Roles of manganese in photosystem II dynamics to irradiations and temperatures
Xuejing HOU, Harvey J. M. HOU
Roles of manganese in photosystem II dynamics to irradiations and temperatures
The most amazing chemistry is the light-driven water splitting reaction occurred in the oxygen-evolving complex of phototsystem II in higher plants, green algae, and cyanobacteria. Mn, in the form of Mn4CaO5 cluster in photosystem II, is responsible for the catalytic water splitting reaction as well as plays roles in photosystem II dynamics to irradiation and temperatures. Manganese hypothesis of UV-initiated photoinhibition as a direct target is established, and thermal inactivation of photosystem II involves the valence and structural changes of manganese. Recent progresses in understanding the roles of manganese in photoinhibition especially under UV light and in thermal inactivation including elevated temperatures using synthetic models and native PS II complexes are summarized and evaluated. Potential problems and possible solutions are discussed and presented.
photosynthesis / manganese / photosystem II / irradiation / temperature / stress
[1] |
Adir N, Zer H, Shochat S, Ohad I (2003). Photoinhibition——a historical perspective. Photosynth Res, 76(1/3): 343–370
CrossRef
Pubmed
Google scholar
|
[2] |
Allakhverdiev S I, Kreslavski V D, Klimov V V, Los D A, Carpentier R, Mohanty P (2008). Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res, 98(1–3): 541–550
CrossRef
Pubmed
Google scholar
|
[3] |
Allakhverdiev S I, Murata N (2004). Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta, 1657(1): 23–32
CrossRef
Pubmed
Google scholar
|
[4] |
Allakhverdiev S I, Murata N (2008). Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res, 98(1–3): 529–539
CrossRef
Pubmed
Google scholar
|
[5] |
Allakhverdiev S I, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov V V, Mimuro M (2010). Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc Natl Acad Sci USA, 107(8): 3924–3929
CrossRef
Pubmed
Google scholar
|
[6] |
Allakhverdiev S I, Tsuchiya T, Watabe K, Kojima A, Los D A, Tomo T, Klimov V V, Mimuro M (2011). Redox potentials of primary electron acceptor quinone molecule (QA)- and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc Natl Acad Sci USA, 108(19): 8054–8058
CrossRef
Pubmed
Google scholar
|
[7] |
Antal T K, Lo W, Armstrong W H, Tyystjärvi E (2009). Illumination with ultraviolet or visible light induces chemical changes in the water-soluble manganese complex, [Mn4O6(bpea)4]Br4. Photochem Photobiol, 85(3): 663–668
CrossRef
Pubmed
Google scholar
|
[8] |
Aro E M, Virgin I, Andersson B (1993). Photoinhibition of photosystem II. inactivation, protein damage and turnover. Biochim Biophys Acta, 1143(2): 113–134
CrossRef
Pubmed
Google scholar
|
[9] |
Barbara Demmig-Adams W W A, Autar K M (2007). Photoprotection, Photoinhibition, Gene regulation, and Environment. The Netherlands: Springer
|
[10] |
Barber J, Andersson B (1992). Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci, 17(2): 61–66
CrossRef
Pubmed
Google scholar
|
[11] |
Blankenship R E (2002). Molecular Mechanisms of Photosynthesis. Blackwell Science
|
[12] |
Brudvig G W (2008). Water oxidation chemistry of photosystem II. Philos Trans R Soc Lond B Biol Sci, 363(1494): 1211–1219, discussion 1218–1219
CrossRef
Pubmed
Google scholar
|
[13] |
Cady C W, Brudvig G W (2008). Functional manganese model chemistry relevant to the oxygen-evolving complex of photosystem II: oxidation of a Mn(III,IV) complex coupled to deprotonation of a terminal water ligand. In: Allen J P, Osmond B, Golbeck JH, and Gantt E Eds, Photosynthesis: Energy from the Sun. Springer, 377–382
