Photosynthetica 2018, 56(1):279-293 | DOI: 10.1007/s11099-018-0793-9

Ferredoxin: the central hub connecting photosystem I to cellular metabolism

J. Mondal1, B. D. Bruce1,2,*
1 Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee at Knoxville, Knoxville, USA
2 Graduate School of Genome Science and Technology, University of Tennessee at Knoxville, Knoxville, USA

Ferredoxin (Fd) is a small soluble iron-sulfur protein essential in almost all oxygenic photosynthetic organisms. It contains a single [2Fe-2S] cluster coordinated by four cysteine ligands. It accepts electrons from the stromal surface of PSI and facilitates transfer to a myriad of acceptors involved in diverse metabolic processes, including generation of NADPH via Fd-NADP-reductase, cyclic electron transport for ATP synthesis, nitrate reduction, nitrite reductase, sulfite reduction, hydrogenase and other reductive reactions. Fd serves as the central hub for these diverse cellular reactions and is integral to complex cellular metabolic networks. We describe advances on the central role of Fd and its evolutionary role from cyanobacteria to algae/plants. We compare structural diversity of Fd partners to understand this orchestrating role and shed light on how Fd dynamically partitions between competing partner proteins to enable the optimum transfer of PSI-derived electrons to support cell growth and metabolism.

Additional key words: cellular metabolism; electron transfer; ferredoxin; global interaction; oxidation-reduction

Received: August 21, 2017; Accepted: February 7, 2018; Published: March 1, 2018  Show citation

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Mondal, J., & Bruce, B.D. (2018). Ferredoxin: the central hub connecting photosystem I to cellular metabolism. Photosynthetica, 56(SPECIAL ISSUE), 279-293. doi: 10.1007/s11099-018-0793-9
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    References

    1. Akagi J.M.: The participation of a ferredoxin of Clostridium nigrificans in sulfite reduction.-Biochem. Biophys. Res. Co. 21: 72-77, 1965. Go to original source...
    2. Akashi T., Matsumura T., Ideguchi T.: Comparison of the electrostatic binding sites on the surface of ferredoxin for two ferredoxin-dependent enzymes, ferredoxin-NADP(+) reductase and sulfite reductase.-J. Biol. Chem. 274: 29399-29405, 1999. Go to original source...
    3. Appel J., Schulz R.: Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?-J. Photoch. Photobio. B 47: 1-11, 1998. Go to original source...
    4. Arizmendi J.M., Serra J.L.: Composition of the ferredoxin-nitrite reductase from the cyanobacterium Phormidium laminosum.-Biochem. Soc. T. 18: 637-638, 19
    5. Arnon D.I., Allen M.B., Whatley F.R.: Photosynthesis by isolated chloroplasts.-Nature 174: 394-396, 1954. Go to original source...
    6. Arnon D.I., Tsujimoto H.Y., McSwain B.D.: Ferredoxin and photosynthetic phosphorylation.-Nature 214: 562-566, 1967. Go to original source...
    7. Arnon D.I., Whatley F.R., Allen M.B.: Triphosphopyridine nucleotide as a catalyst of photosynthetic phosphorylation.-Nature 180: 182-185, 1957. Go to original source...
    8. Balsera M., Uberegui E., Susanti D. et al.: Ferredoxin: thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria.-Planta 237: 619-635, 2013. Go to original source...
    9. Beale S.I., Cornejo J.: Biosynthesis of phycobilins. Ferredoxinmediated reduction of biliverdin catalyzed by extracts of Cyanidium caldarium.-J. Biol. Chem. 266: 22328-22332, 1991. Go to original source...
    10. Benemann J.R., Berenson J.A., Kaplan N.O., Kamen M.D.: Hydrogen evolution by a chloroplast-ferredoxin-hydrogenase system.-P. Natl. Acad. Sci. USA 70: 2317-2320, 1973. Go to original source...
    11. Bes M.T., Parisini E., Inda L.A. et al.: Crystal structure determination at 1.4 Å resolution of ferredoxin from the green alga Chlorella fusca.-Structure 7: 1201-1202, 19 Go to original source...
