Photosystem I pp 683-696 | Cite as

Convergent Evolution of Cytochrome c6 and Plastocyanin

  • Miguel A. De la Rosa
  • Fernando P. Molina-Heredia
  • Manuel Hervás
  • José A. Navarro
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 24)

Abstract

Cytochrome c6 and plastocyanin are an excellent case study of the convergent evolution of proteins. The two molecules differ in their primary sequence and 3D structure but function in a similar way to transfer electrons from cytochrome b 6 f to Photosystem I. It seems that cytochrome c6 was first “discovered” by Nature when iron was much more available than copper because of the reducing character of the Earth’s atmosphere. As the atmospheric molecular oxygen concentration began to rise because of photosynthetic activity, the relative bioavailabilities of iron and copper declined and rose, respectively, and cytochrome c6 was replaced with plastocyanin.

Keywords

Fermentation Chlorophyll Ozone Respiration Proline 

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References

  1. Albarrán C, Navarro JA, Molina-Heredia FP, Murdoch PS, De la Rosa MA and Hervás M (2005) Laser flash-induced kinetic analysis of cytochrome f oxidation by wild-type and mutant plastocyanin from the cyanobacterium Nostoc sp. PCC 7119. Biochemistry 44: 11601–11607PubMedCrossRefGoogle Scholar
  2. Babu CR, Volkman BF and Bullerjahn GS (1999) NMR solution structure of plastocyanin from the photosynthetic prokaryote Prochlorothrix hollandica. Biochemistry 38: 4988–4995PubMedCrossRefGoogle Scholar
  3. Beißinger M, Sticht H, Sutter M, Ejchart A, Haehnel W and Rosch P (1998) Solution structure of cytochrome c6 from the thermophilic cyanobacterium Synechococcus elongatus. EMBO J 17: 27–36PubMedCrossRefGoogle Scholar
  4. Berkner LV and Marshall LC (1965) History of major atmospheric components. Proc Natl Acad Sci USA 53: 1215–1225CrossRefGoogle Scholar
  5. Cavet JS, Borrelly GPM and Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27: 165–181PubMedCrossRefGoogle Scholar
  6. Chitnis PR, Purvis D and Nelson N (1991) Molecular cloning and targeted mutagenesis of the gene psaF encoding subunit III of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 266: 20146–20151PubMedGoogle Scholar
  7. Crichton RR and Pierre JL (2001) Old iron, young copper: from Mars to Venus. Biometals 14: 99–112PubMedCrossRefGoogle Scholar
  8. Crowley B, Díaz-Quintana A, Molina-Heredia FP, Nieto P, Sutter M, Haehnel W, De la Rosa MA and Ubbink M (2002) The interactions of cyanobacterial cytochrome c6 and cytochrome f characterized by NMR. J Biol Chem 277: 48685–48689PubMedCrossRefGoogle Scholar
  9. De la Cerda B, Díaz-Quintana A, Navarro JA, Hervás M and De la Rosa MA (1999) Site-directed mutagenesis of cytochrome c6 from Synechocystis sp. PCC 6803. The heme-protein possesses a negatively charged area that may be isofunctional with the acidic patch of plastocyanin. J Biol Chem 274: 13292–13297PubMedCrossRefGoogle Scholar
  10. De la Rosa MA, Navarro JA, Díaz-Quintana A, De la Cerda B, Molina-Heredia FP, Balme A, Murdoch PS, Díaz-Moreno I, Durán RV and Hervás M (2002) An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c6 and plastocyanin. Bioelectrochemistry 55: 41–45PubMedCrossRefGoogle Scholar
  11. Des Marais DJ (1998) Earth’s early biosphere. Gravit Space Biol Bull 11: 23–30PubMedGoogle Scholar
  12. Díaz-Moreno I, Díaz-Quintana A, De la Rosa MA and Ubbink M (2005) Structure of the complex between plastocyanin and cytochrome f from the cyanobacterium Nostoc sp. PCC 7119 as determined by paramagnetic NMR. J Biol Chem 280: 18908–18915PubMedCrossRefGoogle Scholar
  13. Díaz-Quintana A, Navarro JA, Hervás M, Molina-Heredia FP, De la Cerda B and De la Rosa MA (2003) A comparative structural and functional analysis of cyanobacterial plastocyanin and cytochrome c6 as alternative donors to photosystem I. Photosynth Res 75: 97–110PubMedCrossRefGoogle Scholar
