The Function of PsbS Protein in Plant Photosynthesis Regulation
Main Article Content
Abstract
Abstract: Photosynthesis transforms sun light energy into chemical energy of organic compounds, which sustain almost all life on the planet. In high light conditions, the energy absorbed that excess their photosynthesis capacity can be formed ROS (Reactive Oxygen Species) that are very dangerous for plant. To prevent ROS and plant photoprotection, the plant develop a mechanism which harmlessly dissipate excess light energy absorbed as heat called NPQ (Non Photochemical Quenching). In this paper, we review the researches of PsbS protein of photosystem II which is known have a key role in the NPQ activation. The NPQ capacity is correlate to PsbS level in plant leaf. The protein PsbS is as sensor of lumenal pH for NPQ activation. It is also proposed reorganisation control of grana membrane in high light condition. This protein maybe is not bound pigments, but it is related to zeaxanthin for complete NPQ activation. So PsbS has the important role for resistance of plant to high light. The investigation of PsbS protein could open the photosynthesis light harvesting regulation perspective for improve plant productivity.
Keywords: Light, NPQ, photosynthesis, PsbS protein, ROS.
References
[1] K.K. Niyogi, Photoprotection revisited: Genetic and molecular approaches, Annu.Rev.Plant Physiol.Plant Mol.Biol. 50 (1999) 333.
[2] Z. Li, S. Wakao, B.B. Fischer, K.K. Niyogi, Sensing and responding to excess light, Annu Rev Plant Biol 60 (2009) 239.
[3] P.A. Davis, R.P. Hangarter, Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves, Photosynth Res (2012).
[4] C.A. Wraight, A.R. Crofts, Energy-dependent quenching of chlorophyll alpha fluorescence in isolated chloroplasts, Eur J Biochem 17 (1970) 319.
[5] G.H. Krause, C. Vernotte, J.M. Briantais, Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae, Biochim.Biophys.Acta 679 (1982) 116.
[6] P. Muller, X.P. Li, K.K. Niyogi, Non-photochemical quenching. A response to excess light energy, Plant Physiol 125 (2001) 1558.
[7] P. Horton, A.V. Ruban, Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection, J.Exp.Bot. 56 (2005) 365.
[8] C. Funk, I. Adamska, B.R. Green, B. Andersson, G. Renger, The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments, J.Biol.Chem. 270 (1995) 30141.
[9] X.P. Li, O. Bjorkman, C. Shih, A.R. Grossman, M. Rosenquist, S. Jansson, K.K. Niyogi, A pigment-binding protein essential for regulation of photosynthetic light harvesting, Nature 403 (2000) 391.
[10] X.P. Li, P. Muller-Moule, A.M. Gilmore, K.K. Niyogi, PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition, Proc Natl Acad Sci U S A 99 (2002) 15222.
[11] X.P. Li, A.M. Gilmore, S. Caffarri, R. Bassi, T. Golan, D. Kramer, K.K. Niyogi, Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein, J Biol Chem 279 (2004) 22866.
[12] U. Ljungberg, H.E. Akerlund, B. Andersson, Isolation and characterization of the 10-kDa and 22-kDa polypeptides of higher plant photosystem 2, Eur J Biochem 158 (1986) 477.
[13] S. Kim, E. Pichersky, C.F. Yocum, Topological studies of spinach 22 kDa protein of Photosystem II, Biochim Biophys Acta 1188 (1994) 339.
[14] T. Golan, P. Muller-Moule, K.K. Niyogi, Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants, Plant Cell Environ 29 (2006) 879.
[15] L. Kalituho, T. Grasses, M. Graf, J. Rech, P. Jahns, Characterization of a nonphotochemical quenching-deficient Arabidopsis mutant possessing an intact PsbS protein, xanthophyll cycle and lumen acidification, Planta 223 (2006) 532.
[16] S. Kereiche, A.Z. Kiss, R. Kouril, E.J. Boekema, 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) 759.
[17] M.P. Johnson, A.V. Ruban, Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation, Plant J 61 (2010) 283.
[18] S. Hubbart, O.O. Ajigboye, P. Horton, E.H. Murchie, The photoprotective protein PsbS exerts control over CO(2) assimilation rate in fluctuating light in rice, Plant Journal 71 (2012) 402.
[19] M.P. Johnson, A.V. Ruban, Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced DeltapH, J Biol Chem 286 (2011) 19973.
[20] G. Bonente, B.D. Howes, S. Caffarri, G. Smulevich, R. Bassi, Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro, J Biol Chem 283 (2008) 8434.
[21] G. Bonente, M. Ballottari, T.B. Truong, T. Morosinotto, T.K. Ahn, G.R. Fleming, K.K. Niyogi, R. Bassi, Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii, PLoS Biol 9 (2011) e1000577.
[22] A.Z. Kiss, A.V. Ruban, P. Horton, The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes, Journal of Biological Chemistry 283 (2008) 3972.
[23] I. Kasajima, K. Ebana, T. Yamamoto, K. Takahara, M. Yano, M. Kawai-Yamada, H. Uchimiya, Molecular distinction in genetic regulation of nonphotochemical quenching in rice, Proc Natl Acad Sci U S A 108 (2011) 13835.
