Dissipative pathways in the photosystem-II antenna in plants

Journal of Photochemistry and Photobiology B: Biology

Volumn 152, Issue , 2015, Pages 215-226

  Duffy, Christopher D P ^a   Ruban, Alexander V ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Chlorophyll; Energy transfer; Light harvesting; Non photochemical fluorescence quenching; Photosystem II; Xanthophylls

Indexed keywords

PROTEIN; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II;

ANTENNA; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; LIGHT INTENSITY; MACHINE; NONHUMAN; PHOTOSYSTEM II; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; STOICHIOMETRY; CHEMISTRY; ENZYMOLOGY; METABOLISM; PLANT;

ENERGY TRANSFER; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS;

EID: 84947781135     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2015.09.011     Document Type: Review

References (138)

1. G.R. Fleming, G.S. Schlau-Cohen, K. Amarnath, and J. Zaks Design principles of photosynthetic light-harvesting Faraday Discuss. 155 2012 27 41
2. A.V. Ruban, M.P. Johnson, and C.D.P. Duffy The photoprotective molecular switch in the photosystem II antenna Biochim. Biophys. Acta Bioenerg. 1817 2012 167 181
3. C.D.P. Duffy, L. Valkunas, and A.V. Ruban Light-harvesting processes in the dynamic photosynthetic antenna Phys. Chem. Chem. Phys. 15 2013 18752 18770
4. B. Demmig-Adams, J.J. Stewart, T.A. Burch, and W.W. Adams III Insights from placing photosynthetic light-harvesting into context J. Phys. Chem. Lett. 5 2014 2880 2889
5. B. Demmig-Adams, C.M. Cohu, O. Muller, and W. Adams III Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons Photosynth. Res. 113 2012 75 88
6. S.B. Powles Photoinhibition of photosynthesis induced by visible light Ann. Rev. Plant Physiol. 35 1984 15 44
7. I. Ohad, D.J. Kyle, and C.J. Arntzen Membrane-protein damage and repair - removal and replacement of inactivated 32-kiladalton polypeptides in chloroplast membranes J. Cell Biol. 99 1984 481 485
8. W.W. Adams III, O. Muller, C.M. Cohu, and B. Demmig-Adams May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth. Res. 117 2013 31 44
9. C.A. Wraight, and A.R. Crofts Energy-dependent quenching of chlorophyll a fluorescence in isolated chloroplasts Eur. J. Biochem. 17 1970 319 327
10. J.M. Briantais, C. Vemotte, M. Picaud, and G.H. Krause A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts Biochim. Biophys. Acta 548 1979 128 138
11. E. Weis, and J.A. Berry Quantum efficiency of photosystem-II in relation to energy-dependent quenching of chlorophyll fluorescence Biochim. Biophys. Acta 894 1987 198 208
12. M.A. Ware, E. Belgio, and A.V. Ruban Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities Photosynth. Res. 2015 10.1007/s11120-015-0102-4
13. G.H. Krause, and U. Behrend ΔpH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts FEBS Lett. 200 1986 298 302
14. G.H. Krause, H. Laasch, and E. Weis Regulation of thermal dissipation of absorbed light energy in chloroplasts indicated by energy dependent fluorescence quenching Plant Physiol. Biochem. 26 1988 445 452
15. G. Noctor, D. Rees, A. Young, and P. Horton The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts Biochim. Biophys. Acta 1057 1991 320 330
16. G. Noctor, A.V. Ruban, and P. Horton Interactions between the effects of potentiators and antagonists of Delta pH-dependent thermal dissipation of excitation energy in spinach thylakoids Biochim Biophys. Acta 1183 1993 339 344
17. H.Y. Yamamoto, and L. Kamite The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500 nm region Biochim. Biophys. Acta 267 1972 538 543