    12. Blanco N.E., Ceccoli R.D., Via M.V. et al.: Expression of the minor isoform pea ferredoxin in tobacco alters photosynthetic electron partitioning and enhances cyclic electron flow.-Plant Physiol. 161: 866-879, 2013. Go to original source...
    13. Böhme H.: On the role of ferredoxin and ferredoxin-NADP+ reductase in cyclic electron transport of spinach chloroplasts.-FEBS J. 72: 283-289, 1977. Go to original source...
    14. Brand J.J., Wright J.N., Lien S.: Hydrogen production by eukaryotic algae.-Biotechnol. Bioeng. 33: 1482-1488, 1989. Go to original source...
    15. Buchanan B.B.: Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development.-Arch. Biochem. Biophys. 288: 1-9, 1991. Go to original source...
    16. Buchanan B.B., Schürmann P., Wolosiuk R.A., Jacquot J.P.: The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond.-Photosynth. Res. 73: 215-222, 2002. Go to original source...
    17. Busch A.W.U., Reijerse E.J., Lubitz W. et al.: Structural and mechanistic insight into the ferredoxin-mediated two-electron reduction of bilins.-Biochem. J. 439: 257-264, 2011. Go to original source...
    18. Cashman D.J., Zhu T., Simmerman R.F. et al.: Molecular interactions between photosystem I and ferredoxin: an integrated energy frustration and experimental model.-J. Mol. Recognit. 27: 597-608, 2014. Go to original source...
    19. Chang C.H., King P.W., Ghirardi M.L., Kim K.: Atomic resolution modeling of the ferredoxin:[FeFe] hydrogenase complex from Chlamydomonas reinhardtii.-Biophys. J. 93: 3034-3045, 20
    20. Chen J.S., Blanchard D.K.: A simple hydrogenase-linked assay for ferredoxin and flavodoxin.-Anal. Biochem. 93: 216-222, 1979. Go to original source...
    21. Curtis V.A., Siedow J.N., San Pietro A.: Studies on photosystem I. II. Involvement of ferredoxin in cyclic electron flow.-Arch. Biochem. Biophys. 158: 898-902, 1973. Go to original source...
    22. Dai S., Johansson K., Miginiac-Maslow M.: Structural basis of redox signaling in photosynthesis: structure and function of ferredoxin:thioredoxin reductase and target enzymes.-Photosynth. Res. 79: 233-248, 2004. Go to original source...
    23. Dai S., Schwendtmayer C., Johansson K. et al.: How does light regulate chloroplast enzymes? Structure-function studies of the ferredoxin/thioredoxin system.-Q. Rev. Biophys. 33: 67-108, 2000. Go to original source...
    24. DalCorso G., Pesaresi P., Masiero S. et al: A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis.-Cell 132: 273-285, 2008. Go to original source...
    25. Dammeyer T., Frankenberg-Dinkel N.: Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms.-Photochem. Photobiol. S. 7: 1121-1130, 2008. Go to original source...
    26. Davenport H.E., Hill R., Whatley F.R.: A natural factor catalyzing reduction of methaemoglobin by isolated chloroplasts.-P. Roy. Soc. B-Biol. Sci. 139: 346-358, 1952. Go to original source...
    27. Diakonova A.N., Khrushchev S.S., Kovalenko I.B. et al.: Influence of pH and ionic strength on electrostatic properties of ferredoxin, FNR, and hydrogenase and the rate constants of their interaction.-Phys. Biol. 13: 056004, 2016. Go to original source...
    28. Domínguez-Martín M.A., Gómez-Baena G., Díez J. et al.: Quantitative proteomics shows extensive remodeling induced by nitrogen limitation in Prochlorococcusmarinus SS120.-mSystems 2: m8-17, 2017. Go to original source...
    29. Dose M.M., Hirasawa M., Kleis-SanFrancisco S. et al.: The ferredoxin-binding site of ferredoxin: Nitrite oxidoreductase. Differential chemical modification of the free enzyme and its complex with ferredoxin.-Plant Physiol. 114: 1047-1053, 1997. Go to original source...
