Refined structure-based simulation of plant light-harvesting complex II: Linear optical spectra of trimers and aggregates

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 8, 2012, Pages 1446-1460

  Müh, Frank ^a   Renger, Thomas ^a  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

Author keywords

Antenna protein; Chlorophyll; Circular dichroism; Linear dichroism; Non photochemical quenching; Xanthophyll

Indexed keywords

CHLOROPHYLL; IONONE DERIVATIVE; LIGHT HARVESTING COMPLEX II; NEOXANTHIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VIOLAXANTHIN; XANTHOPHYLL;

CIRCULAR DICHROISM; CONFERENCE PAPER; CONFORMATION; CRYSTAL STRUCTURE; DIPOLE; FLUORESCENCE; LIGHT; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PIGMENTATION; PLANT LEAF; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SIMULATION; TEMPERATURE DEPENDENCE;

CIRCULAR DICHROISM; LIGHT-HARVESTING PROTEIN COMPLEXES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EMBRYOPHYTA;

EID: 84862202845     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.02.016     Document Type: Conference Paper

References (113)

1. M.F. Hohmann-Marriott, and R.E. Blankenship Evolution of photosynthesis Annu. Rev. Plant Biol. 62 2011 515 548
2. G. Renger Primary Processes of Photosynthesis, Principles and Apparatus 2008 Royal Society Chemistry Publishing Cambridge, U.K.
3. A.J. Hoff, and J. Deisenhofer Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria Phys. Rep. 287 1997 2 247
4. J.H. Golbeck Photosystem I - the light-driven plastocyanin:ferredoxin oxidoreductase Govindjee Advances in Photosynthesis and Respiration 2006 Springer Dordrecht
5. T. Cardona, A. Sedoud, N. Cox, and A.W. Rutherford Charge separation in photosystem II: a comparative and evolutionary overview Biochim. Biophys. Acta 1817 2012 26 43
6. F. Müh, C. Glöckner, J. Hellmich, and A. Zouni Light-induced quinone reduction in photosystem II Biochim. Biophys. Acta 1817 2012 44 65
7. F. Müh, and A. Zouni Light-induced water oxidation in photosystem II Front. Biosci. 17 2011 3072 3132
8. B.R. Green, and W.W. Parson Light-harvesting antennas in photosynthesis N. Govindjee, Advances in Phothosynthesis and Respiration 2003 Springer (Kluwer Academic Publishers) Dordrecht, The Netherlands
9. A. Amunts, and N. Nelson Functional organization of a plant photosystem I: evolution of a highly efficient photochemical machine Plant Physiol. Biochem. 46 2008 228 237
10. F. Müh, T. Renger, and A. Zouni Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: a closer look at the antenna system and the small membrane-intrinsic subunits Plant Physiol. Biochem. 46 2008 238 264
11. A.M. Gilmore, and X.-P. Li Regulatory control of antenna function in plants G. Renger, Primary Processes of Photosynthesis, Principles and Apparatus 2008 RSC Publishing Cambridge, U.K. 369 390
12. H. van Amerongen, and R. Croce Structure and function of photosystem II light-harvesting proteins (Lhcb) of higher plants G. Renger, Primary Processes of Photosynthesis, Principles and Apparatus 2008 RSC Publishing Cambridge, U. K. 329 367
13. R. Croce, and H. van Amerongen Light-harvesting and structural organization of photosystem II: from individual complexes to thylakoid membrane J. Photochem. Photobiol. B 104 2011 142 153
14. M. Ballottari, J. Girardon, L. Dall'osto, and R. Bassi Evolution and functional properties of photosystem II light harvesting complexes in eukaryotes Biochim. Biophys. Acta 1817 2012 143 157
15. S. Caffarri, R. Kouril, S. Kereiche, E.J. Boekema, and R. Croce Functional architecture of higher plant photosystem II supercomplexes EMBO J. 28 2009 3052 3063
16. P. Horton, M.P. Johnson, M.L. Perez-Bueno, A.Z. Kiss, and A.V. Ruban Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J. 275 2008 1069 1079