18. H.Y. Yamamoto Biochemistry of the violaxanthin cycle in higher plants Pure Appl. Chem. 51 1979 639 648
19. B. Demmig-Adams Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin Biochim. Biophys. Acta 1020 1990 1 24
20. P. Horton, A.V. Ruban, and M. Wentworth Allosteric regulation of the light harvesting system of photosystem II (review) Phil. Trans. R. Soc. Lond. B 355 2000 1361 1370
21. B. Demmig, K. Winter, A. Kruger, and F.C. Czygan Photoinhibition and zeaxanthin formation in intact leaves: a possible role of the xanthophyll cycle in the dissipation of excess light Plant Physiol. 84 1987 218 224
22. B. Demmig-Adams, K. Winter, A. Kruger, and F.-Z. Czygan Zeaxanthin synthesis, energy dissipation, and photoprotection of photosystem II at chilling temperatures Plant Physiol. 90 1989 894 898
23. B. Demmig-Adams, K. Winter, A. Krüger, and F.-C. Czygan Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves Plant Physiol. 90 1989 881 886
24. H.A. Frank, and R.J. Cogdell Carotenoids in photosynthesis Photochem. Photobiol. 63 1996 257 264
25. A.V. Ruban, and P. Horton The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach Plant Physiol. 119 1999 531 542
26. A.V. Ruban, D. Phillip, A.J. Young, and P. Horton Excited-state energy level does not determine the differential effect of violaxanthin and zeaxanthin on chlorophyll fluorescence quenching in the isolated light-harvesting complex of photosystem II Photochem. Photobiol. 68 1998 829 834
27. M.P. Johnson, M.L. Perez-Bueno, A. Zia, P. Horton, and A.V. Ruban 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 2009 1061 1075
28. X.P. Li, O. Björkman, C. Shih, and A.R. Grossman A pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 403 2000 391 395
29. A. Kiss, A.V. Ruban, and P. Horton The PsbS protein controls the organisation of the photosystem II antenna in higher plant thylakoid membranes J. Biol. Chem. 283 2008 3972 3978
30. C. Funk, I. Adamska, B.R. Green, B. Andersson, and G. Renger The nuclear-encoded chlorophyll-binding Photosystem-II-S protein is stable in the absence of pigments J. Biol. Chem. 270 1995 30141 30147
31. P. Dominici, S. Caffarri, F. Armenante, S. Ceoldo, M. Crimi, and R. Bassi Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant J. Biol. Chem. 277 2002 22750 22758
32. M. Aspinall-O'Dea, M. Wentworth, A.A. Pascal, B. Robert, A.V. Ruban, and P. Horton 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
33. X.P. Li, A.M. Gilmore, S. Caffarri, R. Bassi, T. Golan, D. Kramer, and K.K. Niyogi Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein J. Biol. Chem. 279 2004 22866 22874
34. S. Crouchman, A.V. Ruban, and P. Horton PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin FEBS Lett. 580 2006 2053 2058
35. G. Bonente, B.D. Howes, S. Caffarri, G. Smulevich, and R. Bassi Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro J. Biol. Chem. 283 2008 8434 8445
36. A. Zia, M.P. Johnson, and A.V. Ruban Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana Planta 233 2011 1253 1264
37. S. Kereïche, A.Z. Kiss, R. Kouril, E.J. Boekema, and P. Horton The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts FEBS Lett. 584 2010 754 764
38. K. Oxborough, and P. Horton A study of the regulation and function of energy-dependent quenching in pea-chloroplasts Biochim. Biophys. Acta 934 1988 135 143
39. P. Horton, and A.V. Ruban Regulation of photosystem II (review) Photosynth. Res. 34 1992 375 385
40. G.H. Krause Changes in chlorophyll fluorescence in relation to light-dependent cation transfer across thylakoid membranes Biochim. Biophys. Acta 333 1974 301 313
