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Interaction and electron transfer between ferredoxin–NADP+ oxidoreductase and its partners: structural, functional, and physiological implications

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Abstract

Ferredoxin–NADP+ reductase (FNR) catalyzes the last step of linear electron transfer in photosynthetic light reactions. The FAD cofactor of FNR accepts two electrons from two independent reduced ferredoxin molecules (Fd) in two sequential steps, first producing neutral semiquinone and then the fully anionic reduced, or hydroquinone, form of the enzyme (FNRhq). FNRhq transfers then both electrons in a single hydride transfer step to NADP+. We are presenting the recent progress in studies focusing on Fd:FNR interaction and subsequent electron transfer processes as well as on interaction of FNR with NADP+/H followed by hydride transfer, both from the structural and functional point of views. We also present the current knowledge about the physiological role(s) of various FNR isoforms present in the chloroplasts of higher plants and the functional impact of subchloroplastic location of FNR. Moreover, open questions and current challenges about the structure, function, and physiology of FNR are discussed.

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References

  • Aliverti A, Lubberstedt T, Zanetti G, Herrmann RG, Curti B (1991) Probing the role of lysine 116 and lysine 244 in the spinach ferredoxin-NADP + reductase by site-directed mutagenesis. J Biol Chem 266:17760–17763

    CAS  PubMed  Google Scholar 

  • Aliverti A, Piubelli L, Zanetti G, Lubberstedt T, Herrmann RG, Curti B (1993) The role of cysteine residues of spinach ferredoxin-NADP + reductase as assessed by site-directed mutagenesis. BioChemistry 32:6374–6380

    Article  CAS  PubMed  Google Scholar 

  • Aliverti A, Corrado ME, Zanetti G (1994) Involvement of lysine-88 of spinach ferredoxin-NADP + reductase in the interaction with ferredoxin. FEBS Lett 343:247–250

    Article  CAS  PubMed  Google Scholar 

  • Aliverti A, Bruns CM, Pandini VE, Karplus PA, Vanoni MA, Curti B, Zanetti G (1995) 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 34:8371–8379

    Article  CAS  PubMed  Google Scholar 

  • Aliverti A, Deng Z, Ravasi D, Piubelli L, Karplus PA, Zanetti G (1998) Probing the function of the invariant glutamyl residue 312 in spinach ferredoxin-NADP + reductase. J Biol Chem 273:34008–34015

    Article  CAS  PubMed  Google Scholar 

  • Aliverti A, Faber R, Finnerty CM, Ferioli C, Pandini V, Negri A, Karplus PA, Zanetti G (2001) Biochemical and crystallographic characterization of ferredoxin-NADP + reductase from nonphotosynthetic tissues. BioChemistry 40:14501–14508

    Article  CAS  PubMed  Google Scholar 

  • Aliverti A, Pandini V, Pennati A, de Rosa M, Zanetti G (2008) Structural and functional diversity of ferredoxin-NADP + reductases. Arch Biochem Biophys 474:283–291. doi: 10.1016/j.abb.2008.02.014

    Article  CAS  PubMed  Google Scholar 

  • Alte F, Stengel A, Benz JP, Petersen E, Soll J, Groll M, Bölter B (2010) Ferredoxin: NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc Natl Acad Sci USA 107:19260–19265. doi:10.1073/pnas.1009124107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen B, Scheller HV, Møller BL (1992) The PSI-E subunit of photosystem I binds ferredoxin:NADP + oxidoreductase. FEBS Lett 311:169–173

    Article  CAS  PubMed  Google Scholar 

  • Arakaki AK, Ceccarelli EA, Carrillo N (1997) Plant-type ferredoxin-NADP + reductases: a basal structural framework and a multiplicity of functions. FASEB J 11:133–140

    CAS  PubMed  Google Scholar 

  • Arakaki AK, Orellano EG, Calcaterra NB, Ottado J, Ceccarelli EA (2001) Involvement of the flavin si-face tyrosine on the structure and function of ferredoxin-NADP + reductases. J Biol Chem 276:44419–44426. doi:10.1074/jbc.M107568200

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1991) Photosynthetic electron transport: emergence of a concept, 1949–59. Photosynth Res 29:117–131. doi:10.1007/BF00036216

    CAS  PubMed  Google Scholar 

  • Arnon DI, Chain RK (1975) Regulation of ferredoxin-catalyzed photosynthetic phosphorylations. Proc Natl Acad Sci USA 72:4961–4965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balsera M, Stengel A, Soll J, Bölter B (2007) Tic62: a protein family from metabolism to protein translocation. BMC Evol Biol 7:43. doi:10.1186/1471-2148-7-43

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Batie CJ, Kamin H (1984a) Electron transfer by ferredoxin:NADP + reductase. Rapid-reaction evidence for participation of a ternary complex. J Biol Chem 259:11976–11985

    CAS  PubMed  Google Scholar 

  • Batie CJ, Kamin H (1984b) Ferredoxin:NADP + oxidoreductase. Equilibria in binary and ternary complexes with NADP + and ferredoxin. J Biol Chem 259:8832–8839

    CAS  PubMed  Google Scholar 

  • Batie CJ, Kamin H (1986) Association of ferredoxin-NADP + reductase with NADP(H) specificity and oxidation-reduction properties. J Biol Chem 261:11214–11223

