plants. Biochem. Biophys. Res. Commun. 355 (2007) 457-463
111. Yamamoto H.Y., Nakayama T.O.M., and Chichester C.O. Studies on the light and dark interconversions of leaf xanthophylls. Arch. Biochem. Biophys. 97 (1962) 168-173
112. Yamamoto H.Y. Xanthophyll Cycles, Methods in Enzymology, Vol. 110 (1985), Academic Press 303-312
113. Trémoliéres A., Dubacq J.P., Ambard-Bretteville F., and RÈmy R. Lipid composition of chlorophyl-protein complexes: specific enrichment in trans-hexadecenoic acid of an oligomeric form of light-harvesting chlorophyll a/b protein. FEBS Lett. 130 (1981) 27-31
114. Nussberger S., Dorr K., Wang D.N., and Kuhlbrandt W. Lipid-protein interactions in crystals of plant light-harvesting complex. J. Mol. Biol. 234 (1993) 347-356
115. Pascal A.A., Liu Z., Broess K., van Oort B., van Amerongen H., Wang C., Horton P., Robert B., Chang W., and Ruban A. Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436 (2005) 134-137
116. Ruban A.V., Horton P., and Robert B. Resonance Raman spectroscopy of the photosystem II light-harvesting complex of green plants: a comparison of trimeric and aggregated states. Biochemistry 34 (1995) 2333-2337
117. 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. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450 (2007) 575-578
118. Amunts A., Drory O., and Nelson N. The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447 (2007) 58-63
119. Das D., Krishna S.S., McMullan D., Miller M.D., Xu Q., Abdubek P., Acosta C., Astakhova T., Axelrod H.L., Burra P., Carlton D., Chiu H.-J., Clayton T., Deller M.C., Duan L., Elias Y., Elsliger M.-A., Ernst D., Feuerhelm J., Grzechnik A., Grzechnik S.K., Hale J., Han G.W., Jaroszewski L., Jin K.K., Klock H.E., Knuth M.W., Kozbial P., Kumar A., Marciano D., Morse A.T., Murphy K.D., Nigoghossian E., Okach L., Oommachen S., Paulsen J., Reyes R., Rife C.L., Sefcovic N., Tien H., Trame C.B., Trout C.V., Bedem H.V.D., Weekes D., White A., Hodgson K.O., Wooley J., Deacon A.M., Godzik A., Lesley S.A., and Wilson I.A. Crystal structure of the Fic (Filamentation induced by cAMP) family protein SO4266 (gi|24375750) from Shewanella oneidensis MR-1 at 1.6 Å resolution. Proteins: Struct. Funct. Bioinf. 75 (2009) 264-271
120. Haripal P.K., Raval H.K., Raval M.K., Rawal R.M., Biswal B., and Biswal U.C. Three-dimensional model of zeaxanthin binding PsbS protein associated with nonphotochemical quenching of excess quanta of light energy absorbed by the photosynthetic apparatus. J. Mol. Model. 12 (2006) 847-853
121. Müller P., Li X.-P., and Niyogi K.K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125 (2001) 1558-1566
122. Külheim C., Ågren J., and Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 297 (2002) 91-93
123. Ruban A., and Horton P. Spectroscopy of non-photochemical and photochemical quenching of chlorophyll fluorescence in leaves; evidence for a role of the light harvesting complex of Photosystem II in the regulation of energy dissipation. Photosynth. Res. 40 (1994) 181-190
124. Ide J.P., Klug D.R., Kühlbrandt W., Giorgi L.B., and Porter G. The state of detergent solubilized light-harvesting chlorophyll-a/b protein complex as monitored by picosecond time-resolved fluorescence and circular-dichroism. Biochim. Biophys. Acta 893 (1987) 349-364
125. Mullineaux C.W., Pascal A.A., Horton P., and Holzwarth A.R. Excitation-energy quenching in aggregates of the LHC II chlorophyll-protein complex: a time-resolved fluorescence study. Biochim. Biophys. Acta 1141 (1993) 23-28
126. Ruban A.V., and Horton P. Mechanism of [Delta]pH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. I. Spectroscopic analysis of isolated light-harvesting complexes. Biochim. Biophys. Acta 1102 (1992) 30-38
127. Vasil'ev S., Irrgang K.D., Schrotter T., Bergmann A., Eichler H.J., and Renger G. Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. Biochemistry 36 (1997) 7503-7512
