Towards an understanding of redox heterogeneity of the photosystem II cytochrome b559 in the native membrane

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• 作者：Olga P. Kaminskaya ; Vladimir A. Shuvalov
• 关键词：Photosystem II ; Cyt b559 ; Plastoquinone ; Redox interaction
• 刊名：European Biophysics Journal
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：45
• 期：2
• 页码：129-138
• 全文大小：706 KB
• 参考文献：Arnon DI, Tang GMS (1988) Cytochrome b-559 and proton conductance in oxygenic photosynthesis. Proc Natl Acad Sci USA 85:9524–9528PubMedCentral CrossRef PubMed
  Babcock GT, Widger WR, Cramer WA, Oertling WA, Metz JG (1985) Axial ligands of chloroplast cytochrome b-559: identification and requirement for a heme-cross-linked polypeptide structure. Biochemistry 24:3638–3645CrossRef PubMed
  Barber J, De Las Rivas J (1993) A functional model for the role of cytochrome b559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA 90:10942–10946PubMedCentral CrossRef PubMed
  Ben-Hayyim G (1974) Light-induced absorbance changes of the high-potential cytochrome b559 in chloroplasts. Eur J Biochem 41:191–196CrossRef PubMed
  Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties. FEBS Lett 134:231–234CrossRef
  Berthomieu C, Boussac A, Mäntele W, Breton J, Nabedryk E (1992) Molecular changes following oxidoreduction of cytochrome b559 characterized by Fourier transform infrared difference spectroscopy and electron paramagnetic resonance: photooxidation in photosystem II and electrochemistry of isolated cytochrome b559 and iron protoporphyrin IX-bisimidazole model compounds. Biochemistry 31:11460–11471CrossRef PubMed
  Biedermann G (1956) The basicity constant of p-benzoquinone. Acta Chem Scand 10:1340–1344CrossRef
  Bishop CA, Tong LKJ (1965) Equilibria of substituted semiquinones at high pH. J Am Chem Soc 87:501–505CrossRef
  Böhme H, Kunert KJ (1980) Photoreactions of cytochromes in algal chloroplasts. Eur J Biochem 106:329–336CrossRef PubMed
  Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. Biochemistry 31:11449–11459CrossRef PubMed
  Butler WL (1978) On the role of cytochrome b559 in oxygen evolution in photosynthesis. FEBS Lett 95:19–25CrossRef
  Canaani O, Havaux M (1990) Evidence for a biological role in photosynthesis for cytochrome b-559— a component of photosystem II reaction center. Proc Natl Acad Sci USA 87:9295–9299PubMedCentral CrossRef PubMed
  Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817:26–43CrossRef PubMed
  Cox RP, Bendall DS (1972) The effects on cytochrome b-559HP and P546 of treatments that inhibit oxygen evolution by chloroplasts. Biochim Biophys Acta 283:124–135CrossRef PubMed
  Cox RP, Bendall DS (1974) The functions of plastoquinone and β-carotene in photosystem II of chloroplasts. Biochim Biophys Acta 347:49–59CrossRef PubMed
  Crofts AR, Wright CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185CrossRef
  Desbois A, Lutz M (1992) Redox control of proton transfers in membrane b-type cytochromes: an absorption and resonance Raman study on bis(imidazole) and bis(imidazolate) model complexes of iron-protoporphyrin. Eur Biophys J 20:321–335
  Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580CrossRef PubMed
  Diner BA, Petrouleas V, Wendoloski JJ (1991) The iron-quinone electron-acceptor complex of photosystem II. Physiol Plant 81:423–436CrossRef
  Erixon K, Lozier R, Butler WL (1972) The redox state of cytochrome b559 in spinach chloroplasts. Biochim Biophys Acta 267:375–382CrossRef PubMed
  Faller P, Pascal A, Rutherford AW (2001) β-carotene redox reactions in photosystem II: electron transfer pathway. Biochemistry 40:6431–6440CrossRef PubMed
  Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Biol 16:334–342CrossRef
  Guskov A, Gabdulkhakov A, Broser M, Glöckner C, Hellmich J, Kern J, Frank J, Müh F, Saenger W, Zouni A (2010) Recent progress in the crystallographic studies of photosystem II. ChemPhysChem 11:1160–1171CrossRef PubMed
  Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195CrossRef PubMed
  Hasegawa K, Noguchi T (2014) Molecular interactions of the quinone electron acceptors QA, QB, and QC in photosystem II as studied by the fragment molecular orbital method. Photosynth Res 120:113–123CrossRef PubMed
  Heber U, Kirk MR, Boardman NK (1979) Photoreactions of cytochrome b-559 and cyclic electron flow in photosystem II of intact chloroplasts. Biochim Biophys Acta 546:292–306CrossRef PubMed
  Horton P, Croze E (1977) The relationship between the activity of chloroplast photosystem II and the midpoint oxidation-reduction potential of cytochrome b-559. Biochim Biophys Acta 462:86–101CrossRef PubMed
  Ishikita H, Saenger W, Biesiadka J, Loll B, Knapp EW (2006) How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870. Proc Natl Acad Sci USA 103:9855–9860PubMedCentral CrossRef PubMed
  Iwasaki I, Tamura N, Okayama S (1995) Effects of light stress on redox potential forms of Cyt b-559 in photosystem II membranes depleted of water-oxidizing complex. Plant Cell Physiol 36:583–589
  Kaminskaya OP, Shuvalov VA (2013) Biphasic reduction of cytochrome b559 by plastoquinol in photosystem II membrane fragments. Evidence for two types of cytochrome b559/plastoquinone redox equilibria. Biochim Biophys Acta 1827:471–483CrossRef PubMed
  Kaminskaya O, Kurreck J, Irrgang KD, Renger G, Shuvalov VA (1999) Redox and spectral properties of cytochrome b559 in different preparations of photosystem II. Biochemistry 38:16223–16235CrossRef PubMed