[24] A.V. Ruban, E.H. Murchie, Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: A new approach, Biochim Biophys Acta 1817 (2012) 977.
[25] G.H. Krause, E. Weis, Chlorophyll fluorescence and photosynthesis: The basics, Ann.Rev.Plant Physiol. 42 (1991) 313.
[26] P. Horton, A.V. Ruban, R.G. Walters, Regulation of Light harvesting in Green Plants, Annu.Rev.Plant Physiol.Plant Mol.Biol. 47 (1996) 655.
[27] L. Dall'Osto, S. Caffarri, R. Bassi, A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26, Plant Cell 17 (2005) 1217.
[28] M. Nilkens, E. Kress, P. Lambrev, Y. Miloslavina, M. Muller, A.R. Holzwarth, P. Jahns, Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis, Biochim Biophys Acta 1797 (2010) 466.
[29] C. Wilhelm, D. Selmar, Energy dissipation is an essential mechanism to sustain the viability of plants: The physiological limits of improved photosynthesis, J Plant Physiol 168 (2011) 79.
[30] A.V. Ruban, M.P. Johnson, C.D. Duffy, The photoprotective molecular switch in the photosystem II antenna, Biochim Biophys Acta 1817 (2012) 167.
[31] N.E. Holt, D. Zigmantas, L. Valkunas, X.P. Li, K.K. Niyogi, G.R. Fleming, Carotenoid cation formation and the regulation of photosynthetic light harvesting, Science 307 (2005) 433.
[32] 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, R. van Grondelle, Identification of a mechanism of photoprotective energy dissipation in higher plants, Nature 450 (2007) 575.
[33] S. Bode, C.C. Quentmeier, P.N. Liao, N. Hafi, T. Barros, L. Wilk, F. Bittner, 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.
[34] A.R. Holzwarth, Y. Miloslavina, M. Nilkensb, P. Jahnsb, Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence, Chemical Physics Letters 483 (2009) 262.
[35] E. Bergantino, A. Segalla, A. Brunetta, E. Teardo, F. Rigoni, G.M. Giacometti, I. Szabo, Light- and pH-dependent structural changes in the PsbS subunit of photosystem II, Proc Natl Acad Sci U S A 100 (2003) 15265.
[36] S. Kim, P. Sandusky, N.R. Bowlby, R. Aebersold, B.R. Green, S. Vlahakis, C.F. Yocum, E. Pichersky, Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II, FEBS Lett 314 (1992) 67.
[37] T. Iwasaki, Y. Saito, E. Harada, M. Kasai, K. Shoji, M. Miyao, N. Yamamoto, Cloning of cDNA encoding the rice 22 kDa protein of Photosystem II (PSII-S) and analysis of light-induced expression of the gene, Gene 185 (1997) 223.
[38] M. Wallbraun, S. Kim, B.R. Creen, B. Piechulla, E. Pichersky, Nucleotide Sequence of a Tomato psbS Gene, Plant Physiol Biochem 106 (1994 ) 1703.
[39] R. Harrer, R. Bassi, M.G. Testi, C. Sch„fer, Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L.(liverwort), which contains reaction center and antenna proteins, Eur.J.Biochem. 255 (1998) 196.
[40] A.D. Heiber, O. Kawabata, H.Y. Yamamoto, Significance of the lipid phase in the dynamics and functions of the xanthophyll cycle as revealed by PsbS overexpression in tobacco, Plant Cell Physiol 45 (2005) 92.
[41] G. Bonente, F. Passarini, S. Cazzaniga, C. Mancone, M.C. Buia, M. Tripodi, R. Bassi, S. Caffarri, The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching, Photochem Photobiol 84 (2008) 1359.
[42] G. Peers, T.B. Truong, E. Ostendorf, A. Busch, D. Elrad, A.R. Grossman, M. Hippler, K.K. Niyogi, An ancient light-harvesting protein is critical for the regulation of algal photosynthesis, Nature 462 (2009) 518.
[43] G. Bonente, S. Pippa, S. Castellano, R. Bassi, M. Ballottari, Acclimation of Chlamydomonas reinhardtii to different growth irradiances, J Biol Chem 287 (2012) 5833.
[44] C. Gerotto, A. Alboresi, G.M. Giacometti, R. Bassi, T. Morosinotto, Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature, Plant Cell Environ 34 (2011) 922.
[45] N. Wedel, R. Klein, U. Ljungberg, B. Andersson, R.G. Herrmann, The single-copy gene psbS codes for a phylogenetically intriguing 22 kDa polypeptide of photosystem II, FEBS Lett 314 (1992) 61.
[46] C. Funk, W.P. Schr”der, B.R. Green, G. Renger, B. Andersson, The Intrinsic 22 kDa Protein Is a Chlorophyll-Binding Subunit of Photosystem II, FEBS Lett. 342 (1994) 261.
[47] P. Dominici, S. Caffarri, F. Armenante, S. Ceoldo, M. Crimi, R. Bassi, Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant, Journal of Biological Chemistry 277 (2002) 22750.