    CAS  PubMed  Google Scholar 

  • Benz JP, Stengel A, Lintala M, Lee YH, Weber A, Philippar K, Gügel IL, Kaieda S, Ikegami T, Mulo P, Soll J, Bölter B (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21:3965–3983. doi:10.1105/tpc.109.069815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benz JP, Lintala M, Soll J, Mulo P, Bölter B (2010) A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids. Trends Plant Sci 15:608–613. doi:10.1016/j.tplants.2010.08.008

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya AK, Meyer TE, Cusanovich MA, Tollin G (1987) Laser flash photolysis studies of electron transfer between ferredoxin-NADP + reductase and several high-potential redox proteins. BioChemistry 26:758–764

    Article  CAS  PubMed  Google Scholar 

  • Bojko M, Kruk J, Wieckowski S (2003) Plastoquinones are effectively reduced by ferredoxin: NADP+ oxidoreductase in the presence of sodium cholate micelles. Significance for cyclic electron transport and chlororespiration. Phytochemistry 64(6):1055–1060

    Article  CAS  PubMed  Google Scholar 

  • Bowsher CG, Eyres LM, Gummadova JO, Hothi P, McLean KJ, Munro AW, Scrutton NS, Hanke GT, Sakakibara Y, Hase T (2011) Identification of N-terminal regions of wheat leaf ferredoxin NADP + oxidoreductase important for interactions with ferredoxin. BioChemistry 50:1778–1787. doi:10.1021/bi1014562

    Article  CAS  PubMed  Google Scholar 

  • Bruns CM, 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 247:125–145

    Article  CAS  PubMed  Google Scholar 

  • Carrillo N, Ceccarelli EA (2003) Open questions in ferredoxin-NADP + reductase catalytic mechanism. Eur J Biochem 270:1900–1915

    Article  CAS  PubMed  Google Scholar 

  • Cassan N, Lagoutte B, Sétif P (2005) Ferredoxin-NADP + reductase. Kinetics of electron transfer, transient intermediates, and catalytic activities studied by flash-absorption spectroscopy with isolated photosystem I and ferredoxin. J Biol Chem 280:25960–25972. doi:10.1074/jbc.M503742200

    Article  CAS  PubMed  Google Scholar 

  • Catalano-Dupuy DL, Musumeci MA, Lopez-Rivero A, Ceccarelli EA (2011) A highly stable plastidic-type ferredoxin-NADP(H) reductase in the pathogenic bacterium Leptospira interrogans. PLoS ONE 6:e26736. doi:10.1371/journal.pone.0026736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceccarelli EA, Arakaki AK, Cortez N, Carrillo N (2004) Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases. Biochim Biophys Acta 1698:155–165. doi:10.1016/j.bbapap.2003.12.005

    Article  CAS  PubMed  Google Scholar 

  • Chan RL, Ceccarelli EA, Vallejos RH (1987) Immunological studies of the binding protein for chloroplast ferredoxin-NADP + reductase. Arch Biochem Biophys 253:56–61

    Article  CAS  PubMed  Google Scholar 

  • Clark RD, Hawkesford MJ, Coughlan SJ, Bennett J, Hind G (1984) Association of ferredoxin-NADP + oxidoreductase with the chloroplast cytochrome B-F Complex. FEBS Lett 174:137–142

    Article  CAS  Google Scholar 

  • Corrado ME, Aliverti A, Zanetti G, Mayhew SG (1996) Analysis of the oxidation-reduction potentials of recombinant ferredoxin-NADP + reductase from spinach chloroplasts. Eur J Biochem 239:662–667

    Article  CAS  PubMed  Google Scholar 

  • DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285. doi:10.1016/j.cell.2007.12.028

    Article  CAS  PubMed  Google Scholar 

  • Delano WL (2002) They PyMOL molecular graphics system. DeLano Scientific, San Carlos: http://www.pymol.org

  • Deng Z, Aliverti A, Zanetti G, Arakaki AK, Ottado J, Orellano EG, Calcaterra NB, Ceccarelli EA, Carrillo N, Karplus PA (1999) A productive NADP + binding mode of ferredoxin-NADP + reductase revealed by protein engineering and crystallographic studies. Nat Struct Biol 6:847–853. doi:10.1038/12307

    Article  CAS  PubMed  Google Scholar 

  • Dorowski A, Hofmann A, Steegborn C, Boicu M, Huber R (2001) Crystal structure of paprika ferredoxin-NADP + reductase. Implications for the electron transfer pathway. J Biol Chem 276:9253–9263. doi:10.1074/jbc.M004576200

    Article  CAS  PubMed  Google Scholar 

  • Faro M, Frago S, Mayoral T, Hermoso JA, Sanz-Aparicio J, Gomez-Moreno C, Medina M (2002a) Probing the role of glutamic acid 139 of Anabaena ferredoxin-NADP + reductase in the interaction with substrates. Eur J Biochem 269:4938–4947

    Article  CAS  PubMed  Google Scholar 

  • Faro M, Gomez-Moreno C, Stankovich M, Medina M (2002b) Role of critical charged residues in reduction potential modulation of ferredoxin-NADP + reductase. Eur J Biochem 269:2656–2661

    Article  CAS  PubMed  Google Scholar 

  • Forti G, Bracale M (1984) Ferredoxin-ferredoxin NADP + reductase interaction. FEBS Lett 166:81–84

    Article  CAS  Google Scholar 

  • Foust GP, Mayhew SG, Massey V (1969) Complex formation between ferredoxin triphosphopyridine nucleotide reductase and electron transfer proteins. J Biol Chem 244:964–970