17. N. Betterle, M. Ballottari, S. Zorzan, S. de Bianchi, S. Cazzaniga, L. Dall'Osto, T. Morosinotto, and R. Bassi Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction J. Biol. Chem. 284 2009 15255 15266
18. R. Kouril, J.P. Dekker, and E.J. Boekema Supramolecular organization of photosystem II in green plants Biochim. Biophys. Acta 1817 2012 2 12
19. Y. Umena, K. Kawakami, J.R. Shen, and N. Kamiya Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Nature 473 2011 55 60
20. D. Piano, S. El Alaoui, H.J. Korza, R. Filipek, I. Sabala, P. Haniewicz, C. Buechel, D. De Sanctis, and M. Bochtler Crystallization of the photosystem II core complex and its chlorophyll binding subunit CP43 from transplastomic plants of Nicotiana tabacum Photosynth. Res. 106 2010 221 226
21. Z.F. Liu, H.C. Yan, K.B. Wang, T.Y. Kuang, J.P. Zhang, L.L. Gui, X.M. An, and W.R. Chang Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 2004 287 292
22. J. Standfuss, A.C. Terwisscha van Scheltinga, M. Lamborghini, and W. Kühlbrandt Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution EMBO J. 24 2005 919 928
23. T. Barros, and W. Kühlbrandt Crystallisation, structure and function of plant light-harvesting complex II Biochim. Biophys. Acta 1787 2009 753 772
24. X.W. Pan, M. Li, T. Wan, L.F. Wang, C.J. Jia, Z.Q. Hou, X.L. Zhao, J.P. Zhang, and W.R. Chang Structural insights into energy regulation of light-harvesting complex CP29 from spinach Nat. Struct. Mol. Biol. 18 2011 309 315
25. P. Jahns, D. Latowski, and K. Strzalka Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids Biochim. Biophys. Acta 1787 2009 3 14
26. P. Jahns, and A.R. Holzwarth The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II Biochim. Biophys. Acta 1817 2012 182 193
27. S. de Bianchi, M. Ballottari, L. Dall'Osto, and R. Bassi Regulation of plant light harvesting by thermal dissipation of excess energy Biochem. Soc. Trans. 38 2010 651 660
28. X.P. Li, O. Björkman, C. Shih, A.R. Grossman, M. Rosenquist, S. Jansson, and K.K. Niyogi A pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 403 2000 391 395
29. K.K. Niyogi, X.P. Li, V. Rosenberg, and H.S. Jung Is PsbS the site of non-photochemical quenching in photosynthesis? J. Exp. Bot. 56 2005 375 382
30. H.A. Frank, A. Cua, V. Chynwat, A. Young, D. Gosztola, and M.R. Wasielewski Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis Photosynth. Res. 41 1994 389 395
31. A.V. Ruban, R. Berera, C. Ilioaia, I.H.M. van Stokkum, J.T.M. Kennis, A.A. Pascal, H. van Amerongen, B. Robert, P. Horton, and R. van Grondelle Identification of a mechanism of photoprotective energy dissipation in higher plants Nature 450 2007 575 578
32. H. van Amerongen, and R. van Grondelle Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants J. Phys. Chem. B 105 2001 604 617
33. S. Bode, C.C. Quentmeier, P.N. Liao, N. Hafi, T. Barros, L. Wilk, F. Bittner, and P.J. Walla On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls Proc. Natl. Acad. Sci. U.S.A. 106 2009 12311 12316
34. A.V. Ruban, F. Calkoen, S.L.S. Kwa, R. van Grondelle, P. Horton, and J.P. Dekker Characterisation of LHC II in the aggregated state by linear and circular dichroism spectroscopy Biochim. Biophys. Acta 1321 1997 61 70
35. C.D.P. Duffy, A.V. Ruban, and W. Barford Theoretical investigation of the role of strongly coupled chlorophyll dimers in photoprotection of LHCII J. Phys. Chem. B 112 2008 12508 12515
36. Y. Miloslavina, A. Wehner, P.H. Lambrev, E. Wientjes, M. Reus, G. Garab, R. Croce, and A.R. Holzwarth Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching FEBS Lett. 582 2008 3625 3631
37. M.G. Müller, P. Lambrev, M. Reus, E. Wientjes, R. Croce, and A.R. Holzwarth Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids ChemPhysChem 11 2010 1289 1296