[48] A.V. Ruban, R.G. Walters, P. Horton, The Molecular Mechanism of the Control of Excitation Energy Dissipation in Chloroplast Membranes - Inhibition of DeltapH- Dependent Quenching of Chlorophyll Fluorescence by Dicyclohexylcarbodiimide, FEBS Lett 309 (1992) 175.
[49] X. Li, A. Phippard, J. Pasari, K. Niyogi, Structural-functional analysis of Photosystem II subunit S (PsbS) in vivo, Functional Plant Biology 29 (2002) 1131
[50] E. Bergantino, A. Brunetta, E. Touloupakis, A. Segalla, I. Szabo, G.M. Giacometti, Role of the PSII-H subunit in photoprotection: novel aspects of D1 turnover in Synechocystis 6803, J Biol Chem 278 (2003) 41820.
[51] N. Betterle, M. Ballottari, S. Zorzan, S. de Bianchi, S. Cazzaniga, L. Dall'osto, T. Morosinotto, R. Bassi, Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction, J Biol Chem 284 (2009) 15255.
[52] M.P. Johnson, T.K. Goral, C.D. Duffy, A.P. Brain, C.W. Mullineaux, 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.
[53] D.F. Ghanotakis, C.M. Waggoner, N.R. Bowlby, D.M. Demetriou, G.T. Babcock, C.F. Yocum, Comparative structural and catalytic properties of oxygen- evolving photosystem II preparations, Photosynth.Res. 14 (1987) 191.
[54] E. Thidholm, V. Lindstrom, C. Tissier, C. Robinson, W.P. Schroder, C. Funk, Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer, Febs Letters 513 (2002) 217.
[55] J. Nield, C. Funk, J. Barber, Supermolecular structure of photosystem II and location of the PsbS protein, Philos.Trans.R.Soc.Lond B Biol.Sci. 355 (2000) 1337.
[56] S. Caffarri, R. Kouril, S. Kereiche, E.J. Boekema, R. Croce, Functional architecture of higher plant photosystem II supercomplexes, Embo J 28 (2009) 3052.
[57] E. Teardo, P.P. de Laureto, E. Bergantino, F. Dalla Vecchia, F. Rigoni, D. Szabo, G.M. Giacometti, Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids, Biochimica Et Biophysica Acta-Bioenergetics 1767 (2007) 703.
[58] A.A. Pascal, Z.F. Liu, K. Broess, B. van Oort, H. van Amerongen, C. Wang, P. Horton, B. Robert, W.R. Chang, A. Ruban, Molecular basis of photoprotection and control of photosynthetic light-harvesting, Nature 436 (2005) 134.
[59] P. Horton, M.P. Johnson, M.L. Perez-Bueno, A.Z. Kiss, 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.
[60] Y. Miloslavina, S. de Bianchi, L. Dall'Osto, R. Bassi, A.R. Holzwarth, Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II, J Biol Chem 286 (2011) 36830.
[61] C. Funk, G. Renger, I. Adamska, B. Andersson, P. Schr”der, The PS II-S polypeptide. An atypical CAB protein, From Light to Biophere Vol.I, Kluwer, Dordrecht, 1995, pp. 339-342.
[62] M. Aspinall-O'Dea, M. Wentworth, A. Pascal, B. Robert, A. Ruban, 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.
[63] X.P. Li, A.M. Gilmore, K.K. Niyogi, 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 (2002) 33590.
[64] T. Barros, A. Royant, J. Standfuss, A. Dreuw, W. Kuhlbrandt, Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state, Embo J 28 (2009) 298.
[65] B. Demmig-Adams, Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin, Biochim.Biophys.Acta 1020 (1990) 1.
[66] A.V. Ruban, 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.
[67] R. Bassi, S. Caffarri, Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls, Photosynthesis Research 64 (2000) 243.
[68] S. Crouchman, A. Ruban, P. Horton, PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin, FEBS Lett 580 (2006) 2053.
[69] A. Zia, M.P. Johnson, A.V. Ruban, Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana, Planta 233 (2011).
[70] I.S. Zulfugarov, A. Tovuu, B. Dogsom, C.Y. Lee, C.H. Lee, PsbS-specific zeaxanthin-independent changes in fluorescence emission spectrum as a signature of energy-dependent non-photochemical quenching in higher plants, Photochem Photobiol Sci 9 (2010) 697.
[71] M.P. Johnson, M.L. Perez-Bueno, A. Zia, P. Horton, 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.
[72] P. Jahns, A.R. Holzwarth, The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II, Biochim Biophys Acta 1817 (2012) 182.
[73] K.K. Niyogi, X.P. Li, V. Rosenberg, H.S. Jung, Is PsbS the site of non-photochemical quenching in photosynthesis?, J Exp Bot 56 (2005) 375.
[74] R.G. Walters, A.V. Ruban, P. Horton, Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation, Eur.J.Biochem 226 (1994) 1063.
[75] R.G. Walters, A.V. Ruban, P. Horton, Identification of proton-active residues in a higher plant light- harvesting complex, Proc.Natl.Acad.Sci.USA 93 (1996) 14204.
[76] J. Andersson, R.G. Walters, P. Horton, S. Jansson, Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation Plant Cell 13 (2001) 1193.
[77] S. de Bianchi, L. Dall'Osto, G. Tognon, T. Morosinotto, R. Bassi, 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 (2008) 1012.
