Abstract
3-Å crystal structures of the cytochrome b6f complex have provided a structural framework for the photosynthetic electron transport chain. The structures of the 220,000 molecular weight dimeric cytochrome b6f complex from the thermophilic cyanobacterium, Mastigocladis laminosus (Kurisu et al. 2003, Science 302: 1009–1014), and the green alga, Chlamydomonas reinhardtii (Stroebel et al. 2003, Nature 426: 413–418), are very similar. The latter is the first structure of a integral membrane photosynthetic electron transport complex from a eukaryotic source. The M. laminosus and C. reinhardtii structures have provided structural information and experimental insights to the properties and functions of three native and novel prosthetic groups, a chlorophyll a, a β-carotene, and a unique heme x, one copy of which is found in each monomer of the cytochrome b6f complex, but not the cytochrome bc1 complex from the mitochondrial respiratory chain of animals and yeast. Several functional insights have emerged from the structures including the function of the dimer; the properties of heme x; the function of the inter-monomer quinone-exchange cavity; a quinone diffusion pathway through relatively narrow crevices or portals; a modified reaction scheme for n-side quinone redox reactions; a necessarily novel mechanism for quenching of the bound chlorophyll triplet state; a possible role for the bound chlorophyll a in activation of the LHC kinase; and a structural and assembly role for the four small PetG, L, M, and N subunits. An ‘hors d’oeuvres hypothesis’ for assembly of the complex is proposed for the small ‘hydrophobic stick’ or ‘picket fence’ polypeptides at the periphery of the complex, based on the cis-positive orientation of the small hydrophobic subunits and the ‘toothpick’ binding mode of the β-carotene.
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Abbreviations
- Chl:
-
chlorophyll
- cis-side:
-
the side of membrane from which polypeptides are inserted into a membrane
- cyt:
-
cytochrome
- DOPC:
-
1,2-dioleoyl-sn-glycero-3-phosphocholine
- ISP:
-
iron-sulphur-protien
- LHC:
-
light-harvesting chlorophyll protein
- PC:
-
plastocyanin
- Pet:
-
photosynthetic electron transport
- p-and n-:
-
electrochemically negative and positive sides of the membrane
- SDS-PAGE:
-
sodium-dodecylsulfate polyacrylamide gel electrophoresis
- TM:
-
trans-membrane
References
JF Allen (2004) ArticleTitleCytochrome b6f: structure for signalling and vectorial metabolism Trends Plant Sci 9 130–137
M Avron (1964) ArticleTitleOn the mechanism of photophosphorylation in chloroplasts Rec Chem Prog 25 237–246
J Bennett EK Shaw H Michel (1988) ArticleTitleCytochrome b6f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes Eur J Biochem 171 95–100
MT Black WR Widger WA Cramer (1987) ArticleTitleLarge-scale purification of active cytochrome b6/f complex from spinach chloroplasts Arch Biochem Biophys 252 655–661
NK Boardman JM Anderson (1967) ArticleTitleFractionation of the photochemical systems of photosynthesis. II. Cytochrome and carotenoid contents of particles isolated from spinach chloroplasts Biochim Biophys Acta 143 187–203
RS Cantor (1999) ArticleTitleLipid composition and the lateral pressure profile in bilayers Biophys J 76 2625–2639
CJ Carrell H Zhang WA Cramer JL Smith (1997) ArticleTitleBiological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein Structure 5 1613–1625
CJ Carrell BG Schlarb DS Bendall CJ Howe WA Cramer JL Smith (1999) ArticleTitleStructure of the soluble domain of cytochrome f from the cyanobacterium Phormidium laminosum Biochemistry 38 9590–9599
YI Chi LS Huang Z Zhang JG Fernandez-Velasco EA Berry (2000) ArticleTitleX-ray structure of a truncated form of cytochrome f from Chlamydomonas reinhardtii Biochemistry 39 7689–7701
RD Clark G Hind (1983) ArticleTitleIsolation of a five-polypeptide cytochrome b-f complex from spinach chloroplasts J Biol Chem 258 10348–10354
WA Cramer WL Butler (1967) ArticleTitleLight-induced absorbance changes of two cytochrome b components in the electron-transport system of spinach chloroplasts Biochim Biophys Acta 143 332–339