  14. Dikiy A, Carpentier W, Vandenberghe I, Borsari M, Safarov N, Dikaya A, Beeumen JV and Ciurli S (2002) Structural basis for the molecular properties of cytochrome c6. Biochemistry 41: 14689–14699PubMedCrossRefGoogle Scholar
  15. Durán RV, Hervás M, De la Rosa MA and Navarro JA (2004) The efficient functioning of photosynthesis and respiration in Synechocystis sp. PCC 6803 strictly requires the presence of either cytochrome c6 or plastocyanin. J Biol Chem 279: 7229–7233PubMedCrossRefGoogle Scholar
  16. Frazao C, Soares CM, Carrondo MA, Pohl E, Dauter Z, Wilson KS, Hervás M, Navarro JA, De la Rosa MA and Sheldrick GM (1995) Ab initio determination of the crystal structure of cytochrome c6 and comparison with plastocyanin. Structure 3: 1159–1169PubMedCrossRefGoogle Scholar
  17. Fromme P, Jordan P and Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507: 5–31PubMedCrossRefGoogle Scholar
  18. Gupta R, He Z and Luan S (2002) Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis. Nature 30: 567–571CrossRefGoogle Scholar
  19. Guss JM and Freeman HC (1983) Structure of oxidized poplar plastocyanin at 1.6 Å resolution. J Mol Biol 169: 521–563PubMedCrossRefGoogle Scholar
  20. Guss JM, Harrowell PR, Murata M, Norris VA and Freeman HC (1986) Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values. J Mol Biol 192: 361–387PubMedCrossRefGoogle Scholar
  21. Haehnel W, Hesse V and Pröpper A (1980) Electron transfer from plastocyanin to P700. Function of a subunit of photosystem I reaction center. FEBS Lett 111: 79–82CrossRefGoogle Scholar
  22. Hart SE, Schlarb-Ridley B, Delon C, Bendall DS and Howe CJ (2003) Role of charges of cytochrome f from the cyanobacterium Phormidium laminosum in its interaction with plastocyanin. Biochemistry 42: 4829–4836PubMedCrossRefGoogle Scholar
  23. Hervás M, Ortega JM, Navarro JA, De la Rosa MA and Bottin H (1994) Laser flash kinetic analysis of Synechocystis PCC 6803 cytochrome c6 and plastocyanin oxidation by photosystem I. Biochim Biophys Acta 1184: 235–241CrossRefGoogle Scholar
  24. Hervás M, Navarro JA, Díaz A, Bottin H and De la Rosa MA (1995) Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry 34: 11321–11326PubMedCrossRefGoogle Scholar
  25. Hervás M, Navarro JA and De la Rosa MA (2003) Electron transfer between soluble proteins and membrane complexes in photosynthesis. Accounts Chem Res 36: 798–805CrossRefGoogle Scholar
  26. Hervás M, Díaz-Quintana A, Kerfeld CA, Krogmann DW, De la Rosa MA and Navarro JA (2005) Cyanobacterial photosystem I lacks specificity in its interaction with cytochrome c6 electron donors. Photosynth Res 83: 329–333PubMedCrossRefGoogle Scholar
  27. Hippler M, Drepper F, Farah J and Rochaix JD (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36: 6343–6349PubMedCrossRefGoogle Scholar
  28. Hippler M, Drepper F, Rochaix JD and Mühlenhoff U (1999) Insertion of the N-terminal part of PsaF from Chlamydomonas reinhardtii into photosystem I from Synechococcus elongatus enables efficient binding of algal plastocyanin and cytochrome c6. J Biol Chem 274: 4180–4188PubMedCrossRefGoogle Scholar
  29. Ho KK and Krogmann DW (1984) Electron donors to P700 in cyanobacteria and algae. An instance of unusual genetic variability. Biochim Biophys Acta 766: 310–316CrossRefGoogle Scholar
  30. Hong FT (2004) Molecular electronic switches in photobiology. In: Horspool W and Lenci F (eds) Handbook of Organic Photochemistry and Photobiology, 2nd Edition, Chapter 134. CRC Press, Boca RatonGoogle Scholar
  31. Hope AB (2000) Electron transfer amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. Biochim Biophys Acta 1456: 5–26PubMedCrossRefGoogle Scholar
  32. Kasting JF and Siefert JL (2003) Life and the evolution of Earth’s atmosphere. Science 296: 1066–1068CrossRefGoogle Scholar
  33. Kerfeld CA, Anwar HP, Interrante R, Merchant S and Yeates TO (1995) The structure of chloroplast cytochrome c6 at 1.9 Å resolution: evidence for functional oligomerization. J Mol Biol 250: 627–647PubMedCrossRefGoogle Scholar
