Photosystem I pp 455-476 | Cite as

Electron Transfer From Ferredoxin and Flavodoxin to Ferredoxin:NADP+ Reductase

  • John K. Hurley
  • Gordon Tollin
  • Milagros Medina
  • Carlos Gómez-Moreno
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 24)


An overview is presented of structure/function relationships in the interactions between the small electron transfer proteins ferredoxin (Fd) and flavodoxin (Fld) and the flavoprotein enzyme ferredoxin:NADP+ reductase (FNR), primarily emphasizing the proteins from the cyanobacterium, Anabaena, and the higher plant, spinach. Results are summarized from experiments utilizing rapid-reaction kinetic methods (stopped-flow spectrophotometry and laser flash photolysis) involving wild-type and site-specific mutants of these proteins, redox potential determinations, and X-ray crystallography, including the crystal structure of a Fd/FNR complex. These have provided detailed insights into the protein–protein recognition and electron transfer mechanisms utilized by these systems. Fd and Fld bind to FNR within a concave region of the FNR surface that contains the exposed dimethylbenzene ring of the FAD cofactor. In the Fd case, electron transfer between the iron–sulfur and flavin centers proceeds with a maximum rate constant of 5,500 sec−1 via a direct outer-sphere mechanism. Both electrostatic and hydrophobic interactions occur between the proteins, resulting in a precise surface complementarity.


Spirulina Platensis Crystalline Complex Anabaena Variabilis Midpoint Redox Potential Isoalloxazine Ring 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alam J, Whitaker RA, Krogman DW and Curtis SE (1986) Isolation and sequence of the gene for ferredoxin I from the cyanobacterium Anabaena sp. strain PCC 7120. J Bact 168: 1265–1271PubMedGoogle Scholar
  2. Aliverti A and Zanetti G (1997) A three-domain iron-sulfur flavoprotein obtained through gene fusion of ferredoxin and ferredoxin NADP+ reductase from spinach leaves. Biochemistry 36: 14771–14777PubMedGoogle Scholar
  3. Aliverti A, Piubelli L, Zanetti G, Lübberstedt T, Herrmann RG and Curti B (1993) The role of cysteine residues of spinach ferredoxin reductase as assessed by site-directed mutagenesis. Biochemistry 32: 6374–6380PubMedGoogle Scholar
  4. Aliverti A, Corrado ME and Zanetti G (1994) Involvement of lysine-88 of spinach ferredoxin:NADP+ reductase in the interaction with ferredoxin. FEBS Lett 343: 247–250PubMedGoogle Scholar
  5. Aliverti A, Hagen WR and Zanetti G (1995a) Direct electrochemistry and EPR spectroscopy of spinach ferredoxin mutants with modified electron transfer proteins. FEBS Lett 368: 220–224Google Scholar
  6. Aliverti A, Bruns CM, Pandini VE, Karplus PA, Vanoni MA, Curti B and Zanetti G (1995b) Involvement of serine 96 in the catalytic mechanism of ferredoxin:NADP+ reductase: structure-function relationship as studied by site-directed mutagenesis and x-ray crystallography. Biochemistry 34: 8371–8379Google Scholar
  7. Aliverti A, Livraghi A, Piubelli L and Zanetti G (1997) On the role of the acidic cluster Glu 92-94 of spinach ferredoxin I. Biochim Biophys Acta 1342: 45–50PubMedGoogle Scholar
  8. Aliverti A, Deng Z, Ravasi D, Piubelli L, Karplus PA and Zanetti G (1998) Probing the function of the invariant glutamyl residue 312 in spinach ferredoxin:NADP+ reductase. J Biol Chem 273: 34008–34015PubMedGoogle Scholar
  9. Batie CJ and Kamin H (1981) The relation of pH and oxidation-reduction potential to the association state of the ferredoxin:ferredoxin:NADP+ reductase complex. J Biol Chem 256: 7756–7763PubMedGoogle Scholar
  10. Batie CJ and Kamin H (1984a) Ferredoxin:NADP+ oxidoreductase. Equilibria in binary and ternary complexes with NADP+ and ferredoxin. J Biol Chem 259: 8832–8839Google Scholar
  11. Batie CJ and Kamin H (1984b) Electron transfer by ferredoxin:NADP+ reductase. Rapid-reaction evidence for participation of a ternary complex. J Biol Chem 259: 11976–11985Google Scholar
  12. Beinert H and Kiley PJ (1999) Fe-S proteins in sensing and regulatory functions. Curr Opin Chem Biol 3: 152–157PubMedGoogle Scholar
  13. Beinert H, Holm RH and Münck E (1997) Iron-sulfur clusters: nature’s modular, multipurpose structures. Science 277: 653–659PubMedGoogle Scholar
