Regulation of Reversible Dissociation of LHCII from PSII by Phosphorylation in Plants

Abstract

LHCII is a crucial light-harvesting pigment/protein complex in photosystem II (PSII) supercomplex. It also participates in the light energy redistribution between photosystems and in the photoprotection via its reversible dissociation with PSII and PSI (photosystem I). This reversible detachment of LHCII is regulated by phosphorylation of its own and PSII core protein. Under low light conditions, LHCII is phosphorylated and dissociated with PSII core protein complex and combined with PSI, which balances the excitation energy between PSII and PSI; Under high light environment, the phosphorylation of PSII core proteins makes LHCII detach from PSII. The dissociated LHCII presents in a free state, which involves in the thermal dissipation of excess excitation energy. During photodamage, dual phosphorylations of both PSII core proteins and LHCII complexes occur. The phosphorylation of D1 is conductive to the disintegration of photodamaged PSII and the cycle of repair. In this circumstance, the phosphorylation of LHCII is induced by reactive oxygen species (ROS) and then the phosphorylated LHCII migrates to PSI, into the repair cycle of damaged PSII. The ferredoxin (Fdr) and thioredoxin (Tdr) system may play a possible central role in the phosphorylation regulation on LHCII dissociation.

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Z. Cui, Y. Wang, A. Zhang and L. Zhang, "Regulation of Reversible Dissociation of LHCII from PSII by Phosphorylation in Plants," American Journal of Plant Sciences, Vol. 5 No. 2, 2014, pp. 241-249. doi: 10.4236/ajps.2014.52032.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] E. Hideg and N. Murata, “The Irreversible Photoinhibition of the Photosystem II Complex in Leaves of Vicia faba under Strong Light,” Plant Science, Vol. 130, No. 2, 1997, pp. 151-158.
http://dx.doi.org/10.1016/S0168-9452(97)00227-6
[2] Z. L. Hu, Z. H. Cui, P. Qin, S. Y. Cao, L. J. Zhang and G. Z. Zhou, “Excess Light Energy Dissipation and Photooxidation Defence of Chinese Pine Needles During the Late Winter,” Journal of Shenyang Agricultural University (China), Vol. 43, No. 5, 2012, pp. 555-559.
[3] S. Takahashi and N. Murata, “How Do Environmental Stresses Accelerate Photoinhibition?” Trends in Plant Science, Vol. 13, No. 4, 2008, pp. 178-182.
http://dx.doi.org/10.1016/j.tplants.2008.01.005
[4] Y. P. Wang, Z. H. Cui, Y. S. Zhu, J. J. Fan and L. J. Zhang, “The Comparison of Anatomic Structure and Photoinhibition Characteristics between Different Regions of the C4 Photosynthetic Leaf in Maize (Zea mays L.),” Plant Physiology Journal (China), Vol. 48, No. 6, 2012, pp. 571-576.
[5] C. Critchley and A. W. Russell, “Photoinhibition of Photosynthesis in Vivo: The Role of Protein Turnover in Photosystem II,” Physiologia Plantarum, Vol. 92, No. 1, 1994, pp. 188-196.
http://dx.doi.org/10.1111/j.1399-3054.1994.tb06670.x
[6] J. Kargul and J. Barber, “Photosynthetic Acclimation: Structural Reorganisation of Light Harvesting Antenna— Role of Redox-Dependent Phosphorylation of Major and Minor Chlorophyll a/b Binding Proteins,” FEBS Journal, Vol. 275, No. 6, 2008, pp. 1056-1068.
http://dx.doi.org/10.1111/j.1742-4658.2008.06262.x
[7] G. R. Cui , L. J. Zhang, Y. S. Zhu, Z. H. Cui and Z. H. Li, “Formation of Plant C4 Photosynthetic Pathway and Its Influencing Factors,” Plant Physiology Communications (China), Vol. 7, 2009, pp. 711-720.