41. A.V. Ruban, R.G. Walters, and P. Horton The molecular mechanism of the control of excitation energy dissipation in chloroplast membranes: inhibition of ΔpH-dependent quenching of chlorophyll fluorescence by dicyclohexylcarbodiimide FEBS Lett. 309 1992 175 179
42. R.G. Walters, A.V. Ruban, and P. Horton Light-harvesting complexes bound by dicyclohexylcarbodiimide during inhibition of protective energy dissipation Eur. J. Biochem. 226 1994 1063 1069
43. R.G. Walters, A.V. Ruban, and P. Horton Identification of proton-active residues in a higher plant light-harvesting complex Proc. Natl. Acad. Sci. U. S. A. 93 1996 14204 14209
44. E.K. Zolotareva, V.V. Podorvanov, A.F. Tereshchenko, A.V. Ruban, and P. Horton Energy-dependent tritium incorporation into LHCII proteins of chloroplasts Dokl. Acad. Sci. Ukr. SSR B 11 1999 152 156
45. A.V. Ruban, and P. Horton Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes I: spectroscopic analysis of isolated light-harvesting complexes Biochim. Biophys. Acta 1102 1992 30 38
46. A.V. Ruban, D. Rees, A.A. Pascal, and P. Horton Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes II: the relationships between LHCII aggregation in vitro and qE in isolated thylakoids Biochim. Biophys. Acta 1102 1992 39 44
47. A.V. Ruban, A.J. Young, and P. Horton 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 Biochem. 35 1996 674 678
48. D. Phillip, A.V. Ruban, P. Horton, A. Asato, and A.J. Young Quenching of chlorophyll fluorescence in the major light-harvesting complex of photosystem II: a systematic study of the effect of carotenoid structure Proc. Natl. Acad. Sci. U. S. A. 93 1996 1492 1497
49. A.V. Ruban, F. Calkoen, S.L.S. Kwa, R. van Grondelle, P. Horton, and J.P. Dekker Characterisation of the aggregated state of the light harvesting complex of photosystem II by linear and circular dichroism spectroscopy Biochim. Biophys. Acta 1321 1997 61 70
50. Z. Liu, H. Yan, K. Wang, T. Kuang, J. Zhang, L. Gui, X. An, and W. Chang Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 2004 287 292
51. A.A. Pascal, L. Zhenfeng, K. Broess, B. van Oort, H. van Amerongen, C. Wang, P. Horton, B. Robert, W. Chang, and A.V. Ruban Molecular basis for photoprotection and control of photosynthetic light-harvesting Nature 436 2005 134 137
52. R.C. Jennings, F.M. Garlaschi, and G. Zucchelli Light-induced fluorescence quenching in the light-harvesting chlorophyll a/b protein complex Photosynth. Res. 1991 57 64
53. B. van Oort, A. van Hoek, A.V. Ruban, and H. van Amerongen The equilibrium between quenched and non-quenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence J. Phys. Chem. B 111 2007 7631 7637
54. S. Santabarbara, P. Horton, and A.V. Ruban Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex II Biophys. J. 97 2009 1188 1197
55. 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
56. T.P.J. Krüger, C. Ilioaia, L. Valkunas, and R. van Grondelle Fluorescence intermittency from the main plant light-harvesting complex: sensitivity to the local environment J. Phys. Chem. B 115 2011 5083 5095
57. T.P.J. Krüger, E. Wientjes, R. Croce, and R. van Grondelle Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes Proc. Natl. Acad. Sci. U. S. A. 108 2011 13516 13521
58. T.P.J. Krüger, C. Ilioaia, M.P. Johnson, A.V. Ruban, E. Papagiannakis, P. Horton, and R. van Grondelle Controlled disorder in plant light-harvesting complex II explains its photoprotective role Biophys. J. 102 2012 2669 2676