[78] L. Kovacs, J. Damkjaer, S. Kereiche, C. Ilioaia, A.V. Ruban, E.J. Boekema, S. Jansson, P. Horton, Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts, Plant Cell 18 (2006) 3106.
[79] P. Jahns, G.H. Krause, Xanthophyll cycle and energy-dependent fluorescence quenching in leaves from pea plants grown under intermittent light, Planta 192 (1994) 176.
[80] J. Andersson, M. Wentworth, R.G. Walters, C.A. Howard, A.V. Ruban, P. Horton, S. Jansson, Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness, Plant Journal 35 (2003) 350.
[81] J.T. Damkjaer, S. Kereiche, M.P. Johnson, L. Kovacs, A.Z. Kiss, E.J. Boekema, A.V. Ruban, P. Horton, S. Jansson, The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis, Plant Cell 21 (2009) 3245.
[82] P. Horton, A.V. Ruban, M. Wentworth, Allosteric regulation of the light-harvesting system of photosystem II, Philos Trans R Soc Lond B Biol Sci 355 (2000) 1361.
[83] M.L. Perez-Bueno, M.P. Johnson, A. Zia, A.V. Ruban, P. Horton, 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.
[84] J.P. Dekker, E.J. Boekema, Supramolecular organization of thylakoid membrane proteins in green plants, Biochim.Biophys.Acta 1706 (2005) 12.
[85] P. Horton, A.V. Ruban, D. Rees, A.A. Pascal, G. Noctor, A.J. Young, Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex, FEBS Lett 292 (1991) 1.
[86] Y. Miloslavina, A. Wehner, P.H. Lambrev, E. Wientjes, M. Reus, G. Garab, R. Croce, A.R. Holzwarth, Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching, FEBS Lett 582 (2008) 3625.
[87] P. Horton, M. Wentworth, A. Ruban, Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching, Febs Letters 579 (2005) 4201.
[88] T.K. Ahn, T.J. Avenson, M. Ballottari, Y.C. Cheng, K.K. Niyogi, R. Bassi, G.R. Fleming, Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein, Science 320 (2008) 794.
[89] P.N. Liao, C.P. Holleboom, L. Wilk, W. Kuhlbrandt, P.J. Walla, Correlation of Car S(1) --> Chl with Chl --> Car S(1) energy transfer supports the excitonic model in quenched light harvesting complex II, J Phys Chem B 114 (2010) 15650.
[90] M.G. Muller, P. Lambrev, M. Reus, E. Wientjes, R. Croce, A.R. Holzwarth, Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids, Chemphyschem 11 (2010) 1289.
[91] A.M. Gilmore, Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves, Physiological Plantarum 99 (1997) 197.
[92] K.K. Niyogi, A.R. Grossman, O. Bjorkman, Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion, Plant Cell 10 (1998) 1121.
[93] P. Joliot, G.N. Johnson, Regulation of cyclic and linear electron flow in higher plants, Proc Natl Acad Sci U S A 108 (2011) 13317.
[94] L. Kalituho, K.C. Beran, P. Jahns, The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin, Plant Physiol 143 (2007) 1861.
[95] A.V. Ruban, A.J. Young, A.A. Pascal, P. Horton, The effects of illumination on the xanthophyll composition of the photosystem II light-harvesting complexes of spinach thylakoid membranes, Plant Physiol. 104 (1994) 227.
[96] H.E. Akerlund, B. Andersson, A. Persson, P.A. Albertsson, Isoelectric points of spinach thylakoid membrane surfaces as determined by cross partition, Biochim Biophys Acta 552 (1979) 238.
[97] D.M. Kramer, C.A. Sacksteder, J.A. Cruz, How acidic is the lumen, Photosynth. Res. 60 (1999) 151.
[98] P. Jahns, D. Latowski, K. Strzalka, Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids, Biochim Biophys Acta 1787 (2009) 3.
[99] X.G. Zhu, S.P. Long, D.R. Ort, Improving photosynthetic efficiency for greater yield, Annu Rev Plant Biol 61 (2010) 235.
[100] E.H. Murchie, M. Pinto, P. Horton, Agriculture and the new challenges for photosynthesis research, New Phytol 181 (2009) 532.
[101] E.H. Murchie, K.K. Niyogi, Manipulation of photoprotection to improve plant photosynthesis, Plant Physiol 155 (2011) 86.
[102] J. Beckmann, F. Lehr, G. Finazzi, B. Hankamer, C. Posten, L. Wobbe, O. Kruse, Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii, J Biotechnol 142 (2009) 70.
[103] C. Kulheim, J. Agren, S. Jansson, Rapid regulation of light harvesting and plant fitness in the field, Science 297 (2002) 91.
[104] N.M. Krah, B.A. Logan, Loss of psbS expression reduces vegetative growth, reproductive output, and light-limited, but not light-saturated, photosynthesis in Arabidopsis thaliana (Brassicaceae) grown in temperate light environments, Am J Bot 97 (2010) 644.
[105] S. Hubbart, O.O. Ajigboye, P. Horton, E.H. Murchie, The photoprotective protein PsbS exerts control over CO(2) assimilation rate in fluctuating light in rice, Plant J 71 (2012) 402.