WA Cramer H Zhang J Yan G Kurisu JL Smith (2004) ArticleTitleEvolution of photosynthesis: time-independent structure of the cytochrome b6f complex Biochemistry 43 5921–5929
HE Davenport R Hill (1952) ArticleTitleThe preparation and some properties of cytochrome f Proc Roy Soc Lond B Biol Sci 139 327–345
C Vitry Particlede A Desbois V Redeker F Zito FA Wollman (2004) ArticleTitleBiochemical and spectroscopic characterization of the covalent binding of heme to cytochrome b6 Biochemistry 43 3956–3968
PN Furbacher ME Girvin WA Cramer (1989) ArticleTitleOn the question of interheme electron transfer in the chloroplast cytochrome b6 in situ Biochemistry 28 8990–8998
JC Gray (1978) ArticleTitlePurification and properties of monomeric cytochrome f from charlock, Sinapis arvensis L Eur J Biochem 82 133–141
EB Gutierrez-Cirlos BL Trumpower (2002) ArticleTitleInhibitory analogs of ubiquinol act anti-cooperatively on the Yeast cytochrome bc1 complex Evidence for an alternating, half-of-the-sites mechanism of ubiquinol oxidation J Biol Chem 277 1195–1202
G Hind JM Olson (1966) ArticleTitleLight-induced changes in cytochrome b6 in spinach chloroplasts Brookhaven Symp Biol 19 188–194
D Huang RM Everly RH Cheng JB Heymann H Schagger V Sled T Ohnishi TS Baker WA Cramer (1994) ArticleTitleCharacterization of the chloroplast cytochrome b6f complex as a structural and functional dimer Biochemistry 33 4401–4409
C Hunte J Koepke C Lange T Rossmanith H Michel (2000) ArticleTitleStructure at 2.3 Å resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment Structure 8 669–684
E Hurt G Hauska (1981) ArticleTitleA cytochrome f/b6 complex of five polypeptides with plastoquinol-plastocyanin-oxidoreductase activity from spinach chloroplasts Eur J Biochem 117 591–595
EC Hurt G Hauska (1983) ArticleTitlecytochrome b6 from isolated cytochrome b6f complexes: evidence for two spectral forms with different midpoint potentials FEBS Lett 153 413–419
S Iwata C Ostermeier B Ludwig H Michel (1995) ArticleTitleStructure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans Nature 376 660–669
S Iwata M Saynovits TA Link H Michel (1996) ArticleTitleStructure of a water soluble fragment of the ‘Rieske’ iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 Å resolution Structure 4 567–579
P Joliot A Joliot (1988) ArticleTitleThe low-potential electron-transfer chain in the cytochrome b/f complex Biochem Biophys Acta 933 319–333
DM Kramer AR Crofts (1994) ArticleTitleRe-examination of the properties and function of the b cytochrome of the thylakoid cytochrome bf complex Biochem Biophys Acta 1184 193–201
LI Krishtalik WA Cramer (1995) ArticleTitleOn the physical basis for the cis-positive rule describing protein orientation in biological membranes FEBS Lett 369 140–143
J Kroliczewski A Szczepaniak (2002) ArticleTitleIn vitro reconstitution of the spinach chloroplast cytochrome b6 protein from a fusion protein expressed in Escherichia coli Biochim Biophys Acta 1598 177–184
G Kurisu H Zhang JL Smith WA Cramer (2003) ArticleTitleStructure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity Science 302 1009–1014
EM Landau JP Rosenbusch (1996) ArticleTitleLipidic cubic phases: a novel concept for the crystallization of membrane proteins Proc Natl Acad Sci USA 93 14532–14535
J Lavergne (1983) ArticleTitleMembrane potential-dependent reduction of cytochrome b6 in an algal mutant lacking Photosystem I centers Biochem Biophys Acta 725 25–33
TA Link WR Hagen AJ Pierik C Assmann G Jagow Particlevon (1992) ArticleTitleDetermination of the redox properties of the Rieske [2Fe-2S] cluster of bovine heart bc1 complex by direct electrochemistry of a water-soluble fragment Eur J Biochem 208 685–691
R Malkin HB Posner (1978) ArticleTitleOn the site of function of the Rieske iron-sulfur center in the chloroplast electron transport chain Biochim Biophys Acta 501 552–554
SE Martinez D Huang A Szczepaniak WA Cramer JL Smith (1994) ArticleTitleCrystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation Structure 2 95–105
SE Martinez D Huang M Ponomarev WA Cramer JL Smith (1996) ArticleTitleThe heme redox center of chloroplast cytochrome f is linked to a buried five-water chain Protein Sci 5 1081–1092
