Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

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 QC present in the unusual singly protonated form (QCH). 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Scheme 1
Fig. 2
Fig. 3
Scheme 2

Similar content being viewed by others

References

  • Arnon DI, Tang GMS (1988) Cytochrome b-559 and proton conductance in oxygenic photosynthesis. Proc Natl Acad Sci USA 85:9524–9528

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 24:3638–3645

    Article  CAS  PubMed  Google Scholar 

  • 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 90:10942–10946

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ben-Hayyim G (1974) Light-induced absorbance changes of the high-potential cytochrome b559 in chloroplasts. Eur J Biochem 41:191–196

    Article  CAS  PubMed  Google Scholar 

  • 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 134:231–234

    Article  CAS  Google Scholar 

  • 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 31:11460–11471

    Article  CAS  PubMed  Google Scholar 

  • Biedermann G (1956) The basicity constant of p-benzoquinone. Acta Chem Scand 10:1340–1344

    Article  CAS  Google Scholar 

  • Bishop CA, Tong LKJ (1965) Equilibria of substituted semiquinones at high pH. J Am Chem Soc 87:501–505

    Article  CAS  Google Scholar 

  • Böhme H, Kunert KJ (1980) Photoreactions of cytochromes in algal chloroplasts. Eur J Biochem 106:329–336

    Article  PubMed  Google Scholar 

  • Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. Biochemistry 31:11449–11459

    Article  CAS  PubMed  Google Scholar 

  • Butler WL (1978) On the role of cytochrome b559 in oxygen evolution in photosynthesis. FEBS Lett 95:19–25

    Article  CAS  Google Scholar 

  • 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 87:9295–9299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817:26–43

    Article  CAS  PubMed  Google Scholar 

  • Cox RP, Bendall DS (1972) The effects on cytochrome b-559HP and P546 of treatments that inhibit oxygen evolution by chloroplasts. Biochim Biophys Acta 283:124–135

    Article  CAS  PubMed  Google Scholar 

  • Cox RP, Bendall DS (1974) The functions of plastoquinone and β-carotene in photosystem II of chloroplasts. Biochim Biophys Acta 347:49–59

    Article  CAS  PubMed  Google Scholar 

  • Crofts AR, Wright CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580

    Article  CAS  PubMed  Google Scholar 

  • Diner BA, Petrouleas V, Wendoloski JJ (1991) The iron-quinone electron-acceptor complex of photosystem II. Physiol Plant 81:423–436

    Article  CAS  Google Scholar 

  • Erixon K, Lozier R, Butler WL (1972) The redox state of cytochrome b559 in spinach chloroplasts. Biochim Biophys Acta 267:375–382

    Article  CAS  PubMed  Google Scholar 

  • Faller P, Pascal A, Rutherford AW (2001) β-carotene redox reactions in photosystem II: electron transfer pathway. Biochemistry 40:6431–6440

    Article  CAS  PubMed  Google Scholar 

  • 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 16:334–342

    Article  CAS  Google Scholar 

  • 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 11:1160–1171

    Article  CAS  PubMed  Google Scholar 

  • Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195

    Article  CAS  PubMed  Google Scholar 

  • 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 120:113–123

    Article  CAS  PubMed  Google Scholar 

  • 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 546:292–306

    Article  CAS  PubMed  Google Scholar 

  • 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 462:86–101

    Article  CAS  PubMed  Google Scholar 

  • 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 103:9855–9860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 1827:471–483

    Article  CAS  PubMed  Google Scholar 

  • 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 38:16223–16235

    Article  CAS  PubMed  Google Scholar 

  • 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 1708:333–341

    Article  CAS  PubMed  Google Scholar 

  • 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 46:1091–1105

    Article  CAS  PubMed  Google Scholar 

  • 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 1767:550–558

    Article  CAS  PubMed  Google Scholar 

  • Krishtalik LI, Tae GS, Cherepanov DA, Cramer WA (1993) The redox properties of cytochromes b imposed by the membrane electrostatic environment. Biophys J 65:184–195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laisk A, Eichelmann H, Oja V (2015) Oxidation of plastohydroquinone by photosystem II and by dioxygen in leaves. Biochim Biophys Acta 1847:565–575

    Article  CAS  PubMed  Google Scholar 

  • 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 1231:289–296

    Article  Google Scholar 

  • Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65

    Article  PubMed  Google Scholar 

  • Okayama S, Butler WL (1972) Extraction and reconstitution of photosystem II. Plant Physiol 49:769–774