  Kaminskaya O, Kern J, Shuvalov VA, Renger G (2005) Extinction coefficients of cytochromes b559 and c550 of Thermosynechococcus elongatus and Cyt b559/PS II stoichiometry of higher plants. Biochim Biophys Acta 1708:333–341CrossRef PubMed
  Kaminskaya O, Shuvalov VA, Renger G (2007a) Evidence for a novel quinone binding site in the photosystem II complex that regulates the redox potential of cytochrome b559. Biochemistry 46:1091–1105CrossRef PubMed
  Kaminskaya O, Shuvalov VA, Renger G (2007b) Two reaction pathways for transformation of high potential cytochrome b559 of photosystem II into the intermediate potential form. Biochim Biophys Acta 1767:550–558CrossRef PubMed
  Krishtalik LI, Tae GS, Cherepanov DA, Cramer WA (1993) The redox properties of cytochromes b imposed by the membrane electrostatic environment. Biophys J 65:184–195PubMedCentral CrossRef PubMed
  Laisk A, Eichelmann H, Oja V (2015) Oxidation of plastohydroquinone by photosystem II and by dioxygen in leaves. Biochim Biophys Acta 1847:565–575CrossRef PubMed
  McNamara VP, Gounaris K (1995) Granal photosystem II complexes contain only the high redox potential form of cytochrome b-559 which is stabilised by the ligation of calcium. Biochim Biophys Acta 1231:289–296CrossRef
  Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65CrossRef PubMed
  Okayama S, Butler WL (1972) Extraction and reconstitution of photosystem II. Plant Physiol 49:769–774PubMedCentral CrossRef PubMed
  Ortega JM, Hervas M, Losada M (1988) Redox and acid-base characterization of cytochrome b-559 in photosystem II particles. Eur J Biochem 171:449–455CrossRef PubMed
  Ortega JM, Hervas M, Losada M (1989) Isolation and comparison of molecular properties of cytochrome b-559 from both spinach thylakoids and PS II particles. Z Naturforsch C 44:415–422
  Ortega JM, Hervas M, Losada M (1990) Distinctive stability of the reduced and oxidized forms of high-potential cytochrome b-559 in photosystem II particles. Plant Sci 68:71–75CrossRef
  Pospíšil P (2011) Enzymatic function of cytochrome b559 in photosystem II. J Photochem Photobiol B 104:341–347CrossRef PubMed
  Renger G, Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98:53–80CrossRef PubMed
  Rich PR, Bendall DS (1980) The redox potentials of the b-type cytochromes of higher plant chloroplasts. Biochim Biophys Acta 591:153–161CrossRef PubMed
  Roncel M, Ortega JM, Losada M (2001) Factors determining the special redox properties of photosynthetic cytochrome b559. Eur J Biochem 268:4961–4968CrossRef PubMed
  Roncel M, Boussac A, Zurita JL, Bottin H, Sugiura M, Kirilovsky D, Ortega JM (2003) Redox properties of the photosystem II cytochromes b559 and c550 in the cyanobacterium Thermosynechococcus elongatus. J Biol Inorg Chem 8:206–216CrossRef PubMed
  Saito K, Ishida T, Sugiura M, Kawakami K, Umena Y, Kamiya N, Shen JR, Ishikita H (2011) Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center. J Am Chem Soc 133:14379–14388CrossRef PubMed
  Samson G, Fork DC (1992) Simultaneous photoreduction and photooxidation of cytochrome b-559 in photosystem II treated with carbonylcyanide-m-chlorophenylhydrazone. Photosynth Res 33:203–212CrossRef PubMed
  Shibamoto T, Kato Y, Watanabe T (2008) Spectroelectrochemistry of cytochrome b559 in the D1-D2-Cyt b559 complex from spinach. FEBS Lett 582:1490–1494CrossRef PubMed
  Shinkarev VP (2006) Ubiquinone (coenzyme Q10) binding sites: low dielectric constant of the gate prevents the escape of the semiquinone. FEBS Lett 580:2534–2539CrossRef PubMed
  Shinopoulos KE, Brudwig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817:66–75CrossRef PubMed
  Stewart DH, Brudvig GW (1998) Cytochrome b559 of photosystem II. Biochim Biophys Acta 1367:63–87CrossRef PubMed
  Swallow AJ (1982) Physical chemistry of semiquinones. In: Trumpower BL (ed) Function of quinones in energy conserving systems. Academic Press, New York, pp 59–72
  Thompson LK, Brudwig GW (1988) Cytochrome b-559 may function to protect photosystem II from photoinhibition. Biochemistry 27:6653–6658CrossRef PubMed
  Thompson LK, Miller AF, Buser CA, De Paula JC, Brudwig GW (1989) Characterization of the multiple forms of cytochrome b559 in photosystem II. Biochemistry 28:8048–8056CrossRef PubMed
  Tracewell CA, Brugwig GW (2008) Characterization of the secondary electron-transfer pathway intermediates of photosystem II containing low-potential cytochrome b559. Photosynth Res 98:189–197CrossRef PubMed
  Tsujimoto HY, Arnon DI (1985) Differential inhibition by plastoquinone analogues of photoreduction of cytochrome b-559 in chloroplasts. FEBS Lett 179:51–54CrossRef
  Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Ǻ. Nature 473:55–60CrossRef PubMed
  Vennam PR, Fisher N, Krzyaniak MD, Kramer D, Bowman MK (2013) A caged, destabilized, free radical intermediate in the Q-cycle. ChemBioChem 14:1745–1753PubMedCentral CrossRef PubMed
  Völker M, Ono T, Inoue Y, Renger G (1985) Effect of trypsin on PS-II particles. Correlation between Hill-activity, Mn-abundance and peptide pattern. Biochim Biophys Acta 806:25–34CrossRef
  Wada K, Arnon DI (1971) Three forms of cytochrome b559 and their relation to the photosynthetic activity of chloroplasts. Proc Natl Acad Sci USA 68:3064–3068PubMedCentral CrossRef PubMed
  Whitmarsh J, Cramer WA (1978) A pathway for the reduction of cytochrome b-559 by photosystem II in chloroplasts. Biochim Biophys Acta 501:83–93CrossRef PubMed
  Wydrzynski T, Satoh K (eds) (2005) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Netherlands
  