  14. Bhattacharyya AK, Meyer TE and Tollin G (1986) Reduction kinetics of the ferredoxin-ferredoxin-NADP+ reductase complex. Biochemistry 25: 4655–4661Google Scholar
  15. Binda C, Coda A, Aliverti A, Zanetti G and Mattevi A (1998) Structure of the mutant E92K of [2Fe-2S] ferredoxin I from Spinacia oleracea at 1.7 Å resolution. Acta Cryst D54: 1353–1358Google Scholar
  16. Böhme H and Haselkorn R (1988) Molecular cloning and nucleotide sequence analysis of the gene coding for the heterocyst ferredoxin from the cyanobacterium Anabaena sp. strain PCC 7120. Mol Gen Genet 214: 278–285PubMedGoogle Scholar
  17. Böhme H and Haselkorn R (1989) Expression of Anabaena ferredoxin genes in Escherichia coli. Plant Mol Biol 12: 667–672Google Scholar
  18. Böhme H and Schrautemeier B (1987) Comparative characterization of ferredoxin from heterocysts and vegetative cells of Anabaena variabilis. Biochim Biophys Acta 891: 1–7Google Scholar
  19. Bruns CM and Karplus PA (1995) Refined crystal structure of spinach ferredoxin reductase at 1.7 Å resolution: oxidized, reduced and 2′-phospho-5′-AMP bound states. J Mol Biol 247: 125–145PubMedGoogle Scholar
  20. Cammack R, Rao KK, Bargeron CP, Hutson KG, Andrew PW and Rogers LJ (1977) Midpoint redox potentials of plant and algal ferredoxins. Biochem J 168: 205–209PubMedGoogle Scholar
  21. Carrillo N and Ceccarelli EA (2003) Open questions in ferredoxin-NADP+ reductase catalytic mechanism. Eur J Biochem 270: 1900–1915PubMedGoogle Scholar
  22. Casaus JL, Navarro JA, Hervas M, Lostao A, De la Rosa MA, Gomez-Moreno C, Sancho J and Medina M (2002) Ana- baena sp. PCC 7119 flavodoxin as electron carrier from photosystem I to ferredoxin-NADP+ reductase. Role of Trp(57) and Tyr(94). J Biol Chem 277: 22338–22344PubMedGoogle Scholar
  23. Cheng H, Xia B, Reed GH and Markley JL (1994) Optical, EPR, and 1H NMR spectroscopy of serine-ligated [2Fe-2S] ferredoxins produced by site-directed mutagenesis of cysteine residues in recombinant Anabaena 7120 vegetative ferredoxin. Biochemistry 33: 3155–3164PubMedGoogle Scholar
  24. Cheng H, Westler WM, Oh B-H and Markley JL (1995) Protein expression, selective isotopic labeling, and analysis of hyperfine-shifted NMR signals of Anabaena 7120 vegetative [2Fe-2S] ferredoxin. Arch Biochem Biophys 316: 619–634PubMedGoogle Scholar
  25. Corrado ME, Aliverti A, Zanetti G and Mayhew SG (1996) Analysis of the oxidation-reduction potentials of recombinant ferredoxin-NADP+ reductase from spinach chloroplasts. Eur J Biochem 239: 662–667PubMedGoogle Scholar
  26. De Pascalis AR, Jelesarov I, Ackermann F, Koppenol WH, Hirasawa M, Knaff DB and Bosshard HR (1993) Binding of ferredoxin to ferredoxin:NADP+ reductase: the role of carboxyl groups, electrostatic surface potential, and molecular dipole moment. Protein Sci 2: 1126–1135PubMedGoogle Scholar
  27. Drennan CL, Pattridge KA, Weber CH, Metzger AL, Hoover DM and Ludwig ML (1999) Refined structures of oxidized flavodoxin from Anacystis nidulans. J Mol Biol 294: 711–724PubMedGoogle Scholar
  28. Dugard LB, La Mar GN, Banci L and Bertine L (1990) Identification of localized redox states in plant-type two-iron ferredoxins using the nuclear overhauser effect. Biochemistry 29: 2263–2271Google Scholar
  29. Faro M, Gómez-Moreno C, Stankovich M and Medina M (2002a) Role of critical charged residues in reduction potential modulation of ferredoxin-NADP+ reductase. Differential stabilization of FAD redox forms. Eur J Biochem 269: 2656–2661Google Scholar
  30. Faro M, Frago S, Mayoral T, Hermoso JA, Sanz-Aparicio J, Gómez-Moreno C and Medina M (2002b) Probing the role of the glutamic 139 residue in Anabaena ferredoxin-NADP+ reductase in its interaction with substrates. Eur J Biochem 269: 4938–4947Google Scholar
  31. Fillat MF, Borrias WE and Weisbeek PJ (1991) Cloning of the ferredoxin-NADP+-oxidoreductase gene and overexpression of a synthetic flavodoxin gene from the cyanobacteria Anabaena PCC 7119. In: Curti B, Ronchi S and Zanetti G (eds) Flavins and Flavoproteins 1990, pp 445–448. Walter de Gruyter & Co., BerlinGoogle Scholar
  32. Fillat MF, Pacheco MC, Peleato ML and Gómez-Moreno C (1994) Overexpression of ferredoxin-NADP+ reductase from Anabaena sp. PCC 7119 in E. coli. In: Yagi K (ed) Flavins and Flavoproteins 1993, pp 447–450. Walter de Gruyter & Co., BerlinGoogle Scholar
