Ironies in photosynthetic electron transport: a personal perspective

  • William A. Cramer
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 20)

Abstract

In this brief personal perspective, studies, mainly in my laboratory, directed toward understanding of the structure and function of the Fe-metalloprotein electron transport carriers of oxygenic photosynthesis are discussed. This level of understanding and the description of the events that led to this level are inevitably incomplete. The Fe-proteins considered are those, cytochromes b-559 (560), f, b 6, and x, and the Rieske [2Fe−2S] iron-sulfur protein, which have now been placed in a structural context as a result of X-ray diffraction analysis of crystals of Photosystem II and the cytochrome b 6 f complex and the Photosystem II reaction center.

Key words

Jerry Babcock Derek Bendall Mick Black L. Bogorad Herbert Böhme Warren L. Butler Tony Crofts crystal structure cytochrome cytochrome b6f complex electron transfer Mike Everly Paul Furbacher Mark Girvin John Gray Reinhold Herrmann Peter Horton Deru Huang Anne and Pierre Joliot Bessel Kok Genji Kurisu Dick Malkin Daniel Picot plastoquinone Misha Ponamarev Jean-Luc Popot proton transfer Rieske iron-sulfur protein Janet Smith Glenda Soriano David Stroebel Gun-Sik Tae Achim Trebst Olivier Vallon Julian Whitelegge John Whitmarsh Bill Widger X-ray diffraction Jiusheng Yan Huamin Zhang 

