Summary
The photosystem II core complex (PSIIcc) is a complicated membrane protein occurring in oxygenic photosynthetic organisms that catalyzes a key reaction, the light-induced oxidation of water. It consists of 17 membrane-spanning α-helical and three membrane-extrinsic protein subunits and binds nearly 100 cofactors. Among them is a heme protein composed of one heme b group ligated by two low molecular weight subunits with one transmembrane helix each, referred to as cytochrome (cyt) b 559. Despite extensive research, the role of cyt b 559 in PSIIcc is still not known. In the present chapter, the structure of cyt b 559 is reviewed based on recent crystallographic work together with its unusually complex redox behavior, and some ideas are discussed concerning a possible function of this unique heme protein.
Dedicated to the memory of Gernot Renger
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- 1.
The subscript number refers to the first observation of cyt b 559 due to a difference spectrum peak at 559 nm (Boardman and Anderson 1967). Curiously, the absorption maximum was later found to be rather close to 560 nm (Tae et al. 1993), and it was proposed to use the notation “cyt b 560” (Cramer 2004). Nonetheless, the common nomenclature “cyt b 559” appears to be irreversibly established, so that we use it here.
Abbreviations
- Car:
-
β-carotene
- Chl:
-
Chlorophyll
- Cyt:
-
Cytochrome
- DCMU:
-
3-(3,4-dichlorophenyl)-1, 1-dimethylurea
- DQH2 :
-
Duroquinol
- EPR:
-
Electron paramagnetic resonance
- HP:
-
High potential
- IP:
-
Intermediate potential
- LMW:
-
Low molecular weight subunit
- LP:
-
Low potential
- PQ:
-
Plastoquinone
- PQH2 :
-
Plastoquinol
- PSII:
-
Photosystem II
- PSIIcc:
-
Photosystem II core complex
- RC:
-
Reaction center
- ROS:
-
Reactive oxygen species
- RR:
-
Resonance Raman
- TMH:
-
Trans-membrane helix
- VLP:
-
Very low potential
- WOC:
-
Water-oxidizing complex
References
Ahmad I, Giorgi LB, Barber J, Porter G, Klug DR (1993) Redox potentials of cytochrome b-559 in the D1/D2/cytochrome b-559 reaction centre of Photosystem II. Biochim Biophys Acta 1143:239–242
Akdogan Y, Anbazhagan V, Hinderberger D, Schneider D (2012) Heme binding constricts the conformational dynamics of the cytochrome b 559’ heme binding cavity. Biochemistry 51:7149–7156
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
Barber J, De Las Rivas J (1993) A functional model for the role of cytochrome b 559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA 90:10942–10946
Barkigia KM, Chantranupong L, Smith KM, Fajer J (1988) Structural and theoretical models of photosynthetic chromophores. Implications for redox, light absorption properties and vectorial electron flow. J Am Chem Soc 110:7566–7567
Beck WF, de Paula JC, Brudvig GW (1985) Active and resting states of the O2-evolving complex of Photosystem II. Biochemistry 24:3035–3043
Bérczi A, Moller IM (2000) Redox enzymes in the plant plasma membrane and their possible roles. Plant Cell Environ 23:1287–1302
Bergström J, Vänngard T (1982) EPR signals and orientation of cytochromes in the spinach chloroplast thylakoid membrane. Biochim Biophys Acta 682:452–456
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
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
Biesiadka J, Loll B, Kern J, Irrgang KD, Zouni A (2004) Crystal structure of cyanobacterial Photosystem II at 3.2 Å resolution: a closer look at the Mn-cluster. Phys Chem Chem Phys 6:4733–4736
Boardman NK, Anderson JM (1967) Fractionation of photochemical systems of photosynthesis. 2. Cytochrome and carotenoid contents of particles isolated from spinach chloroplasts. Biochim Biophys Acta 143:187–203
Bondarava N, de Pascalis L, Al-Babili S, Goussias C, Golecki JR, Beyer P, Bock R, Krieger-Liszkay A (2003) Evidence that cytochrome b 559 mediates the oxidation of reduced plastoquinone in the dark. J Biol Chem 278:13554–13560
Boussac A, Koyama K, Sugiura M (2013) The Tll0287 protein is a hemoprotein associated with the PsbA2-Photosystem II complex in Thermosynechococcus elongatus. Biochim Biophys Acta 1827:1174–1182
Brandl M, Weiss MS, Jabs A, Sühnel J, Hilgenfeld R (2001) C − H · · · π-interactions in proteins. J Mol Biol 307:357–377