[8] H. Kirchhoff, “Architectural Switches in Plant Thylakoid Membranes,” Photosynthesis Research, Vol. 116, No. 2-3, 2013, pp. 481-487.
http://dx.doi.org/10.1007/s11120-013-9843-0
[9] A. Haldrup, P. E. Jensen, C. Lunde and H. V. Scheller, “Balance of Power: A View of the Mechanism of Photosynthetic State Transitions,” Trends in Plant Science, Vol. 6, No. 7, 2001, pp. 301-305.
http://dx.doi.org/10.1016/S1360-1385(01)01953-7
[10] J. F. Allen, “State Transitions—A Question of Balance,” Science, Vol. 299, No. 5612, 2003, pp. 1530-1532.
http://dx.doi.org/10.1126/science.1082833
[11] L. Dietzel, K. Bräutigam and T. Pfannschmidt, “Photosynthetic Acclimation: State Transitions and Adjustment of Photosystem Stoichiometry—Functional Relationships between Short-Term and Long-Term Light Quality Acclimation in Plants,” FEBS Journal, Vol. 275, No. 6, 2008, pp. 1080-1088.
http://dx.doi.org/10.1111/j.1742-4658.2008.06264.x
[12] S. Puthiyaveetil, “A Mechanism for Regulation of Chloroplast LHC II Kinase by Plastoquinol and Thioredoxin,” FEBS Letters, Vol. 585, No. 12, 2011, pp. 1717-1721.
http://dx.doi.org/10.1016/j.febslet.2011.04.076
[13] R. G. Walters and P. Horton, “Resolution of Components of Non-Photochemical Chlorophyll Fluorescence Quenching in Barley Leaves,” Photosynthesis Research, Vol. 27, No. 2, 1991, pp. 121-133.
http://dx.doi.org/10.1007/BF00033251
[14] H. B. Zhang and D. Q. Xu, “Role of Light-Harvesting Complex 2 Dissociation in Protecting the Photosystem 2 Reaction Centres against Photodamage in Soybean Leaves and Thylakoids,” Photosynthetica, Vol. 41, No. 3, 2003, pp. 383-391.
http://dx.doi.org/10.1023/B:PHOT.0000015462.71601.d7
[15] O. Kruse, “Light-Induced Short-Term Adaptation Mechanisms under Redox Control in the PSII-LHCII Supercomplex: LHC II State Transitions and PS II Repair Cycle,” Naturwissenschaften, Vol. 88, No. 7, 2001, pp. 284-292. http://dx.doi.org/10.1007/s001140100232
[16] P. Martinsuo, S. Pursiheimo, E. M. Aro and E. Rintamäki, “Dithiol Oxidant and Disulfide Reductant Dynamically Regulate the Phosphorylation of Light-Harvesting Complex II Proteins in Thylakoid Membranes,” Plant Physiology, Vol. 133, No. 1, 2003, pp. 37-46.
http://dx.doi.org/10.1104/pp.103.027268
[17] V. Bonardi, P. Pesaresi, T. Becker, E. Schleiff, R. Wagner, T. Pfannschmidt, P. Jahns and D. Leister, “Photosystem II Core Phosphorylation and Photosynthetic Acclimation Require Two Different Protein Kinases,” Nature, Vol. 437, No. 7062, 2005, pp. 1179-1182.
http://dx.doi.org/10.1038/nature04016
[18] T. Mikko, M. Piippo, M. Suorsa, S. Sirpiö, P. Mulo, J. Vainonen, A. V. Vener, Y. Allahverdiyeva and E. M. Aro, “State Transitions Revisited—A Buffering System for Dynamic Low Light Acclimation of Arabidopsis,” Plant Molecular Biology, Vol. 62, No. 4-5, 2006, pp. 779-793.