    CAS  PubMed  Google Scholar 

  • Fredricks WW, Gehl JM (1982) Kinetics of extraction of ferredoxin-nicotinamide adenine dinucleotide phosphate reductase from spinach chloroplasts. Arch Biochem Biophys 213:67–72

    Article  CAS  PubMed  Google Scholar 

  • Goss T, Hanke G (2014) The end of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons? Curr Protein Pept Sci 15:385–393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green LS, Yee BC, Buchanan BB, Kamide K, Sanada Y, Wada K (1991) Ferredoxin and ferredoxin-NADP reductase from photosynthetic and nonphotosynthetic tissues of tomato. Plant Physiol 96:1207–1213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grzyb J, Malec P, Rumak I, Garstka M, Strzałka K (2008) Two isoforms of ferredoxin:NADP(+) oxidoreductase from wheat leaves: purification and initial biochemical characterization. Photosynth Res 96:99–112. doi:10.1007/s11120-008-9289-y

    Article  CAS  PubMed  Google Scholar 

  • Guedeney G, Corneille S, Cuiné S, Peltier G (1996) Evidence for an association of ndh B, ndh J gene products and ferredoxin-NADP-reductase as components of a chloroplastic NAD(P)H dehydrogenase complex. FEBS Lett 378:277–280

    Article  CAS  PubMed  Google Scholar 

  • Gummadova JO, Fletcher GJ, Moolna A, Hanke GT, Hase T, Bowsher CG (2007) Expression of multiple forms of ferredoxin NADP + oxidoreductase in wheat leaves. J Exp Bot 58:3971–3985. doi: 10.1093/jxb/erm252

    Article  CAS  PubMed  Google Scholar 

  • Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ 36:1071–1084. doi:10.1111/pce.12046

    Article  CAS  PubMed  Google Scholar 

  • Hanke G, Okutani S, Satomi Y, Takao T, Suzuki, Hase T (2005) Multiple iso-proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation. Plant Cell Environ 28:1146–1157

    Article  CAS  Google Scholar 

  • Hanke GT, Endo T, Satoh F, Hase T (2008) Altered photosynthetic electron channelling into cyclic electron flow and nitrite assimilation in a mutant of ferredoxin:NADP(H) reductase. Plant Cell Environ 31:1017–1028. doi:10.1111/j.1365-3040.2008.01814.x

    Article  CAS  PubMed  Google Scholar 

  • Hermoso JA, Mayoral T, Faro M, Gomez-Moreno C, Sanz-Aparicio J, 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(5):1133–1142. doi:10.1016/S0022-2836(02)00388-1

    Article  CAS  Google Scholar 

  • Hurley J, Cheng H, Xia B, Markley J, Medina M, Gomez-Moreno C, Tollin G (1993a) An aromatic amino acid is required at position 65 in Anabaena ferredoxin for rapid electron transfer to ferredoxin:NADP + reductase. J Am Chem Soc 115:11698–11701. doi:10.1021/ja00078a006

    Article  CAS  Google Scholar 

  • Hurley JK, Salamon Z, Meyer TE, Fitch JC, Cusanovich MA, Markley JL, Cheng H, Xia B, Chae YK, Medina M et al (1993b) Amino acid residues in Anabaena ferredoxin crucial to interaction with ferredoxin-NADP + reductase: site-directed mutagenesis and laser flash photolysis. BioChemistry 32:9346–9354

    Article  CAS  PubMed  Google Scholar 

  • Hurley JK, Medina M, Gomez-Moreno C, Tollin G (1994) Further characterization by site-directed mutagenesis of the protein-protein interface in the ferredoxin/ferredoxin:NADP + reductase system from Anabaena: requirement of a negative charge at position 94 in ferredoxin for rapid electron transfer. Arch Biochem Biophys 312:480–486

    Article  CAS  PubMed  Google Scholar 

  • Hurley JK, Schmeits JL, Genzor C, Gómez-Moreno C, Tollin G (1996) 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: 243–250. doi:10.1006/abbi.1996.0387

    Article  CAS  PubMed  Google Scholar 

  • 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, Tollin G (1997) Structure-function relationships in Anabaena ferredoxin: correlations between X-ray crystal structures, reduction potentials, and rate constants of electron transfer to ferredoxin:NADP + reductase for site-specific ferredoxin mutants. BioChemistry 36:11100–11117

    Article  CAS  PubMed  Google Scholar 

  • Hurley JK, Hazzard JT, Martínez-Júlvez M, Medina M, Gómez-Moreno C, 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(8):1614–1622

    Article  Google Scholar 

  • Hurley JK, Faro M, Brodie TB, Hazzard JT, Medina M, Gómez-Moreno C, Tollin G (2000) Highly nonproductive complexes with Anabaena ferredoxin at low ionic strength are induced by nonconservative amino acid substitutions at Glu139 in Anabaena ferredoxin:NADP + reductase. BioChemistry 39:13695–13702

    Article  CAS  PubMed  Google Scholar 

  • Hurley JK, Morales R, Martínez-Júlvez M, Brodie TB, Medina M, Gómez-Moreno C, Tollin G (2002) Structure-function relationships in Anabaena ferredoxin/ferredoxin-NADP + reductase electron transfer: insights from site-directed mutagenesis, transient absorption spectroscopy and X-ray crystallography. Biochim Biophys Acta 1554:5–21