Bricker TM, Burnap RL (2005) The extrinsic proteins of Photosystem II. In: Wydrzynski T, Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht, pp 95–120
Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of Photosystem II. Biochim Biophys Acta 1817:121–142
Brose K, Zouni A, Müh F, Mroginski MA, Maultzsch J (2013) Simulations of the polarisation-dependent Raman intensity of β-carotene in Photosystem II crystals. Chem Phys 418:65–73
Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b 559 in oxygen-evolving Photosystem II. Biochemistry 31:11449–11459
Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant Photosystem II supercomplexes. EMBO J 28:3052–3063
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
Chapman DJ, Gounaris K, Barber J (1988) Electron-transport properties of the isolated D1-D2-cytochrome b-559 Photosystem II reaction centre. Biochim Biophys Acta 933:423–431
Choma C, Gratkowski H, Lear JD, DeGrado WF (2000) Asparagine-mediated self-association of a model transmembrane helix. Nat Struct Biol 7:161–166
Chothia C, Levitt M, Richardson D (1977) Structure of proteins – packing of α-helices and pleated sheets. Proc Natl Acad Sci USA 74:4130–4134
Cramer WA (2004) Ironies in photosynthetic electron transport: a personal perspective. Photosynth Res 80:293–305
Cramer WA, Whitmarsh J (1977) Photosynthetic cytochromes. Annu Rev Plant Physiol 28:133–172
Crowder MS, Prince RC, Bearden A (1982) Orientation of membrane-bound cytochromes in chloroplasts, detected by low-temperature EPR spectroscopy. FEBS Lett 144:204–208
Faller P, Fufezan C, Rutherford AW (2005) Side-path electron donors: cytochrome b 559, chlorophyll Z and β-carotene. In: Wydrzynski T, Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht, pp 347–365
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Frank HA, Brudvig GW (2004) Redox functions of carotenoids in photosynthesis. Biochemistry 43:8607–8615
Gámiz-Hernández AP, Kieseritzky G, Galstyan AS, Demir-Kavuk O, Knapp EW (2010) Understanding properties of cofactors in proteins: redox potentials of synthetic cytochromes b. ChemPhysChem 11:1196–1206
García-Cerdán JG, Sveshnikov D, Dewez D, Jansson S, Funk C, Schröder WP (2009) Antisense inhibition of the PsbX protein affects PSII integrity in the higher plant Arabidopsis thaliana. Plant Cell Physiol 50:191–202
Garewal HS, Wasserman AR (1974a) Triton X-100-4 M urea as an extraction medium for membrane proteins. I. Purification of chloroplast cytochrome b 559. Biochemistry 13:4063–4071
Garewal HS, Wasserman AR (1974b) Triton X-100-4 M urea as an extraction medium for membrane proteins. II. Molecular properties of pure cytochrome b 559: a lipoprotein containing small polypeptide chains and a limited lipid composition. Biochemistry 13:4072–4079
Guerrero F, Zurita JL, Roncel M, Kirilovsky D, Ortega JM (2014) The role of the high potential form of the cytochrome b559: study of Thermosynechococcus elongatus mutants. Biochim Biophys Acta 1837:908–919
Gurezka R, Langosch D (2001) In vitro selection of membrane-spanning leucine zipper protein-protein interaction motifs using POSSYCCAT. J Biol Chem 276:45580–45587
Gurezka R, Laage R, Brosig B, Langosch D (1999) A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments. J Biol Chem 274:9265–9270
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial Photosystem II at 2.9 Å resolution: role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342
Guskov A, Gabdulkhakov A, Broser M, Glöckner C, Hellmich J, Kern J, Frank J, …, Zouni A (2010) Recent progress in the crystallographic studies of photosystem II. ChemPhysChem 11:1160–1171
Hager M, Hermann M, Biehler K, Krieger-Liszkay A, Bock R (2002) Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of Photosystem II, reduced Photosystem I levels, and hypersensitivity to light. J Biol Chem 277:14031–14039
Herrmann RG, Alt J, Schiller B, Widger WR, Cramer WA (1984) Nucleotide-sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome – implications for the structure of the membrane protein. FEBS Lett 176:239–244
Horton P, Croze E (1977) The relationship between activity of chloroplast Photosystem II and the midpoint oxidation-reduction potential of cytochrome b-559. Biochim Biophys Acta 462:86–101
Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33–38
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 1827:471–483
Kaminskaya O, Kurreck J, Irrgang KD, Renger G, Shuvalov VA (1999) Redox and spectral properties of cytochrome b 559 in different preparations of Photosystem II. Biochemistry 38:16223–16235
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
Kaminskaya O, Shuvalov VA, Renger G (2007) Evidence for a novel quinone-binding site in the Photosystem II (PS II) complex that regulates the redox potential of cytochrome b559. Biochemistry 46:1091–1105
Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100:98–103
Kashino Y, Takahashi T, Inoue-Kashino N, Ban A, Ikeda Y, Satoh K, Sugiura M (2007) Ycf12 is a core subunit in the Photosystem II complex. Biochim Biophys Acta 1767:1269–1275
Kato Y, Shibamoto T, Yamamoto S, Watanabe T, Ishida N, Sugiura M, Rappaport F, Boussac A (2012) Influence of the PsbA1/PsbA3, Ca2+/Sr2+ and Cl-/Br- exchanges on the redox potential of the primary quinone QA in Photosystem II from Thermosynechococcus elongatus as revealed by spectroelectrochemistry. Biochim Biophys Acta 1817:1998–2004
Katoh H, Ikeuchi M (2001) Targeted disruption of psbX and biochemical characterization of Photosystem II complex in the thermophilic cyanobacterium Synechococcus elongatus. Plant Cell Physiol 42:179–188
Kawakami K, Iwai M, Ikeuchi M, Kamiya N, Shen JR (2007) Location of PsbY in oxygen-evolving Photosystem II revealed by mutagenesis and X-ray crystallography. FEBS Lett 581:4983–4987
Kern J, Guskov A (2011) Lipids in Photosystem II: multifunctional cofactors. J Photochem Photobiol B 104:19–34
Kern J, Loll B, Lüneberg C, DiFiore D, Biesiadka J, Irrgang KD, Zouni A (2005) Purification, characterisation and crystallisation of Photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim Biophys Acta 1706:147–157
Kim SJ, Robinson D, Robinson C (1996) An Arabidopsis thaliana cDNA encoding PS II-X, a 4.1 kDa component of Photosystem II: a bipartite presequence mediates SecA/delta pH-independent targeting into thylakoids. FEBS Lett 390:175–178
Komenda J, Reisinger V, Müller BC, Dobáková M, Granvogl B, Eichacker LA (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the Photosystem II reaction center complex in Synechocystis PCC 6803. J Biol Chem 279:48620–48629
Komenda J, Nickelsen J, Tichy M, Prasil O, Eichacker LA, Nixon PJ (2008) The cyanobacterial homologue of HCF136/YCF48 is a component of an early Photosystem II assembly complex and is important for both the efficient assembly and repair of Photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 283:22390–22399
Koua FH, Umena Y, Kawakami K, Shen JR (2013) Structure of Sr-substituted Photosystem II at 2.1 Å resolution and its implications in the mechanism of water oxidation. Proc Natl Acad Sci USA 110:3889–3894
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
Kruk J, Strzalka K (1999) Dark reoxidation of the plastoquinone-pool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids. Photosynth Res 62:273–279
Kruk J, Strzalka K (2001) Redox changes of cytochrome b 559 in the presence of plastoquinones. J Biol Chem 276:86–91
Kuwabara T, Murata N (1982) Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the Photosystem II particles of spinach-chloroplasts. Plant Cell Physiol 23:533–539
Langosch D, Arkin IT (2009) Interaction and conformational dynamics of membrane-spanning protein helices. Protein Sci 18:1343–1358
Lind LK, Shukla VK, Nyhus KJ, Pakrasi HB (1993) Genetic and immunological analyses of the cyanobacterium Synechocystis sp. PCC 6803 show that the protein encoded by the psbJ gene regulates the number of Photosystem II centers in thylakoid membranes. J Biol Chem 268:1575–1579
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 438:1040–1044
Loll B, Broser M, Kos PB, Kern J, Biesiadka J, Vass I, Saenger W, Zouni A (2008) Modeling of variant copies of subunit D1 in the structure of Photosystem II from Thermosynechococcus elongatus. Biol Chem 389:609–617
Lu PL, Ma D, Yan CY, Gong XQ, Du MJ, Shi YG (2014) Structure and mechanism of a eukaryotic transmembrane ascorbate-dependent oxidoreductase. Proc Natl Acad Sci USA 111:1813–1818
