A systematic survey of conserved histidines in the core subunits of Photosystem I by site-directed mutagenesis reveals the likely axial ligands of P700

EMBO Journal

Volumn 17, Issue 1, 1998, Pages 50-60

  Redding, Kevin ^a   MacMillan, Fraser ^b   Leibl, Winfried ^b   Brettel, Klaus ^b   Hanley, Jonathan ^b   Rutherford, A William ^b   Breton, Jacques ^b   Rochaix, Jean David ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b CEA SACLAY   (France)

Author keywords

Chlamydomonas reinhardtii; EPR; FTIR; Photosystem I; Site directed mutagenesis

Indexed keywords

CHLOROPHYLL; GLUTAMINE; HISTIDINE; LEUCINE; MEMBRANE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; GREEN ALGA; INFRARED SPECTROSCOPY; NONHUMAN; PHOTOSYSTEM I; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

ANIMALS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; ELECTRON SPIN RESONANCE SPECTROSCOPY; HISTIDINE; LIGANDS; LIGHT-HARVESTING PROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM I PROTEIN COMPLEX; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 0032472375     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.1.50     Document Type: Article

References (66)

1. Bendall, D.S. and Manasse, R.S. (1995) Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta, 1229, 23-38.
2. Bennoun, P. and Chua, N.H. (1976) Methods for the detection and characterization of photosynthetic mutants in Chlamydomonas reinhardtii. In Bücher, T., Neupert, W., Sebald, W. and Werner, S. (eds), Genetics and Biogenesis of Chloroplasts and Mitochondria. North-Holland Publishing Company, Amsterdam, pp. 33-39.
3. Bennoun, P., Spierer-Herz, M., Erickson, J., Girard-Bascou, J., Pierre, Y., Delosme, M. and Rochaix, J.-D. (1986) Characterization of Photosystem II mutants of Chlamydomonas reinhardtii lacking the psbA gene. Plant Mol. Biol., 6, 151-160.
4. Boyer, P.D. (1993) The binding change mechanism for ATP synthase -some probabilities and possibilities. Biochim. Biophys. Acta, 1140, 215-250.
5. Boynton, J.E. et al. (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science, 240, 1534-1538.
6. Breton, J. (1977) Dichroism of transient absorbance changes in the red spectral region using oriented chloroplasts II. P-700 absorbance changes. Biochim. Biophys. Acta, 459, 66-75.
7. Brettel, K. (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim. Biophys. Acta, 1318, 322-373.
8. Büttner, M., Xie, D., Nelson, H., Pinther, W., Hauska, G. and Nelson, N. (1992a) Photosynthetic reaction center genes in green sulfur bacteria and in photosystem 1 are related. Proc. Natl Acad. Sci. USA, 89, 8135-8139.
9. Büttner, M., Xie, D.L., Nelson, H., Pinther, W., Hauska, G. and Nelson, N. (1992b) The photosystem I-like P840-reaction center of green S-bacteria is a homodimer. Biochim. Biophys. Acta, 1101, 154-156.
10. Bylina, E. and Youvan, D. (1988) Directed mutations affecting spectroscopic and electron transfer properties of the primary donor in the photosynthetic reaction center. Proc. Natl Acad. Sci. USA, 85, 7226-7230.
11. Bylina, E.J., Kolaczkowski, S.V., Norris, J.R. and Youvan, D.C. (1990) EPR characterization of genetically modified reaction centers of Rhodobacter capsulatus. Biochemistry, 29, 6203-6210.
12. Chitnis, P.R. (1996) Photosystem I. Plant Physiol., 111, 661-669.
13. Choquet, Y., Goldschmidt-Clermont, M., Girard-Bascou, J., Kuck, U., Bennoun, P. and Rochaix, J.D. (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell, 52, 903-913.
14. Chua, N.H. and Bennoun, P. (1975) Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl Acad. Sci. USA, 72, 2175-2179.
15. Coleman, W.J. and Youvan, D.C. (1990) Spectroscopic analysis of genetically modified photosynthetic reaction centers. Annu. Rev. Biophys. Biophys. Chem., 19, 333-367.