59. L. Valkunas, J. Chmeliov, T.P.J. Krüger, C. Ilioaia, and R. van Grondelle How photosynthetic proteins switch J. Phys. Chem. Lett. 3 2012 2779 2784
60. T. Barros, A. Royant, J. Standfuss, A. Dreuw, and W. Kuhlbrandt Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state EMBO J. 28 2009 298 306
61. A.V. Ruban, R. Berera, C. Ilioaia, I.H. van Stokkum, J.T. 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
62. B. Robert, P. Horton, A.A. Pascal, and A.V. Ruban Insights into the molecular dynamics of plant light-harvesting proteins in vivo Trends Plant Sci. 9 2004 385 390
63. 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 Biochem. 37 1998 546 551
64. 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 xanthophyll in LHCII Biochem. 41 2002 9139 9144
65. A. Pandit, T. Morosinotto, M. Reus, A.R. Holzwarth, R. Bassi, and H.J.M. de Groot First solid-state NMR analysis of uniformly (13)C-enriched major light-harvesting complexes from Chlamydomonas reinhardtii and identification of protein and cofactor spin clusters Biochim. Biophys. Acta Bioenerg. 1807 2011 437 443
66. A. Pandit, M. Reus, T. Morosinotto, R. Bassi, A.R. Holzwarth, and H.J.M. de Groot An NMR comparison of the light-harvesting complex II (LHCII) in active and photoprotective states reveals subtle changes in the chlorophyll a ground-state electronic structures Biochim. Biophys. Acta Bioenerg. 1827 2013 738 744
67. C.D.P. Duffy, A.P. Pandit, and A.V. Ruban Modelling the NMR Signatures associated with the functional conformational switch in the major light-harvesting antenna of photosystem II in higher plants PCCP 16 2014 5571 5580
68. M. Mozzo, F. Passarini, R. Bassi, H. van Amerongen, and R. Croce Photoprotection in higher plants: the putative quenching site is conserved in outer light-harvesting complexes of photosystem II Biochim. Biophys. Acta 1777 2008 1263 1267
69. H.A. Frank, V. Chynwat, R.Z.B. Desamero, R. Farhoosh, J. Erickson, and J. Bautista On the photophysics and photochemical properties of carotenoids and their role as light-harvesting pigments in photosynthesis Pure Appl. Chem. 69 1997 2117 2124
70. V. Chynwat, and H. Frank The application of the energy gap law to the S1 energies and dynamics of carotenoids Chem. Phys. 194 1995 237 244
71. R. Engleman, and J. Jortner The energy gap law for radiationless transitions in large molecules Mol. Phys. 18 1970 145 164
72. H.A. Frank, J.A. Bautista, J.S. Josue, and A.J. Young Mechanism of nonphotochemical quenching in green plants. Energies of the lowest excited singlet state of zeaxanthin and violaxanthin Biochem. 39 2000 2831 2837
73. T. Polivka, J.H. Herek, D. Zigmantas, H.E. Akerlund, and V. Sundstrom Direct observation of the (forbidden) S1 state in carotenoids Proc. Natl. Acad. Sci. U. S. A. 96 1999 4914 4917
74. T. Polivka, D. Zigmantas, V. Sundstrom, E. Formaggio, G. Cinque, and R. Bassi Carotenoid S(1) state in a recombinant light-harvesting complex of photosystem II Biochem. 41 2002 439 450
75. A. Dreuw Influence of geometry relaxation on the energies of the S1 and S2 states of violaxanthin, zeaxanthin, and lutein J. Phys. Chem. A 110 2006 4592 4599
76. K. Schulten, I. Ohmine, and M. Karplus Correlation effects in the spectra of polyenes J. Chem. Phys. 64 1976 4422 4441
77. J. Chmeliov, W.P. Bricker, C.S. Lo, E. Jouin, L. Valkunas, A.V. Ruban, and C.D.P. Duffy An 'all pigment' model of excitation quenching in LHCII Phys. Chem. Chem. Phys. 17 2015 15857 15867
78. 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