|
[14] |
Carpentier R (2005). Influence of high light intensity on photosynthesis: Photoinhibition and energy dissipation. In: Mohammad P. Ed., Handbook of Photosynthesis, 2nd Ed., Taylor & Francis, 327–342
|
[15] |
Chen H, Tagore R, Olack G, Vrettos J S, Weng T C, Penner-Hahn J, Crabtree R H, Brudvig G W (2007). Speciation of the catalytic oxygen evolution system: [MnIII/IV2(μ-O)2(terpy)2(H2O)2](NO3)3+HSO5-]. Inorg Chem, 46(1): 34–43
CrossRef
Pubmed
Google scholar
|
[16] |
Chow W S (1994). Photoprotection and photoinhibitory damage. Adv Mol Cell Biol, 10: 151–196
CrossRef
Google scholar
|
[17] |
Dau H, Liebisch P, Haumann M (2003). X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers—potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal Bioanal Chem, 376(5): 562–583
CrossRef
Pubmed
Google scholar
|
[18] |
Delosme R (2003). On some aspects of photosynthesis revealed by photoacoustic studies: a critical evaluation. Photosynth Res, 76(1/3): 289–301
CrossRef
Pubmed
Google scholar
|
[19] |
Delosme R, Beal D, Joliot P (1994). Photoacoustic detection of flash-induced charge separation in photosynthetic systems. Spectral dependence of the quantum yield. Biochim Biophys Acta, 1185(1): 56–64
CrossRef
Google scholar
|
[20] |
Diner B A, Babcock G T (1996). Structure, dynamics, and energy conversion efficiency in photosystem II. In: Ort D R, Yocum C F Eds, Oxygenic Photosynthesis: The Light Reactions, Kluwer Academic Publishers, 213–247
|
[21] |
Diner B A, Rappaport F (2002). Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol, 53(1): 551–580
CrossRef
Pubmed
Google scholar
|
[22] |
Edens G J, Gunner M R, Xu Q, Mauzerall D (2000). The enthalpy and entropy of reaction for formation of P+
CrossRef
Google scholar
|
[23] |
Ferreira K N, Iverson T M, Maghlaoui K, Barber J, Iwata S (2004). Architecture of the photosynthetic oxygen-evolving center. Science, 303(5665): 1831–1838
CrossRef
Pubmed
Google scholar
|
[24] |
Frank H A, Brudvig G W (2004). Redox functions of carotenoids in photosynthesis. Biochemistry, 43(27): 8607–8615
CrossRef
Pubmed
Google scholar
|
[25] |
Govindjee S M, Seibert M (2010). Picosecond spectroscopy of the isolated reaction centers from the photosystems of oxygenic photosynthesis—ten years (1987–1997) of fun : a tribute to Michael R. Wasielewski on his 60th birthday. Photosynth Res, 103(1): 1–6
CrossRef
Pubmed
Google scholar
|
[26] |
Hakala M, Rantamäki S, Puputti E M, Tyystjärvi T, Tyystjärvi E (2006). Photoinhibition of manganese enzymes: insights into the mechanism of photosystem II photoinhibition. J Exp Bot, 57(8): 1809–1816
CrossRef
Pubmed
Google scholar
|
[27] |
Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005). Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta, 1706(1–2): 68–80
CrossRef
Pubmed
Google scholar
|
[28] |
Henry M, Hoffman M (1979). Photophysics and photochemistry of aromatic nitrogen heterocycles. Fluorescence from 2,2'-bipyridine and 1,10-phenanthroline. J Phys Chem, 83(5): 618–625
CrossRef
Google scholar
|
[29] |
Hideg E, Spetea C, Vass I (1994). Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy. Biochim Biophys Acta, 1186(3): 143–152
CrossRef
Google scholar
|
[30] |
Hou H J M, Mauzerall D (2006). The A-Fx to FA/B step in synechocystis 6803 photosystem I is entropy driven. J Am Chem Soc, 128(5): 1580–1586
CrossRef
Pubmed
Google scholar
|
[31] |
Hou H J M, Mauzerall D (2011). Listening to PS II: enthalpy, entropy, and volume changes. J Photochem Photobiol B, 104(1-2): 357–365
CrossRef
Pubmed
Google scholar
|
[32] |