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ortega JM, Hervas M, Losada M (1988) Redox and acid-base characterization of cytochrome b-559 in photosystem II particles. Eur J Biochem 171:449–455

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 68:71–75

    Article  CAS  Google Scholar 

  • Pospíšil P (2011) Enzymatic function of cytochrome b559 in photosystem II. J Photochem Photobiol B 104:341–347

    Article  PubMed  Google Scholar 

  • Renger G, Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98:53–80

    Article  CAS  PubMed  Google Scholar 

  • Rich PR, Bendall DS (1980) The redox potentials of the b-type cytochromes of higher plant chloroplasts. Biochim Biophys Acta 591:153–161

    Article  CAS  PubMed  Google Scholar 

  • Roncel M, Ortega JM, Losada M (2001) Factors determining the special redox properties of photosynthetic cytochrome b559. Eur J Biochem 268:4961–4968

    Article  CAS  PubMed  Google Scholar 

  • 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 8:206–216

    Article  CAS  PubMed  Google Scholar 

  • 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 133:14379–14388

    Article  CAS  PubMed  Google Scholar 

  • Samson G, Fork DC (1992) Simultaneous photoreduction and photooxidation of cytochrome b-559 in photosystem II treated with carbonylcyanide-m-chlorophenylhydrazone. Photosynth Res 33:203–212

    Article  CAS  PubMed  Google Scholar 

  • Shibamoto T, Kato Y, Watanabe T (2008) Spectroelectrochemistry of cytochrome b559 in the D1-D2-Cyt b559 complex from spinach. FEBS Lett 582:1490–1494

    Article  CAS  PubMed  Google Scholar 

  • Shinkarev VP (2006) Ubiquinone (coenzyme Q10) binding sites: low dielectric constant of the gate prevents the escape of the semiquinone. FEBS Lett 580:2534–2539

    Article  CAS  PubMed  Google Scholar 

  • Shinopoulos KE, Brudwig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817:66–75

    Article  CAS  PubMed  Google Scholar 

  • Stewart DH, Brudvig GW (1998) Cytochrome b559 of photosystem II. Biochim Biophys Acta 1367:63–87

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Thompson LK, Brudwig GW (1988) Cytochrome b-559 may function to protect photosystem II from photoinhibition. Biochemistry 27:6653–6658

    Article  CAS  PubMed  Google Scholar 

  • Thompson LK, Miller AF, Buser CA, De Paula JC, Brudwig GW (1989) Characterization of the multiple forms of cytochrome b559 in photosystem II. Biochemistry 28:8048–8056

    Article  CAS  PubMed  Google Scholar 

  • Tracewell CA, Brugwig GW (2008) Characterization of the secondary electron-transfer pathway intermediates of photosystem II containing low-potential cytochrome b559. Photosynth Res 98:189–197

    Article  CAS  PubMed  Google Scholar 

  • Tsujimoto HY, Arnon DI (1985) Differential inhibition by plastoquinone analogues of photoreduction of cytochrome b-559 in chloroplasts. FEBS Lett 179:51–54

    Article  CAS  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Ǻ. Nature 473:55–60

    Article  CAS  PubMed  Google Scholar 

  • Vennam PR, Fisher N, Krzyaniak MD, Kramer D, Bowman MK (2013) A caged, destabilized, free radical intermediate in the Q-cycle. ChemBioChem 14:1745–1753

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 806:25–34

    Article  Google Scholar 

  • Wada K, Arnon DI (1971) Three forms of cytochrome b559 and their relation to the photosynthetic activity of chloroplasts. Proc Natl Acad Sci USA 68:3064–3068

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whitmarsh J, Cramer WA (1978) A pathway for the reduction of cytochrome b-559 by photosystem II in chloroplasts. Biochim Biophys Acta 501:83–93

    Article  CAS  PubMed  Google Scholar 

  • Wydrzynski T, Satoh K (eds) (2005) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Netherlands

    Google Scholar 

Download references

Acknowledgments

The financial support from the RF program “Leading Scientific Schools” (grant NSh-4771.2014.4) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia

    Olga P. Kaminskaya & Vladimir A. Shuvalov

Authors
  1. Olga P. Kaminskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladimir A. Shuvalov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olga P. Kaminskaya.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaminskaya, O.P., Shuvalov, V.A. Towards an understanding of redox heterogeneity of the photosystem II cytochrome b559 in the native membrane. Eur Biophys J 45, 129–138 (2016). https://doi.org/10.1007/s00249-015-1082-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-015-1082-1

Keywords

Search

Navigation