  33. Foust GP and Massey V (1967) Studies of ferredoxin-TPN reductase and ferredoxin from spinach. Fed Proc 26: 732Google Scholar
  34. Foust GP, Mayhew SG and Massey V (1969) Complex formation between ferredoxin triphosphopyridine nucleotide reductase and electron transfer proteins. J Biol Chem 244: 964–970PubMedGoogle Scholar
  35. Freigang J, Diederichs K, Schaefer KP, Welte W and Paul R (2002) Crystal structure of oxidized flavodoxin, an essential protein in Helicobacter pylori. Protein Sci 11: 253–261PubMedGoogle Scholar
  36. Fritz J, Müller F and Mayhew SG (1973) Electron-nuclear double resonance study of flavodoxin from Peptostreptococcus elsdenii. Helv Chim Acta 56: 2250–2254PubMedGoogle Scholar
  37. Fu W, Drozdzewski PM, Davies MD, Sligar SG and Johnson MK (1992) Resonance Raman and magnetic circular dichroism studies of reduced [2Fe-2S] proteins. J Biol Chem 267: 15502–15510PubMedGoogle Scholar
  38. Fukuyama K, Matsubara H and Rogers LJ (1992) Crystal structure of oxidized flavodoxin from a red alga Chondrus crispus refined at 1.8 A resolution. Description of the flavin mononucleotide binding site. J Mol Biol 225: 775–789PubMedGoogle Scholar
  39. Fukuyama K, Ueki N, Nakamura H, Tsukihara T and Matsubara H (1995) Tertiary structure of [2Fe-2S] ferredoxin from Spirulina platensis refined at 2.5 Å resolution: structural comparisons of plant-type ferredoxins and electrostatic potential analysis. J Biochem 117: 1017–1023PubMedGoogle Scholar
  40. Gómez-Moreno C, Choy M and Edmondson DE (1979) Purification and properties of the bacterial flavoenzyme thiamine dehydrogenase. J Biol Chem 254: 7630–7635PubMedGoogle Scholar
  41. Gómez-Moreno C, Martínez-Júlvez M, Fillat MF, Hurley JK and Tollin G (1995) Molecular recognition in electron transfer proteins. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 627–632. Kluwer Academic Publishers, The NetherlandsGoogle Scholar
  42. Hermoso JA, Mayoral T, Faro M, Gómez-Moreno C, Sanz-Aparicio J and Medina M (2002) Mechanism of coenzyme recognition and binding revealed by crystal structure analysis of ferredoxin-NADP+ reductase complexed with NADP+. J Mol Biol 319: 1133–1142PubMedGoogle Scholar
  43. Holden HM, Jacobson BL, Hurley JK, Tollin G, Oh B-H, Skjeldal L, Chae YK, Cheng H, Xia B and Markley JL (1994) Structure-function studies of [2Fe-2S] ferredoxins. J Bioenerg Biomembr 26: 67–88PubMedGoogle Scholar
  44. Hurley JK, Salamon Z, Meyer TE, Fitch JC, Cusanovich MA, Markley JL, Cheng H, Xia B, Chae YK, Medina M, Gómez-Moreno C and Tollin G (1993a) Amino acid residues in Anabaena ferredoxin crucial to interaction with ferredoxin-NADP+ reductase: site-directed mutagenesis and laser flash photolysis. Biochemistry 32: 9346–9354Google Scholar
  45. Hurley JK, Cheng H, Xia B, Markley JL, Medina M, Gómez-Moreno C and Tollin G (1993b) An aromatic amino acid is required at position 65 in Anabaena ferredoxin for rapid electron transfer to ferredoxin:NADP+ reductase. J Am Chem Soc 115: 11698–11701Google Scholar
  46. Hurley JK, Medina M, Gómez-Moreno C and Tollin G (1994) Further characterization by site-directed mutagenesis of the protein–protein interface in the ferredoxin/ferredoxin: NADP+ system from Anabaena: requirement for a negative charge at position 94 in ferredoxin for rapid electron transfer. Arch Biochem Biophys 312: 480–486PubMedGoogle Scholar
  47. Hurley JK, Fillat MF, Gómez-Moreno C and Tollin G (1996a) Electrostatic and hydrophobic interactions during complex formation and electron transfer in the ferredoxin/ ferredoxin:NADP+ reductase system from Anabaena. J Am Chem Soc 118: 5526–5531Google Scholar
  48. Hurley JK, Schmeits JL, Genzor C, Gómez-Moreno C and Tollin G (1996b) Charge reversal mutations in a conserved acidic patch in Anabaena ferredoxin can attenuate or enhance electron transfer to ferredoxin:NADP+ reductase by altering protein/protein orientation within the intermediate complex. Arch Biochem Biophys 333: 243–250Google Scholar