Hou H J M, Shen G, Boichenko V A, Golbeck J H, Mauzerall D (2009). Thermodynamics of charge separation of photosystem I in the menA and menB null mutants of Synechocystis sp. PCC 6803 determined by pulsed photoacoustics. Biochemistry, 48(8): 1829–1837
CrossRef
Pubmed
Google scholar
|
[33] |
Hou J M, Boichenko V A, Diner B A, Mauzerall D (2001a). Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes. Biochemistry, 40(24): 7117–7125
CrossRef
Pubmed
Google scholar
|
[34] |
Hou J M, Boichenko V A, Wang Y C, Chitnis P R, Mauzerall D (2001b). Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: a pulsed photoacoustic study of electron transfer in photosystem I reveals a similarity to bacterial reaction centers in both volume change and entropy. Biochemistry, 40(24): 7109–7116
CrossRef
Pubmed
Google scholar
|
[35] |
Hughes A V, Rees P, Heathcote P, Jones M R (2006). Kinetic analysis of the thermal stability of the photosynthetic reaction center from Rhodobacter sphaeroides. Biophys J, 90(11): 4155–4166
CrossRef
Pubmed
Google scholar
|
[36] |
Jegerschöld C, Styring S (1991). Fast oxygen-independent degradation of the D1 reaction center protein in photosystem II. FEBS Lett, 280(1): 87–90
CrossRef
Pubmed
Google scholar
|
[37] |
Joliot P, Barbieri G, Chabaud R (1969). Model of the System II photochemical centers. Photochem Photobiol, 10: 309–329
CrossRef
Google scholar
|
[38] |
Jones L W, Kok B (1966). Photoinhibition of chloroplast reactions. II. Multiple effects. Plant Physiol, 41(6): 1044–1049
CrossRef
Pubmed
Google scholar
|
[39] |
Kamiya N, Shen J R (2003). Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA, 100(1): 98–103
CrossRef
Pubmed
Google scholar
|
[40] |
Kashiyama Y, Miyashita H, Ohkubo S, Ogawa N O, Chikaraishi Y, Takano Y, Suga H, Toyofuku T, Nomaki H, Kitazato H, Nagata T, Ohkouchi N (2008). Evidence of global chlorophyll d. Science, 321(5889): 658
CrossRef
Pubmed
Google scholar
|
[41] |
Kok B, Forbush B, McGloin M (1970). Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochem Photobiol, 11(6): 457–475
CrossRef
Pubmed
Google scholar
|
[42] |
Kok B, Gassner E B, Rurainski H J (1966). Photoinhibition of chloroplast reactions. Photochem Photobiol, 4(2): 215–227
CrossRef
Pubmed
Google scholar
|
[43] |
Kramer D M (2010). The photonic “smart grid” of the chloroplast in action. Proc Natl Acad Sci USA, 107(7): 2729–2730
CrossRef
Pubmed
Google scholar
|
[44] |
Krivanek R, Dau H, Haumann M (2008). Enthalpy changes during photosynthetic water oxidation tracked by time-resolved calorimetry using a photothermal beam deflection technique. Biophys J, 94(5): 1890–1903
CrossRef
Pubmed
Google scholar
|
[45] |
Kyle D J, Ohad I, Arntzen C J (1984). Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA, 81(13): 4070–4074
CrossRef
Pubmed
Google scholar
|
[46] |
Limburg J, Vrettos J S, Chen H, de Paula J C, Crabtree R H, Brudvig G W (2001). Characterization of the O2-evolving reaction catalyzed by [(terpy)(H2O)Mn(III)(O)2Mn(IV)(OH2)(terpy)](NO3)3 (terpy = 2,2′:6,2″-terpyridine). J Am Chem Soc, 123(3): 423–430
CrossRef
Pubmed
Google scholar
|
[47] |
Limburg J, Vrettos J S, Liable-Sands L M, Rheingold A L, Crabtree R H, Brudvig G W (1999). A functional model for O-O bond formation by the O2-evolving complex in photosystem II. Science, 283(5407): 1524–1527
CrossRef
Pubmed
Google scholar
|
[48] |
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005). Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature, 438(7070): 1040–1044
CrossRef
Pubmed
Google scholar
|
[49] |
Mauzerall D (2006). Thermodynamics in photosystem I. In J. Golbeck(ed): Photosystem I: The Light-Driven Plastocyanin: Ferredoxin Oxidoreductase, Dordrecht: Springer, 571–581
|
[50] |
Mauzerall D (2010). Changes in enthalpy of the Joliot-Kok four step cycle to produce oxygen in photosynthesis. Biophys J, 98: 173a