Mant A, Robinson C (1998) An Arabidopsis cDNA encodes an apparent polyprotein of two non-identical thylakoid membrane proteins that are associated with Photosystem II and homologous to algal ycf32 open reading frames. FEBS Lett 423:183–188
McNamara VP, Gounaris K (1995) Granal Photosystem II complexes contain only the high redox potential form of cytochrome b-559 which is stabilized by the ligation of calcium. Biochim Biophys Acta 1231:289–296
Meetam M, Keren N, Ohad I, Pakrasi HB (1999) The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 121:1267–1272
Moore DT, Berger BW, DeGrado WF (2008) Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure 16:991–1001
Mor TS, Ohad I, Hirschberg J, Pakrasi HB (1995) An unusual organization of the genes encoding cytochrome b 559 in Chlamydomonas reinhardtii: psbE and psbF genes are separately transcribed from different regions of the plastid chromosome. Mol Gen Genet 246:600–604
Morais F, Barber J, Nixon PJ (1998) The chloroplast-encoded a subunit of cytochrome b-559 is required for assembly of the Photosystem two complex in both the light and the dark in Chlamydomonas reinhardtii. J Biol Chem 273:29315–29320
Mörschel E, Schatz GH (1987) Correlation of Photosystem II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172:145–154
Moskalenko AA, Barbato R, Giacometti GM (1992) Investigation of the neighbour relationships between Photosystem II polypeptides in the two types of isolated reaction centres (D1/D2/cytb 559 and CP47/D1/D2/cyt b 559 complexes). FEBS Lett 314:271–274
Müh F, Zouni A (2013) The nonheme iron in Photosystem II. Photosynth Res 116:295–314
Müh F, Renger T, Zouni A (2008) Crystal structure of cyanobacterial Photosystem II at 3.0 Å resolution: a closer look at the antenna system and the small membrane-intrinsic subunits. Plant Physiol Biochem 46:238–264
Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in Photosystem II. Biochim Biophys Acta 1817:44–65
Müller B, Eichacker LA (1999) Assembly of the D1 precursor in monomeric Photosystem II reaction center precomplexes precedes chlorophyll a-triggered accumulation of reaction center II in barley etioplasts. Plant Cell 11:2365–2377
Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710
Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta 1817:247–257
Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, …, Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9:123–130, Suppl. 135–148
Nanba O, Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84:109–112
Nixon PJ, Michoux F, Yu JF, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of Photosystem II. Ann Bot 106:1–16
Nowaczyk MM, Sander J, Grasse N, Cormann KU, Rexroth D, Bernat G, Rögner M (2010) Dynamics of the cyanobacterial photosynthetic network: communication and modification of membrane protein complexes. Eur J Cell Biol 89:974–982
Nowaczyk MM, Krause K, Mieseler M, Sczibilanski A, Ikeuchi M, Rögner M (2012) Deletion of psbJ leads to accumulation of Psb27-Psb28 Photosystem II complexes in Thermosynechococcus elongatus. Biochim Biophys Acta 1817:1339–1345
Nowicka B, Kruk J (2010) Occurrence, biosynthesis and function of isoprenoid quinones. Biochim Biophys Acta 1797:1587–1605
Ohad I, Dal Bosco C, Herrmann RG, Meurer J (2004) Photosystem II proteins PsbL and PsbJ regulate electron flow to the plastoquinone pool. Biochemistry 43:2297–2308
Olea C, Boon EM, Pellicena P, Kuriyan J, Marletta MA (2008) Probing the function of heme distortion in the H-NOX family. ACS Chem Biol 3:703–710
Olea C, Kuriyan J, Marletta MA (2010) Modulating heme redox potential through protein-induced porphyrin distortion. J Am Chem Soc 132:12794–12795
Ortega JM, Hervás M, Losada M (1988) Redox and acid-base characterization of cytochrome b-559 in Photosystem II particles. Eur J Biochem 171:449–455
Ortega JM, Hervas M, Delarosa MA, Losada M (1994) Redox properties of cytochrome b559 in photosynthetic membranes from the cyanobacterium Synechocystis sp. PCC 6803. J Plant Physiol 144:454–461
Pakrasi HB, Williams JG, Arntzen CJ (1988) Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b 559 in Photosystem II. EMBO J 7:325–332
Pakrasi HB, Deciechi P, Whitmarsh J (1991) Site directed mutagenesis of the heme axial ligands of cytochrome b559 affects the stability of the Photosystem II complex. EMBO J 10:1619–1627