  49. Hurley JK, Weber-Main AM, Stankovich MT, Benning MM, Thoden JB, Vanhooke JL, Holden HM, Chae YK, Xia B, Cheng H, Markley JL, Martínez-Júlvez M, Gómez-Moreno C, Schmeits JL and Tollin G (1997a) Structure-function relationships in Anabaena ferredoxin: correlations between x-ray crystal structures, reduction potentials, and rate constants for electron transfer to ferredoxin:NADP+ reductase for site-specific ferredoxin mutants. Biochemistry 36: 11100–11117Google Scholar
  50. Hurley JK, Weber-Main AM, Hodges AE, Stankovich MT, Benning MM, Holden HM, Cheng H, Xia B, Markley JL, Genzor C, Gómez-Moreno C, Hafezi R and Tollin G (1997b) Iron-sulfur cluster cysteine-to-serine mutants of Anabaena [2Fe-2S] ferredoxin exhibit unexpected redox properties and are competent in electron transfer to ferredoxin:NADP+ reductase. Biochemistry 36: 15109–15117Google Scholar
  51. Hurley JK, Hazzard JT, Martínez-Júlvez M, Medina M, Gómez-Moreno C and Tollin G (1999) Electrostatic forces involved in orienting Anabaena ferredoxin during binding to Anabaena ferredoxin:NADP+ reductase: site-specific mutagenesis, transient kinetic measurements, and electrostatic surface potentials. Protein Sci 8: 1614–1622PubMedGoogle Scholar
  52. Hurley JK, Faro M, Brodie TB, Hazzard JT, Medina M, Gómez-Moreno C and Tollin G (2000) Highly nonproductive complexes with Anabaena ferredoxin at low ionic strength are induced by nonconservative amino acid substitutions at Glu 139 in Anabaena ferredoxin:NADP+ reductase. Biochemistry 39: 13695–13702PubMedGoogle Scholar
  53. Hurley JK, Morales R, Martínez-Júlvez M, Brody TB, Medina M, Gómez-Moreno C and Tollin G (2002) Structure-function relationships in Anabaena ferredoxin/ferredoxin:NADP+ electron transfer: insights from site-directed mutagenesis, transient absorption measurements and X-ray crystallography. Biochim Biophys Acta 1554: 5–21PubMedGoogle Scholar
  54. Jacobson BL, Chae YK, Markley JL, Rayment I and Holden HM (1993) Molecular structure of the oxidized, recombinant, heterocyst [2Fe-2S] ferredoxin from Anabaena 7120 determined to 1.7-Å resolution. Biochemistry 32: 6788–6793PubMedGoogle Scholar
  55. Jelesarov I and Bosshard HR (1994) Thermodynamics of ferredoxin binding to ferredoxin:NADP+ reductase and the role of water at the complex interface. Biochemistry 33: 13321–13328PubMedGoogle Scholar
  56. Jelesarov I, De Pascalis AR, Koppenol WH, Hirasawa M, Knaff DB and Bosshard HR (1993) Ferredoxin binding site on ferredoxin:NADP+ reductase. Differential chemical modification of free and ferredoxin-bound enzyme. Eur J Biochem 216: 57–66PubMedGoogle Scholar
  57. Jenkins CM, Genzor, CG, Fillat MF, Waterman MR and Gómez-Moreno M (1997) Negatively charged Anabaena flavodoxin residues (Asp144 and Glu145) are important for reconstitution of cytochrome P450 17 alpha-hydroxylase activity. J Biol Chem 36: 22509–22513Google Scholar
  58. Johnson MK (1994) Iron-sulfur proteins. In: King RB (ed) Encyclopedia of inorganic chemistry, pp 1896–1915. John Wiley and Sons, New YorkGoogle Scholar
  59. Kang CH, Ferguson-Miller S and Margoliash E (1977) Steady state kinetics and binding of eukaryotic cytochromes c with yeast cytochrome c peroxidase. Biochemistry 252: 919–926Google Scholar
  60. Karplus PA (1991) Structure/function of spinach ferredoxin:NADP+ oxidoreductase. In: Curti B, Ronchi S and Zanetti G (eds) Flavins and Flavoproteins 1990, pp 449–455. Walter de Gruyter & Co., BerlinGoogle Scholar
  61. Karplus PA, Daniels MJ and Herriot JR (1991) Atomic structure of ferredoxin-NADP+ reductase: prototype for a structurally novel flavoenzyme family. Science 251: 60–66PubMedGoogle Scholar
  62. Keirns JJ and Wang JH (1972) Studies on nicotinamide adenine dinucleotide phosphate reductase from spinach chloroplasts. J Biol Chem 22: 7374–7382Google Scholar
  63. Knaff DB (1996) Ferredoxin and ferredoxin-dependent enzymes. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 333–361. Kluwer Academic Publishers, DordrechtGoogle Scholar
  64. Knauf MA, Lohr F, Curley GP, O’Farrell P, Mayhew SG, Muller F and Ruterjans H (1993) Homonuclear and heteronuclear NMR studies of oxidized Desulfovibrio vulgaris flavodoxin. Sequential assignments and identification of secondary structure elements. Eur J Biochem 213: 167–184PubMedGoogle Scholar
  65. Kurisu G, Kusunoki M, Katoh E, Yamazaki T, Teshima K, Onda Y, Kimata-Ariga Y and Hase T (2001) Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase. Nat Struct Biol 8: 117–121PubMedGoogle Scholar