    30. Droux M., Miginiac-Maslow M., Jacquot J.P. et al.: Ferredoxinthioredoxin reductase: a catalytically active dithiol group links photoreduced ferredoxin to thioredoxin functional in photosynthetic enzyme regulation.-Arch. Biochem. Biophys. 256: 372-380, 1987. Go to original source...
    31. Essemine J., Qu M., Mi H., Zhu X.G.: Response of chloroplast NAD(P)H dehydrogenase-mediated cyclic electron flow to a shortage or lack in ferredoxin-quinone oxidoreductasedependent pathway in rice following short-term heat stress.-Front. Plant Sci. 7: 383, 2016. Go to original source...
    32. Forestier M., King P., Zhang L. et al.: Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions.-Eur. J. Biochem. 270: 2750-2758, 2003. Go to original source...
    33. Foyer C.H., Ferrario-Méry S., Noctor G.: Interactions between carbon and nitrogen metabolism.-In: Lea P.J., Morot-Gaudry J.-F. (ed.): Plant Nitrogen. Pp. 237-254. Springer, Berlin 2001. Go to original source...
    34. Fredricks W.W., Stadtman E.R.: The role of ferredoxin in the hydrogenase system from Clostridium kluyveri.-J. Biol. Chem. 240: 4065-4071, 1965. Go to original source...
    35. Fry I., Papageorgiou G., Telor E., Packer L.: Reconstitution of a system for H-2 Evolution with chloroplasts, ferredoxin, and hydrogenase.-Z. Naturforsch. C 32: 110-117, 1977. Go to original source...
    36. Garcia-Sanchez M.I., Gotor C., Jacquot J.P. et al.: Critical residues of Chlamydomonas reinhardtii ferredoxin for interaction with nitrite reductase and glutamate synthase revealed by site-directed mutagenesis.-Eur. J. Biochem. 250: 364-368, 1997. Go to original source...
    37. Ghirardi M.L.: Hydrogen production by photosynthetic green algae.-Indian J. Biochem. Bio. 43: 201-210, 2006.
    38. Gómez-Lojero C., Pérez-Gómez B., Shen G. et al.: Interaction of ferredoxin:NADP+ oxidoreductase with phycobilisomes and phycobilisome substructures of the cyanobacterium Synechococcus sp. strain PCC 7002.-Biochemistry 42: 13800-13811, 2003. Go to original source...
    39. Goñi G., Serrano A., Frago S. et al.: Flavodoxin-mediated electron transfer from photosystem I to ferredoxin-NADP+ reductase in Anabaena: role of flavodoxin hydrophobic residues in protein-protein interactions.-Biochemistry 47: 1207-1217, 2008. Go to original source...
    40. Gou P., Hanke G.T., Kimata-Ariga Y. et al.: Higher order structure contributes to specific differences in redox potential and electron transfer efficiency of root and leaf ferredoxins.-Biochemistry 45: 14389-14396, 2006. Go to original source...
    41. Gutekunst K., Chen X., Schreiber K. et al.: The bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions.-J. Biol. Chem. 289: 1930-1937, 2014. Go to original source...
    42. Halbleib C.M., Ludden P.W.: Regulation of biological nitrogen fixation.-J. Nutr. 130: 1081-1084, 2000. Go to original source...
    43. Hanke G., Mulo P.: Plant type ferredoxins and ferredoxindependent metabolism.-Plant Cell Environ. 36: 1071-1084, 2013. Go to original source...
    44. Happe T., Kaminski A.: Differential regulation of the Fehydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii.-Eur. J. Biochem. 269: 1022-1032, 20 Go to original source...
    45. Hase T., Schürmann P., Knaff D.B.: The interaction of ferredoxin with ferredoxin-dependent enzymes.-In: Golbeck J.H. (ed.): Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase. Pp. 477-498. Springer, Dordrecht 2006. Go to original source...
    46. Hennies H.H.: (1975) [A ferredoxin-linked sulfite reductase from Spinacia oleracea.]-Z. Naturforsch. C 30: 359-362, 1975. Go to original source...