128. Barzda V., de Grauw C.J., Vroom J., Kleima F.J., van Grondelle R., van Amerongen H., and Gerritsen H.C. Fluorescence lifetime heterogeneity in aggregates of LHCII revealed by time-resolved microscopy. Biophys. J. 81 (2001) 538-546
129. Kirchhoff H., Hinz H.J., and Rosgen J. Aggregation and fluorescence quenching of chlorophyll a of the light-harvesting complex II from spinach in vitro. Biochim. Biophys. Acta 1606 (2003) 105-116
130. Lambrev P.H., Varkonyi Z., Krumova S., Kovacs L., Miloslavina Y., Holzwarth A.R., and Garab G. Importance of trimer-trimer interactions for the native state of the plant light-harvesting complex II. Biochim. Biophys. Acta 1767 (2007) 847-853
131. van Oort B., van Hoek A., Ruban A.V., and van Amerongen H. Aggregation of light-harvesting complex II leads to formation of efficient excitation energy traps in monomeric and trimeric complexes. FEBS Lett. 581 (2007) 3528-3532
132. Ruban A.V., Dekker J.P., Horton P., and Grondelle R.V.A.N. Temperature dependence of chlorophyll fluorescence from light-harvesting complex II of higher plants. Photochem. Photobiol. 61 (1995) 216-221
133. Gilmore A.M., and Hazlett T.L. Govindjee, xanthophyll cycle-dependent quenching of photosystem ii chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 2273-2277
134. Ruban A.V., Rees D., Noctor G.D., Young A., and Horton P. Long-wavelength chlorophyll species are associated with amplification of high-energy-state excitation quenching in higher plants. Biochim. Biophys. Acta 1059 (1991) 355-360
135. Horton P., Ruban A.V., Rees D., Pascal A.A., Noctor G., and Young A.J. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett. 292 (1991) 1-4
136. Horton P., Wentworth M., and Ruban A. Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett. 579 (2005) 4201-4206
137. Miloslavina Y., Wehner A., Lambrev P.H., Wientjes E., Reus M., Garab G., Croce R., and Holzwarth A.R. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett. 582 (2008) 3625-3631
138. Jahns P., Latowski D., and Strzalka K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 1787 (2009) 3-14
139. Wentworth M., Ruban A.V., and Horton P. Chlorophyll fluorescence quenching in isolated light harvesting complexes induced by zeaxanthin. FEBS Lett. 471 (2000) 71-74
140. Avenson T.J., Ahn T.K., Zigmantas D., Niyogi K.K., Li Z., Ballottari M., Bassi R., and Fleming G.R. Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283 (2008) 3550-3558
141. Amarie S., Standfuss J., Barros T., Kühlbrandt W., Dreuw A., and Wachtveitl J. Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis. J. Phys. Chem. B. 111 (2007) 3481-3487
142. Bode S., Quentmeier C.C., Liao P.-N., Barros T., and Walla P.J. Xanthophyll-cycle dependence of the energy transfer between carotenoid dark states and chlorophylls in NPQ mutants of living plants and in LHC II. Chem. Phys. Lett. 450 (2008) 379-385
143. Dreuw A., and Wormit M. Simple replacement of violaxanthin by zeaxanthin in LHC-II does not cause chlorophyll fluorescence quenching. J. Inorg. Biochem. 102 (2008) 458-465
144. Demmig B., Winter K., Kruger A., and Czygan F.C. Photoinhibition and zeaxanthin formation in intact leaves: a possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant. Physiol. 84 (1987) 218-224
145. Avenson T.J., Ahn T.K., Niyogi K.K., Ballottari M., Bassi R., and Fleming G.R. Lutein can act as a switchable charge-transfer quencher in the CP26 light-harvesting complex. J. Biol. Chem. (2008)
146. Perez-Bueno M.L., Johnson M.P., Zia A., Ruban A.V., and Horton P. The Lhcb protein and xanthophyll composition of the light harvesting antenna controls the DeltapH-dependency of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett. 582 (2008) 1477-1482
147. Dall'Osto L., Caffarri S., and Bassi R. A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant. Cell. 17 (2005) 1217-1232.