38. N.E. Holt, D. Zigmantas, L. Valkunas, X.P. Li, K.K. Niyogi, and G.R. Fleming Carotenoid cation formation and the regulation of photosynthetic light harvesting Science 307 2005 433 436
39. T.K. Ahn, T.J. Avenson, M. Ballottari, Y.C. Cheng, K.K. Niyogi, R. Bassi, and G.R. Fleming Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein Science 320 2008 794 797
40. V.I. Novoderezhkin, and R. van Grondelle Physical origins and models of energy transfer in photosynthetic light-harvesting Phys. Chem. Chem. Phys. 12 2010 7352 7365
41. P.W. Hemelrijk, S.L.S. Kwa, R. van Grondelle, and J.P. Dekker Spectroscopic properties of LHC-II, the main light-harvesting chlorophyll-a/b protein complex from chloroplast membranes Biochim. Biophys. Acta 1098 1992 159 166
42. S. Nussberger, J.P. Dekker, W. Kühlbrandt, B.M. van Bolhuis, R. van Grondelle, and H. van Amerongen Spectroscopic characterization of three different monomeric forms of the main chlorophyll a/b binding protein from chloroplast membranes Biochemistry 33 1994 14775 14783
43. y-level structure and dynamics of solubilized light-harvesting complex II of green plants: pressure and hole burning studies J. Phys. Chem. A 103 1999 2412 2421
44. J. Pieper, K.D. Irrgang, M. Rätsep, R. Jankowiak, T. Schrötter, J. Voigt, G.J. Small, and G. Renger Effects of aggregation on trimeric light-harvesting complex II of green plants: a hole-burning study J. Phys. Chem. A 103 1999 2422 2428
45. R. Remelli, C. Varotto, D. Sandona, R. Croce, and R. Bassi Chlorophyll binding to monomeric light-harvesting complex - a mutation analysis of chromophore-binding residues J. Biol. Chem. 274 1999 33510 33521
46. H. Rogl, R. Schödel, H. Lokstein, W. Kühlbrandt, and A. Schubert Assignment of spectral substructures to pigment-binding sites in higher plant light-harvesting complex LHC-II Biochemistry 41 2002 2281 2287
47. H. van Amerongen, S.L.S. Kwa, B.M. van Bolhuis, and R. van Grondelle Polarized fluorescence and absorption of macroscopically aligned light harvesting complex II Biophys. J. 67 1994 837 847
48. C.C. Gradinaru, S. Özdemir, D. Gülen, I.H.M. van Stokkum, R. van Grondelle, and H. van Amerongen The flow of excitation energy in LHCII monomers: implications for the structural model of the major plant antenna Biophys. J. 75 1998 3064 3077
49. V.I. Novoderezhkin, M.A. Palacios, H. van Amerongen, and R. van Grondelle 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
50. J. Pieper, M. Rätsep, K.D. Irrgang, and A. Freiberg Chromophore-chromophore and chromophore-protein interactions in monomeric light-harvesting complex II of green plants studied by spectral hole burning and fluorescence line narrowing J. Phys. Chem. B 113 2009 10870 10880
51. R. Jankowiak, M. Reppert, V. Zazubovich, J. Pieper, and T. Reinot Site selective and single complex laser-based spectroscopies: a window on excited state electronic structure, excitation energy transfer, and electron-phonon coupling of selected photosynthetic complexes Chem. Rev. 111 2011 4546 4598
52. C. Tietz, F. Jelezko, U. Gerken, S. Schuler, A. Schubert, H. Rogl, and J. Wrachtrup Single molecule spectroscopy on the light-harvesting complex II of higher plants Biophys. J. 81 2001 556 562
53. T.P.J. Krüger, V.I. Novoderezhkin, C. Ilioaia, and R. van Grondelle Fluorescence spectral dynamics of single LHCII trimers Biophys. J. 98 2010 3093 3101
54. G.S. Schlau-Cohen, T.R. Calhoun, N.S. Ginsberg, E.L. Read, M. Ballottari, R. Bassi, R. van Grondelle, and G.R. Fleming Pathways of energy flow in LHCII from two-dimensional electronic spectroscopy J. Phys. Chem. B 113 2009 15352 15363