[106] I.S. Zulfugarov, O.K. Ham, S.R. Mishra, J.Y. Kim, K. Nath, H.Y. Koo, H.S. Kim, Y.H. Moon, G. An, C.H. Lee, Dependence of reaction center-type energy-dependent quenching on photosystem II antenna size, Biochim Biophys Acta 1767 (2007) 773.
[107] M. Ballottari, L. Dall'Osto, T. Morosinotto, R. Bassi, Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation, J Biol Chem 282 (2007) 8947.
[108] T. Roach, A. Krieger-Liszkay, The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana, Biochim Biophys Acta 1817 (2012) 2158.
[2] Z. Li, S. Wakao, B.B. Fischer, K.K. Niyogi, Sensing and responding to excess light, Annu Rev Plant Biol 60 (2009) 239.
[3] P.A. Davis, R.P. Hangarter, Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves, Photosynth Res (2012).
[4] C.A. Wraight, A.R. Crofts, Energy-dependent quenching of chlorophyll alpha fluorescence in isolated chloroplasts, Eur J Biochem 17 (1970) 319.
[5] G.H. Krause, C. Vernotte, J.M. Briantais, Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae, Biochim.Biophys.Acta 679 (1982) 116.
[6] P. Muller, X.P. Li, K.K. Niyogi, Non-photochemical quenching. A response to excess light energy, Plant Physiol 125 (2001) 1558.
[7] P. Horton, A.V. Ruban, Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection, J.Exp.Bot. 56 (2005) 365.
[8] C. Funk, I. Adamska, B.R. Green, B. Andersson, G. Renger, The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments, J.Biol.Chem. 270 (1995) 30141.
[9] X.P. Li, O. Bjorkman, C. Shih, A.R. Grossman, M. Rosenquist, S. Jansson, K.K. Niyogi, A pigment-binding protein essential for regulation of photosynthetic light harvesting, Nature 403 (2000) 391.
[10] X.P. Li, P. Muller-Moule, A.M. Gilmore, K.K. Niyogi, PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition, Proc Natl Acad Sci U S A 99 (2002) 15222.
[11] X.P. Li, A.M. Gilmore, S. Caffarri, R. Bassi, T. Golan, D. Kramer, K.K. Niyogi, Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein, J Biol Chem 279 (2004) 22866.
[12] U. Ljungberg, H.E. Akerlund, B. Andersson, Isolation and characterization of the 10-kDa and 22-kDa polypeptides of higher plant photosystem 2, Eur J Biochem 158 (1986) 477.
[13] S. Kim, E. Pichersky, C.F. Yocum, Topological studies of spinach 22 kDa protein of Photosystem II, Biochim Biophys Acta 1188 (1994) 339.
[14] T. Golan, P. Muller-Moule, K.K. Niyogi, Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants, Plant Cell Environ 29 (2006) 879.
[15] L. Kalituho, T. Grasses, M. Graf, J. Rech, P. Jahns, Characterization of a nonphotochemical quenching-deficient Arabidopsis mutant possessing an intact PsbS protein, xanthophyll cycle and lumen acidification, Planta 223 (2006) 532.
[16] S. Kereiche, A.Z. Kiss, R. Kouril, E.J. Boekema, 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) 759.
[17] M.P. Johnson, A.V. Ruban, Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation, Plant J 61 (2010) 283.
[18] S. Hubbart, O.O. Ajigboye, P. Horton, E.H. Murchie, The photoprotective protein PsbS exerts control over CO(2) assimilation rate in fluctuating light in rice, Plant Journal 71 (2012) 402.
[19] M.P. Johnson, A.V. Ruban, Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced DeltapH, J Biol Chem 286 (2011) 19973.
[20] G. Bonente, B.D. Howes, S. Caffarri, G. Smulevich, R. Bassi, Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro, J Biol Chem 283 (2008) 8434.
[21] G. Bonente, M. Ballottari, T.B. Truong, T. Morosinotto, T.K. Ahn, G.R. Fleming, K.K. Niyogi, R. Bassi, Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii, PLoS Biol 9 (2011) e1000577.
[22] A.Z. Kiss, A.V. Ruban, P. Horton, The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes, Journal of Biological Chemistry 283 (2008) 3972.
[23] I. Kasajima, K. Ebana, T. Yamamoto, K. Takahara, M. Yano, M. Kawai-Yamada, H. Uchimiya, Molecular distinction in genetic regulation of nonphotochemical quenching in rice, Proc Natl Acad Sci U S A 108 (2011) 13835.
[24] A.V. Ruban, E.H. Murchie, Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: A new approach, Biochim Biophys Acta 1817 (2012) 977.
[25] G.H. Krause, E. Weis, Chlorophyll fluorescence and photosynthesis: The basics, Ann.Rev.Plant Physiol. 42 (1991) 313.
[26] P. Horton, A.V. Ruban, R.G. Walters, Regulation of Light harvesting in Green Plants, Annu.Rev.Plant Physiol.Plant Mol.Biol. 47 (1996) 655.
[27] L. Dall'Osto, S. Caffarri, R. Bassi, A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26, Plant Cell 17 (2005) 1217.