  34. Kohzuma T, Inoue T, Yoshizaki F, Sasakawa Y, Onodera K, Nagatomo S, Kitagawa T, Uzawa S, Isobe Y, Sugimura Y, Gotowda M and Kai Y (1999) The structure and unusual pH dependence of plastocyanin from the fern Dryopteris crassirhizoma. The protonation of an active site histidine is hindered by π–π interactions. J Biol Chem 274: 11817–11823PubMedCrossRefGoogle Scholar
  35. Lee BH, Hibino T, Takabe T, Weisbeek PJ and Takabe T (1995) Site-directed mutagenetic study on the role of negative patches on silene plastocyanin in the interactions with cytochrome f and photosystem I. J Biochem Tokyo 117: 1209–1217PubMedGoogle Scholar
  36. Macalady J and Banfield JF (2003) Molecular geomicrobiology: genes and geochemical cycling. Earth Planet Sci Lett 209: 1–17CrossRefGoogle Scholar
  37. Mathis P and Sétif P (1981) Near infra-red absorption spectra of the chlorophyll a cations and triplet state in vitro and in vivo. Isr J Chem 21: 316–320Google Scholar
  38. Metzger SU, Pakrasi HB and Whitmarsh J (1995) Characterization of a double deletion mutant that lacks cytochrome c6 and cytochrome cM in Synechocystis 6803. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, pp 823–826. Kluwer Academic Publishers, DordrechtGoogle Scholar
  39. Molina-Heredia FP, Díaz-Quintana A, Hervás M, Navarro JA and De la Rosa MA (1999) Site-directed mutagenesis of cytochrome c6 from Nostoc species PCC 7119. Identification of surface residues of the hemeprotein involved in photosystem I reduction. J Biol Chem 274: 33565–33570PubMedCrossRefGoogle Scholar
  40. Molina-Heredia FP, Hervás M, Navarro JA and De la Rosa MA (2001) A single arginyl residue in plastocyanin and cytochrome c6 from the cyanobacterium Anabaena sp. PCC 7119 is required for efficient reduction of photosystem I. J Biol Chem 276: 601–605PubMedCrossRefGoogle Scholar
  41. Molina-Heredia FP, Balme A, Hervás M, Navarro JA and De la Rosa MA (2002) A comparative structural and functional analysis of cytochrome cM cytochrome c6 and plastocyanin from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 517: 50–54PubMedCrossRefGoogle Scholar
  42. Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervás M, Howe CJ and De la Rosa MA (2003) Photosynthesis: a new function for an old cytochrome? Nature 424: 33–34PubMedCrossRefGoogle Scholar
  43. Navarro JA, Hervás M and De la Rosa MA (1997) Co-evolution of cytochrome c6 and plastocyanin, mobile proteins transferring electrons from cytochrome b6−f to photosystem I. J Biol Inorg Chem 2: 11–22CrossRefGoogle Scholar
  44. Navarro JA, Hervás M, Sun J, De la Cerda B, Chitnis PR and De la Rosa MA (2001a) Negatively charged residues in the H loop of PsaB subunit in photosystem I from Synechocystis sp. PCC 6803 appear to be responsible for electrostatic repulsions with plastocyanin. Photosynth Res 65: 63–68CrossRefGoogle Scholar
  45. Navarro JA, Myshkin E, De la Rosa MA, Bullerjahn GS and Hervás M (2001b) The unique proline of the Prochlorothrix hollandica plastocyanin hydrophobic patch impairs electron transfer to photosystem I. J Biol Chem 276: 37501–37505CrossRefGoogle Scholar
  46. Navarro JA, Lowe C, Amons R, Kohzuma T, Canters G, De la Rosa MA, Ubbink M and Hervás M (2004) Functional characterization of the evolutionarily divergent fern plastocyanin. Eur J Biochem 271: 3449–3456PubMedCrossRefGoogle Scholar
  47. Newman DK and Banfield JF (2002) Geomicrobiology: how molecular-scale interactions underpin biogeochemical systems. Science 296: 1071–1077PubMedCrossRefGoogle Scholar
  48. Ochiai EI (1983) Copper and the biological evolution. Biosystems 16: 81–86PubMedCrossRefGoogle Scholar
  49. Peschek G (1999) Photosynthesis and respiration of cyanobacteria. In: Peschek GA, Loeffelhord W and Schmetterer G (eds) The Phototrophic Prokaryotes, pp 201–209. Kluwer Academic/Plenum Publishers, New YorkGoogle Scholar