16. Cui, L., Bingham, S.E., Kuhn, M., Kass, H., Lubitz, W. and Webber, A.N. (1995) Site-directed mutagenesis of conserved histidines in the helix VIII domain of PsaB impairs assembly of the photosystem I reaction center without altering spectroscopic characteristics of P700. Biochemistry, 34, 1549-1558.
17. Deisenhofer, J. and Michel, H. (1989) Nobel lecture. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J., 8, 2149-2170.
18. Deisenhofer, J., Epp, O., Sinning, I. and Michel, H. (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol., 246, 429-157.
19. Farah, J., Rappaport, F., Choquet, Y., Joliot, P. and Rochaix, J.-D. (1995) Isolation of a psaF-deficient mutant of Chlamydomonas reinhardtii: efficient interaction of plastocyanin with the photosystem I reaction center is mediated by the PsaF subunit. EMBO J., 14, 4976-4984.
20. Fenton, J.M. and Crofts, A.R. (1990) Computer aided imaging of photosynthetic systems: application of video imaging to the study of fluorescence induction in green plants and photosynthetic bacteria. Photosyn. Res., 26, 59-66.
21. Fischer, N., Stampacchia, O., Redding, K. and Rochaix, J.D. (1996) Selectable marker recycling in the chloroplast. Mol. Gen. Genet., 251, 373-380.
22. Fischer, N., Setif, P. and Rochaix, J.D. (1997) Targeted mutations in the psaC gene of Chlamydomonas reinhardtii: preferential reduction of FB at low temperature is not accompanied by altered electron flow from photosystem I to ferredoxin. Biochemistry, 36, 93-102.
23. 700 chlorophyll a proteins of maize photosystem I: Predictions based on the primary sequences and features shared by other chlorophyll proteins. Molecular Biology of the Photosynthetic Apparatus. Cold Spring Harbor Laboratory Press, New York, pp. 111-120.
24. Fromme, P. (1996) Structure and function of photosystem I. Curr. Opin. Struct. Biol., 6, 473-484.
25. Garnier, J., Guyon, D. and Picaud, A. (1979) Characterization of new strains of nonphotosynthetic mutants of Chlamydomonas reinhardtii. I. Fluorescence, photochemical activities, chlorophyll-protein complexes. Plant Cell Physiol., 20, 1013-1027.
26. Golbeck, J.H. and Bryant, D.A. (1991) Photosystem I. In Lee, C.P. (ed.), Current Topics in Bioenergetics: Light-Driven Reactions in Bioenergetics. Academic Press, New York, Vol. 16, pp. 83-177.
27. Goldschmidt-Clermont, M. (1991) Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker for site-directed transformation of Chlamydomonas. Nucleic Acids Res., 19, 4083-4089.
28. X binding region of Photosystem 1 by site directed mutation of PsaA in Chlamydomonas reinhardtii. Photosyn. Res., 46, 257-264.
29. Harris, E.H. (1989) The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego.
30. Hippler, M., Drepper, F., Farah, J. and Rochaix, J.D. (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry, 36, 6343-6349.
31. Huber, M., Isaacson, R., Abresch, E., Gaul, D., Schenck, C. and Feher, G. (1996) Electronic structure of the oxidized primary electron donor of the HL(M202) and HL(L173) heterodimer mutants of the photosynthetic bacterium Rhodobacter sphaeroides: ENDOR on single crystals of reaction centers. Biochim. Biophys. Acta, 1273, 108-128.
32. Käß, H. (1995) Die struktur des primären donators P700 in Photosystem I: Untersuchungen mit methoden der stationären und gepulsten elektronsprinresonanz. PhD thesis. Technische Universität Berlin, Germany.
33. 700 in Photosystem I and of chlorophyll a. Chem. Phys. Lett., 251, 193-203.
34. Krauss, N., Schubert, W.D., Klukas, O., Fromme, P., Witt, H.T. and Saenger, W. (1996) Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nature Struct. Biol., 3, 965-973.