[28] M. Nilkens, E. Kress, P. Lambrev, Y. Miloslavina, M. Muller, A.R. Holzwarth, P. Jahns, Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis, Biochim Biophys Acta 1797 (2010) 466.
[29] C. Wilhelm, D. Selmar, Energy dissipation is an essential mechanism to sustain the viability of plants: The physiological limits of improved photosynthesis, J Plant Physiol 168 (2011) 79.
[30] A.V. Ruban, M.P. Johnson, C.D. Duffy, The photoprotective molecular switch in the photosystem II antenna, Biochim Biophys Acta 1817 (2012) 167.
[31] N.E. Holt, D. Zigmantas, L. Valkunas, X.P. Li, K.K. Niyogi, G.R. Fleming, Carotenoid cation formation and the regulation of photosynthetic light harvesting, Science 307 (2005) 433.
[32] 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, R. van Grondelle, Identification of a mechanism of photoprotective energy dissipation in higher plants, Nature 450 (2007) 575.
[33] S. Bode, C.C. Quentmeier, P.N. Liao, N. Hafi, T. Barros, L. Wilk, F. Bittner, 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.
[34] A.R. Holzwarth, Y. Miloslavina, M. Nilkensb, P. Jahnsb, Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence, Chemical Physics Letters 483 (2009) 262.
[35] E. Bergantino, A. Segalla, A. Brunetta, E. Teardo, F. Rigoni, G.M. Giacometti, I. Szabo, Light- and pH-dependent structural changes in the PsbS subunit of photosystem II, Proc Natl Acad Sci U S A 100 (2003) 15265.
[36] S. Kim, P. Sandusky, N.R. Bowlby, R. Aebersold, B.R. Green, S. Vlahakis, C.F. Yocum, E. Pichersky, Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II, FEBS Lett 314 (1992) 67.
[37] T. Iwasaki, Y. Saito, E. Harada, M. Kasai, K. Shoji, M. Miyao, N. Yamamoto, Cloning of cDNA encoding the rice 22 kDa protein of Photosystem II (PSII-S) and analysis of light-induced expression of the gene, Gene 185 (1997) 223.
[38] M. Wallbraun, S. Kim, B.R. Creen, B. Piechulla, E. Pichersky, Nucleotide Sequence of a Tomato psbS Gene, Plant Physiol Biochem 106 (1994 ) 1703.
[39] R. Harrer, R. Bassi, M.G. Testi, C. Sch„fer, Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L.(liverwort), which contains reaction center and antenna proteins, Eur.J.Biochem. 255 (1998) 196.
[40] A.D. Heiber, O. Kawabata, H.Y. Yamamoto, Significance of the lipid phase in the dynamics and functions of the xanthophyll cycle as revealed by PsbS overexpression in tobacco, Plant Cell Physiol 45 (2005) 92.
[41] G. Bonente, F. Passarini, S. Cazzaniga, C. Mancone, M.C. Buia, M. Tripodi, R. Bassi, S. Caffarri, The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching, Photochem Photobiol 84 (2008) 1359.
[42] G. Peers, T.B. Truong, E. Ostendorf, A. Busch, D. Elrad, A.R. Grossman, M. Hippler, K.K. Niyogi, An ancient light-harvesting protein is critical for the regulation of algal photosynthesis, Nature 462 (2009) 518.
[43] G. Bonente, S. Pippa, S. Castellano, R. Bassi, M. Ballottari, Acclimation of Chlamydomonas reinhardtii to different growth irradiances, J Biol Chem 287 (2012) 5833.
[44] C. Gerotto, A. Alboresi, G.M. Giacometti, R. Bassi, T. Morosinotto, Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature, Plant Cell Environ 34 (2011) 922.
[45] N. Wedel, R. Klein, U. Ljungberg, B. Andersson, R.G. Herrmann, The single-copy gene psbS codes for a phylogenetically intriguing 22 kDa polypeptide of photosystem II, FEBS Lett 314 (1992) 61.
[46] C. Funk, W.P. Schr”der, B.R. Green, G. Renger, B. Andersson, The Intrinsic 22 kDa Protein Is a Chlorophyll-Binding Subunit of Photosystem II, FEBS Lett. 342 (1994) 261.
[47] P. Dominici, S. Caffarri, F. Armenante, S. Ceoldo, M. Crimi, R. Bassi, Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant, Journal of Biological Chemistry 277 (2002) 22750.
[48] A.V. Ruban, R.G. Walters, P. Horton, The Molecular Mechanism of the Control of Excitation Energy Dissipation in Chloroplast Membranes - Inhibition of DeltapH- Dependent Quenching of Chlorophyll Fluorescence by Dicyclohexylcarbodiimide, FEBS Lett 309 (1992) 175.
[49] X. Li, A. Phippard, J. Pasari, K. Niyogi, Structural-functional analysis of Photosystem II subunit S (PsbS) in vivo, Functional Plant Biology 29 (2002) 1131
[50] E. Bergantino, A. Brunetta, E. Touloupakis, A. Segalla, I. Szabo, G.M. Giacometti, Role of the PSII-H subunit in photoprotection: novel aspects of D1 turnover in Synechocystis 6803, J Biol Chem 278 (2003) 41820.