148. Crouchman S., Ruban A., and Horton P. PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett. 580 (2006) 2053-2058
149. Horton P., Ruban A.V., and Wentworth M. Allosteric regulation of the light-harvesting system of photosystem II. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 355 (2000) 1361-1370
150. Frank H.A., Cua A., Chynwat V., Young A., Gosztola D., and Wasielewski M.R. Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth. Res. 41 (1994) 389-395
151. Dreuw A., Fleming G.R., and Head-Gordon M. Chlorophyll fluorescence quenching by xanthophylls. Phys. Chem. Chem. Phys. 5 (2003) 3247-3256
152. Holt N.E., Zigmantas D., Valkunas L., Li X.P., Niyogi K.K., and Fleming G.R. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307 (2005) 433-436
153. Ahn T.K., Avenson T.J., Ballottari M., Cheng Y.-C., Niyogi K.K., Bassi R., and Fleming G.R. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320 (2008) 794-797
154. Niyogi K.K., Grossman A.R., and Bjorkman O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell. 10 (1998) 1121-1134
155. Beddard G.S., and Porter G. Concentration quenching in chlorophyll. Nature 260 (1976) 366-367
156. Moya I., Silvestri M., Vallon O., Cinque G., and Bassi R. Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40 (2001) 12552-12561
157. Gilmore A.M., and Yamamoto H.Y. Dark induction of zeaxanthin-dependent nonphotochemical fluorenscence quenching mediated by ATP. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1899-1903
158. van Oort B., van Hoek A., Ruban A.V., and van Amerongen H. Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. J. Phys. Chem. B. 111 (2007) 7631-7637
159. Ilioaia C., Johnson M.P., Horton P., and Ruban A.V. Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J. Biol. Chem. 283 (2008) 29505-29512
160. Barros T., Royant A., Standfuss J., Dreuw A., and Kuhlbrandt W. Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J. 28 (2009) 298-306
161. Li X.P., Bjorkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S., and Niyogi K.K. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 (2000) 391-395
162. Funk C., Adamska I., Green B.R., Andersson B., and Renger G. The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments. J. Biol. Chem. 270 (1995) 30141-30147
163. Aspinall-O'Dea M., Wentworth M., Pascal A., Robert B., Ruban A., and Horton P. In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 16331-16335
164. Bonente G., Howes B.D., Caffarri S., Smulevich G., and Bassi R. Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J. Biol. Chem. 283 (2008) 8434-8445
165. Bergantino E., Segalla A., Brunetta A., Teardo E., Rigoni F., Giacometti G.M., and Szabo I. Light- and pH-dependent structural changes in the PsbS subunit of photosystem II. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15265-15270
166. Li X.-P., Phippard A., Pasari J., and Niyogi K.K. Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Funct. Plant Biol. 29 (2002) 1131-1139
167. Teardo E., de Laureto P.P., Bergantino E., Dalla Vecchia F., Rigoni F., Szabo I., and Giacometti G.M. Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochim. Biophys. Acta 1767 (2007) 703-711
168. Szabo I., Bergantino E., and Giacometti G.M. Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep. 6 (2005) 629-634
169. Deisenhofer J., Epp O., Miki K., Huber R., and Michel H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318 (1985) 618-624
170. Henderson R., Baldwin J.M., Ceska T.A., Zemlin F., Beckmann E., and Downing K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213 (1990) 899-929
171. Weiss M.S., Wacker T., Weckesser J., Welte W., and Schulz G.E. The three-dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett. 267 (1990) 268-272
172. Cowan S.W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R.A., Jansonius J.N., and Rosenbusch J.P. Crystal structures explain functional properties of two E. coli porins. Nature 358 (1992) 727-733
173. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 32 (2004) 1792-1797
174. Crimi M., Dorra D., Bosinger C.S., Giuffra E., Holzwarth A.R., and Bassi R. Time-resolved fluorescence analysis of the recombinant photosystem II antenna complex CP29. Effects of zeaxanthin, pH and phosphorylation. Eur. J. Biochem. 268 (2001) 260-267