79. T.J. Avenson, T.K. Ahn, D. Zigmantas, K.K. Niyogi, Z. Li, M. Ballotari, R. Bassi, and G.R. Fleming Zeaxanthin radical cation formation in minor light harvesting complexes of higher plant antenna J. Biol. Chem. 283 2008 3550 3558
80. S. Amarie, J. Standfuss, T. Barros, W. Kühlbrandt, A. Dreuw, and J. Wachtveitl Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis J. Phys. Chem. B 111 2007 3481 3487
81. A.S. Davydov The theory of molecular excitons Sov. Phys. Usp. 82 1964 145 178
82. A. Dreuw, G. Fleming, and M. Head-Gordon Role of electron-transfer quenching of chlorophyll fluorescence by carotenoids in non-photochemical quenching of green plants Biochem. Soc. Trans. 33 2005 858 862
83. T.J. Avenson, T.K. Ahn, K.K. Niyogi, M. Ballotarri, R. Bassi, and G. Fleming Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex J. Biol. Chem. 284 2009 2830 2835
84. Z. Li, T.K. Ahn, T.J. Avenson, M. Ballotarri, J.A. Cruz, D.M. Kramer, R. Bassi, G. Fleming, J.D. Keasling, and K.K. Niyogi Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant Plant Cell 21 2009 1798 1812
85. C.D.P. Duffy, J. Chmeliov, M. Macernis, J. Sulskus, L. Valkunas, and A.V. Ruban Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII J. Phys. Chem. B 117 2013 10974 10986
86. V.I. Novoderezhkin, M.A. Palacios, H. van Amerongen, and R. van Grondelle Exciton dynamics in the LHCII complex of higher plants: modelling based on the 2.72 Angstrom crystal structure J. Phys. Chem. B 109 2005 10493 10504
87. V.I. Novoderezhkin, and R. van Grondelle Physical origins and models of energy transfer in photosynthetic light-harvesting Phys. Chem. 12 2010 7352 7365
88. 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
89. F. Müh, M.E. Madjet, and T. Renger Structure-based identification of energy sinks in plant light-harvesting complex II J. Phys. Chem. B 114 2010 13517 13535
90. F. Müh, and T. Renger Refined structure-based simulation of plant light-harvesting complex II: linear optical spectra of trimers and aggregates Biochim. Biophys. Acta 1817 2012 1446 1460
91. H. Staleva, J. Komenda, M.K. Shukla, V. Šlouf, R. Kaňa, T. Polívka, and R. Sobotka Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins Nat. Chem. Biol. 11 2015 287 291
92. P.N. Liao, S. Bode, L. Wilk, N. Hafi, and P.J. Walla Correlation of electronic carotenoid-chlorophyll interactions and fluorescence quenching with the aggregation of native LHCII and chlorophyll deficient mutants Chem. Phys. 373 2010 50 55
93. C.-P. Holleboom, and P.J. Walla The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting Photosynth. Res. 119 2014 215 221
94. P.N. Liao, C.P. Holleboom, L. Wilk, W. Kühlbrandt, and P.J. Walla Correlation of Car S1 → Chl with Chl → Car S1 energy transfer supports the excitonic model in quenched light harvesting complex II J. Phys. Chem. B 114 2010 15650 15655
95. C.-P. Holleboom, D.A. Gacek, P.-N. Liao, M. Negretti, R. Croce, and P.J. Walla Carotenoid-chlorophyll coupling and fluorescence quenching in aggregated minor PSII proteins CP24 and CP29 Photosynth. Res. 124 2015 171 180
96. 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. 111 2011 227 235
97. M. Krikunova, A. Kummrow, B. Voigt, M. Rini, H. Lokstein, A. Moskalenko, H. Scheer, A. Razjivin, and D. Leupold Fluorescence of native and carotenoid-depleted LH2 from Chromatium minutissimum, originating from simultaneous two-photon absorption in the spectral range of the presumed (optically "dark") S1 state of carotenoids FEBS Lett. 528 2002 227 229
98. I. Stepanenko, V. Kompanetz, Z. Makhneva, S. Chekalin, A. Moskalenko, and A. Razjivin Two-photon excitation spectroscopy of carotenoid-containing and carotenoid-depleted LH2 complexes of purple bacteria J. Phys. Chem. B 113 2009 11720 11723