  66. Lostao A, Gómez-Moreno C, Mayhew SG and Sancho J (1997) Differential stabilization of the three FMN redox forms by tyrosine 94 and tryptophan 57 in flavodoxin from Anabaena and its influence on the redox potentials. Biochemistry 36: 14334–14344PubMedGoogle Scholar
  67. Lovenberg W (ed) (1973) (1974) (1977) Iron-Sulfur Proteins, Vol. I, II, III. Academic Press, New YorkGoogle Scholar
  68. Ludwig ML, Pattridge KA, Metzger AL, Dixon MM, Eren M, Feng Y and Swenson RP (1997) Control of oxidation-reduction potentials in flavodoxin from Clostridium beijerinckii: the role of conformation changes. Biochemistry 36: 1259–1280PubMedGoogle Scholar
  69. Malkin R (1996) Photosystem I electron transfer reactions –components and kinetics. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 333–361. Kluwer Academic Publishers, DordrechtGoogle Scholar
  70. Martínez-Júlvez M, Medina M, Hurley JK, Hafezi R, Brodie TB, Tollin G and Gómez-Moreno C (1998a) Lys 75 of Anabaena ferredoxin-NADP+ reductase is a critical residue for binding ferredoxin and flavodoxin during electron transfer. Biochemistry 37: 13604–13613Google Scholar
  71. Martínez-Júlvez M, Hermoso J, Hurley JK, Mayoral T, Sanz-Aparicio J, Tollin G, Gómez-Moreno C and Medina M (1998b) Role of Arg100 and Arg264 from Anabaena PCC 7119 ferredoxin-NADP+ reductase: binding and electron transfer. Biochemistry 37: 17680–17691Google Scholar
  72. Martínez-Júlvez M, Medina M and Gómez-Moreno C (1999) Ferredoxin-NADP+ reductase uses the same site for the interaction with ferredoxin and flavodoxin. J Biol Inorg Chem 4: 568–578PubMedGoogle Scholar
  73. Martínez-Júlvez M, Nogués I, Faro M, Hurley JK, Brodie TB, Mayoral T, Sanz-Aparicio J, Hermoso JA, Stankovich MT, Medina M, Tollin G and Gómez-Moreno C (2001) Role of a cluster of hydrophobic residues near the FAD cofactor in Anabaena PCC 7119 ferrredoxin-NADP+ reductase for optimal complex formation and electron transfer to ferredoxin. J Biol Chem 276: 27498–27510PubMedGoogle Scholar
  74. Masaki R, Yoshikawa S and Matsubara H (1982a) Steady-state kinetics of oxidation of reduced ferredoxin with ferredoxin-NADP+ reductase. Biochim Biophys Acta 700: 101–109Google Scholar
  75. Masaki R, Matsumoto M, Yoshikawa S and Matsubara H (1982b) Steady state and transient kinetics of reduced ferredoxin with ferredoxin-NADP+ reductase. In: Massey V and Williams CH (eds) Flavins and Flavoproteins, pp 675–678. Elsevier, North HollandGoogle Scholar
  76. Matsubara H and Hase T (1983) Phylogenetic consideration of ferredoxins sequences in plants, particularly algae. In: Jensen U and Fairbrothers DE (eds) Proteins and Nucleic Acids in Plant Systematics, pp 168–181. Springer-Verlag, BerlinGoogle Scholar
  77. Matsubara H and Saeki K (1992) Structural and functional diversity of ferredoxins and related proteins. In: Cammack R and Sykes AG (eds) Advances in Inorganic Chemistry, Iron-Sulfur Proteins, Vol 38, pp 223–280. Academic Press, Inc., San Diego, CAGoogle Scholar
  78. Mauk MR, Ferrer JC and Mauk AG (1994) Proton linkage in formation of the cytochrome c-cytochrome c peroxidase complex: electrostatic properties of the high- and low-affinity cytochrome binding sites on the peroxidase. Biochemistry 33: 12609–12614PubMedGoogle Scholar
  79. Mayoral T, Medina M, Sanz-Aparicio J, Gómez-Moreno C and Hermoso JA (2000) Structural basis of the catalytic role of Glu301 in Anabaena PCC 7119 ferredoxin-NADP+ reductase revealed by X-ray crystallography. Proteins: Struct Funct Gen 38: 60–69Google Scholar
  80. Medina M and Gómez-Moreno C (2004) Interaction of ferredoxin-NADP+ reductase with its substrates: optimal interaction for efficient electron transfer. Photosynth Res 79: 113–131.PubMedGoogle Scholar
  81. Medina M, Méndez E and Gómez-Moreno C (1992a) Identification of arginyl residues involved in the binding of ferredoxin-NADP+ reductase from Anabaena sp. 7119 to its substrates. Arch Biochem Biophys 299: 281–286Google Scholar
  82. Medina M, Méndez E and Gómez-Moreno C (1992b) Lysine residues on ferredoxin-NADP+ reductase from Anabaena sp. 7119 involved in substrate binding. FEBS Lett 298: 25–28Google Scholar