[51] N. Betterle, M. Ballottari, S. Zorzan, S. de Bianchi, S. Cazzaniga, L. Dall'osto, T. Morosinotto, R. Bassi, Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction, J Biol Chem 284 (2009) 15255.
[52] M.P. Johnson, T.K. Goral, C.D. Duffy, A.P. Brain, C.W. Mullineaux, 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.
[53] D.F. Ghanotakis, C.M. Waggoner, N.R. Bowlby, D.M. Demetriou, G.T. Babcock, C.F. Yocum, Comparative structural and catalytic properties of oxygen- evolving photosystem II preparations, Photosynth.Res. 14 (1987) 191.
[54] E. Thidholm, V. Lindstrom, C. Tissier, C. Robinson, W.P. Schroder, C. Funk, Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer, Febs Letters 513 (2002) 217.
[55] J. Nield, C. Funk, J. Barber, Supermolecular structure of photosystem II and location of the PsbS protein, Philos.Trans.R.Soc.Lond B Biol.Sci. 355 (2000) 1337.
[56] S. Caffarri, R. Kouril, S. Kereiche, E.J. Boekema, R. Croce, Functional architecture of higher plant photosystem II supercomplexes, Embo J 28 (2009) 3052.
[57] E. Teardo, P.P. de Laureto, E. Bergantino, F. Dalla Vecchia, F. Rigoni, D. Szabo, G.M. Giacometti, Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids, Biochimica Et Biophysica Acta-Bioenergetics 1767 (2007) 703.
[58] A.A. Pascal, Z.F. Liu, K. Broess, B. van Oort, H. van Amerongen, C. Wang, P. Horton, B. Robert, W.R. Chang, A. Ruban, Molecular basis of photoprotection and control of photosynthetic light-harvesting, Nature 436 (2005) 134.
[59] P. Horton, M.P. Johnson, M.L. Perez-Bueno, A.Z. Kiss, 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.
[60] Y. Miloslavina, S. de Bianchi, L. Dall'Osto, R. Bassi, A.R. Holzwarth, Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II, J Biol Chem 286 (2011) 36830.
[61] C. Funk, G. Renger, I. Adamska, B. Andersson, P. Schr”der, The PS II-S polypeptide. An atypical CAB protein, From Light to Biophere Vol.I, Kluwer, Dordrecht, 1995, pp. 339-342.
[62] M. Aspinall-O'Dea, M. Wentworth, A. Pascal, B. Robert, A. Ruban, 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.
[63] X.P. Li, A.M. Gilmore, K.K. Niyogi, 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 (2002) 33590.
[64] T. Barros, A. Royant, J. Standfuss, A. Dreuw, W. Kuhlbrandt, Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state, Embo J 28 (2009) 298.
[65] B. Demmig-Adams, Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin, Biochim.Biophys.Acta 1020 (1990) 1.
[66] A.V. Ruban, 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.
[67] R. Bassi, S. Caffarri, Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls, Photosynthesis Research 64 (2000) 243.
[68] S. Crouchman, A. Ruban, P. Horton, PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin, FEBS Lett 580 (2006) 2053.
[69] A. Zia, M.P. Johnson, A.V. Ruban, Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana, Planta 233 (2011).
[70] I.S. Zulfugarov, A. Tovuu, B. Dogsom, C.Y. Lee, C.H. Lee, PsbS-specific zeaxanthin-independent changes in fluorescence emission spectrum as a signature of energy-dependent non-photochemical quenching in higher plants, Photochem Photobiol Sci 9 (2010) 697.
[71] M.P. Johnson, M.L. Perez-Bueno, A. Zia, P. Horton, 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.
[72] P. Jahns, A.R. Holzwarth, The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II, Biochim Biophys Acta 1817 (2012) 182.
[73] K.K. Niyogi, X.P. Li, V. Rosenberg, H.S. Jung, Is PsbS the site of non-photochemical quenching in photosynthesis?, J Exp Bot 56 (2005) 375.
[74] R.G. Walters, A.V. Ruban, P. Horton, Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation, Eur.J.Biochem 226 (1994) 1063.
[75] R.G. Walters, A.V. Ruban, P. Horton, Identification of proton-active residues in a higher plant light- harvesting complex, Proc.Natl.Acad.Sci.USA 93 (1996) 14204.
[76] J. Andersson, R.G. Walters, P. Horton, S. Jansson, Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation Plant Cell 13 (2001) 1193.
[77] S. de Bianchi, L. Dall'Osto, G. Tognon, T. Morosinotto, R. Bassi, 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 (2008) 1012.
[78] L. Kovacs, J. Damkjaer, S. Kereiche, C. Ilioaia, A.V. Ruban, E.J. Boekema, S. Jansson, P. Horton, Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts, Plant Cell 18 (2006) 3106.
[79] P. Jahns, G.H. Krause, Xanthophyll cycle and energy-dependent fluorescence quenching in leaves from pea plants grown under intermittent light, Planta 192 (1994) 176.
[80] J. Andersson, M. Wentworth, R.G. Walters, C.A. Howard, A.V. Ruban, P. Horton, S. Jansson, Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness, Plant Journal 35 (2003) 350.