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References

  1. Avron M and Chance B (1965) The relation of light-induced oxidation-reduction changes in cytochrome f of isolated chloroplasts to photophosphorylation. In: Thomas JB and Goedheer JC (ed) Currents in Photosynthesis, pp 455–463. Donker, Rotterdam, The NetherlandsGoogle Scholar
  2. Babcock GT, Widger WR, Cramer WA, Oertling W and Metz JG (1985) Axial ligands of cytochrome b-559: identification and requirement for a heme-cross-linked polypeptide structure. Biochemistry 24: 3638–3645PubMedCrossRefGoogle Scholar
  3. Barber J (2002) Photosystem II: a multisubunit membrane protein that oxidises water. Curr Opin Struct Biol 12: 523–530PubMedCrossRefGoogle Scholar
  4. Black MT, Widger WR and Cramer WA (1987) Large-scale purification of active cytochrome b 6 f complex. Arch Biochem Biophys 252: 655–661PubMedCrossRefGoogle Scholar
  5. Boardman NK and Anderson JM (1967) Fractionation of the photochemical systems of photosynthesis II. Cytochrome and carotenoid contents of particles isolated from spinach chloroplasts. Biochim Biophys Acta 143: 187–203PubMedCrossRefGoogle Scholar
  6. Butler WL (1978) On the role of cytochrome b-559 in oxygen evolution in photosynthesis. FEBS Lett 95: 19–25CrossRefGoogle Scholar
  7. Carrell CJ, Zhang H, Cramer WA and Smith JL (1997) Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein. Structure 5: 1613–1625PubMedCrossRefGoogle Scholar
  8. Carrell CJ, Schlarb BG, Howe CJ, Bendall DS, Cramer WA and Smith JL (1999) Structure of the cytochrome f soluble domain from Phormidium laminosus: convergent evolution of the membrane-bound c-type cytochromes from respiratory and photosynthetic bc complexes. Biochemistry 38: 9590–9599PubMedCrossRefGoogle Scholar
  9. Chance B (2004) The stopped-flow method and chemical intermediates in enzyme reactions — a personal essay. Photosynth Res 80: 387–400PubMedCrossRefGoogle Scholar
  10. Chance B and Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17: 65–135Google Scholar
  11. Cramer WA and Butler WL (1967) Light-induced absorbance changes of two b cytochromes in spinach chloroplasts. Biochim Biophys Acta 143: 332–339PubMedCrossRefGoogle Scholar
  12. Cramer WA, Fan HN and Böhme H (1971) High and low potential states of the chloroplast cytochrome b-559 and thermodynamic control of non-cyclic electron transport. J Bioenerg 2: 289–303PubMedCrossRefGoogle Scholar
  13. Cramer WA, Engelman DM, von Heijne G and Rees DC (1992) Forces involved in the assembly and stabilization of membrane proteins. FASEB J 6: 3397–3402PubMedGoogle Scholar
  14. Crofts AR, Yun CH, Gennis RB and Mahalingham S (1990) Prediction of structure for cytochrome b from sequence data: what information is available from sequence comparison. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol III, pp 263–266. Kluwer Academic Publishers, Dordrecht/Boston/LondonGoogle Scholar
  15. Crofts AR, Hong SJ, Ugulava N, Barquera B, Gennis RB, Guergova-Kuras M and Berry E (1999) Pathways for proton release during ubihydroquinone oxidation by the bc1 complex. Proc Natl Acad Sci USA 96: 10021–10026PubMedCrossRefGoogle Scholar
  16. Crofts AR, Guergova-Kuras M, Kuras R, Ugulava N, Li J and Hong S (2000) Proton-coupled electron transfer at the Qo-site: what type of mechanism can account for the high activation barrier? Biochim Biophys Acta 1459: 456–466PubMedCrossRefGoogle Scholar
  17. Fan HN and Cramer WA (1970) The redox potential of cytochrome b-559 and b-563 in spinach chloroplasts. Biochim Biophys Acta 216: 200–207PubMedCrossRefGoogle Scholar
  18. Furbacher PN, Girvin ME and Cramer WA (1989) On the question of interheme electron transfer in the chloroplast cytochrome b 6 in situ. Biochemistry 28: 8990–8998PubMedCrossRefGoogle Scholar
  19. Girvin ME (1985) Electron and Proton Transfer in the Quinone-Cytochrome b-f Region of Chloroplasts. Purdue University, West Lafayette, IndianaGoogle Scholar
  20. Girvin ME and Cramer WA (1984) A redox study of the electron transport pathway responsible for generation of the slow electrochromic phase in chloroplasts. Biochim Biophys Acta 767: 29–38PubMedCrossRefGoogle Scholar
  21. Govindjee and Krogmann D (2004) Discoveries in oxygenic photosynthesis (1727–2003): a perspective. Photosynth Res 80: 15–57PubMedCrossRefGoogle Scholar
  22. Gray J (1978) Purification and properties of a monomeric cytochrome f from Charlock. Eur J Biochem 82: 113–141CrossRefGoogle Scholar
