Abstract
All oxygenic photosynthetically derived reducing equivalents are utilized by combinations of a single multifuctional electron carrier protein, ferredoxin (Fd), and several Fd-dependent oxidoreductases. We report the first crystal structure of the complex between maize leaf Fd and Fd-NADP+ oxidoreductase (FNR). The redox centers in the complex — the 2Fe–2S cluster of Fd and flavin adenine dinucleotide (FAD) of FNR — are in close proximity; the shortest distance is 6.0 Å. The intermolecular interactions in the complex are mainly electrostatic, occurring through salt bridges, and the interface near the prosthetic groups is hydrophobic. NMR experiments on the complex in solution confirmed the FNR recognition sites on Fd that are identified in the crystal structure. Interestingly, the structures of Fd and FNR in the complex and in the free state differ in several ways. For example, in the active site of FNR, Fd binding induces the formation of a new hydrogen bond between side chains of Glu 312 and Ser 96 of FNR. We propose that this type of molecular communication not only determines the optimal orientation of the two proteins for electron transfer, but also contributes to the modulation of the enzymatic properties of FNR.
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References
Knaff, D.B. In Photosynthesis; the light reactions. (eds Ort, D.R. & Yocum, C.F.) 333–361 (Kluwer Academic Publishers, Dordrecht; 1996).
Fukuyama, K. et al. Nature 286, 522–524 (1980).
Karplus, P.A., Daniels, M.J. & Herriott, J.R. Science 251, 60–66 (1991).
Dai, S. et al. Science 287, 655–658 (2000).
Bruns, C.M. & Karplus, P.A. J. Mol. Biol. 247, 125–145 (1995).
Zanetti, G. et al. Biochemistry 27, 3753–3759 (1988).
De Pascalis, A.R. et al. Protein Sci. 2, 1126–1135 (1993).
Aliverti, A., Corrado, M.E. & Zanetti, G. FEBS Lett. 343, 247–250 (1994).
Akashi, T. et al. J. Biol. Chem. 274, 29399–29405 (1999).
Hurley, J.K. et al. Protein Sci. 8, 1614–1622 (1999).
De Pascalis, A.R., Schurmann, P. & Bosshard, F.R. FEBS Lett. 337, 217–220 (1994).
Hurley, J.K. et al. J. Am. Chem. Soc. 115, 11698–11701 (1993).
Matsumura, T. et al. Plant Physiol. 119. 481–488 (1999).
Binda, C., Coda, A., Aliverti, A., Zanetti, G. & Mattevi, A. Acta Crystallogr. D 54, 1353–1358 (1998).
Holden, H.M. et al. J. Bioenerg. Biomembr. 26, 67–88 (1994).
Jacobson, B.L., Chae, Y.K., Markely, J.L. Rayment, I. & Holden, H.M. Biochemistry 33, 13321–13328 (1993).
Batie, C.J. & Kamin, H. J. Biol. Chem. 256, 7756–7763 (1981).
Walker, M.C., Pueyo, J.J., Navarro, J.A., Gomez-Moreno, C. & Tollin, G. Arch. Biochem. Biophys. 287, 351–358 (1991).
Kimata-Ariga, Y. et al. EMBO J. 19, 5041–5050 (2000).
Aliverti, A. et al. J. Biol. Chem. 273, 34008–34015 (1998).
Deng, Z., et al. Nature Struct. Biol. 6, 847–853 (1999).
Correll, C.C., Batie, C.J., Ballou, D.P. & Ludwig, M.L. Science 258, 1604–1610 (1992).
Correll, C.C., Ludwig, M.L., Bruns, C.M. & Karplus, P.A. Protein Sci. 2, 2112–2133 (1993)
Onda, Y. et al. Plant Physiol. 123, 1037–1045 (2000).
Rossmann, M.G. & van Beek, C.G. Acta Crystallogr. D 55, 1631–1640 (1999).
CCP4. Acta Crystallogr. D 50, 760–763 (1994).
Brünger, A.T. et al. Acta Crystallogr. D 54, 905–921 (1998).
Delaglio, F. et al. J. Biol. NMR 6, 277–293 (1995).
Garrett, D.S., Powers, R., Gronenborn, A.M. & Clore, G.M. J. Magn. Reson. 95, 214–220 (1991).
Esnouf, R.M. J. Mol. Graph. 15, 132–134 (1997).
Merritt, E.A. & Murphy, M.E.P. Acta Crystallogr. D 50, 869–873 (1994).
Diederichs, K. & Karplus, P.A. Nature Struct. Biol. 4, 269–275 (1997).
Acknowledgements
We thank T. Tsukihara (IPR, Osaka University), N. Kamiya (Riken), M. Kawamoto (JASRI), and N. Igarashi, M. Suzuki, N. Watanabe and N. Sakabe (PF, KEK) for their helpful discussions of crystallography, and R. Igarashi for the initial crystallization trial. This work was supported in part by grants-in-aid from the Ministry of Culture, Education, Science and Sports of Japan (G.K., M.K., O.Y. and T.H.), from the Ministry of Agriculture, Forestry and Fisheries of Japan (E.K.), and ACT-JST of Japan (M.K.) and the BRAIN, Japan (T.Y.).
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Kurisu, G., Kusunoki, M., Katoh, E. et al. Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase. Nat Struct Mol Biol 8, 117–121 (2001). https://doi.org/10.1038/84097
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DOI: https://doi.org/10.1038/84097
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