http://dx.doi.org/10.1007/s11103-006-9044-8
[19] C. W. Mullineaux, E. Bittersmann, J. F. Allen and A. R. Holzwarth, “Picosecond Time-Resolved Fluorescence Emission Spectra Indicate Decreased Energy Transfer from the Phycobilisome to Photosystem II in Light-State 2 in the Cyanobacterium Synechococcus 6301,” Biochimica et Biophysica Acta (BBA)—Bioenergetics, Vol. 1015, No. 2, 1990, pp. 231-242.
http://dx.doi.org/10.1016/0005-2728(90)90025-Y
[20] F. A. Wollman, “State Transitions Reveal the Dynamics and Flexibility of the Photosynthetic Apparatus,” Embo Journal, Vol. 20, No. 14, 2001, pp. 3623-3630.
http://dx.doi.org/10.1093/emboj/20.14.3623
[21] G. C. Owens and I. Ohad, “Phosphorylation of Chlamydomonas reinhardi Chloroplast Membrane Proteins in Vivo and in Vitro,” The Journal of Cell Biology, Vol. 93, No. 3, 1982, pp. 712-718.
http://dx.doi.org/10.1083/jcb.93.3.712
[22] M. Rott, N. F. Martins, W. Thiele, W. Lein, R. Bock, D. M. Kramer and M. A. Schöttler, “ATP Synthase Repression in Tobacco Restricts Photosynthetic Electron Transport, CO2 Assimilation, and Plant Growth by Overacidification of the Thylakoid Lumen,” Plant Cell, Vol. 23, No. 1, 2011, pp. 304-321.
http://dx.doi.org/10.1105/tpc.110.079111
[23] 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, Vol. 428, No. 6980, 2004, pp. 287-292.
http://dx.doi.org/10.1038/nature02373
[24] J. P. Dekker and E. J. Boekema, “Supramolecular Organization of Thylakoid Membrane Proteins in Green Plants,” Biochimica et Biophysica Acta (BBA)—Bioenergetics, Vol. 1706, No. 1-2, 2005, pp. 12-39.
http://dx.doi.org/10.1016/j.bbabio.2004.09.009
[25] S. Caffarri, R. Croce, L. Cattivelli and R. Bassi, “A Look within LHCII: Differential Analysis of the Lhcb1-3 Complexes Building the Major Trimeric Antenna Complex of Higher-Plant Photosynthesis,” Biochemistry, Vol. 43, No. 29, 2004, pp. 9467-9476.
[26] A. E. Yakushevska, W. Keegstra, E. J. Boekema, J. P. Dekker, J. Andersson, S. Jansson, A. V. Ruban and P. Horton, “The Structure of Photosystem II in Arabidopsis: Localization of the CP26 and CP29 Antenna Complexes,” Biochemistry, Vol. 42, No. 3, 2003, pp. 608-613.
http://dx.doi.org/10.1021/bi027109z
[27] B. van Oort, M. Alberts, S. de Bianchi, L. Dall’Osto, R. Bassi, G. Trinkunas, R. Croce and H. van Amerongen, “Effect of Antenna-Depletion in Photosystem II on Excitation Energy Transfer in Arabidopsis thaliana,” Biophysical Journal, Vol. 98, No. 5, 2010, pp. 922-931.
http://dx.doi.org/10.1016/j.bpj.2009.11.012
[28] B. Zybailov, H. Rutschow, G. Friso, A. Rudella, O. Emanuelsson, Q. Sun and K. J. van Wijk, “Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome,” PLoS One, Vol. 3, No. 4, 2008, p. e1994.
[29] S. Reiland, G. Messerli, K. Baerenfaller, B. Gerrits, A. Endler, J. Grossmann, W. Gruissem and S. Baginsky, “Large-Scale Arabidopsis Phosphoproteome Profiling Reveals Novel Chloroplast Kinase Substrates and Phosphorylation Networks,” Plant Physiology, Vol. 150, No. 2, 2009, pp. 889-903.
http://dx.doi.org/10.1104/pp.109.138677
[30] M. Tikkanen, M. Nurmi, S. Kangasjarvi and E. M. Aro, “Core Protein Phosphorylation Facilitates the Repair of Photodamaged Photosystem II at High Light,” Biochimica et Biophysica Acta, Vol. 1777, No. 11, 2008, pp. 1432-1437.