    47. Hertle A.P., Blunder T., Wunder T. et al.: PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow.-Mol. Cell 49: 511-523, 2013. Go to original source...
    48. Hirasawa M., Chang K.T., Knaff D.B.: The interaction of ferredoxin and glutamate synthase-cross-linking and immunological studies.-Arch. Biochem. Biophys. 286: 171-177, 1991. Go to original source...
    49. Hirasawa M., de Best J.H., Knaff D.B.: The effect of lysinemodifying and arginine-modifying reagents on spinach ferredoxin-nitrite oxidoreductase.-BBA-Bioenergetics 1140: 304-312, 1993. Go to original source...
    50. Hirasawa M., Hurley J.K., Salamon Z. et al.: Oxidation-reduction and transient kinetic studies of spinach ferredoxin-dependent glutamate synthase.-Arch. Biochem. Biophys. 330: 209-215, 1996. Go to original source...
    51. Hirasawa M., Knaff D.B.: The role of lysine and arginine residues at the ferredoxin-binding site of spinach glutamate synthase.-BBA-Bioenergetics 1144: 85-91, 1993. Go to original source...
    52. Hirasawa M., Tollin G., Salamon Z., Knaff D.B.: Transient kinetic and oxidation-reduction studies of spinach ferredoxin:nitrite oxidoreductase.-Biochim. Biophys. Acta 1185: 336-345, 1994. Go to original source...
    53. Hirasawa M., Tripathy J.N., Somasundaram R. et al.: The interaction of spinach nitrite reductase with ferredoxin: a sitedirected mutation study.-Mol. Plant. 2: 407-415, 2009. Go to original source...
    54. Hirasawa M., Tripathy J.N., Sommer F. et al.: Enzymatic properties of the ferredoxin-dependent nitrite reductase from Chlamydomonas reinhardtii. Evidence for hydroxylamine as a late intermediate in ammonia production.-Photosynth. Res. 103: 67-77, 2010. Go to original source...
    55. Hosler J.P., Yocum C.F.: Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport: Effect of DCMU and the NADPH/NADP ratio.-Plant Physiol. 83: 965-969, 1987. Go to original source...
    56. Hu X., Kato Y., Sumida A. et al.: The SUFBC2 D complex is required for the biogenesis of all major classes of plastid Fe-S proteins.-Plant J. 90: 235-248, 2017. Go to original source...
    57. Hurley J.K., Hazzard J.T., Martínez-Júlvez M. et al.: 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: 1614-1622, 1999. Go to original source...
    58. Hurley J.K., Tollin G., Medina M., Gómez-Moreno C.: Electron transfer from ferredoxin and flavodoxin to ferredoxin:NADP+ reductase.-In: Golbeck J.H. (ed.): Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase. Pp. 455-476. Springer, Dordrecht 2006. Go to original source...
    59. Ivanov B.N., Tikhonova L.N.: [Porton uptake by isolated chloroplasts during cyclic and non-cyclic electron transport catalyzed by photosystem I in the presence of ferredoxin].-Biokhimiia 44: 983-989, 1979.
    60. Iwai M., Takizawa K., Tokutsu R. et al.: Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis.-Nature 464: 1210-1213, 2010. Go to original source...
    61. Kameda H., Hirabayashi K., Wada K., Fukuyama K.: Mapping of protein-protein interaction sites in the plant-type [2Fe-2S] ferredoxin.-PLoS ONE 6: e21947, 2011. Go to original source...
    62. Kapoor K., Cashman D.J., Nientimp L. et al.: Binding mechanisms of electron transport proteins with cyanobacterial photosysten I: an integrated computational and experimental model.-J. Phys. Chem. B. 122: 1026-1036, 2018. Go to original source...
    63. Keister D.L., San Pietro A., Stolzenbach F.E.: Photosynthetic pyridine nucleotide reductase. III. Effect of phosphate acceptor system on triphosphopyridine nucleotide reduction.-Arch. Biochem. Biophys. 94: 187-195, 1961. Go to original source...
