Formation of Tyrosine Radicals in Photosystem II Under Far-red Illumination

Overview

Journal Photosynth Res

Publisher Springer

Date 2017 Sep 20

PMID 28924898

Citations 4

Authors

Nigar Ahmadova

Fikret Mamedov

Affiliations

Soon will be listed here.

Abstract

Photosystem II (PS II) contains two redox-active tyrosine residues on the donor side at symmetrical positions to the primary donor, P. Tyr, part of the water-oxidizing complex, is a preferential fast electron donor while Tyr is a slow auxiliary donor to P. We used PS II membranes from spinach which were depleted of the water oxidation complex (Mn-depleted PS II) to study electron donation from both tyrosines by time-resolved EPR spectroscopy under visible and far-red continuous light and laser flash illumination. Our results show that under both illumination regimes, oxidation of Tyr occurs via equilibrium with Tyr at pH 4.7 and 6.3. At pH 8.5 direct Tyr oxidation by P occurs in the majority of the PS II centers. Under continuous far-red light illumination these reactions were less effective but still possible. Different photochemical steps were considered to explain the far-red light-induced electron donation from tyrosines and localization of the primary electron hole (P) on the Chl in Mn-depleted PS II after the far-red light-induced charge separation at room temperature is suggested.

Citing Articles

The Electronic Origin of Far-Red-Light-Driven Oxygenic Photosynthesis.

Sirohiwal A, Pantazis D Angew Chem Int Ed Engl. 2022; 61(16):e202200356.

PMID: 35142017 PMC: 9304563. DOI: 10.1002/anie.202200356.

Protein Matrix Control of Reaction Center Excitation in Photosystem II.

Sirohiwal A, Neese F, Pantazis D J Am Chem Soc. 2020; 142(42):18174-18190.

PMID: 33034453 PMC: 7582616. DOI: 10.1021/jacs.0c08526.

Low red/far-red ratio as a signal promotes carbon assimilation of soybean seedlings by increasing the photosynthetic capacity.

Yang F, Liu Q, Cheng Y, Feng L, Wu X, Fan Y BMC Plant Biol. 2020; 20(1):148.

PMID: 32268881 PMC: 7140557. DOI: 10.1186/s12870-020-02352-0.

Microsolvation of the Redox-Active Tyrosine-D in Photosystem II: Correlation of Energetics with EPR Spectroscopy and Oxidation-Induced Proton Transfer.

Sirohiwal A, Neese F, Pantazis D J Am Chem Soc. 2019; 141(7):3217-3231.

PMID: 30666866 PMC: 6728127. DOI: 10.1021/jacs.8b13123.

References

HILLMANN B, Brettel K, Van Mieghem F, Kamlowski A, Rutherford A, Schlodder E . Charge recombination reactions in photosystem II. 2. Transient absorbance difference spectra and their temperature dependence. Biochemistry. 1995; 34(14):4814-27. DOI: 10.1021/bi00014a039. View

Umena Y, Kawakami K, Shen J, Kamiya N . Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011; 473(7345):55-60. DOI: 10.1038/nature09913. View

Vass I, Styring S . pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry. 1991; 30(3):830-9. DOI: 10.1021/bi00217a037. View

Raszewski G, Saenger W, Renger T . Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J. 2004; 88(2):986-98. PMC: 1305170. DOI: 10.1529/biophysj.104.050294. View

Babcock G, Sauer K . Two electron donation sites for exogenous reductants in chloroplast photosystem II. Biochim Biophys Acta. 1975; 396(1):48-62. DOI: 10.1016/0005-2728(75)90188-7. View

Schlodder E, Renger T, Raszewski G, Coleman W, Nixon P, Cohen R . Site-directed mutations at D1-Thr179 of photosystem II in Synechocystis sp. PCC 6803 modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center. Biochemistry. 2008; 47(10):3143-54. DOI: 10.1021/bi702059f. View

Danielsson R, Suorsa M, Paakkarinen V, Albertsson P, Styring S, Aro E . Dimeric and monomeric organization of photosystem II. Distribution of five distinct complexes in the different domains of the thylakoid membrane. J Biol Chem. 2006; 281(20):14241-9. DOI: 10.1074/jbc.M600634200. View

Saito K, Rutherford A, Ishikita H . Mechanism of tyrosine D oxidation in Photosystem II. Proc Natl Acad Sci U S A. 2013; 110(19):7690-5. PMC: 3651498. DOI: 10.1073/pnas.1300817110. View

Rappaport F, Guergova-Kuras M, Nixon P, Diner B, Lavergne J . Kinetics and pathways of charge recombination in photosystem II. Biochemistry. 2002; 41(26):8518-27. DOI: 10.1021/bi025725p. View

10.

Sjoholm J, Ho F, Ahmadova N, Brinkert K, Hammarstrom L, Mamedov F . The protonation state around Tyr/Tyr in photosystem II is reflected in its biphasic oxidation kinetics. Biochim Biophys Acta Bioenerg. 2016; 1858(2):147-155. DOI: 10.1016/j.bbabio.2016.11.002. View

11.

Roffey R, van Wijk K, Sayre R, Styring S . Spectroscopic characterization of tyrosine-Z in histidine 190 mutants of the D1 protein in photosystem II (PSII) in Chlamydomonas reinhardtii. Implications for the structural model of the donor side of PSII. J Biol Chem. 1994; 269(7):5115-21. View

12.

Buser C, Thompson L, Diner B, Brudvig G . Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry. 1990; 29(38):8977-85. DOI: 10.1021/bi00490a014. View

13.

Schlodder E, Coleman W, Nixon P, Cohen R, Renger T, Diner B . Site-directed mutations at D1-His198 and D1-Thr179 of photosystem II in Synechocystis sp. PCC 6803: deciphering the spectral properties of the PSII reaction centre. Philos Trans R Soc Lond B Biol Sci. 2007; 363(1494):1197-202. PMC: 2614104. DOI: 10.1098/rstb.2007.2215. View

14.

Holzwarth A, Muller M, Reus M, Nowaczyk M, Sander J, Rogner M . Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci U S A. 2006; 103(18):6895-900. PMC: 1458990. DOI: 10.1073/pnas.0505371103. View

15.

Diner B, Rappaport F . Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol. 2002; 53:551-80. DOI: 10.1146/annurev.arplant.53.100301.135238. View

16.

Romero E, Diner B, Nixon P, Coleman W, Dekker J, van Grondelle R . Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants. Biophys J. 2012; 103(2):185-94. PMC: 3400784. DOI: 10.1016/j.bpj.2012.06.026. View

17.

Renger G, Renger T . Photosystem II: The machinery of photosynthetic water splitting. Photosynth Res. 2008; 98(1-3):53-80. DOI: 10.1007/s11120-008-9345-7. View

18.

Grabolle M, Dau H . Energetics of primary and secondary electron transfer in Photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim Biophys Acta. 2005; 1708(2):209-18. DOI: 10.1016/j.bbabio.2005.03.007. View

19.

Gadjieva R, Mamedov F, Renger G, Styring S . Interconversion of low- and high-potential forms of cytochrome b(559) in Tris-washed photosystem II membranes under aerobic and anaerobic conditions. Biochemistry. 1999; 38(32):10578-84. DOI: 10.1021/bi9904656. View

20.

Faller P, Rutherford A, Debus R . Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry. 2002; 41(43):12914-20. DOI: 10.1021/bi026588z. View