[31] S. Bellafiore, F. Barneche, G. Peltier and J. D. Rochaix, “State Transitions and Light Adaptation Require Chloroplast Thylakoid Protein Kinase STN7,” Nature, Vol. 433, No. 7028, 2005, pp. 892-895.
http://dx.doi.org/10.1038/nature03286
[32] R. Fristedt, A. Willig, P. Granath, M. Crèvecoeur, J. D. Rochaix and A. V. Vener, “Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes in Arabidopsis,” Plant Cell, Vol. 21, No. 12, 2009, pp. 3950-3964.
http://dx.doi.org/10.1105/tpc.109.069435
[33] J. D. Rochaix, “Role of Thylakoid Protein Kinases in Photosynthetic Acclimation,” FEBS Letters, Vol. 581, No. 15, 2007, pp. 2768-2775.
http://dx.doi.org/10.1016/j.febslet.2007.04.038
[34] N. Depege, S. Bellafiore and J. D. Rochaix, “Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas,” Science, Vol. 299, No. 5612, 2003, pp. 1572-1575.
http://dx.doi.org/10.1126/science.1081397
[35] S. Lemeille, A. Willig, N. Depège-Fargeix, C. Delessert, R. Bassi and J. D. Rochaix, “Analysis of the Chloroplast Protein Kinase Stt7 during State Transitions,” PLOS Biology, Vol. 7, No. 3, 2009, Article ID: e1000045.
http://dx.doi.org/10.1371/journal.pbio.1000045
[36] I. Carlberg, E. Rintamäki, E. M. Aro and B. Andersson, “Thylakoid Protein Phosphorylation and the Thiol Redox State,” Biochemistry, Vol. 38, No. 10, 1999, pp. 3197-3204. http://dx.doi.org/10.1021/bi982506o
[37] A. Rokka, E. M. Aro, R. G. Herrmann, B. Andersson and A. V. Vener, “Dephosphorylation of Photosystem II Reaction Center Proteins in Plant Photosynthetic Membranes as an Immediate Response to Abrupt Elevation of Temperature,” Plant Physiology, Vol. 123, No. 4, 2000, pp. 1525-1536. http://dx.doi.org/10.1104/pp.123.4.1525
[38] A. Rokka, M. Suorsa, A. Saleem, N. Battchikova and E. M. Aro, “Synthesis and Assembly of Thylakoid Protein Complexes: Multiple Assembly Steps of Photosystem II,” Biochemical Journal, Vol. 388, Pt. 1, 2005, pp. 159-168.
http://dx.doi.org/10.1042/BJ20042098
[39] H. L. Breitholtz, R. Srivastava, E. Tyystjärvi and E. Rintamäki, “LHC II Protein Phosphorylation in Leaves of Arabidopsis thaliana Mutants Deficient in Non-Photochemical Quenching,” Photosynthesis Research, Vol. 84, No. 1-3, 2005, pp. 217-223.
[40] P. Pesaresi, M. Pribil, T. Wunder and D. Leister, “Dynamics of Reversible Protein Phosphorylation in Thylakoids of Flowering Plants: The Roles of STN7, STN8 and TAP38,” Biochimica et Biophysica Acta, Vol. 1807, No. 8, 2011, pp. 887-896.
http://dx.doi.org/10.1016/j.bbabio.2010.08.002
[41] J. Kargul, M. V. Turkina, J. Nield, S. Benson, A. V. Vener and J. Barber, “Light-Harvesting Complex II Protein CP29 Binds to Photosystem I of Chlamydomonas reinhardtii under State 2 Conditions,” FEBS Journal, Vol. 272, No. 18, 2005, pp. 4797-4806.