    64. Kim J.Y., Kinoshita M., Kume S. et al.: Non-covalent forces tune the electron transfer complex between ferredoxin and sulfite reductase to optimize enzymatic activity.-Biochem. J. 473: 3837-3854, 2016a. Go to original source...
    65. Kim J.Y., Nakayama M., Toyota H. et al.: Structural and mutational studies of an electron transfer complex of maize sulfite reductase and ferredoxin.-J. Biochem. 160: 101-109, 2016b. Go to original source...
    66. Kimata-Ariga Y., Hase T.: Multiple complexes of nitrogen assimilatory enzymes in spinach chloroplasts: possible mechanisms for the regulation of enzyme function.-PLoS ONE 9: e108965, 2014. Go to original source...
    67. Koguchi O., Tamura G.: Isolation and partial characterization of homogeneous ferredoxin-sulfite reductase from a red alga, Porphyra yezoensis.-Agr. Biol. Chem. Tokyo 53: 1653-1662, 1989. Go to original source...
    68. Kosourov S., Seibert M., Ghirardi M.L.: Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H-2-producing Chlamydomonas reinhardtii cultures.-Plant Cell Physiol. 44: 146-155, 2003. Go to original source...
    69. Kovalenko I.B., Diakonova A.N., Abaturova A.M. et al.: Direct computer simulation of ferredoxin and FNR complex formation in solution.-Phys Biol 7: 026001, 2010. Go to original source...
    70. Kovalenko I.B., Abaturova A.M., Riznichenko G.Y. et al.: Computer simulation of interaction of photosystem 1 with plastocyanin and ferredoxin.-Biosystems 103: 180-187, 2011. Go to original source...
    71. Krendeleva T.E., Kukarskikh G.P., Timofeev K.N. et al.: Ferredoxin-NADP reductase is involved in the ferredoxindependent cyclic electron transport in isolated thylakoids.-Dokl. Biochem. Biophys. 379: 265-268, 2001. Go to original source...
    72. Krueger R.J., Siegel L.M.: Spinach siroheme enzymes: Isolation and characterization of ferredoxin-sulfite reductase and comparison of properties with ferredoxin-nitrite reductase.-Biochemistry 21: 2892-2904, 1982a. Go to original source...
    73. Krueger R.J., Siegel L.M.: Evidence for siroheme-Fe4S4 interaction in spinach ferredoxin-sulfite reductase.-Biochemistry 21: 2905-2909, 1982b. Go to original source...
    74. Kurisu G., Kusunoki M., Katoh E. et al.: Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP(+) reductase.-Nat. Struct. Biol. 8: 117-121, 2001a. Go to original source...
    75. Kurisu G., Kusunoki M., Kimata-Ariga Y. et al.: Structure of the electron transfer complex between plant type ferredoxin and ferredoxin dependent assimilatory enzymes.-Protein Nucl. Acid Enzyme 46: 1661-1667, 2001b.
    76. Lehtimäki N., Lintala M., Allahverdiyeva Y. et al.: Drought stress-induced upregulation of components involved in ferredoxin-dependent cyclic electron transfer-J. Plant Physiol. 167: 1018-1022, 2010. Go to original source...
    77. Lehtimäki N., Koskela M.M., Dahlstrom K.M. et al.: Posttranslational modifications of FERREDOXIN-NADP+ OXIDOREDUCTASE in Arabidopsis chloroplasts.-Plant Physiol. 166: 1764-1776, 2014. Go to original source...
    78. Long H., Chang C.H., King P.W. et al.: Brownian dynamics and molecular dynamics study of the association between hydrogenase and ferredoxin from Chlamydomonas reinhardtii.-Biophys. J. 95: 3753-3766, 20
    79. Long H., King P.W., Ghirardi M.L. et al.: Hydrogenase/ferredoxin charge-transfer complexes: effect of hydrogenase mutations on the complex association.-J. Phys. Chem. A 113: 4060-4067, 2009. Go to original source...