[81] J.T. Damkjaer, S. Kereiche, M.P. Johnson, L. Kovacs, A.Z. Kiss, E.J. Boekema, A.V. Ruban, P. Horton, S. Jansson, The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis, Plant Cell 21 (2009) 3245.
[82] P. Horton, A.V. Ruban, M. Wentworth, Allosteric regulation of the light-harvesting system of photosystem II, Philos Trans R Soc Lond B Biol Sci 355 (2000) 1361.
[83] M.L. Perez-Bueno, M.P. Johnson, A. Zia, A.V. Ruban, P. Horton, 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.
[84] J.P. Dekker, E.J. Boekema, Supramolecular organization of thylakoid membrane proteins in green plants, Biochim.Biophys.Acta 1706 (2005) 12.
[85] P. Horton, A.V. Ruban, D. Rees, A.A. Pascal, G. Noctor, A.J. Young, Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex, FEBS Lett 292 (1991) 1.
[86] Y. Miloslavina, A. Wehner, P.H. Lambrev, E. Wientjes, M. Reus, G. Garab, R. Croce, A.R. Holzwarth, Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching, FEBS Lett 582 (2008) 3625.
[87] P. Horton, M. Wentworth, A. Ruban, Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching, Febs Letters 579 (2005) 4201.
[88] T.K. Ahn, T.J. Avenson, M. Ballottari, Y.C. Cheng, K.K. Niyogi, R. Bassi, G.R. Fleming, Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein, Science 320 (2008) 794.
[89] P.N. Liao, C.P. Holleboom, L. Wilk, W. Kuhlbrandt, P.J. Walla, Correlation of Car S(1) --> Chl with Chl --> Car S(1) energy transfer supports the excitonic model in quenched light harvesting complex II, J Phys Chem B 114 (2010) 15650.
[90] M.G. Muller, P. Lambrev, M. Reus, E. Wientjes, R. Croce, A.R. Holzwarth, Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids, Chemphyschem 11 (2010) 1289.
[91] A.M. Gilmore, Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves, Physiological Plantarum 99 (1997) 197.
[92] K.K. Niyogi, A.R. Grossman, O. Bjorkman, Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion, Plant Cell 10 (1998) 1121.
[93] P. Joliot, G.N. Johnson, Regulation of cyclic and linear electron flow in higher plants, Proc Natl Acad Sci U S A 108 (2011) 13317.
[94] L. Kalituho, K.C. Beran, P. Jahns, The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin, Plant Physiol 143 (2007) 1861.
[95] A.V. Ruban, A.J. Young, A.A. Pascal, P. Horton, The effects of illumination on the xanthophyll composition of the photosystem II light-harvesting complexes of spinach thylakoid membranes, Plant Physiol. 104 (1994) 227.
[96] H.E. Akerlund, B. Andersson, A. Persson, P.A. Albertsson, Isoelectric points of spinach thylakoid membrane surfaces as determined by cross partition, Biochim Biophys Acta 552 (1979) 238.
[97] D.M. Kramer, C.A. Sacksteder, J.A. Cruz, How acidic is the lumen, Photosynth. Res. 60 (1999) 151.
[98] P. Jahns, D. Latowski, K. Strzalka, Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids, Biochim Biophys Acta 1787 (2009) 3.
[99] X.G. Zhu, S.P. Long, D.R. Ort, Improving photosynthetic efficiency for greater yield, Annu Rev Plant Biol 61 (2010) 235.
[100] E.H. Murchie, M. Pinto, P. Horton, Agriculture and the new challenges for photosynthesis research, New Phytol 181 (2009) 532.
[101] E.H. Murchie, K.K. Niyogi, Manipulation of photoprotection to improve plant photosynthesis, Plant Physiol 155 (2011) 86.
[102] J. Beckmann, F. Lehr, G. Finazzi, B. Hankamer, C. Posten, L. Wobbe, O. Kruse, Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii, J Biotechnol 142 (2009) 70.
[103] C. Kulheim, J. Agren, S. Jansson, Rapid regulation of light harvesting and plant fitness in the field, Science 297 (2002) 91.
[104] N.M. Krah, B.A. Logan, Loss of psbS expression reduces vegetative growth, reproductive output, and light-limited, but not light-saturated, photosynthesis in Arabidopsis thaliana (Brassicaceae) grown in temperate light environments, Am J Bot 97 (2010) 644.
[105] S. Hubbart, O.O. Ajigboye, P. Horton, E.H. Murchie, The photoprotective protein PsbS exerts control over CO(2) assimilation rate in fluctuating light in rice, Plant J 71 (2012) 402.
[106] I.S. Zulfugarov, O.K. Ham, S.R. Mishra, J.Y. Kim, K. Nath, H.Y. Koo, H.S. Kim, Y.H. Moon, G. An, C.H. Lee, Dependence of reaction center-type energy-dependent quenching on photosystem II antenna size, Biochim Biophys Acta 1767 (2007) 773.
[107] M. Ballottari, L. Dall'Osto, T. Morosinotto, R. Bassi, Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation, J Biol Chem 282 (2007) 8947.
[108] T. Roach, A. Krieger-Liszkay, The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana, Biochim Biophys Acta 1817 (2012) 2158.