H Michel (1990) Crystallization of Membrane Proteins CRC Press Boca Raton
N Nelson J Neumann (1972) ArticleTitleIsolation of a cytochrome b6f particle from chloroplasts J Biol Chem 247 1817–1824
E Pebay-Peyroula JP Rosenbusch (2001) ArticleTitleHigh-resolution structures and dynamics of membrane protein-lipid complexes: a critique Curr Opin Struct Biol 11 427–432
EJ Peterman SO Wenk T Pullerits LO Palsson R Grondelle Particlevan JP Dekker M Rogner H Amerongen Particlevan (1998) ArticleTitleFluorescence and absorption spectroscopy of the weakly fluorescent chlorophyll a in cytochrome b6f of Synechocystis PCC6803 Biophys J 75 389–398
Y Pierre C Breyton D Kramer JL Popot (1995) ArticleTitlePurification and characterization of the cytochrome b6f complex from Chlamydomonas reinhardtii J Biol Chem 270 29342–29349
G Sainz CJ Carrell MV Ponamarev GM Soriano WA Cramer JL Smith (2000) ArticleTitleInterruption of the internal water chain of cytochrome f impairs photosynthetic function Biochemistry 39 9164–9173
CL Schmidt R Malkin (1993) ArticleTitleLow molecular weight subunits associated with the cytochrome b6f complexes from spinach and Chlamydomonas reinhardtii Photosynth Res 38 73–81
L Sipos G Heijne Particlevon (1993) ArticleTitlePredicting the topology of eukaryotic membrane proteins Eur J Biochem 213 1333–1340
Smith JL, Zhang H, Yan J, Kurisu G and Cramer WA (2004). cytochrome bc complexes: a common core of structure and function surrounded by diversity in the outlying provinces. Curr Opin Struct Biol
GM Soriano MV Ponamarev CJ Carrell D Xia JL Smith WA Cramer (1999) ArticleTitleComparison of the cytochrome bc1 complex with the anticipated structure of the cytochrome b6f complex: le plus ca change le plus c’est la meme chose J Bioenerg Biomembr 31 201–213
D Stroebel Y Choquet JL Popot D Picot (2003) ArticleTitleAn atypical haem in the cytochrome b6f complex Nature 426 413–418
JP Whitelegge H Zhang R Aguilera RM Taylor WA Cramer (2002) ArticleTitleFull subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+). of an oligomeric membrane protein: cytochrome b6f complex from spinach and the cyanobacterium Mastigocladus laminosus Mol Cell Proteomics 1 816–827
WR Widger WA Cramer RG Herrmann A Trebst (1984) ArticleTitleSequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex: position of the cytochrome b hemes in the membrane Proc Natl Acad Sci USA 81 674–678
RM Wynn J Bertsch BD Bruce R Malkin (1988) ArticleTitleGreen algal cytochrome b6-f complexes: isolation and characterization from Dunaliella saline, Chlamydomonas reinhardtii and Scenedesmus obliquus Biochim Biophys Acta 935 115–122
D Xia CA Yu H Kim JZ Xia AM Kachurin L Zhang L Yu J Deisenhofer (1997) ArticleTitleCrystal structure of the cytochrome bc1 complex from bovine heart mitochondria Science 277 60–66
S Yoshikawa K Shinzawa-Itoh T Tsukihara (1998) ArticleTitleCrystal structure of bovine heart cytochrome c oxidase at 2.8 Å resolution J Bioenerg Biomembr 30 7–14
H Zhang CJ Carrell D Huang V Sled T Ohnishi JL Smith WA Cramer (1996) ArticleTitleCharacterization and crystallization of the lumen side domain of the chloroplast Rieske iron-sulfur protein J Biol Chem 271 31360–31366
H Zhang D Huang WA Cramer (1999) ArticleTitleStoichiometrically bound beta-carotene in the cytochrome b6f complex of oxygenic photosynthesis protects against oxygen damage J Biol Chem 274 1581–1587
H Zhang JP Whitelegge WA Cramer (2001) ArticleTitleFerredoxin:NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex J Biol Chem 276 38159–38165
H Zhang G Kurisu JL Smith WA Cramer (2003) ArticleTitleA defined protein-detergent-lipid complex for crystallization of integral membrane proteins: the cytochrome b6f complex of oxygenic photosynthesis Proc Natl Acad Sci USA 100 5160–5163
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Cramer, W.A., Yan, J., Zhang, H. et al. Structure of the cytochrome b6f complex: new prosthetic groups, Q-space, and the ‘hors d’oeuvres hypothesis’ for assembly of the complex. Photosynth Res 85, 133–143 (2005). https://doi.org/10.1007/s11120-004-2149-5
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DOI: https://doi.org/10.1007/s11120-004-2149-5