    80. Luque I., Flores E., Herrero A.: Molecular mechanism for the operation of nitrogen control in cyanobacteria.-EMBO J. 13: 2862-2869, 1994. Go to original source...
    81. Manzano C., Candau P., Gomez-Moreno C. et al.: Ferredoxindependent photosynthetic reduction of nitrate and nitrite by particles of Anacystis nidulans.-Mol. Cell Biochem. 10: 161-169, 19
    82. Marco P., Kozuleva M., Eilenberg H. et al.: Binding of ferredoxin to algal photosystem I involves a single binding site and is composed of two thermodynamically distinct events.-BBA-Bioenergetics 1859: 234-243, 2018. Go to original source...
    83. Matsuoka M., Kikuchi T.: Sequence analysis on the information of folding initiation segments in ferredoxin-like fold proteins.-BMC Struct. Biol. 14: 15, 2014. Go to original source...
    84. Melis A., Zhang L., Forestier M. et al.: Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii.-Plant Physiol. 122: 127-136, 20
    85. Melis A. Happe T.: Hydrogen production. green algae as a source of energy.-Plant Physiol. 127: 740-748, 2001. Go to original source...
    86. Mi H.L., Endo T., Ogawa T. et al.: Thylakoid membrane-bound, nadph-specific pyridine-nucleotide dehydrogenase complex mediates cyclic electron-transport in the cyanobacterium Synechocystis Sp Pcc-68038.-Plant Cell Physiol. 36: 661-668, 1995a.
    87. Mi H.L., Endo T., Ogawa T. et al.: Cyclic electron transport mediated by thylakoid-bound, NADPH-specific pyridine nucleotide dehydrogenase in cyanobacteria.-In: Mathis P. (ed.): Photosynthesis: From Light to Biosphere, Vol. II. Pp. 871-874. Springer, Dordrecht 1995b. Go to original source...
    88. Mikami B., Ida S.: Spinach ferredoxin-nitrite reductase: characterization of catalytic activity and interaction of the enzyme with substrates.-J. Biochem. 105: 47-50, 1989. Go to original source...
    89. Moolna A., Bowsher C.G.: The physiological importance of photosynthetic ferredoxin NADP+ oxidoreductase (FNR) isoforms in wheat.-J. Exp. Bot. 61: 2669-2681, 2010. Go to original source...
    90. Morales R., Kachalova G., Vellieux F. et al.: Crystallographic studies of the interaction between the ferredoxin-NADP(+) reductase and ferredoxin from the cyanobacterium Anabaena: looking for the elusive ferredoxin molecule.-Acta Crystallogr. D 56: 1408-1412, 2000. Go to original source...
    91. Mortenson L.E., Valentine R.C., Carnahan J.E.: An electron transport factor from Clostridium pasteurianum.-Biochem. Biophys. Res. Co. 7: 448-452, 19
    92. Munekage Y., Hojo M., Meurer J. et al.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis.-Cell 110: 361-371, 20
    93. Munekage Y., Hashimoto M., Miyake C. et al.: Cyclic electron flow around photosystem I is essential for photosynthesis.-Nature 429: 579-582, 2004. Go to original source...
    94. Nakayama M., Akashi T., Hase T.: Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin.-J. Inorg. Biochem. 82: 27-32, 2000. Go to original source...
    95. Nath K., O'Donnell J.P., Lu Y.: Chloroplastic iron-sulfur scaffold protein NFU3 is essential to overall plant fitness.-Plant Signal. Behav. 12: e1282023, 2017. Go to original source...
    96. Neuwirth E.: RColorBrewer: ColorBrewer Palettes. R package version 1.1-2. https://CRAN.R-project.org/package=RColor Brewer, 2014.
    97. Ogawa T.: A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis Pcc6803.-P. Natl. Acad. Sci. USA 88: 4275-4279, 1991. Go to original source...
    98. Omairi-Nasser A., Galmozzi C. V., Latifi A. et al.: NtcA is responsible for accumulation of the small isoform of ferredoxin:NADP oxidoreductase.-Microbiology 160: 789-794, 2014. Go to original source...