99. B. van Oort, R. van Grondelle, and I.H.M. van Stokkum A hidden state in light-harvesting complex II revealed by multipulse spectroscopy J. Phys. Chem. B 119 2015 5184 5193
100. 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 Chem. Phys. Chem. 11 2010 1289 1296
101. 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
102. A.R. Holzwarth, Y. Miloslavina, M. Nilkens, and P. Jahns Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence Chem. Phys. Lett. 483 2009 262 267
103. A.R. Holzwarth, M.G. Muller, M. Reus, M. Nowaczyk, J. Sander, and M. Rogner Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor Proc. Natl. Acad. Sci. U. S. A. 103 2006 6895 6900
104. Y. Miloslavina, M. Szczepaniak, M.G. Muller, J. Sander, M. Nowaczyk, M. Rogner, and A.R. Holzwarth Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study Biochem. 45 2006 2436 2442
105. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 2005 1040 1044
106. K. Broess, G. Trinkunas, A. van Hoek, R. Croce, and H. van Amerongen Determination of the excitation migration time in photosystem II - consequences for the membrane organization and charge separation parameters Biochim. Biophys. Acta Bioenerg. 1777 2008 404 409
107. J.L. Hughes, E. Krausz, P.J. Smith, R.J. Pace, and H. Riesen Probing the lowest energy chlorophyll a states of Photosystem II via selective spectroscopy: new insights on P680 Photosynth. Res. 84 2005 93 98
108. G. Renger, and T. Renger Photosystem II: the machinery of photosynthetic water splitting Photosynth. Res. 98 2008 53 80
109. G. Renger The light reactions of photosynthesis Curr. Biol. 98 2010 1305 1320
110. E. Belgio, M.P. Johnson, S. Jurić, and A.V. Ruban Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime - both the maximum and the nonphotochemically quenched Biophys. J. 102 2012 2761 2771
111. A.G. Ivanov, P.V. Sane, V. Hurry, G. Öquist, and N.P.A. Huner Photosystem II reaction centre quenching: mechanisms and physiological role Photosynth. Res. 98 2008 565 574
112. M. Mamedov, Govindjee V. Nadtochenko, and A. Semenov Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms Photosynth. Res. 125 2015 51 63
113. E. Belgio, E. Kapitonova, J. Chmeliov, C.D.P. Duffy, P. Ungerer, L. Valkunas, and A.V. Ruban Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps Nat. Commun. 4433 2014 10.1038/ncomms5433
114. M. Wahadoszamen, R. Berera, A.M. Aro, E. Romero, and R. van Grondelle Identification of two emitting sites in the dissipative state of the major light harvesting antenna Phys. Chem. Chem. Phys. 14 2012 759 766
115. M. Wahadoszamen, A. Ghazaryan, H.E. Cingil, A.M. Aro, C. Büchel, R. van Grondelle, and R. Berera Stark fluorescence spectroscopy reveals two emitting sites in the dissipative state of FCP antennas Biochim. Biophys. Acta Bioenerg. 1837 2014 193 200
116. G.S. Schlau-Cohen, H.-Y. Yang, T.P.J. Krüger, P. Xu, M. Gwizdala, R. van Grondelle, R. Croce, and W.E. Moerner Single-molecule identification of quenched and unquenched states of LHCII J. Phys. Chem. Lett. 6 2015 860 867
117. P. Jahns, and H.W. Trissl Indications for a dimeric organization of the antenna-depleted reaction center core of photosystem II in thylakoids of intermittent light grown pea plants Biochim. Biophys. Acta 1318 1997 1 5
118. E.J. Boekema, H. van Roon, F. Calkoen, R. Bassi, and J.P. Dekker Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes Biochem. 38 1999 2233 2239