55. T.R. Calhoun, N.S. Ginsberg, G.S. Schlau-Cohen, Y.C. Cheng, M. Ballottari, R. Bassi, and G.R. Fleming Quantum coherence enabled determination of the energy landscape in light-harvesting complex II J. Phys. Chem. B 113 2009 16291 16295
56. G.S. Schlau-Cohen, T.R. Calhoun, N.S. Ginsberg, M. Ballottari, R. Bassi, and G.R. Fleming Spectroscopic elucidation of uncoupled transition energies in the major photosynthetic light-harvesting complex, LHCII Proc. Natl. Acad. Sci. U.S.A. 107 2010 13276 13281
57. J.J. Burke, C.L. Ditto, and C.J. Arntzen Involvement of light-harvesting complex in cation regulation of excitation-energy distribution in chloroplasts Arch. Biochem. Biophys. 187 1978 252 263
58. R. Bassi, M. Silvestri, P. Dainese, I. Moya, and G.M. Giacometti Effects of a nonionic detergent on the spectral properties and aggregation state of the light-harvesting chlorophyll-a/b protein complex (LHCII) J. Photochem. Photobiol. B 9 1991 335 354
59. B. Voigt, M. Krikunova, and H. Lokstein Influence of detergent concentration on aggregation and spectroscopic properties of light-harvesting complex II Photosynth. Res. 95 2008 317 325
60. A.V. Ruban, A. Young, and P. Horton Modulation of chlorophyll fluorescence quenching in isolated light harvesting complex of photosystem II Biochim. Biophys. Acta 1186 1994 123 127
61. P. Horton, M. Wentworth, and A. Ruban Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching FEBS Lett. 579 2005 4201 4206
62. M.P. Johnson, T.K. Goral, C.D. Duffy, A.P. Brain, C.W. Mullineaux, and A.V. Ruban Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts Plant Cell 23 2011 1468 1479
63. H. van Amerongen, L. Valkunas, and R. van Grondelle Photosynthetic Excitons 2000 World Scientific Singapore
64. G. Garab, and H. van Amerongen Linear dichroism and circular dichroism in photosynthesis research Photosynth. Res. 101 2009 135 146
65. T. Renger Theory of excitation energy transfer: from structure to function Photosynth. Res. 102 2009 471 485
66. J. Linnanto, J. Martiskainen, V. Lehtovuori, J. Ihalainen, R. Kananavicius, R. Barbato, and J. Korppi-Tommola Excitation energy transfer in the LHC-II trimer: a model based on the new 2.72 Å structure Photosynth. Res. 87 2006 267 279
67. C. König, and J. Neugebauer First-principles calculation of electronic spectra of light-harvesting complex II Phys. Chem. Chem. Phys. 13 2011 10475 10490
68. F. Müh, M.E. Madjet, J. Adolphs, A. Abdurahman, B. Rabenstein, H. Ishikita, E.W. Knapp, and T. Renger α-Helices direct excitation energy flow in the Fenna-Matthews-Olson protein Proc. Natl. Acad. Sci. U.S.A. 104 2007 16862 16867
69. F. Müh, M.E.A. Madjet, and T. Renger Structure-based identification of energy sinks in plant light-harvesting complex II J. Phys. Chem. B 114 2010 13517 13535
70. T. Renger, M.E. Madjet, A. Knorr, and F. Müh How the molecular structure determines the flow of excitation energy in plant light-harvesting complex II J. Plant Physiol. 168 2011 1497 1509
71. A.A. Pascal, Z.F. Liu, K. Broess, B. van Oort, H. van Amerongen, C. Wang, P. Horton, B. Robert, W.R. Chang, and A. Ruban Molecular basis of photoprotection and control of photosynthetic light-harvesting Nature 436 2005 134 137
72. T. Barros, A. Royant, J. Standfuss, A. Dreuw, and W. Kühlbrandt Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state EMBO J. 28 2009 298 306
73. B. van Oort, A. Maréchal, A.V. Ruban, B. Robert, A.A. Pascal, N.C.A. de Ruijter, R. van Grondelle, and H. van Amerongen Different crystal morphologies lead to slightly different conformations of light-harvesting complex II as monitored by variations of the intrinsic fluorescence lifetime Phys. Chem. Chem. Phys. 13 2011 12614 12622
74. M.A.L. Marques, and E.K.U. Gross Time-dependent density functional theory Annu. Rev. Phys. Chem. 55 2004 427 455