    99. Privalle L.S., Privalle C.T., Leonardy N.J. et al.: Interactions between spinach ferredoxin-nitrite reductase and its substrates. Evidence for the specificity of ferredoxin.-J. Biol. Chem. 260: 14344-14350, 1985. Go to original source...
    100. R Core Team: R: A language and environment for statistical computing.-R Foundation for Statistical Computing, Vienna, Austria. 2013.
    101. R'zaigui M., Hatchikian E.C., Benlian D.: Redox reactions of the hydrogenase-cytochrome C3 system from Desulfovibrio gigas with the synthetic analogue of ferredoxin active site [Fe4S4 (SCH2-CH2OH)4]2-.-Biochem. Biophys. Res. Co. 92: 1258-1265, 19 Go to original source...
    102. Rumpel S., Siebel J.F., Diallo M. et al.: Structural insight into the complex of ferredoxin and [FeFe] hydrogenase from Chlamydomonas reinhardtii.-Chembiochem. 16: 1663-1669, 20 Go to original source...
    103. Saitoh T., Ikegami T., Nakayama M. et al: NMR study of the electron transfer complex of plant ferredoxin and sulfite reductase: mapping the interaction sites of ferredoxin.-J. Biol. Chem. 281: 10482-10488, 2006. Go to original source...
    104. Schmitz O., Kentemich T., Zimmer W. et al.: Identification of the nifJ gene coding for pyruvate: ferredoxin oxidoreductase in dinitrogen-fixing cyanobacteria.-Arch. Microbiol. 160: 62-67, 1993. Go to original source...
    105. Schmitz S., Böhme H.: 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.-BBA-Bioenergetics 1231: 335-341, 1995. Go to original source...
    106. Sekine K., Sakakibara Y., Hase T. et al: A novel variant of ferredoxin-dependent sulfite reductase having preferred substrate specificity for nitrite in the unicellular red alga Cyanidioschyzon merolae.-Biochem. J. 423: 91-98, 2009. Go to original source...
    107. Setif P.: Ferredoxin and flavodoxin reduction by photosystem I.-BBA-Bioenergetics 1507: 161-179, 2001. Go to original source...
    108. Setya A., Murillo M., Leustek T.: Sulfate reduction in higher plants: Molecular evidence for a novel 5'-adenylylsulfate reductase.-P. Natl. Acad. Sci. USA 93: 13383-13388, 1996. Go to original source...
    109. Shahak Y., Crowther D. Hind G.: The involvement of ferredoxin-NADP+ reductase in cyclic electron transport in chloroplasts.-Biochim. Biophys. Acta 636: 234-243, 1981. Go to original source...
    110. Shrestha N.K., Kamachi T., Okura I.: Hydrogen evolution from glucose with the combination of glucose dehydrogenase, ferredoxin NADP reductase and hydrogenase from A. eutrophus H16.-React. Kinet. Catal. L. 70: 281-285, 2000. Go to original source...
    111. Sievers F., Wilm A., Dineen D. et al.: Fast, scalable generation of highquality protein multiple sequence alignments using Clustal Omega.-Mol. Syst. Biol. 7: 2011. Go to original source...
    112. Srivastava A.P., Allen J.P., Vaccaro B.J. et al.: Identification of amino acids at the catalytic site of a ferredoxin-dependent cyanobacterial nitrate reductase.-Biochemistry 54: 5557-5568, 2015. Go to original source...
    113. Staples C.R., Ameyibor E., Fu W. et al.: The function and properties of the iron-sulfur center in spinach ferredoxin: thioredoxin reductase: a new biological role for iron-sulfur clusters.-Biochemistry 35: 11425-11434, 1996. Go to original source...
    114. Suzuki A., Knaff D.B.: Glutamate synthase: structural, mechanistic and regulatory properties, and role in the amino acid metabolism.-Photosynth. Res. 83: 191-217, 2005. Go to original source...
    115. Swamy U., Wang M., Tripathy J.N. et al.: Structure of spinach nitrite reductase: implications for multi-electron reactions by the iron-sulfur:siroheme cofactor.-Biochemistry 44: 16054-16063, 2005. Go to original source...