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213. doi:10.1038/nature08885

    Article  CAS  PubMed  Google Scholar 

  • Jelesarov I, Bosshard HR (1994) Thermodynamics of ferredoxin binding to ferredoxin:NADP + reductase and the role of water at the complex interface. BioChemistry 33:13321–13328

    Article  CAS  PubMed  Google Scholar 

  • Jelesarov I, De Pascalis AR, Koppenol WH, Hirasawa M, Knaff DB, Bosshard HR (1993) Ferredoxin binding site on ferredoxin: NADP + reductase. Differential chemical modification of free and ferredoxin-bound enzyme. Eur J Biochem 216:57–66

    Article  CAS  PubMed  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214. doi:10.1073/pnas.102306999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurić S, Hazler-Pilepić K, Tomasić A, Lepedus H, Jelicić B, Puthiyaveetil S, Bionda T, Vojta L, Allen JF, Schleiff E, Fulgosi H (2009) Tethering of ferredoxin:NADP + oxidoreductase to thylakoid membranes is mediated by novel chloroplast protein TROL. Plant J 60:783–794. doi:10.1111/j.1365-313X.2009.03999.x

    Article  PubMed  CAS  Google Scholar 

  • Karplus PA, Daniels MJ, Herriott JR (1991) Atomic structure of ferredoxin-NADP + reductase: prototype for a structurally novel flavoenzyme family. Science 251:60–66

    Article  CAS  PubMed  Google Scholar 

  • Khruschev SS, Abaturova AM, Diakonova AN, Fedorov VA, Ustinin DM, Kovalenko IB, Riznichenko GY, Rubin AB (2015) [Brownian dynamics simulations of protein-protein interactions in photosynthetic electron transport chain]. Biofizika 60:270–292

    CAS  PubMed  Google Scholar 

  • Kinoshita M, Kim JY, Kume S, Sakakibara Y, Sugiki T, Kojima C, Kurisu G, Ikegami T, Hase T, Kimata-Ariga Y, Lee YH (2015) Physicochemical nature of interfaces controlling ferredoxin NADP(+) reductase activity through its interprotein interactions with ferredoxin. Biochim Biophys Acta 1847:1200–1211. doi:10.1016/j.bbabio.2015.05.023

    Article  CAS  PubMed  Google Scholar 

  • Krapp AR, Rodríguez RE, Poli HO, Paladini DH, Palatnik JF, Carrillo N (2002) The flavoenzyme ferredoxin (flavodoxin)-NADP(H) reductase modulates NADP(H) homeostasis during the soxRS response of Escherichia coli. J Bacteriol 184:1474–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Küchler M, Decker S, Hörmann F, Soll J, Heins L (2002) Protein import into chloroplasts involves redox-regulated proteins. EMBO J 21:6136–6145

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurisu G, Kusunoki M, Katoh E, Yamazaki T, Teshima K, Onda Y, Kimata-Ariga Y, Hase T (2001) Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP(+) reductase. Nat Struct Biol 8:117–121. doi:10.1038/84097

    Article  CAS  PubMed  Google Scholar 

  • Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48:1575–1588. doi:10.1093/pcp/pcm129

    Article  CAS  PubMed  Google Scholar 

  • Lans I, Peregrina JR, Medina M, García-Viloca M, González-Lafont A, Lluch JM (2010) Mechanism of the hydride transfer between Anabaena Tyr303Ser FNRrd/FNRox and NADP+/H. A combined pre-steady-state kinetic/ensemble-averaged transition-state theory with multidimensional tunneling study. J Phys Chem B 114:3368–3379. doi:10.1021/jp912034m

    Article  CAS  PubMed  Google Scholar 

  • Lans I, Medina M, Rosta E, Hummer G, Garcia-Viloca M, Lluch JM, González-Lafont À (2012) Theoretical study of the mechanism of the hydride transfer between ferredoxin-NADP + reductase and NADP+: the role of Tyr303. J Am Chem Soc 134:20544–20553. doi:10.1021/ja310331v

    Article  CAS  PubMed  Google Scholar 

  • Lehtimäki N, Lintala M, Allahverdiyeva Y, Aro EM, Mulo P (2010) Drought stress-induced upregulation of components involved in ferredoxin-dependent cyclic electron transfer. J Plant Physiol 167:1018–1022. doi:10.1016/j.jplph.2010.02.006

    Article  PubMed  CAS  Google Scholar 

  • Lehtimäki N, Koskela MM, Dahlström KM, Pakula E, Lintala M, Scholz M, Hippler M, Hanke GT, Rokka A, Battchikova N, Salminen TA, Mulo P (2014) Posttranslational modifications of ferredoxin-NADP + oxidoreductase in Arabidopsis chloroplasts. Plant Physiol 166:1764–1776. doi:10.1104/pp.114.249094

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lintala M, Allahverdiyeva Y, Kidron H, Piippo M, Battchikova N, Suorsa M, Rintamäki E, Salminen TA, Aro EM, Mulo P (2007) Structural and functional characterization of ferredoxin-NADP+-oxidoreductase using knock-out mutants of Arabidopsis. Plant J 49:1041–1052. doi:10.1111/j.1365-313X.2006.03014.x