  50. Romero A, De la Cerda B, Varela PF, Navarro, JA, Hervás M and De la Rosa MA (1998) The 2.15 Å crystal structure of a triple mutant plastocyanin from the cyanobacterium Synechocystis sp. PCC 6803. J Mol Biol 275: 327–336PubMedCrossRefGoogle Scholar
  51. Sawaya MR, Krogmann DW, Serag A, Ho KK, Yeates TO and Kerfeld CA (2001) Structures of cytochrome c-549 and cytochrome c6 from the cyanobacterium Arthrospira maxima. Biochemistry 40: 9215–9225PubMedCrossRefGoogle Scholar
  52. Sigfridsson K (1998) Plastocyanin, an electron-transfer protein. Photosynth Res 57: 1–28CrossRefGoogle Scholar
  53. Sigfridsson K, Hansson Ö, Karlsson BG, Baltzer L, Nordling M and Lundberg LG (1995) Spectroscopic and kinetic characterization of the spinach plastocyanin mutant Tyr83-His: a histidine residue with a high pKa value. Biochim Biophys Acta 1228: 28–36CrossRefGoogle Scholar
  54. Sommer F, Drepper F and Hippler M (2002) The luminal helix l of PsaB is essential for recognition of plastocyanin or cytochrome c6 and fast electron transfer to photosystem I in Chlamydomonas reinhardtii. J Biol Chem 277: 6573–6581PubMedCrossRefGoogle Scholar
  55. Sun J, Xu W, Hervás M, Navarro JA, De la Rosa MA and Chitnis PR (1999) Oxidising side of the cyanobacterial photosystem I. Evidence for interaction between the electron donor proteins and a luminal surface helix of the PsaB subunit. J Biol Chem 274: 19048–19054PubMedCrossRefGoogle Scholar
  56. Ubbink M, Ejdebäck M, Karlsson BG and Bendall DS (1998) The structure of the complex of plastocyanin and cytochrome f determined by paramagnetic NMR and restrained rigid-body molecular dynamics. Structure 6: 323–335PubMedCrossRefGoogle Scholar
  57. Ullmann GM, Hauswald M, Jensen A, Kostic NM and Knapp E-W (1997) Comparison of the physiologically equivalent proteins cytochrome c6 and plastocyanin on the basis of their electrostatic potentials. Tryptophan 63 in cytochrome c6 may be isofunctional with tyrosine 83 in plastocyanin. Biochemistry 36: 16187–16196PubMedCrossRefGoogle Scholar
  58. Wastl J, Bendall DS and Howe CJ (2002) Higher plants contain a modified cytochrome c6. Trends Plant Sci 7: 244–245PubMedCrossRefGoogle Scholar
  59. Wastl J, Molina-Heredia FP, Hervás M, Navarro JA, De la Rosa MA, Bendall DS and Howe CJ (2004a) Redox properties of Arabidopsis cytochrome c6 are independent of the loop extension specific to higher plants. BBA-Bioenergetics 1657: 115–120Google Scholar
  60. Wastl J, Purton S, Bendall DS and Howe CJ (2004b) Two forms of cytochrome c6 in a single eukaryote. Trends Plant Sci 9: 474–476CrossRefGoogle Scholar
  61. Watkins JA, Cusanovich MA, Meyer TE and Tollin G (1994) A “parallel plate” electrostatic model of bimolecular rate constants applied to electron transfer proteins. Protein Sci 3: 2104–2114PubMedCrossRefGoogle Scholar
  62. Weigel M, Pesaresi P and Leister D (2003a) Tracking the function of the cytochrome c6-like protein in higher plants. Trends Plant Sci 8: 513–517CrossRefGoogle Scholar
  63. Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F and Leister D (2003b) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 15: 31286–31289CrossRefGoogle Scholar
  64. Williams RJP and Fraústo da Silva JJR (1997) The Natural Selection of the Chemical Elements. Oxford University Press, OxfordGoogle Scholar
  65. Wood PM (1978) Interchangeable copper and iron proteins in algal photosynthesis. Studies on plastocyanin and cytochrome c-552 in Chlamydomonas. Eur J Biochem 87: 9–19PubMedCrossRefGoogle Scholar
  66. Xu Q, Chitnis VP, Yu L and Chitnis PR (1994) Function and organization of photosystem I in a cyanobacterial mutant strain that lacks PsaF and PsaJ subunits. J Biol Chem 269: 3205–3211PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Miguel A. De la Rosa
    • 1
  • Fernando P. Molina-Heredia
    • 1
  • Manuel Hervás
    • 1
  • José A. Navarro
    • 1
  1. 1.Instituto de Bioquímica Vegetal y FotosíntesisUniversidad de Sevilla y CSICSevillaSpain

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