    116. Tagawa K., Arnon D.I.: Ferredoxins as electron carriers in photosynthesis and in biological production and consumption of hydrogen gas.-Nature 195: 537-543, 1962. Go to original source...
    117. Talts E., Oja V., Ramma H. et al.: Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under farred light in sunflower leaves.-Photosynth. Res. 94: 109-120, 2007. Go to original source...
    118. Tano K., Schrauzer G.N.: Chemical evolution of a nitrogenase model. VIII. Ferredoxin model compounds as electron transfer catalysts and reducing agents in the simulation of nitrogenase and hydrogenase reactions.-J. Am. Chem. Soc. 97: 5404-5408, 1975. Go to original source...
    119. Tripathy J.N., Hirasawa M., Kim S.K. et al.: The role of tryptophan in the ferredoxin-dependent nitrite reductase of spinach.-Photosynth. Res. 94: 1-12, 2007. Go to original source...
    120. Tsukihira T., Fukuyama K., Nakamura M. et al.: X-ray analysis of a [2Fe-2S] ferrodoxin from Spirulina platensis. Main chain fold and location of side chains at 2.5 A resolution.-J. Biochem. 90: 1763-1773, 1981. Go to original source...
    121. Tsygankov A., Kosourov S., Seibert M. et al.: Hydrogen photoproduction under continuous illumination by sulfur-deprived, synchronous Chlamydomonas reinhardtii cultures.-Int. J. Hydrogen. Energ. 27: 1239-1244, 2002. Go to original source...
    122. van Hoewyk D., Abdel-Ghany S.E., Cohu C.M. et al.: Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS.-P. Natl. Acad. Sci. USA 104: 5686-5691, 2007. Go to original source...
    123. Vangone A., Spinelli R., Scarano V. et al.: COCOMAPS: a web application to analyze and visualize contacts at the interface of biomolecular complexes.-Bioinformatics 27: 2915-2916, 2011. Go to original source...
    124. Vangone A., Oliva R., Cavallo L.: CONS-COCOMAPS: a novel tool to measure and visualize the conservation of inter-residue contacts in multiple docking solutions.-BMC Bioinformatics 13: S19, 2012. Go to original source...
    125. Voss I., Goss T., Murozuka E. et al.: FdC1, a novel ferredoxin protein capable of alternative electron partitioning, increases in conditions of acceptor limitation at photosystem I.-J. Biol. Chem. 286: 50-59, 2011. Go to original source...
    126. Vuorijoki L., Tiwari A., Kallio P. et al.: Inactivation of ironsulfur cluster biogenesis regulator SufR in Synechocystis sp. PCC 6803 induces unique iron-dependent protein-level responses.-Biochim. Biophys. Acta 1861: 1085-1098, 2017. Go to original source...
    127. Wei T., Simko V., Levy M et al.: Corrplot. R package "corrplot": Visualization of a Correlation Matrix (Version 0.82) (https://github.com/taiyun/corrplot), 2017.
    128. Whatley F.R., Allen M.B., Arnon D.I.: Photosynthetic phosphorylation as an anaerobic process.-Biochim. Biophys. Acta 16: 605-606, 1955. Go to original source...
    129. Yang C., Hu H., Ren H. et al: 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, 2016. Go to original source...
    130. Yang J., Xie X., Yang M. et al.: Modular electron-transport chains from eukaryotic organelles function to support nitrogenase activity.-P. Natl. Acad. Sci. USA 114: E2460-E2465, 2017. Go to original source...
    131. Ye J.Y., Wang Y.J.: The involvement of ferredoxin-NADP reductase in the photosynthetic cyclic electron transport.-Acta Biochim. Biophys. Sinica 29: 40-45, 1997.
    132. Yoneyama T., Fujimori T., Yanagisawa S. et al.: 15N tracing studies on in vitro reactions of ferredoxin-dependent nitrite reductase and glutamate synthase using reconstituted electron donation systems.-Plant Cell Physiol. 56: 1154-1161, 2015 Go to original source...

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