    Article  CAS  PubMed  Google Scholar 

  • Lintala M, Allahverdiyeva Y, Kangasjärvi S, Lehtimäki N, Keränen M, Rintamäki E, Aro EM, Mulo P (2009) Comparative analysis of leaf-type ferredoxin-NADP oxidoreductase isoforms in Arabidopsis thaliana. Plant J 57:1103–1115. doi:10.1111/j.1365-313X.2008.03753.x

    Article  CAS  PubMed  Google Scholar 

  • Lintala M, Lehtimäki N, Benz JP, Jungfer A, Soll J, Aro EM, Bölter B, Mulo P (2012) Depletion of leaf-type ferredoxin-NADP(+) oxidoreductase results in the permanent induction of photoprotective mechanisms in Arabidopsis chloroplasts. Plant J 70:809–817. doi:10.1111/j.1365-313X.2012.04930.x

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Júlvez M, Hermoso J, Hurley JK, Mayoral T, Sanz-Aparicio J, Tollin G, Gómez-Moreno C, Medina M (1998a) Role of Arg100 and Arg264 from Anabaena PCC 7119 ferredoxin-NADP + reductase for optimal NADP + binding and electron transfer. BioChemistry 37:17680–17691

    Article  PubMed  Google Scholar 

  • Martínez-Júlvez M, Medina M, Hurley JK, Hafezi R, Brodie TB, Tollin G, Gómez-Moreno C (1998b) Lys75 of Anabaena ferredoxin-NADP + reductase is a critical residue for binding ferredoxin and flavodoxin during electron transfer. BioChemistry 37:13604–13613. doi:10.1021/bi9807411

    Article  PubMed  Google Scholar 

  • Martínez-Júlvez M, Nogués I, Faro M, Hurley JK, Brodie TB, Mayoral T, Sanz-Aparicio J, Hermoso JA, Stankovich MT, Medina M, Tollin G, Gómez-Moreno C (2001) Role of a cluster of hydrophobic residues near the FAD cofactor in Anabaena PCC 7119 ferredoxin-NADP + reductase for optimal complex formation and electron transfer to ferredoxin. J Biol Chem 276:27498–27510. doi:10.1074/jbc.M102112200 pii]

    Article  PubMed  Google Scholar 

  • Martínez-Júlvez M, Medina M, Velázquez-Campoy A (2009) Binding thermodynamics of ferredoxin:NADP + reductase: two different protein substrates and one energetics. Biophys J 96:4966–4975. doi: 10.1016/j.bpj.2009.02.061

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matthijs HC, Coughlan SJ, Hind G (1986) Removal of ferredoxin:NADP + oxidoreductase from thylakoid membranes, rebinding to depleted membranes, and identification of the binding site. J Biol Chem 261:12154–12158

    CAS  PubMed  Google Scholar 

  • Mayoral T, Medina M, Sanz-Aparicio J, Gomez-Moreno C, Hermoso J (2000) Structural basis of the catalytic role of Glu301 in Anabaena PCC 7119 ferredoxin-NADP(+) reductase revealed by X-ray crystallography. Proteins-Struct Funct Genet 38:60–69. doi:10.1002/(SICI)1097-0134(20000101)38:1<60::AID-PROT7>3.0.CO;2-B

    Article  CAS  PubMed  Google Scholar 

  • Mayoral T, Martínez-Júlvez M, Pérez-Dorado I, Sanz-Aparicio J, Gómez-Moreno C, Medina M, Hermoso JA (2005) Structural analysis of interactions for complex formation between ferredoxin-NADP + reductase and its protein partners. Proteins 59:592–602. doi:10.1002/prot.20450

    Article  CAS  PubMed  Google Scholar 

  • Medina M (2009) Structural and mechanistic aspects of flavoproteins: photosynthetic electron transfer from photosystem I to NADP+. FEBS J 276:3942–3958. doi: 10.1111/j.1742-4658.2009.07122.x

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Gómez-Moreno C (2004) Interaction of ferredoxin-NADP + reductase with its substrates: optimal interaction for efficient electron transfer. Photosynth Res 79:113–131. doi:10.1023/B:PRES.0000015386.67746.2c

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Gomez-Moreno C, Tollin G (1992a) Effects of chemical modification of Anabaena flavodoxin and ferredoxin NADP + reductase on the kinetics of interprotein electron-transfer reactions. Eur J Biochem 210:577–583. doi:10.1111/j.1432-1033.1992.tb17457.x

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Mendez E, Gomez-Moreno C (1992b) Identification of arginyl residues involved in the binding of ferredoxin-NADP + reductase from Anabaena sp. PCC 7119 to its substrates. Arch Biochem Biophys 299:281–286

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Méndez E, Gómez-Moreno C (1992c) Lysine residues on ferredoxin-NADP + reductase from Anabaena sp. PCC 7119 involved in substrate binding. FEBS Lett 298:25–28

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Martínez-Júlvez M, Hurley JK, Tollin G, Gómez-Moreno C (1998) Involvement of glutamic acid 301 in the catalytic mechanism of ferredoxin-NADP + reductase from Anabaena PCC 7119. BioChemistry 37:2715–2728. doi:10.1021/bi971795y

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Luquita A, Tejero J, Hermoso J, Mayoral T, Sanz-Aparicio J, Grever K, Gómez-Moreno C (2001) Probing the determinants of coenzyme specificity in ferredoxin-NADP + reductase by site-directed mutagenesis. J Biol Chem 276:11902–11912. doi:10.1074/jbc.M009287200