  83. Medina M, Peleato ML, Mendez E and Gómez-Moreno C (1992c) Identification of specific carboxyl groups on Anabaena PCC 7119 flavodoxin which are involved in the interaction with ferredoxin-NADP+ reductase. Eur J Biochem 203: 373–379Google Scholar
  84. Medina M, Martínez-Júlvez M, Hurley JK, Tollin G and Gómez-Moreno C (1998) Involvement of glutamic acid 301 in the catalytic mechanism of ferredoxin-NADP+ reductase from Anabaena PCC 7119. Biochemistry 37: 2715–2728PubMedGoogle Scholar
  85. Morales R, Charon M-H, Hudry-Clergeon G, Pétillot Y, Norager S, Medina M and Frey M (1999) Refined X-ray structures of the oxidized, at 1.3 Å, and reduced, at 1.17 Å, [2Fe-2S] ferredoxin from the cyanobacterium Anabaena PCC7119 show redox-linked conformational changes. Biochemistry 38: 15764–15773PubMedGoogle Scholar
  86. Morales R, Charon M-H, Kacholova G, Serre L, Medina M, Gómez-Moreno C and Frey M (2000) A redox-dependent interaction between two electron-transfer partners involved in photosynthesis. EMBO Rep 1: 271–276PubMedGoogle Scholar
  87. Nakamura S and Kimura T (1971a) A possible regulation of activity of ferredoxin-NADP+ reductase and ferredoxin system by ionic strength: catalytic significance of the one to one complex. FEBS Lett 15: 352–354Google Scholar
  88. Nakamura S and Kimura T (1971b) Studies on spinach ferredoxin-nicotinomide adenine dinucleotide phosphate reductase. FEBS Lett 15: 352–354Google Scholar
  89. Navarro JA, Hervas M, Genzor CG, Cheddar G, Fillat MF, de la Rosa MA, Gómez-Moreno C, Cheng H, Xia B, Chae YK, Yan H, Wong B, Straus A, Markley JL, Hurley JK and Tollin G (1995) Site-specific mutagenesis demonstrates that the structural requirements for efficient electron transfer in Anabaena ferredoxin and flavodoxin are highly dependent on the reaction partner: kinetic studies with photosystem I, ferredoxin:NADP+ reductase, and cytochrome c. Arch Biochem Biophys 321: 229–238PubMedGoogle Scholar
  90. Nelson N and Neumann J (1968) Interaction between ferredoxin and ferredoxin-NADP+ reductase from chloroplasts. Biochem Biophys Res Comm 30: 142–147PubMedGoogle Scholar
  91. Nogués I, Martínez-Júlvez M, Navarro JA, Hervás M, Armenteros L, de la Rosa MA, Brodie TB, Hurley JK, Tollin G, Gómez-Moreno C and Medina M (2003) Role of hydrophobic interactions in the flavodoxin mediated electron transfer from Photosystem I to ferredoxin-NADP+ reductase in Anabaena PCC 7119. Biochemistry 42: 2036–2045PubMedGoogle Scholar
  92. Nuevo MR, Chu H-H, Vitello LB and Erman JE (1993) Salt-dependent switch in the pathway of electron transfer from cytochrome c to cytochrome c reductase compound I. J Am Chem Soc 115: 5873–5874Google Scholar
  93. Palmer G (1973) Current insights into the active center of spinach ferredoxin and other iron-sulfur proteins. In: Lovenberg W (ed) Iron-Sulfur Proteins, Vol 2, pp 285–325. Academic Press, New YorkGoogle Scholar
  94. Peleato ML, Ayora S, Inda LA and Gómez-Moreno C (1994) Isolation and characterization of two different flavodoxins from the eukaryotic alga Chlorella fusca. Biochem J 302: 807–811PubMedGoogle Scholar
  95. Piubelli L, Aliverti A, Bellintani F and Zanetti G (1996) Mutations of Glu92 in ferredoxin I from spinach leaves produces proteins fully functional in electron transfer but less efficient in supporting NADP+ photoreduction. Eur J Biochem 236: 465–469PubMedGoogle Scholar
  96. Price NT, Smith AJ and Rogers LJ (1992) Relationship of the flavodoxin isoforms from Porphyra umbilicalis. Phytochemistry 30: 2835–2839Google Scholar
  97. Pueyo JJ and Gómez-Moreno C (1991) Purification of ferredoxin-NADP+ reductase, flavodoxin and ferredoxin from a single batch of the cyanobacterium Anabaena PCC7119. Prep Biochem 21: 191–204PubMedGoogle Scholar
  98. Pueyo JJ, Gómez-Moreno C and Mayhew SG (1991) Oxidation-reduction potentials of ferredoxin-NADP+ reductase and flavodoxin from Anabaena PCC 7119 and their electrostatic and covalent complexes. Eur J Biochem 202: 1065–1071PubMedGoogle Scholar
  99. Pueyo JJ, Revilla C, Mayhew SG and Gómez-Moreno C (1992) Complex formation between ferredoxin and ferredoxin-NADP+ reductase from Anabaena PCC 7119: cross-linking studies. Arch Biochem Biophys 294: 367–372PubMedGoogle Scholar