• 作者单位：Olga P. Kaminskaya (1)
  Vladimir A. Shuvalov (1)
  
  1. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia
  
• 刊物类别：Physics and Astronomy
• 刊物主题：Physics
  Biophysics and Biomedical Physics
  Cell Biology
  Biochemistry
  Plant Physiology
  Animal Physiology
  Neurobiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1017

文摘

A complex redox titration pattern of cytochrome (Cyt) b559 in preparations of thylakoid membranes and photosystem (PS) II membrane fragments is commonly attributed to the presence of three conformational forms differing by a structure of the heme microenvironment. However, despite decades of research, structural determinants underlying differences between the redox forms of Cyt b559 have not been defined. In this work, we propose a different interpretation of redox heterogeneity in the native population of Cyt b559 assuming redox interaction between the Cyt b559 heme group and a nearby bound quinone (Q). The interacting quinone is supposed to be plastoquinone Q_C present in the unusual singly protonated form (Q_CH). The model successfully explains the unique redox properties of Cyt b559 and may provide a simple and effective mechanism of redox regulation of secondary electron transport in PS II. At the present time, the model of heme–quinone redox interaction can be considered as an alternative to the idea of conformational differences between the native redox forms of Cyt b559. Keywords Photosystem II Cyt b559 Plastoquinone Redox interaction