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Abagyan R, Gómez-Moreno C, Fernández-Recio J (2008) Docking analysis of transient complexes: interaction of ferredoxin-NADP + reductase with ferredoxin and flavodoxin. Proteins 72:848–862. doi:10.1002/prot.21979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moolna A, Bowsher CG (2010) The physiological importance of photosynthetic ferredoxin NADP + oxidoreductase (FNR) isoforms in wheat. J Exp Bot 61:2669–2681. doi:10.1093/jxb/erq101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morales R, Charon MH, Hudry-Clergeon G, Petillot Y, Norager S, Medina M, 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 38:15764–15773

    Article  CAS  PubMed  Google Scholar 

  • Morales R, Charon MH, Kachalova G, Serre L, Medina M, Gómez-Moreno C, Frey M (2000) A redox-dependent interaction between two electron-transfer partners involved in photosynthesis. EMBO Rep 1:271–276. doi:10.1093/embo-reports/kvd057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morigasaki S, Jin T, Wada K (1993) Comparative Studies on Ferredoxin-NADP + Oxidoreductase isoenzymes derived from different organs by antibodies specific for the radish root- and leaf-enzymes. Plant Physiol 103:435–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulo P (2011) Chloroplast-targeted ferredoxin-NADP + oxidoreductase (FNR): structure, function and location. Biochim Biophys Acta 1807:927–934.doi: 10.1016/j.bbabio.2010.10.001

    Article  CAS  PubMed  Google Scholar 

  • Muraki N, Seo D, Shiba T, Sakurai T, Kurisu G (2010) Asymmetric dimeric structure of ferredoxin-NAD(P) + oxidoreductase from the green sulfur bacterium Chlorobaculum tepidum: implications for binding ferredoxin and NADP+. J Mol Biol 401:403–414. doi: 10.1016/j.jmb.2010.06.024

    Article  CAS  PubMed  Google Scholar 

  • Musumeci MA, Arakaki AK, Rial DV, Catalano-Dupuy DL, Ceccarelli EA (2008) Modulation of the enzymatic efficiency of ferredoxin-NADP(H) reductase by the amino acid volume around the catalytic site. FEBS J 275:1350–1366. doi: 10.1111/j.1742-4658.2008.06298.x

    Article  CAS  PubMed  Google Scholar 

  • Nogués I, Tejero J, Hurley JK, Paladini D, Frago S, Tollin G, Mayhew SG, Gómez-Moreno C, Ceccarelli EA, Carrillo N, Medina M (2004) Role of the C-terminal tyrosine of ferredoxin-nicotinamide adenine dinucleotide phosphate reductase in the electron transfer processes with its protein partners ferredoxin and flavodoxin. BioChemistry 43:6127–6137. doi:10.1021/bi049858h

    Article  PubMed  CAS  Google Scholar 

  • Okutani S, Hanke GT, Satomi Y, Takao T, Kurisu G, Suzuki A, Hase T (2005) Three maize leaf ferredoxin:NADPH oxidoreductases vary in subchloroplast location, expression, and interaction with ferredoxin. Plant Physiol 139:1451–1459. doi:10.1104/pp.105.070813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palatnik JF, Valle EM, Carrillo N (1997) Oxidative stress causes ferredoxin-NADP + reductase solubilization from the thylakoid membranes in methyl viologen-treated plants. Plant Physiol 115:1721–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palatnik JF, Tognetti VB, Poli HO, Rodríguez RE, Blanco N, Gattuso M, Hajirezaei MR, Sonnewald U, Valle EM, Carrillo N (2003) Transgenic tobacco plants expressing antisense ferredoxin-NADP(H) reductase transcripts display increased susceptibility to photo-oxidative damage. Plant J 35:332–341

    Article  CAS  PubMed  Google Scholar 

  • Peregrina JR, Herguedas B, Hermoso JA, Martínez-Júlvez M, Medina M (2009) Protein motifs involved in coenzyme interaction and enzymatic efficiency in Anabaena ferredoxin-NADP + reductase. BioChemistry 48:3109–3119. doi:10.1021/bi802077c

    Article  CAS  PubMed  Google Scholar 

  • Peregrina JR, Sánchez-Azqueta A, Herguedas B, Martínez-Júlvez M, Medina M (2010) Role of specific residues in coenzyme binding, charge-transfer complex formation, and catalysis in Anabaena ferredoxin-NADP + reductase. Biochim Biophys Acta 1797:1638–1646. doi: 10.1016/j.bbabio.2010.05.006

    Article  CAS  PubMed  Google Scholar 

  • Peregrina JR, Lans I, Medina M (2012) The transient catalytically competent coenzyme allocation into the active site of Anabaena ferredoxin NADP+ -reductase. Eur Biophys J 41:117–128. doi:10.1007/s00249-011-0704-5

    Article  CAS  PubMed  Google Scholar 

  • Pessino S, Caelles C, Puigdomènech P, Vallejos RH (1994) Structure and characterization of the gene encoding the ferredoxin-NADP reductase-binding protein from Zea mays L. Gene 147:205–208

    Article  CAS  PubMed  Google Scholar 

  • Piubelli L, Zanetti G, Bosshard HR (1997) Recombinant wild-type and mutant complexes of ferredoxin and ferredoxin:NADP + reductase studied by isothermal titration calorimetry. Biol Chem 378:715–718