119. A.E. Yakushevska, P.E. Jensen, W. Keegstra, H. van Roon, H.V. Scheller, E.J. Boekema, and J.P. Dekker Supermolecular organization of photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana Eur. J. Biochem. 268 2001 6020 6028
120. J.P. Dekker, and E.J. Boekema Supramolecular organization of thylakoid membrane proteins in green plants Biochim. Biophys. Acta 1706 2005 12 39
121. E.J. Boekema, J.F.L. van Breemen, H. van Roon, and J.P. Dekker Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membranes of green plants J. Mol. Biol. 301 2000 1123 1133
122. M.P. Johnson, T.K. Goral, C.D.P. Duffy, A.P.R. 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
123. A.R. Schneider, and P.L. Geissler Coarse-grained computer simulations of dynamics in thylakoid membranes: methods and opportunities Front. Plant Sci. 4 2014 1 6
124. R. Kouril, G.T. Oostergetel, and E.J. Boekema Fine structure of granal thylakoid membrane organization using cryo-electron tomography Biochim. Biophys. Acta 1807 2011 368 374
125. K. Broess, G. Trinkunas, C.D. van der Weij-de Wit, J.P. Dekker, A. van Hoek, and H. van Amerongen Excitation energy transfer and charge separation in photosystem II membranes revisited Biophys. 91 2006 3776 3786
126. L. Valkunas, G. Trinkunas, J. Chmeliov, and A.V. Ruban Modelling of exciton quenching in photosystem II Phys. Chem. Chem. Phys. 11 2009 7576 7584
127. D.I.G. Bennett, K. Amarnath, and G.R. Fleming A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes J. Am. Chem. Soc. 135 2013 9164 9173
128. U. Schreiber, U. Schliwa, and W. Bilger Continuous recording of photochemical and non-photochemical chlorophyll quenching with a new type of modulation fluorometer Photosynth. Res. 10 1986 51 62
129. L. Valkunas, V. Cervinskas, and F. van Mourik Energy transfer and connectivity in chloroplasts: competition between trapping and annihilation in pulsed fluorescence induction experiments J. Phys. Chem. B 101 1997 7327 7331
130. J. Lavorel, and P. Joliot A connected model of the photosynthetic unit Biophys. J. 12 1972 815 831
131. G. Paillotin Movement of excitations in the photosynthetic domains of photosystem II J. Theory. Biol. 58 1976 237 252
132. L. Valkunas, N.E. Geacintov, L. France, and J. Bretont The dependence of the shapes of fluorescence induction curves in chloroplasts on the duration of illumination pulses Biophys. J. 59 1991 397 408
133. D.M. Kramer, G. Johnson, O. Kiirats, and G.E. Edwards New fluorescence parameters for determination of QA redox state and excitation energy fluxes Photosynth. Res. 79 2004 209 218
134. N.R. Baker Chlorophyll fluorescence: a probe of photosynthesis in vivo Annul. Rev. Plant Biol. 59 2008 89 113
135. A. Melis, G.E. Guenthery, P.J. Morrissey, and M.L. Ghirardi Photosystem II heterogeneity in chloroplasts from applications of chlorophyll fluorescence H.K. Lichtenthaler, Applications of Chlorophyll Fluorescence in Photosynthesis Research, Stress Physiology, Hydrobiology and Remote Sensing 1988 Kluwer Academic Publishers 33 43
136. T.K. Goral, M.P. Johnson, C.D.P. Duffy, A.P.R. Brain, A.V. Ruban, and C.W. Mullineaux Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J. 69 2012 289 301
137. S. Malkin, P.A. Armond, and D.C. Fork Photosystem II photosynthetic unit sizes from fluorescence induction in leaves: correlation to photosynthetic capacity Plant Physiol. 67 1981 570 579
138. B. Demmig-Adams, O. Muller, J.J. Stewart, C.M. Cohu, and W.W. Adams III Chloroplast thylakoid structure in evergreen leaves employing strong thermal energy dissipation J. Photochem. Photobiol. B March 26 2015 10.1016/j.jphotobiol.2015.03.014 (available online)