|
[51] |
Melis A (1999). Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci, 4: 130–135
|
[52] |
Mielke S P, Kiang N Y, Blankenship R E, Gunner M R, Mauzerall D (2011). Efficiency of photosynthesis in a Chl d-utilizing cyanobacterium is comparable to or higher than that in Chl a-utilizing oxygenic species. Biochim Biophys Acta, 1807(9): 1231–1236
CrossRef
Pubmed
Google scholar
|
[53] |
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996). Chlorophyll d as a major pigment. Nature, 383(6599): 402
CrossRef
Google scholar
|
[54] |
Murakami A, Miyashita H, Iseki M, Adachi K, Mimuro M (2004). Chlorophyll d in an epiphytic cyanobacterium of red algae. Science, 303(5664): 1633
CrossRef
Pubmed
Google scholar
|
[55] |
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev S I (2007). Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta, 1767(6): 414–421
CrossRef
Pubmed
Google scholar
|
[56] |
Nash D, Miyao M, Murata N (1985). Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta, 807(2): 127–133
CrossRef
Google scholar
|
[57] |
Nishiyama Y, Allakhverdiev S I, Murata N (2005). Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res, 84(1–3): 1–7
CrossRef
Pubmed
Google scholar
|
[58] |
Nishiyama Y, Allakhverdiev S I, Murata N (2006). A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta, 1757(7): 742–749
CrossRef
Pubmed
Google scholar
|
[59] |
Niyogi K K (1999). Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol, 50(1): 333–359
CrossRef
Pubmed
Google scholar
|
[60] |
Ohad I, Adir N, Koike H, Kyle D J, Inoue Y (1990). Mechanism of photoinhibition in vivo. A reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. J Biol Chem, 265(4): 1972–1979
Pubmed
|
[61] |
Ohad I, Keren N, Zer H, Gong H, Mor T S, Gal A, Tal S, Eisenberg-Domovich Y (1994). Light induced degradation of the photochemical reaction center II-D1 protein in vivo: An intergrative approach. In: Baker NR, Bowyer JR, Eds, Photoinhibition of Photosynthesis. Oxford: Bios Scientific Publishers, 161–177
|
[62] |
Ohnishi N, Allakhverdiev S I, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005). Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry, 44(23): 8494–8499
CrossRef
Pubmed
Google scholar
|
[63] |
Pearcy R W, Berry J A, Fork D C (1977). Effects of growth temperature on the thermal stability of the photosynthetic apparatus of Atriplex lentiformis (Torr.) Wats. Plant Physiol, 59(5): 873–878
CrossRef
Pubmed
Google scholar
|
[64] |
Peng D C, Hou J M, Kuang T Y, Tang C Q, Tang P S (1999). Light-induced damage of photosystem II primary electron donor P680: A high performance liquid chromatographic analysis of pigment content in D1/D2/cytochrome b559 complex under photoinhibitory conditions. J Integr Plant Biol, 41: 1307–1311
|
[65] |
Pospísil P, Michael H, Dittmer J, Solé V A, Dau H (2003). Stepwise transition of the tetra-manganese complex of photosystem II to a binuclear Mn2(μ-O)2 complex in response to a temperature jump: a time-resolved structural investigation employing x-ray absorption spectroscopy. Biophys J, 84(2 Pt 1): 1370–1386
CrossRef
Pubmed
Google scholar
|
[66] |
Pospísil P, Snyrychová I, Naus J (2007). Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature: EPR spin-trapping study. Biochim Biophys Acta, 1767(6): 854–859
CrossRef
Pubmed
Google scholar
|
[67] |
Powles S B (1984). Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol, 35(1): 15–44
CrossRef
Google scholar
|
[68] |
Rappaport F, Guergova-Kuras M, Nixon P J, Diner B A, Lavergne J (2002). Kinetics and pathways of charge recombination in photosystem II. Biochemistry, 41(26): 8518–8527
CrossRef