  23. Herrmann RG, Alt J, Schiller B, Widger WR and 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: 239–244CrossRefGoogle Scholar
  24. Horton P and Cramer WA (1975) Acid-base induced redox changes of the chloroplast cytochrome b-559. FEBS Lett 56: 244–247PubMedCrossRefGoogle Scholar
  25. Horton P, Whitmarsh J and Cramer WA (1976) On the specific site of action of 3-(3,4-dichlorophenyl)-1,1-dimethylurea in chloroplasts: inhibition of a dark acid-induced decrease in midpoint potential of cytochrome b-559. Arch Biochem Biophys 176: 519–524PubMedCrossRefGoogle Scholar
  26. Huang D, Everly RM, Cheng RH, Heymann JB, Schägger H, Sled V, Ohnishi T, Baker TS and Cramer WA (1994) Characterization of the chloroplast cytochrome b 6 f complex as a structural and functional dimer. Biochemistry 33: 4401–4409PubMedCrossRefGoogle Scholar
  27. Iwata S, Ostermeier C, Ludwig B and Michel M (1995) Structure at 2.5Å resolution of the cytochrome c oxidase from Paracoccus denitirificans. Nature 376: 660–669PubMedCrossRefGoogle Scholar
  28. Joliot P and Joliot A (1994) Mechanism of electron transfer in the cytochrome b/f cycle of algae: the semiquinone cycle. Proc Natl Acad Sci USA 91: 1034–1038PubMedCrossRefGoogle Scholar
  29. Kamiya N and Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7Å resolution. Proc Natl Acad Sci USA 100: 98–103PubMedCrossRefGoogle Scholar
  30. Knaff DB and Arnon DI (1969) Light-induced oxidation of a b-cytochrome at −189°C Proc Natl Acad Sci USA 63: 956–962PubMedCrossRefGoogle Scholar
  31. Kramer DM and Crofts AR (1993) Re-examination of the properties and function of the b cytochromes of the thylakoid cytochrome bf complex. Biochim Biophys Acta 1184: 193–201Google Scholar
  32. Krishtalik LI, Tae GS, Cherepanov DA and Cramer WA (1993) The redox properties of cytochromes b imposed by the membrane electrostatic environment. Biophys J 65: 184–195PubMedGoogle Scholar
  33. Kurisu G, Zhang H, Smith JL and Cramer WA (2003) Structure and mechanism of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 100: 6713–6723Google Scholar
  34. Kyte J and Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132PubMedCrossRefGoogle Scholar
  35. Link TA, Hagen WR, Pierik AJ, Assmann AJ and von Jagow G (1992) Determination 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: 685–691PubMedCrossRefGoogle Scholar
  36. Martinez SE, Smith JL, Huang D, Szczepaniak A and Cramer WA (1992) Crystallographic studies of the lumen-side domain of turnip cytochrome f. In: Murata N (ed) Research in Photosynthesis, Vol. II, pp 495–498. Kluwer, DordrechtGoogle Scholar
  37. Martinez SE, Huang D, Szczepaniak A, Cramer WA and Smith JL (1994) Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2: 95–105PubMedCrossRefGoogle Scholar
  38. Nanba O and Satoh K (1987) Isolation of a photosystem II reaction center consisting of D1 and D2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112PubMedCrossRefGoogle Scholar
  39. Pearson DC, Gross EL and David ES (1996) Electrostatic properties of cytochrome f: implications for docking with plastocyanin. Biophys J 71: 64–76PubMedGoogle Scholar
  40. Ponamarev MV, Schlarb B, Carrell CJ, Howe CJ, Smith JL, Bendall DS and Cramer WA (2000) Tryptophan-heme π-electrostatic interactions in cytochrome f of oxygenic photosynthesis. Biochemistry 39: 5971–5976PubMedCrossRefGoogle Scholar
  41. Rich PR, Madgwick SA and Moss DA (1991) The interaction of duroquinol, DBMIB, and NQNO with the cytochrome b 6 f complex. Biochim Biophys Acta 1058: 312–328Google Scholar
  42. Satoh K (2003) The identification of the photosystem II reaction center: a personal story. Photosynth Res 76: 233–240PubMedCrossRefGoogle Scholar
  43. Schütz M, Zirngibl S, le Coutre J, Büttner M, Xie DL, Nelson N, Deutzmann N and Hauska G (1994) A transcription unit for the Rieske FeS-protein and cytochrome b in Chlorobium limicola combines characteristics of the bc1/b 6 f-types. Photosynth Res 39: 163–174CrossRefGoogle Scholar
  44. Shuvalov VA, Fiege R, Schreiber U, Lendzian F and Lubitz W (1995) EPR study of cytochrome in the D1D2 Cyt b-559 complex. Biochim Biophys Acta 1228: 175–180CrossRefGoogle Scholar
  45. Soriano G, Ponamarev M, Tae GS and Cramer WA (1996) Effect of the interdomain basic region of cytochrome f on its redox reactions in vivo. Biochemistry 35: 14590–14598PubMedCrossRefGoogle Scholar
  46. Soriano GM, Krishtalik LI and Cramer WA (1997) Electrostatic effects on electron transfer kinetics in the cytochrome f-plastocyanin complex. Biophys J 73: 3265–3276PubMedCrossRefGoogle Scholar