    CAS  PubMed  Google Scholar 

  • Piubelli L, Aliverti A, Arakaki AK, Carrillo N, Ceccarelli EA, Karplus PA, Zanetti G (2000) Competition between C-terminal tyrosine and nicotinamide modulates pyridine nucleotide affinity and specificity in plant ferredoxin-NADP + reductase. J Biol Chem 275:10472–10476

    Article  CAS  PubMed  Google Scholar 

  • Pueyo JJ, Gómez-Moreno C (1991) Purification of ferredoxin-NADP + reductase, flavodoxin and ferredoxin from a single batch of the cyanobacterium Anabaena PCC 7119. Prep Biochem 21:191–204

    CAS  PubMed  Google Scholar 

  • Quiles J, Cuello J (1998) Association of ferredoxin-NADP oxidoreductase with the chloroplastic pyridine nucleotide dehydrogenase complex in barley leaves. Plant Physiol 117:235–244

    Article  Google Scholar 

  • Rodriguez RE, Lodeyro A, Poli HO, Zurbriggen M, Peisker M, Palatnik JF, Tognetti VB, Tschiersch H, Hajirezaei MR, Valle EM, Carrillo N (2007) Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress. Plant Physiol 143:639–649. doi:10.1104/pp.106.090449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051. doi:10.1111/j.1365-3040.2007.01675.x

    Article  CAS  PubMed  Google Scholar 

  • Saen-Oon S, Cabeza de Vaca I, Masone D, Medina M, Guallar V (2015) A theoretical multiscale treatment of protein-protein electron transfer: The ferredoxin/ferredoxin-NADP(+) reductase and flavodoxin/ferredoxin-NADP(+) reductase systems. Biochim Biophys Acta 1847:1530–1538. doi:10.1016/j.bbabio.2015.09.002

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Azqueta A, Musumeci MA, Martínez-Júlvez M, Ceccarelli EA, Medina M (2012) Structural backgrounds for the formation of a catalytically competent complex with NADP(H) during hydride transfer in ferredoxin-NADP + reductases. Biochim Biophys Acta 1817:1063–1071. doi: 10.1016/j.bbabio.2012.04.009

    Google Scholar 

  • Sánchez-Azqueta A, Catalano-Dupuy DL, López-Rivero A, Tondo ML, Orellano EG, Ceccarelli EA, Medina M (2014a) Dynamics of the active site architecture in plant-type Ferredoxin-NADP(+) reductases catalytic complexes. Biochim Biophys Acta. doi: 10.1016/j.bbabio.2014.06.003

    Google Scholar 

  • Sánchez-Azqueta A, Herguedas B, Hurtado-Guerrero R, Hervás M, Navarro JA, Martínez-Júlvez M, Medina M (2014b) A hydrogen bond network in the active site of Anabaena ferredoxin-NADP(+) reductase modulates its catalytic efficiency. Biochim Biophys Acta 1837:251–263. doi:10.1016/j.bbabio.2013.10.010

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Azqueta A, Martínez-Júlvez M, Hervás M, Navarro JA, Medina M (2014c) External loops at the ferredoxin-NADP(+) reductase protein-partner binding cavity contribute to substrates allocation. Biochim Biophys Acta 1837:296–305. doi:10.1016/j.bbabio.2013.11.016

    Article  PubMed  CAS  Google Scholar 

  • Sancho J, Gómez-Moreno C (1991) Interaction of ferredoxin-NADP + reductase from Anabaena with its substrates. Arch Biochem Biophys 288:231–238

    Article  CAS  PubMed  Google Scholar 

  • Schilder J, Ubbink M (2013) Formation of transient protein complexes. Curr Opin Struct Biol 23:911–918. doi:10.1016/j.sbi.2013.07.009

    Article  CAS  PubMed  Google Scholar 

  • Serre L, Vellieux FM, Medina M, Gómez-Moreno C, Fontecilla-Camps JC, Frey M (1996) X-ray structure of the ferredoxin:NADP + reductase from the cyanobacterium Anabaena PCC 7119 at 1.8 Å resolution, and crystallographic studies of NADP + binding at 2.25 Å resolution. J Mol Biol 263: 20–39. doi: 10.1006/jmbi.1996.0553

    Article  CAS  PubMed  Google Scholar 

  • Setif P (2006) Electron transfer from the bound iron-sulfur clusters to ferredoxin/flavodoxin: kinetic and structural properties of ferredoxin/flavodoxin reduction by photosystem I. In: Golbeck JH (ed) Photosystem I The light-driven plastocyanin:ferredoxin oxidoreductase (Advances in Photosynthesis and Respiration.). Springer, Dordrecht, pp 439–454

    Chapter  Google Scholar 

  • Shahak Y, Crowther D, Hind G (1981) The involvement of ferredoxin-NADP + reductase in cyclic electron transport in chloroplasts. Biochim Biophys Acta 636:234–243

    Article  CAS  PubMed  Google Scholar 

  • Shin M, Ishida H, Nozaki Y (1985) A new protein factor, connectein, as a constituent of the large form of ferredoxin NADP + reductase. Plant Cell Physiol 26:559–563.