http://dx.doi.org/10.1111/j.1742-4658.2005.04894.x
[42] M. V. Turkina, J. Kargul, A. Blanco-Rivero, A. Villarejo, J. Barber and A. V. Vener, “Environmentally Modulated Phosphoproteome of Photosynthetic Membranes in the Green Alga Chlamydomonas reinhardtii,” Molecular & Cellular Proteomics, Vol. 5, No. 8, 2006, pp. 1412-1425.
http://dx.doi.org/10.1074/mcp.M600066-MCP200
[43] M. Hansson, T. Dupuis, R. Strömquist, B. Andersson, A. V. Vener and I. Carlberg, “The Mobile Thylakoid Phosphoprotein TSP9 Interacts with the Light-Harvesting Complex II and the Peripheries of Both Photosystems,” Journal of Biological Chemistry, Vol. 282, No. 22, 2007, pp. 16214-16222.
http://dx.doi.org/10.1074/jbc.M605833200
[44] R. Fristedt, I. Carlberg, A. Zygadlo, M. Piippo, M. Nurmi, E. M. Aro, H. V. Scheller and A. V. Vener, “Intrinsically Unstructured Phosphoprotein TSP9 Regulates Light Harvesting in Arabidopsis thaliana,” Biochemistry, Vol. 48, No. 2, 2009, pp. 499-509.
http://dx.doi.org/10.1021/bi8016334
[45] R. Fristedt and A. V. Vener, “High Light Induced Disassembly of Photosystem II Supercomplexes in Arabidopsis Requires STN7-Dependent Phosphorylation of CP29,” PLoS ONE, Vol. 6, No. 9, 2011, Article ID: e24565.
http://dx.doi.org/10.1371/journal.pone.0024565
[46] M. Pribil, P. Pesaresi, A. Hertle, H. Alexander, B. Roberto and L. Dario, “Role of Plastid Protein Phosphatase TAP38 in LHCII Dephosphorylation and Thylakoid Electron Flow,” PLoS Biology, Vol. 8, No. 1, 2010, Article ID: e1000288. http://dx.doi.org/10.1371/journal.pbio.1000288
[47] A. Shapiguzov, B. Ingelsson, I. Samol, C. Andres, F. Kessler, J. D. Rochaix, A. V. Vener and M. Goldschmidt-Clermont, “The PPH1 Phosphatase Is Specifically Involved in LHCII Dephosphorylation and State Transitions in Arabidopsis,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 10, 2010, pp. 4782-4787. http://dx.doi.org/10.1073/pnas.0913810107
[48] E. Rintamäki, P. Martinsuo, S. Pursiheimo and E. M. Aro, “Cooperative Regulation of Light-Harvesting Complex II Phosphorylation via the Plastoquinol and FerredoxinThioredoxin System in Chloroplasts,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 97, No. 21, 2000, pp. 11644-11649.
http://dx.doi.org/10.1073/pnas.180054297
[49] P. Singh-Rawal, A. Jajoo, S. Mathur, P. Mehta and S. Bharti, “Evidence that pH Can Drive State Transitions in Isolated Thylakoid Membranes from Spinach,” Photochemical and Photobiological Sciences, Vol. 9, No. 6, 2010, pp. 830837. http://dx.doi.org/10.1039/c0pp00055h
[50] S. S. Hong and D. Q. Xu, “Light-Induced Increase in Initial Chlorophyll Fluorescence Fo Level and the Reversible Inactivation of PS II Reaction Centers in Soybean Leaves,” Photosynthesis Research, Vol. 61, No. 3, 1999, pp. 269-280.
http://dx.doi.org/10.1023/A:1006357203466
[51] D. Elrad, K. K. Niyogi and A. R. Grossman, “A Major Light-Harvesting Polypeptide of Photosystem II Functions in Thermal Dissipation,” Plant Cell, Vol. 14, No. 8, 2002, pp. 1801-1816.