Pogson BJ, Rissler HM, Frank HA (2005) The role of carotenoids in energy quenching. In: Wydrzynski T, Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht, pp 515–537
Pospisil P (2011) Enzymatic function of cytochrome b 559 in Photosystem II. J Photochem Photobiol B 104:341–347
Radmer R, Cammarata K, Tamura N, Ollinger O, Cheniae G (1986) Depletion of Photosystem II-extrinsic proteins. 1. Effects on O2-flash and N2-flash yields and steady-state O2 evolution. Biochim Biophys Acta 850:21–32
Regel RE, Ivleva NB, Zer H, Meurer J, Shestakov SV, Herrmann RG, Pakrasi HB, Ohad I (2001) Deregulation of electron flow within Photosystem II in the absence of the PsbJ protein. J Biol Chem 276:41473–41478
Renger G (ed) (2008) Primary Processes of Photosynthesis – Principles and Apparatus, vol 1, 2, Comprehensive Series in Photochemistry and Photobiology, vol 8, 9. RSC Publishing, Cambridge
Renger T, Schlodder E (2011) Optical properties, excitation energy and primary charge transfer in Photosystem II: theory meets experiment. J Photochem Photobiol B 104:126–141
Roncel M, Ortega JM, Losada M (2001) Factors determining the special redox properties of photosynthetic cytochrome b559. Eur J Biochem 268:4961–4968
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
Sander J, Nowaczyk M, Buchta J, Dau H, Vass I, Deak Z, Dorogi M, …, Rögner M (2010) Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection. J Biol Chem 285:29851–29856
Shelnutt JA, Song XZ, Ma JG, Jia SL, Jentzen W, Medforth CJ (1998) Nonplanar porphyrins and their significance in proteins. Chem Soc Rev 27:31–41
Sheridan RP, Levy RM, Salemme FR (1982) α-helix dipole model and electrostatic stabilization of 4-α-helical proteins. Proc Natl Acad Sci USA 79:4545–4549
Shi LX, Schröder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex, Photosystem II. Biochim Biophys Acta 1608:75–96
Shi LX, Hall M, Funk C, Schröder WP (2012) Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins. Biochim Biophys Acta 1817:13–25
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
Shinopoulos KE, Brudvig GW (2012) Cytochrome b 559 and cyclic electron transfer within Photosystem II. Biochim Biophys Acta 1817:66–75
Shinopoulos KE, Yu J, Nixon PJ, Brudvig GW (2014) Using site-directed mutagenesis to probe the role of the D2 carotenoid in the secondary electron-transfer pathway of Photosystem II. Photosynth Res 120:141–152
Shuvalov VA (1994) Composition and function of cytochrome b559 in reaction centers of Photosystem II of green plants. J Bioenerg Biomembr 26:619–626
Shuvalov VA, Schreiber U, Heber U (1994) Spectral and thermodynamic properties of the two hemes of the D1D2cytochrome b-559 complex of spinach. FEBS Lett 337:226–230
Sicora CI, Ho FM, Salminen T, Styring S, Aro EM (2009) Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. Biochim Biophys Acta 1787:105–112
Stewart AC, Bendall DS (1980) Photosynthetic electron transport in a cell-free preparation from the thermophilic blue-green alga Phormidium laminosum. Biochem J 188:351–361
Stewart DH, Brudvig GW (1998) Cytochrome b 559 of Photosystem II. Biochim Biophys Acta 1367:63–87
Sugiura M, Inoue Y (1999) Highly purified thermo-stable oxygen-evolving Photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol 40:1219–1231
Sugiura M, Iwai E, Hayashi H, Boussac A (2010a) Differences in the interactions between the subunits of Photosystem II dependent on D1 protein variants in the thermophilic cyanobacterium Thermosynechococcus elongatus. J Biol Chem 285:30008–30018
Sugiura M, Kato Y, Takahashi R, Suzuki H, Watanabe T, Noguchi T, Rappaport F, Boussac A (2010b) Energetics in Photosystem II from Thermosynechococcus elongatus with a D1 protein encoded by either the psbA 1 or psbA 3 gene. Biochim Biophys Acta 1797:1491–1499
Sugiura M, Ogami S, Kusumi M, Un S, Rappaport F, Boussac A (2012) Environment of TyrZ in Photosystem II from Thermosynechococcus elongatus in which PsbA2 is the D1 protein. J Biol Chem 287:13336–13347
Sugiura M, Azami C, Koyama K, Rutherford AW, Rappaport F, Boussac A (2014) Modification of the pheophytin redox potential in Thermosynechococcus elongatus Photosystem II with PsbA3 as D1. Biochim Biophys Acta 1837:139–148
Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro EM (2004) Protein assembly of Photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271:96–107
Swiatek M, Regel RE, Meurer J, Wanner G, Pakrasi HB, Ohad I, Herrmann RG (2003) Effects of selective inactivation of individual genes for low-molecular-mass subunits on the assembly of Photosystem II, as revealed by chloroplast transformation: the psbEFLJ operon in Nicotiana tabacum. Mol Genet Genomics 268:699–710
Tae GS, Cramer WA (1992) Truncation of the COOH-terminal domain of the psbE gene product in Synechocystis sp. PCC 6803: requirements for Photosystem II assembly and function. Biochemistry 31:4066–4074
Tae GS, Cramer WA (1994) Topography of the heme prosthetic group of cytochrome b-559 in the Photosystem II reaction center. Biochemistry 33:10060–10068
Tae GS, Black MT, Cramer WA, Vallon O, Bogorad L (1988) Thylakoid membrane protein topography: transmembrane orientation of the chloroplast cytochrome b-559 psbE gene product. Biochemistry 27:9075–9080
Tae GS, Everly RM, Cramer WA, Madgwick SA, Rich PR (1993) On the question of the identity of cytochrome b 560 in thylakoid stromal membranes. Photosynth Res 36:141–146
Thompson LK, Brudvig GW (1988) Cytochrome b-559 may function to protect Photosystem II from photoinhibition. Biochemistry 27:6653–6658
Thompson LK, Miller AF, Buser CA, de Paula JC, Brudvig GW (1989) Characterization of the multiple forms of cytochrome b 559 in Photosystem II. Biochemistry 28:8048–8056
Thompson SJ, Robinson C, Mant A (1999) Dual signal peptides mediate the signal recognition particle/sec-independent insertion of a thylakoid membrane polyprotein, PsbY. J Biol Chem 274:4059–4066
Thornton LE, Roose JL, Pakrasi HB, Ikeuchi M (2005) The low molecular weight proteins of Photosystem II. In: Wydrzynski T, Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht, pp 121–137
Tiwari A, Pospisil P (2009) Superoxide oxidase and reductase activity of cytochrome b559 in Photosystem II. Biochim Biophys Acta 1787:985–994
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å. Nature 473:55–60
Vallon O, Tae GS, Cramer WA, Simpson D, Hoyer-Hansen G, Bogorad L (1989) Visualization of antibody binding to the photosynthetic membrane: the transmembrane orientation of cytochrome b-559. Biochim Biophys Acta 975:132–141
Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209–217
Völker M, Ono T, Inoue Y, Renger G (1985) Effect of trypsin on PSII particles. Correlation between hill-activity, Mn-abundance and peptide pattern. Biochim Biophys Acta 806:25–34
Walters RFS, DeGrado WF (2006) Helix-packing motifs in membrane proteins. Proc Natl Acad Sci USA 103:13658–13663
Waters ML (2002) Aromatic interactions in model systems. Curr Opin Chem Biol 6:736–741
Whitmarsh J, Pakrasi HB (1996) Form and function of cytochrome b-559. In: Ort DR, Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions. Kluwer, Dordrecht, pp 249–264
Widger WR, Cramer WA, Hermodson M, Herrmann RG (1985) Evidence for a hetero-oligomeric structure of the chloroplast cytochrome b-559. FEBS Lett 191:186–190
Yamashita T (1986) Modification of oxygen evolving center by tris-washing. Photosynth Res 10:473–481
Zhou FX, Cocco MJ, Russ WP, Brunger AT, Engelman DM (2000) Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat Struct Biol 7:154–160
Zouni A (2008) From cell growth to the 3.0 Å resolution crystal structure of cyanobacterial Photosystem II. In: Renger G (ed) Primary Processes of Photosynthesis, Principles and Apparatus, vol 2. RSC Publishing, Cambridge, MA, pp 193–236
Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743
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This work was supported by the Deutsche Forschungsgemeinschaft through SFB 1078 (project A5) and Cluster of Excellence “UniCat” coordinated by the Technische Universität Berlin (project E3/D3).
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Müh, F., Zouni, A. (2016). Cytochrome b 559 in Photosystem II. In: Cramer, W., Kallas, T. (eds) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Advances in Photosynthesis and Respiration, vol 41. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7481-9_8
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