Pubmed
Google scholar
|
[69] |
Renger G, Volker M, Eckert H J, Fromme P, Hohm-Veit S, Graber P (1989). On the mechanism of photosystem II deterioration by UV-B irradiation. Photochem Photobiol, 49(1): 97–105
CrossRef
Google scholar
|
[70] |
Rutherford A W, Boussac A (2004). Biochemistry. Water photolysis in biology. Science, 303(5665): 1782–1784
CrossRef
Pubmed
Google scholar
|
[71] |
Sakuragi Y, Zybailov B, Shen G, Jones A D, Chitnis P R, van der Est A, Bittl R, Zech S, Stehlik D, Golbeck J H, Bryant D A (2002). Insertional inactivation of the menG gene, encoding 2-phytyl-1,4-naphthoquinone methyltransferase of Synechocystis sp. PCC 6803, results in the incorporation of 2-phytyl-1,4-naphthoquinone into the A(1) site and alteration of the equilibrium constant between A(1) and F(X) in photosystem I. Biochemistry, 41(1): 394–405
CrossRef
Pubmed
Google scholar
|
[72] |
Sarvikas P, Hakala-Yatkin M, Dönmez S, Tyystjärvi E (2010a). Short flashes and continuous light have similar photoinhibitory efficiency in intact leaves. J Exp Bot, 61(15): 4239–4247
CrossRef
Pubmed
Google scholar
|
[73] |
Sarvikas P, Tyystjärvi T, Tyystjärvi E (2010b). Kinetics of prolonged photoinhibition revisited: photoinhibited Photosystem II centres do not protect the active ones against loss of oxygen evolution. Photosynth Res, 103(1): 7–17
CrossRef
Pubmed
Google scholar
|
[74] |
Setlik I, Allakhverdiev S I, Nedbal L, Setlikova E, Klimov V V (1990). Three types of photosystem II photoinactivation. 1. Damaging processes on the acceptor side. Photosynth Res, 23: 39–48
|
[75] |
Shipton C A, Barber J (1991). Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci USA, 88(15): 6691–6695
CrossRef
Pubmed
Google scholar
|
[76] |
Shipton C A, Barber J (1992). Characterisation of photoinduced breakdown of the D1-polypeptide in isolated reaction centres of Photosystem II. Biochim Biophys Acta, 1099(1): 85–90
CrossRef
Pubmed
Google scholar
|
[77] |
Shipton C A, Barber J (1994). In vivo and in vitro photoinhibition reactions generate similar degradation fragments of D1 and D2 photosystem-II reaction-centre proteins. Eur J Biochem, 220(3): 801–808
CrossRef
Pubmed
Google scholar
|
[78] |
Stewart D H, Brudvig G W (1998). Cytochrome b559 of photosystem II. Biochim Biophys Acta, 1367(1–3): 63–87
CrossRef
Pubmed
Google scholar
|
[79] |
Szabó I, Bergantino E, Giacometti G M (2005). Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep, 6(7): 629–634
CrossRef
Pubmed
Google scholar
|
[80] |
Szilárd A, Sass L, Deák Z, Vass I (2007). The sensitivity of Photosystem II to damage by UV-B radiation depends on the oxidation state of the water-splitting complex. Biochim Biophys Acta, 1767(6): 876–882
CrossRef
Pubmed
Google scholar
|
[81] |
Tagore R, Chen H, Zhang H, Crabtree R H, Brudvig G W (2007a). Homogeneous water oxidation by a di-μ-oxo dimanganese complex in the presence of Ce4+. Inorg Chim Acta, 360(9): 2983–2989
CrossRef
Google scholar
|
[82] |
Tagore R, Crabtree R H, Brudvig G W (2007b). Distinct mechanisms of bridging-oxo exchange in di-μ-O dimanganese complexes with and without water-binding sites: implications for water binding in the O2-evolving complex of photosystem II. Inorg Chem, 46(6): 2193–2203
CrossRef
Pubmed
Google scholar
|
[83] |
Takahashi S, Murata N (2008). How do environmental stresses accelerate photoinhibition? Trends Plant Sci, 13(4): 178–182
CrossRef
Pubmed
Google scholar
|
[84] |
Telfer A (2005). Too much light? How β-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci, 4(12): 950–956
CrossRef
Pubmed
Google scholar
|
[85] |
Telfer A, He W Z, Barber J (1990). Spectral resolution of more than one chlorophyll electron donor in the isolated photosystem II reaction center complex. Biochim Biophys Acta, 1017(2): 143–151