http://dx.doi.org/10.1105/tpc.002154
[52] J. P. Vainonen, M. Hansson and A. V. Vener, “STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins,” Journal of Biological Chemistry, Vol. 280, No. 39, 2005, pp. 33679-33686. http://dx.doi.org/10.1074/jbc.M505729200
[53] J. P. Vainonen, Y. Sakuragi, S. Stael, M. Tikkanen, Y. Allahverdiyeva, V. Paakkarinen, E. Aro, M. Suorsa, H. V. Scheller, A. V. Vener and E. M. Aro, “Light Regulation of CaS, a Novel Phosphoprotein in the Thylakoid Membrane of Arabidopsis thaliana,” FEBS Journal, Vol. 275, No. 8, 2008, pp. 1767-1777.
http://dx.doi.org/10.1111/j.1742-4658.2008.06335.x
[54] A. V. Vener, A. Rokka, H. Fulgosi, B. Andersson and R. G. Herrmann, “A Cyclophilin-Regulated PP2A-Like Protein Phosphatase in Thylakoid Membranes of Plant Chloroplasts,” Biochemistry, Vol. 38, No. 45, 1999, pp. 14955-14965. http://dx.doi.org/10.1021/bi990971v
[55] E. Rintamäki, R. Kettunen and E. M. Aro, “Differential D1 Dephosphorylation in Functional and Photodamaged Photosystem II Centers. Dephosphorylation Is a Prerequisite for Degradation of Damaged D1,” Journal of Biological Chemistry, Vol. 271, No. 25, 1996, pp. 14870-14875.
http://dx.doi.org/10.1074/jbc.271.25.14870
[56] I. Samol, A. Shapiguzov, B. Ingelsson, G. Fucile, M. Crèvecoeur, A. V. Vener, J. D. Rochaix and M. Goldschmidt-Clermont, “Identification of a Photosystem II Phosphatase Involved in Light Acclimation in Arabidopsis,” Plant Cell, Vol. 24, No. 6, 2012, pp. 2596-2609.
http://dx.doi.org/10.1105/tpc.112.095703
[57] J. D. Rochaix, S. Lemeille, A. Shapiguzov, I. Samol, G. Fucile, A. Willig and M. Goldschmidt-Clermont, “ Protein Kinases and Phosphatases Involved in the Acclimation of the Photosynthetic Apparatus to a Changing Light Environment,” Philosophical Transactions of the Royal Society of London series B-Biological Sciences, Vol. 367, No. 1608, 2012, pp. 3466-3474.
http://dx.doi.org/10.1098/rstb.2012.0064
[58] K. J. Dietz and T. Pfannschmidt, “Novel Regulators in Photosynthetic Redox Control of Plant Metabolism and Gene Expression,” Plant Physiology, Vol. 155, No. 4, 2011, pp. 1477-1485.
http://dx.doi.org/10.1104/pp.110.170043
[59] L. Lupínková and J. Komenda, “Oxidative Modifications of the Photosystem II D1 Protein by Reactive Oxygen Species: From Isolated Protein to Cyanobacterial Cells,” Photochemistry and Photobiology, Vol. 79, No. 2, 2004, pp. 152-162.
[60] I. Vass, “Role of Charge Recombination Processes in Photodamage and Photoprotection of the Photosystem II Complex,” Physiologia Plantarum, Vol. 142, No. 1, 2011, pp. 6-16.
http://dx.doi.org/10.1111/j.1399-3054.2011.01454.x
[61] S. I. Allakhverdiev, Y. Nishiyama, S. Takahashi, S. Miyairi, I. Suzuki and N. Murata, “Systematic Analysis of the Relation of Electron Transport and ATP Synthesis to the Photodamage and Repair of Photosystem II in Synechocystis,” Plant Physiology, Vol. 137, No. 1, 2005, pp. 263-273. http://dx.doi.org/10.1104/pp.104.054478
[62] N. Murata, S. Takahashi, Y. Nishiyama and S. I. Allakhverdiev, “Photoinhibition of Photosystem II under Environmental Stress,” Biochimica et Biophysica Acta (BBA)— Bioenergetics, Vol. 1767, No. 6, 2007, pp. 414-421.
