Roles of manganese in photosystem II dynamics to irradiations and temperatures
Received date: 28 Feb 2012
Accepted date: 10 Apr 2012
Published date: 01 Jun 2013
Copyright
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.
Key words： photosynthesis; manganese; photosystem II; irradiation; temperature; stress
Xuejing HOU , Harvey J. M. HOU . Roles of manganese in photosystem II dynamics to irradiations and temperatures[J]. Frontiers in Biology, 2013 , 8(3) : 312 -322 . DOI: 10.1007/s11515-012-1214-2
| 1 |
Adir N, Zer H, Shochat S, Ohad I (2003). Photoinhibition——a historical perspective. Photosynth Res, 76(1/3): 343–370
|
| 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
|
| 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
|
| 4 |
Allakhverdiev S I, Murata N (2008). Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res, 98(1–3): 529–539
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 16 |
Chow W S (1994). Photoprotection and photoinhibitory damage. Adv Mol Cell Biol, 10: 151–196
|
| 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
|
| 18 |
Delosme R (2003). On some aspects of photosynthesis revealed by photoacoustic studies: a critical evaluation. Photosynth Res, 76(1/3): 289–301
|
| 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
|
| 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
|
| 22 |
Edens G J, Gunner M R, Xu Q, Mauzerall D (2000). The enthalpy and entropy of reaction for formation of P+
|
| 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
|
| 24 |
Frank H A, Brudvig G W (2004). Redox functions of carotenoids in photosynthesis. Biochemistry, 43(27): 8607–8615
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 37 |
Joliot P, Barbieri G, Chabaud R (1969). Model of the System II photochemical centers. Photochem Photobiol, 10: 309–329
|
| 38 |
Jones L W, Kok B (1966). Photoinhibition of chloroplast reactions. II. Multiple effects. Plant Physiol, 41(6): 1044–1049
|
| 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
|
| 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
|
| 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
|
| 42 |
Kok B, Gassner E B, Rurainski H J (1966). Photoinhibition of chloroplast reactions. Photochem Photobiol, 4(2): 215–227
|
| 43 |
Kramer D M (2010). The photonic “smart grid” of the chloroplast in action. Proc Natl Acad Sci USA, 107(7): 2729–2730
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 53 |
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996). Chlorophyll d as a major pigment. Nature, 383(6599): 402
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 59 |
Niyogi K K (1999). Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol, 50(1): 333–359
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 67 |
Powles S B (1984). Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol, 35(1): 15–44
|
| 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
|
| 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
|
| 70 |
Rutherford A W, Boussac A (2004). Biochemistry. Water photolysis in biology. Science, 303(5665): 1782–1784
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 78 |
Stewart D H, Brudvig G W (1998). Cytochrome b559 of photosystem II. Biochim Biophys Acta, 1367(1–3): 63–87
|
| 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
|
| 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
|
| 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
|
| 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
|
| 83 |
Takahashi S, Murata N (2008). How do environmental stresses accelerate photoinhibition? Trends Plant Sci, 13(4): 178–182
|
| 84 |
Telfer A (2005). Too much light? How β-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci, 4(12): 950–956
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 90 |
Tyystjarvi E (2008). Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev, 252(3–4): 361–376
|
| 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
|
| 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
|
| 93 |
van Gorkom H J (1985). Electron transfer in photosystem II. Photosynth Res, 6(2): 97–112
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
/
| 〈 |
|
〉 |