CrossRef
Google scholar
|
[86] |
Thompson L K, Blaylock R, Sturtevant J M, Brudvig G W (1989). Molecular basis of the heat denaturation of photosystem II. Biochemistry, 28(16): 6686–6695
CrossRef
Pubmed
Google scholar
|
[87] |
Thompson L K, Sturtevant J M, Brudvig G W (1986). Differential scanning calorimetric studies of photosystem II: evidence for a structural role for cytochrome b559 in the oxygen-evolving complex. Biochemistry, 25(20): 6161–6169
CrossRef
Pubmed
Google scholar
|
[88] |
Tomo T, Allakhverdiev S I, Mimuro M (2011). Constitution and energetics of photosystem I and photosystem II in the chlorophyll d-dominated cyanobacterium Acaryochloris marina. J Photochem Photobiol B, 104(1–2): 333–340
CrossRef
Pubmed
Google scholar
|
[89] |
Tracewell C A, Vrettos J S, Bautista J A, Frank H A, Brudvig G W (2001). Carotenoid photooxidation in photosystem II. Arch Biochem Biophys, 385(1): 61–69
CrossRef
Pubmed
Google scholar
|
[90] |
Tyystjarvi E (2008). Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev, 252(3–4): 361–376
CrossRef
Google scholar
|
[91] |
Umena Y, Kawakami K, Shen J R, Kamiya N (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature, 473(7345): 55–60
CrossRef
Pubmed
Google scholar
|
[92] |
Usov O M, Grigoryants V M, Tagore R, Brudvig G W, Scholes C P (2007). Hyperfine coupling to the bridging 17O in the di-μ-oxo core of a Mn(III)-Mn(IV) model significant to the core electronic structure of the O2-evolving complex in photosystem II. J Am Chem Soc, 129(39): 11886–11887
CrossRef
Pubmed
Google scholar
|
[93] |
van Gorkom H J (1985). Electron transfer in photosystem II. Photosynth Res, 6(2): 97–112
CrossRef
Google scholar
|
[94] |
van Grondelle R, Dekker J P, Gillbro T, Sundstrom V (1994). Energy transfer and trapping in photosynthesis. Biochim Biophys Acta, 1187(1): 1–65
CrossRef
Google scholar
|
[95] |
Vass I, Gatzen G, Holzwarth A R (1993). Picosecond time-resolved fluorescence studies on photoinhibition and double reduction of QA in photosystem II. Biochim Biophys Acta, 1183(2): 388–396
CrossRef
Google scholar
|
[96] |
Vrettos J S, Brudvig G W (2002). Water oxidation chemistry of photosystem II. Philos Trans R Soc Lond B Biol Sci, 357(1426): 1395–1404, discussion 1404–1405, 1419–1420
CrossRef
Pubmed
Google scholar
|
[97] |
Wei Z, Cady C W, Brudvig G W, Hou H J M (2011). Photodamage of a Mn(III/IV)-oxo mixed-valence compound and photosystem II: evidence that a high-valent manganese species is responsible for UV-induced photodamage of the oxygen-evolving complex in photosystem II. J Photochem Photobiol B, 104(1–2): 118–125
CrossRef
Pubmed
Google scholar
|
[98] |
Yano J, Kern J, Irrgang K D, Latimer M J, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra V K (2005). X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc Natl Acad Sci USA, 102(34): 12047–12052
CrossRef
Pubmed
Google scholar
|
[99] |
Yano J, Yachandra V K (2008). Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy. Inorg Chem, 47(6): 1711–1726
CrossRef
Pubmed
Google scholar
|
[100] |
Zhang F, Cady C W, Brudvig Gary W, Hou H J M (2011). Thermal Stability of [Mn(III)(O)2Mn(IV)(H2O)2(Terpy)2](NO3)3 (Terpy = 2,2':6',2'-terpyridine) in aqueous solution. Inorg Chim Acta, 366(1): 128–133
CrossRef
Google scholar
|
[101] |
Zsiros O, Allakhverdiev S I, Higashi S, Watanabe M, Nishiyama Y, Murata N (2006). Very strong UV-A light temporally separates the photoinhibition of photosystem II into light-induced inactivation and repair. Biochim Biophys Acta, 1757(2): 123–129
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