  47. Soriano GM, Ponamarev MV, Piskorowsk R and Cramer WA (1998) Identification of the basic residues of cytochrome f responsible for the electrostatic docking interaction in vitro: relevance to the electron transfer reaction in vivo. Biochemistry 37: 15120–15128PubMedCrossRefGoogle Scholar
  48. Stewart DH and Brudvig GW (1998) Cytochrome b559 of photosystem II. Biochim Biophys Acta 1367: 63–87PubMedCrossRefGoogle Scholar
  49. Stroebel D, Choquet Y, Popot JL and Picot D (2003) An atypical heme in the cytochrome b 6 f complex. Nature 426: 413–418PubMedCrossRefGoogle Scholar
  50. Szczepaniak A, Huang D, Keenan TW and Cramer WA (1991) Electrostatic destabilization of the cytochrome b 6 f complex in the thylakoid membrane. EMBO J 10: 2757–2764PubMedGoogle Scholar
  51. Tae GS and Cramer WA (1989) Lumen-side topography of the α-subunit of the chloroplast cytochrome b-559. FEBS Lett 259: 161–164PubMedCrossRefGoogle Scholar
  52. Tae GS and Cramer WA (1994) Topography of the heme prosthetic group of cytochrome b-559 in the photosystem II reaction center. Biochemistry 33: 10060–10068PubMedCrossRefGoogle Scholar
  53. Tae GS, Black MT, Cramer WA, Vallon O and Bogorad L (1988) Thylakoid membrane protein topography: transmembrane orientation of the chloroplast cytochrome b-559 psbE gene product. Biochemistry 27: 9075–9080PubMedCrossRefGoogle Scholar
  54. Tae GS, Everly RM, Cramer WA, Madgwick SA and Rich PR (1993) On the question of the identity of cytochrome b-560 in thylakoid stromal membranes. Photosynth Res 36: 141–146CrossRefGoogle Scholar
  55. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R and Yoshikawa S (1995) Structures of metal sites of oxidized bovine heart cytochrome oxidase. Science 269: 1069–1074PubMedGoogle Scholar
  56. Ulrich EL, Girvin ME, Cramer WA and Markley JL (1985) Location and mobility of ubiquinones of different chain lengths in artificial membrane vesicles. Biochemistry 24: 2501–2508PubMedCrossRefGoogle Scholar
  57. Vallon O, Tae Cramer WA, Simpson D, Hoyer-Hansen G and Bogorad L (1989) Visualization of antibody-binding to the photosynthetic membrane: the transmembrane orientation of cytochrome b-559. Biochim Biophys Acta 975: 132–141PubMedGoogle Scholar
  58. Westhoff P, Alt J, Widger WR, Cramer WA and Herrmann RG (1985) Localization of the gene for apocytochrome b-559 on the plastid chromosome of spinach. Plant Mol Biol 4: 103–110CrossRefGoogle Scholar
  59. Whitelegge JP, Zhang H, Aguilera R, Taylor RM and Cramer WA (2002) Full unit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein. Mol Cell Proteomics 1: 816–827PubMedCrossRefGoogle Scholar
  60. Whitmarsh J and Cramer WA (1978) Kinetics of the photoreduction of cytochrome b-559 by photosystem II in chloroplasts. Biochim Biophys Acta 460: 280–289Google Scholar
  61. Widger WR, Cramer WA, Hermodson M, Meyer D and Gullifor M (1984a) Purification and partial amino acid sequence of the chloroplast cytochrome b-559. J Biol Chem 259: 3870–3876PubMedGoogle Scholar
  62. Widger WR, Cramer WA, Herrmann RG and Trebst A (1984b) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b 6 f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81: 674–678PubMedCrossRefGoogle Scholar
  63. Widger WR, Cramer WA, Hermodson M and Herrmann RG (1985) Evidence for a hetero-oligomeric structure of the chloroplast cytochrome b-559. FEBS Lett 191: 186–190CrossRefGoogle Scholar
  64. Yan J and Cramer WA (2003) Functional insensitivity of the cytochrome b 6 f complex to structure changes of the hinge region of the Rieske iron-sulfur protein. J Biol Chem 278: 20925–20933PubMedCrossRefGoogle Scholar
  65. Zhang H, Huang D and Cramer WA (1999) Stoichiometrically bound β-carotene in the cytochrome b 6 f complex of oxygenic photosynthesis protects against oxygen damage. J Biol Chem 274: 1581–1587PubMedCrossRefGoogle Scholar
  66. Zhang H, Whitelegge JP and Cramer WA (2001) Flavonucleotide: ferredoxin reductase is a subunit of the plant cytochrome b 6 f complex. J Biol Chem 276: 38159–38165PubMedGoogle Scholar
  67. Zhang H, Kurisu G, Smith JL and Cramer WA (2003) A defined protein-detergent-lipid complex for crystallization of integral membrane proteins. Proc Natl Acad Sci USA 100: 5160–5163PubMedCrossRefGoogle Scholar
  68. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W and Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • William A. Cramer
    • 1
  1. 1.Department of Biological Sciences, Lilly Hall of Life SciencesPurdue UniversityWest LafayetteUSA

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