75. A. Dreuw, and M. Head-Gordon Single-reference ab initio methods for the calculation of excited states of large molecules Chem. Rev. 105 2005 4009 4037
76. S. Hirata, and M. Head-Gordon Time-dependent density functional theory within the Tamm-Dancoff approximation Chem. Phys. Lett. 314 1999 291 299
77. T. Renger, M.E. Madjet, F. Müh, I. Trostmann, F.J. Schmitt, C. Theiss, H. Paulsen, H.J. Eichler, A. Knorr, and G. Renger Thermally activated superradiance and intersystem crossing in the water-soluble chlorophyll binding protein J. Phys. Chem. B 113 2009 9948 9957
78. M.E. Madjet, F. Müh, and T. Renger Deciphering the influence of short-range electronic couplings on optical properties of molecular dimers: application to special pairs in photosynthesis J. Phys. Chem. B 113 2009 12603 12614
79. A. Szabo, and N.S. Ostlund Modern Quantum Chemistry: Introduction to Advanced Electronic Structure Theory 1st ed. 1989 McGraw-Hill New York
80. M.E. Madjet, A. Abdurahman, and T. Renger Intermolecular coulomb couplings from ab initio electrostatic potentials: application to optical transitions of strongly coupled pigments in photosynthetic antennae and reaction centers J. Phys. Chem. B 110 2006 17268 17281
81. B.R. Brooks, C.L. Brooks, A.D. Mackerell, L. Nilsson, R.J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, A. Caflisch, L. Caves, Q. Cui, A.R. Dinner, M. Feig, S. Fischer, J. Gao, M. Hodoscek, W. Im, K. Kuczera, T. Lazaridis, J. Ma, V. Ovchinnikov, E. Paci, R.W. Pastor, C.B. Post, J.Z. Pu, M. Schaefer, B. Tidor, R.M. Venable, H.L. Woodcock, X. Wu, W. Yang, D.M. York, and M. Karplus CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
82. G. Kieseritzky, and E.W. Knapp Optimizing pK(A) computation in proteins with pH adapted conformations Proteins 71 2008 1335 1348
83. D. Bashford Macroscopic electrostatic models for protonation states in proteins Front. Biosci. 9 2004 1082 1099
84. G.M. Ullmann, and E.W. Knapp Electrostatic models for computing protonation and redox equilibria in proteins Eur. Biophys. J. 28 1999 533 551
85. J. Adolphs, F. Müh, M.E. Madjet, and T. Renger Calculation of pigment transition energies in the FMO protein Photosynth. Res. 95 2008 197 209
86. J. Adolphs, F. Müh, M.E. Madjet, M. Schmidt am Busch, and T. Renger Structure-based calculations of optical spectra of photosystem I suggest an asymmetric light-harvesting process J. Am. Chem. Soc. 132 2010 3331 3343
87. T. Renger, and F. Müh Theory of excitonic couplings in dielectric media. Foundation of Poisson-TrEsp method and application to photosystem I trimers Photosynth. Res. 2011 10.1007/s11120-011-9685-6
88. R.S. Knox, and B.Q. Spring Dipole strengths in the chlorophylls Photochem. Photobiol. 77 2003 497 501
89. T. Renger, I. Trostmann, C. Theiss, M.E. Madjet, M. Richter, H. Paulsen, H.J. Eichler, A. Knorr, and G. Renger Refinement of a structural model of a pigment-protein complex by accurate optical line shape theory and experiments J. Phys. Chem. B 111 2007 10487 10501
90. T. Renger, and R.A. Marcus On the relation of protein dynamics and exciton relaxation in pigment-protein complexes: an estimation of the spectral density and a theory for the calculation of optical spectra J. Chem. Phys. 116 2002 9997 10019
91. V. Novoderezhkin, A. Marin, and R. van Grondelle Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield-Förster picture Phys. Chem. Chem. Phys. 13 2011 17093 17103
92. G. Raszewski, W. Saenger, and T. Renger Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor Biophys. J. 88 2005 986 998
93. J. Pieper, R. Schödel, K.D. Irrgang, J. Voigt, and G. Renger Electron-phonon coupling in solubilized LHC II complexes of green plants investigated by line-narrowing and temperature-dependent fluorescence spectroscopy J. Phys. Chem. B 105 2001 7115 7124