  100. Rao ST, Shaffie F, Yu C, Satyshur KA, Stockman BJ, Markley JL and Sundarlingam M (1992) Structure of the oxidized long-chain flavodoxin from Anabaena 7120 at 2 Å resolution. Protein Sci 1: 1413–1427PubMedGoogle Scholar
  101. Rogers LJ (1987) Ferredoxins, flavodoxins and related proteins: structure, function and evolution. In: Fay P and Van Baalen C (eds) The Cyanobacteria, pp 35–67. Elsevier, AmsterdamGoogle Scholar
  102. Rypniewski WR, Breiter DR, Benning MM, Wesenberg G, Oh B-H, Markley JL, Rayment I and Holden HM (1991) Crystallization and structure determination to 2.5-Å resolution of the oxidized [2Fe-2S] ferredoxin from Anabaena 7120. Biochemistry 30: 4126–4131PubMedGoogle Scholar
  103. Sancho J, Peleato ML, Gómez-Moreno C and Edmondson DE (1988) Purification and properties of ferredoxin-NADP+ oxidoreductase from the nitrogen-fixing cyanobacteria Anabaena variabilis. Arch Biochem Biophys 260: 200–207PubMedGoogle Scholar
  104. Sancho J, Medina M and Gómez-Moreno C (1990) Arginyl groups involved in the binding of Anabaena ferredoxin-NADP+ reductase to NADP+ and to ferredoxin. Eur J Biochem 187: 39–48PubMedGoogle Scholar
  105. Sands RH and Dunham WR (1975) Spectroscopic studies on two-iron ferredoxins. In: Engström A, Ehrenberg A, Keynes RD and Felsenfeld G (eds) Quarterly Reviews of Biophysics, Vol 7, pp 443–504. Cambridge University Press, CambridgeGoogle Scholar
  106. Schmitz S and Böhme H (1995) Amino acid residues involved in functional interaction of vegetative cell ferredoxin from the cyanobacterium Anabaena sp. PCC 7120 with ferredoxin:NADP+ reductase, nitrite reductase and nitrate reductase. Biochim Biophys Acta 1231: 335–341Google Scholar
  107. Schmitz S, Martínez-Júlvez M, Gómez-Moreno C and Böhme H (1998) Interaction of positively charged amino acid residues of recombinant, cyanobacterial ferredoxin:NADP+ reductase with ferredoxin probed by site-directed mutagenesis. Biochim Biophys Acta 1363: 85–93PubMedGoogle Scholar
  108. Serre L, Vellieux FMD, Medina M, Gómez-Moreno C, Fontecilla-Camps JC and Frey M (1996) X-ray structure of the ferredoxin:NADP+ reductase from the cyanobacterium Anabaena PCC 7119 at 1.8 Å resolution, and the crystallographic studies of NADP+ binding at 2.25 Å resolution. J Mol Biol 263: 20–39PubMedGoogle Scholar
  109. Shin M and San Pietro A (1968) Complex formation of ferredoxin-NADP reductase with ferredoxin and with NADP. Biochem Biophys Res Comm 33: 38–42PubMedGoogle Scholar
  110. Shin M, Tagawa K and Arnon DI (1963) Crystallization of ferredoxin-TPN reductase and its role in the photosynthetic apparatus of chloroplasts. Biochem Zeitsch 338: 84–96Google Scholar
  111. Skjeldal L, Westler WM, Oh B-H, Krezel AM, Holden HM, Jacobson BL, Rayment I and Markley JL (1991) Two-dimensional magnetization exchange spectroscopy of Anabaena 7120 ferredoxin. Nuclear overhauser effect and electron self-exchange cross peaks from amino acid residues surrounding the 2Fe-2S cluster. Biochemistry 30: 7363–7368PubMedGoogle Scholar
  112. Smillie RM (1965) Isolation of phytoflavin, a flavoprotein with chloroplast ferredoxin activity. Plant Physiol 40: 1124–1165PubMedGoogle Scholar
  113. Smith JM, Smith WH and Knaff DB (1981) Electrochemical titrations of ferredoxin-ferredoxin:NADP+ oxidoreductase complex. Biochim Biophys Acta 635: 405–411PubMedGoogle Scholar
  114. Sticht H and Rösch P (1998) The structure of iron-sulfur proteins. Progr Biophys Mol Biol 70, 95–136Google Scholar
  115. Stombaugh NA, Sundquist JE, Burris RH and Orme-Johnson WH (1976) Oxidation-reduction properties of several low potential iron-sulfur proteins and of methylviologen. Biochemistry 15: 2633–2641PubMedGoogle Scholar
  116. Swenson RP and Krey GD (1994) Site-directed mutagenesis of tyrosine-98 in the flavodoxin from Desulfovibrio vulgaris (Hildenborough): regulation of oxidation-reduction properties of the bound FMN cofactor by aromatic, solvent, and electrostatic interactions. Biochemistry 33: 15298–15308PubMedGoogle Scholar
  117. Tagawa K and Arnon DI (1962) Ferredoxins as electron carriers in photosynthesis and the biological production and consumption of hydrogen gas. Nature 195: 537–543PubMedGoogle Scholar
  118. Tagawa K and Arnon DI (1968) Oxidation reduction potentials and stoichiometry of electron transfer in ferredoxins. Biochim Biophys Acta 153: 602–613PubMedGoogle Scholar