http://dx.doi.org/10.1016/j.bbabio.2006.11.019
[63] R. Barbato, G. Friso, F. Rigoni, F. Dalla Vecchia and G. M. Giacometti, “Structural Changes and Lateral Redistribution of Photosystem II during Donor Side Photoinhibition of Thylakoids,” Journal of Cell Biology, Vol. 119, No. 2, 1992, pp. 325-335.
http://dx.doi.org/10.1083/jcb.119.2.325
[64] M. Tikkanen and E. M. Aro, “Thylakoid Protein Phosphorylation in Dynamic Regulation of Photosystem II in Higher Plants,” Biochimica et Biophysica Acta (BBA)— Bioenergetics, Vol. 1817, No. 1, 2012, pp. 232-238.
http://dx.doi.org/10.1016/j.bbabio.2011.05.005
[65] P. F. Huesgen, H. Schuhmann and I. Adamska, “The Family of Deg Proteases in Cyanobacteria and Chloroplasts of Higher Plants,” Physiologia Plantarum, Vol. 123, No. 4, 2005, pp. 413-420.
http://dx.doi.org/10.1111/j.1399-3054.2005.00458.x
[66] M. Lindahl, C. Spetea, T. Hundal, A. B. Oppenheim, Z. Adam and B. Andersson, “The Thylakoid FtsH Protease Plays a Role in the Light-Induced Turnover of the Photosystem II D1 Protein,” Plant Cell, Vol. 12, No. 3, 2000, pp. 419-431.
[67] R. Fristedt, P. Granath and A. V. Vener, “A Protein Phosphorylation Threshold for Functional Stacking of Plant Photosynthetic Membranes,” PLoS ONE, Vol. 5, No. 6, 2010, Article ID: e10963.
http://dx.doi.org/10.1371/journal.pone.0010963
[68] E. M. Aro, S. McCaffery and J. M. Anderson, “Photoinhibition and D1 Protein Degradation in Peas Acclimated to Different Growth Irradiances,” Plant Physiology, Vol. Vol. 103, No. 3, 1993, pp. 835-843.
[69] J. M. Anderson and E. M. Aro, “Grana Stacking and Protection of Photosystem II in Thylakoid Membranes of Higher Plant Leaves under Sustained High Irradiance: An Hypothesis,” Photosynthesis Research, Vol. 41, No. 2, 1994, pp. 315-326.
http://dx.doi.org/10.1007/BF00019409
[70] L. Chen, H. Jia, Q. Tian, L. Du, Y. Gao, X. Miao and Y. Liu, “Protecting Effect of Phosphorylation on Oxidative Damage of D1 Protein by Down-Regulating the Production of Superoxide Anion in photosystem II Membranes under High Light,” Photosynthesis Research, Vol. 112, No. 2, 2012, pp. 141-148.
http://dx.doi.org/10.1007/s11120-012-9750-9
[71] Y. E. Chen, Z. Y. Zhao, H. Y. Zhang, X. Y. Zeng and S. Yuan, “The Significance of CP29 Reversible Phosphorylation in Thylakoids of Higher Plants under Environmental Stresses,” Journal of Experimental Botany, Vol. 64, No. 5, 2013, pp. 1167-1178.
http://dx.doi.org/10.1093/jxb/ert002
[72] T. K. Goral, M. P. Johnson, A. P. Brain, H. Kirchhoff, A. V. Ruban and C. W. Mullineaux, “Visualizing the Mobility and Distribution of Chlorophyll Proteins in Higher Plant Thylakoid Membranes: Effects of Photoinhibition and Protein Phosphorylation,” Plant Journal, Vol. 62, No. 6, 2010, pp. 948-959.

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