    Article  CAS  Google Scholar 

  • Shin M, Tsujita M, Tomizawa H, Sakihama N, Kamei K, Oshino R (1990) Proteolytic degradation of ferredoxin-NADP reductase during purification from spinach. Arch Biochem Biophys 279:97–103

    Article  CAS  PubMed  Google Scholar 

  • Soncini FC, Vallejos RH (1989) The chloroplast reductase-binding protein is identical to the 16.5-kDa polypeptide described as a component of the oxygen-evolving complex. J Biol Chem 264:21112–21115

    CAS  PubMed  Google Scholar 

  • Stengel A, Benz P, Balsera M, Soll J, Bölter B (2008) TIC62 redox-regulated translocon composition and dynamics. J Biol Chem 283:6656–6667. doi:10.1074/jbc.M706719200

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M (2015) Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages. Front Plant Sci 6:800. doi:10.3389/fpls.2015.00800

    Article  PubMed  PubMed Central  Google Scholar 

  • Tejero J, Martínez-Júlvez M, Mayoral T, Luquita A, Sanz-Aparicio J, Hermoso JA, Hurley JK, Tollin G, Gómez-Moreno C, Medina M (2003) Involvement of the pyrophosphate and the 2′-phosphate binding regions of ferredoxin-NADP + reductase in coenzyme specificity. J Biol Chem 278:49203–49214. doi:10.1074/jbc.M307934200

    Article  CAS  PubMed  Google Scholar 

  • Tejero J, Pérez-Dorado I, Maya C, Martínez-Júlvez M, Sanz-Aparicio J, Gómez-Moreno C, Hermoso JA, Medina M (2005) C-terminal tyrosine of ferredoxin-NADP + reductase in hydride transfer processes with NAD(P)+/H. BioChemistry 44:13477–13490. doi:10.1021/bi051278c

    Article  CAS  PubMed  Google Scholar 

  • Tejero J, Peregrina JR, Martínez-Júlvez M, Gutiérrez A, Gómez-Moreno C, Scrutton NS, Medina M (2007) Catalytic mechanism of hydride transfer between NADP+/H and ferredoxin-NADP + reductase from Anabaena PCC 7119. Arch Biochem Biophys 459:79–90. doi: 10.1016/j.abb.2006.10.023

    Article  CAS  PubMed  Google Scholar 

  • Thomas JC, Ughy B, Lagoutte B, Ajlani G (2006) A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci USA 103:18368–18373. doi:10.1073/pnas.0607718103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twachtmann M, Altmann B, Muraki N, Voss I, Okutani S, Kurisu G, Hase T, Hanke GT (2012) N-terminal structure of maize ferredoxin:NADP + reductase determines recruitment into different thylakoid membrane complexes. Plant Cell 24:2979–2991. doi: 10.1105/tpc.111.094532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ubbink M (2012) Dynamics in transient complexes of redox proteins. Biochem Soc Trans 40:415–418. doi:10.1042/BST20110698

    Article  CAS  PubMed  Google Scholar 

  • Vallejos RH, Ceccarelli E, Chan R (1984) Evidence for the existence of a thylakoid intrinsic protein that binds ferredoxin-NADP + oxidoreductase. J Biol Chem 259:8048–8051

    CAS  PubMed  Google Scholar 

  • Velázquez-Campoy A, Goñi G, Peregrina JR, Medina M (2006) Exact analysis of heterotropic interactions in proteins: Characterization of cooperative ligand binding by isothermal titration calorimetry. Biophys J 91:1887–1904. doi: 10.1529/biophysj.106.086561

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vishniac W, Ochoa S (1952) Fixation of carbon dioxide coupled to photochemical reduction of pyridine nucleotides by chloroplast preparations. J Biol Chem 195:75–93

    CAS  PubMed  Google Scholar 

  • Walker MC, Pueyo JJ, Gómez-Moreno C, Tollin G (1990) Comparison of the kinetics of reduction and intramolecular electron transfer in electrostatic and covalent complexes of ferredoxin-NADP + reductase and flavodoxin from Anabaena PCC 7119. Arch Biochem Biophys 281:76–83

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Hu H, Ren H, Kong Y, Lin H, Guo J, Wang L, He Y, Ding X, Grabsztunowicz M, Mulo P, Chen T, Liu Y, Wu Z, Wu Y, Mao C, Wu P, Mo X (2016) Light-induced rice1 regulates light-dependent attachment of leaf-type ferredoxin-NADP + oxidoreductase to the thylakoid membrane in rice and Arabidopsis. Plant Cell 28:712–728. doi:10.1105/tpc.15.01027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanetti G, Gozzer C, Sacchi G, Curti B (1979) Modification of arginyl residues in ferredoxin-NADP + reductase from spinach leaves. Biochim Biophys Acta 568:127–134

    Article  CAS  PubMed  Google Scholar 

  • Zanetti G, Aliverti A, Curti B (1984) A cross-linked complex between ferredoxin and ferredoxin-NADP + reductase. J Biol Chem 259:6153–6157

    CAS  PubMed  Google Scholar 

  • Zhang H, Whitelegge JP, Cramer WA (2001) Ferredoxin:NADP + oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J Biol Chem 276:38159–38165. doi:10.1074/jbc.M105454200

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work has been supported by MINEICO, Spain (BIO2013-42978-P and BIO2016-75183-P AEI/FEDER, UE to M.M.) and the Academy of Finland (Centre of Excellence in the Molecular Biology of Primary Producers 271832 to P.M.).

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Mulo, P., Medina, M. Interaction and electron transfer between ferredoxin–NADP+ oxidoreductase and its partners: structural, functional, and physiological implications. Photosynth Res 134, 265–280 (2017). https://doi.org/10.1007/s11120-017-0372-0

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