  119. Tsukihara T, Kobayashi M, Nakamura M, Katsube Y, Fukuyama K, Hase T and Matsubara H (1982) Structure-function relationship of [2Fe-2S] ferredoxins and design of a model molecule. Biosystems 15: 243–257PubMedGoogle Scholar
  120. Tsukihara T, Fukuyama K, Mizushima M, Harioka T, Kusunoki M, Katsube Y, Hase T and Matsubara H (1990) Structure of the [2Fe-2S] ferredoxin I from blue-green alga Aphanothece sacrum. J Mol Biol 216: 399–410PubMedGoogle Scholar
  121. Ullmann GM, Hauswald M, Jensen A and Knapp EW (2000) Structural alignment of ferredoxin and flavodoxin based on electrostatic potentials: implications for their interactions with photosystem I and ferredoxin-NADP+ reductase. Proteins 38: 301–309PubMedGoogle Scholar
  122. van Mierlo CP, Muller F and Vervoort J (1990) Secondary and tertiary structure characteristics of Megasphaera elsdenii flavodoxin in the reduced state as determined by two-dimensional 1H NMR. Eur J Biochem 189: 589–600PubMedGoogle Scholar
  123. Verhagen MFJM, Link TA and Hagen WR (1995) Electrochemical study of the redox properties of [2Fe-2S] ferredoxins. Evidence of superreduction of the rieske [2Fe-2S] cluster. FEBS Lett 361: 75–78PubMedGoogle Scholar
  124. Vidakovic M, Fraczkiewicz G, Dave BC, Czernuszewicz RS and Germanas J (1995) The environment of [2Fe-2S] clusters in ferredoxins: the role of residue 45 probed by site-directed mutagenesis. Biochemistry 34: 13906–13913PubMedGoogle Scholar
  125. Vieira BJ and Davis DJ (1986) Interaction of ferredoxin with ferredoxin:NADP reductase: effects of chemical modification of ferredoxin. Arch Biochem Biophys 247: 140–146PubMedGoogle Scholar
  126. Vieira BJ, Colvert KK and Davis DJ (1986) Chemical modification and cross-linking as probes of regions on ferredoxin involved in interaction with ferredoxin:NADP reductase. Biochim Biophys Acta 851: 109–122PubMedGoogle Scholar
  127. Walker MC, Pueyo JJ, Navarro JA, Gómez-Moreno C and Tollin G (1991) Laser flash photolysis studies of reduction of ferredoxins and ferredoxin-NADP+ reductases from Anabaena PCC 7119 and spinach: electrostatic effects on intracomplex electron transfer. Arch Biochem Biophys 287: 351–358PubMedGoogle Scholar
  128. Walsh MA, McCarthy A, O’Farrell PA, McArdle P, Cunningham PD, Mayhew SG and Higgins TM (1998) X-ray crystal structure of the Desulfovibrio vulgaris (Hildenborough) apoflavodoxin-riboflavin complex. Eur J Biochem 258: 362–371PubMedGoogle Scholar
  129. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS and Kim JJ (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94: 8411–8416PubMedGoogle Scholar
  130. Weber-Main AM, Hurley JK, Cheng H, Xia B, Chae YK, Markley JL, Martínez-Júlvez M, Gómez-Moreno C, Stankovich MT and Tollin G (1998) An electrostatic, kinetic and spectroscopic characterization of [2Fe-2S] vegetative and heterocyst ferredoxins from Anabaena 7120 with mutations in the cluster binding loop. Arch Biochem Biophys 355: 181–188PubMedGoogle Scholar
  131. Zanetti G, Aliverti A and Curti B (1984) A cross-linked complex between ferredoxin and ferredoxin-NADP+ reductase. J Biol Chem 259: 6153–6157PubMedGoogle Scholar
  132. Zanetti G, Morelli D, Ronchi S, Negri A, Aliverti A and Curti B (1988) Structural studies on the interaction between ferredoxin and ferredoxin:NADP+ reductase. Biochemistry 27: 3753–3759Google Scholar
  133. Zanetti G, Aliverti A, Ravasi D, Curti B, Deng Z and Karplus PA (1997) On the role of glutamate 312 of spinach ferredoxin:NADP+ reductase. In: Stevenson KJ, Massey V and Williams CH Jr (eds) Flavins and Flavoproteins 1996, pp 509–512. University of Calgary Press, Calgary, AlbertaGoogle Scholar
  134. Zhou J, Nocek JM, DeVan ML and Hoffman BM (1995) Inhibitor-enhanced electron transfer: copper cytochrome c as a redox-inert probe of ternary complexes. Science 269: 204–207PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • John K. Hurley
    • 1
  • Gordon Tollin
    • 1
  • Milagros Medina
    • 2
  • Carlos Gómez-Moreno
    • 2
  1. 1.Department of Biochemistry and Molecular BiophysicsUniversity of ArizonaTucsonUSA
  2. 2.Departmento de Bioquímica y Biología Molecular y CelularUniversidad de ZaragozaZaragozaSpain

Personalised recommendations