94. G. Zucchelli, P. Dainese, R.C. Jennings, J. Breton, F.M. Garlaschi, and R. Bassi Gaussian decomposition of absorption and linear dichroism spectra of outer antenna complexes of photosystem II Biochemistry 33 1994 8982 8990
95. G. Zucchelli, F.M. Garlaschi, and R.C. Jennings Thermal broadening analysis of the light harvesting complex II absorption spectrum Biochemistry 35 1996 16247 16254
96. E.W. Thulstrup, and J. Michl A critical comparison of methods for analysis of linear dichroism of solutes in stretched polymers J. Phys. Chem. 84 1980 82 93
97. E.W. Thulstrup, and J. Michl Orientation and linear dichroism of symmetrical aromatic molecules imbedded in stretched polyethylene J. Am. Chem. Soc. 104 1982 5594 5604
98. S. Fujiwara, K. Kikuchi, and H. Kokubun Solute orientation in stretched polymer J. Phys. Chem. 88 1984 5482 5486
99. S. Georgakopoulou, G. van der Zwan, R. Bassi, R. van Grondelle, H. van Amerongen, and R. Croce Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization Biochemistry 46 2007 4745 4754
100. C. Ilioaia, M.P. Johnson, P.N. Liao, A.A. Pascal, R. van Grondelle, P.J. Walla, A.V. Ruban, and B. Robert Photoprotection in plants involves a change in lutein 1 binding domain in the major light-harvesting complex of photosystem II J. Biol. Chem. 286 2011 27247 27254
101. C. Ilioaia, M.P. Johnson, C.D. Duffy, A.A. Pascal, R. van Grondelle, B. Robert, and A.V. Ruban Origin of absorption changes associated with photoprotective energy dissipation in the absence of zeaxanthin J. Biol. Chem. 286 2011 91 98
102. A.V. Ruban, P. Horton, and B. Robert 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
103. C. Ilioaia, M.P. Johnson, P. Horton, and A.V. Ruban 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
104. P. Gast, P.W. Hemelrijk, H.J. van Gorkom, and A.J. Hoff The association of different detergents with the photosynthetic reaction center protein of Rhodobacter sphaeroides R26 and the effects on its photochemistry Eur. J. Biochem. 239 1996 805 809
105. F. Müh, J. Rautter, and W. Lubitz Effects of zwitterionic detergents on the primary donor of bacterial reaction centers Ber. Bunsen Ges. Phys. Chem. 100 1996 1974 1977
106. F. Müh, and A. Zouni Micelle formation in the presence of photosystem I Biochim. Biophys. Acta 1778 2008 2298 2307
107. A. Dreuw, P.H.P. Harbach, J.M. Mewes, and M. Wormit Quantum chemical excited state calculations on pigment-protein complexes require thorough geometry re-optimization of experimental crystal structures Theor. Chem. Acc. 125 2010 419 426
108. V. Barzda, E.J.G. Peterman, R. van Grondelle, and H. van Amerongen The influence of aggregation on triplet formation in light-harvesting chlorophyll a/b pigment-protein complex II of green plants Biochemistry 37 1998 546 551
109. S.S. Lampoura, V. Barzda, G.M. Owen, A.J. Hoff, and H. van Amerongen Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII Biochemistry 41 2002 9139 9144
110. H. Lokstein, A. Betke, M. Krikunova, K. Teuchner, and B. Voigt Elucidation of structure-function relationships in plant major light-harvesting complex (LHC II) by nonlinear spectroscopy Photosynth. Res. 2011 10.1007/s11120-011-9700-y
111. E.J.G. Peterman, F.M. Dukker, R. van Grondelle, and H. van Amerongen Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants Biophys. J. 69 1995 2670 2678
112. M. Di Valentin, F. Biasibetti, S. Ceola, and D. Carbonera Identification of the sites of chlorophyll triplet quenching in relation to the structure of LHC-II from higher plants. Evidence from EPR spectroscopy J. Phys. Chem. B 113 2009 13071 13078
113. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38