35. Kruip, J., Chitnis, P.R., Lagoutte, B., Rogner, M. and Boekema, E.J. (1997) Structural organization of the major subunits in cyanobacterial photosystem 1. Localization of subunits psac, -d, -e, -f, and -j. J. Biol. Chem., 272, 17061-17069.
36. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J. and Rochaix, J.D. (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell, 58, 869-876.
37. Kuck, U., Choquet, Y., Schneider, M., Dron, M. and Bennoun, P. (1987) Structural and transcriptional analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardtii: evidence for in vivo trans-splicing. EMBO J., 6, 2185-2192.
38. Kuhlbrandt, W. and Wang, D.N. (1991) Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature, 350, 130-134.
39. Liebl, U., Mockensturm-Wilson, M., Trost, J., Brune, D., Blankenship, R. and Vermaas, W. (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proc. Natl Acad. Sci. USA, 90, 7124-7128.
40. Lubitz, W. (1991) EPR and ENDOR studies of chlorophyll cation and anion radicals. In Scheer, H. (ed.), Chlorophylls. CRC Press, Boca Raton, pp. 903-944.
41. +. Biochemistry, 35, 13288-13293.
42. Melkozemov, A.N., Su, H., Lin, S., Bingham, S., Webber, A.N. and Blankenship, R.E. (1997) Specific mutation near the primary donor in photosystem I from Chlamydomonas reinhardtii alters the trapping time and spectroscopic properties of P700. Biochemistry, 36, 2898-2907.
43. Nabedryk, E. (1996) Light-induced Fourier transform infrared difference spectroscopy of the primary electron donor in photosynthetic reaction centers. In Mantsch, H. and Chapman, D. (eds). Infrared Spectroscopy of Biomolecules. Wily-Liss, New York, pp. 39-81.
44. Nabedryk, E., Leonhard, M., Mantele, W. and Breton, J. (1990) Fourier transform infrared difference spectroscopy shows no evidence for an enolization of chlorophyll a upon cation formation either in vitro or during P700 photooxidation. Biochemistry, 29, 3242-3247.
45. Nabedryk, E., Allen, J.P., Taguchi, A.K., Williams, J.C., Woodbury, N.W. and Breton, J. (1993) Fourier transform infrared study of the primary electron donor in chromatophores of Rhodobacter sphaeroides with reaction centers genetically modified at residues M160 and L131. Biochemistry, 32, 13879-13885.
46. Newman, S.M., Gillham, N.W., Harris, E.H., Johnson, A.M. and Boynton, J.E. (1991) Targeted disruption of chloroplast genes in Chlamydomonas reinhardtii. Mol. Gen. Genet., 230, 65-74.
47. Nickelsen, J., van Dillewijn, J., Rahire, M. and Rochaix, J.D. (1994) Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J., 13, 3182-3191.
48. Nitschke, W. and Rutherford, A.W. (1991) Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem. Sci., 16, 241-245.
49. Nitschke, W., Mattioli, T. and Rutherford, A.W. (1996) The FeS-type photosystems and the evolution of photosynthetic reaction centers. In Baltscheffsky, H. (ed.), Origin and Evolution of Biological Energy Conversion. VCH Publishers, New York, pp. 177-203.
50. Ohad, I., Adir, N., Koike, H., Kyle, D.J. and Inoue, Y. (1990) Mechanism of photoinhibition m vivo. A reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. J. Biol. Chem., 265, 1972-1979.
51. Picard, V., Ersdal-Badju, E., Lu, A. and Bock, S.C. (1994) A rapid and efficient one-tube PCR-based mutagenesis technique using Pfu DNA polymerase. Nucleic Acids Res., 22, 2587-2591.
52. Porra, R., Thompson, W. and Kriedemann, P. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta, 975, 384-394.
53. Rautter, J., Lendzian, F., Lubitz, W., Wang, S. and Allen, J.P. (1994) Comparative study of reaction centers from photosynthetic purple bacteria: electron paramagnetic resonance and electron nuclear double resonance spectroscopy. Biochemistry, 33, 12077-12084.
54. Rochaix, J.D. (1992) Post-transcriptional steps in the expression of chloroplast genes. Annu. Rev. Cell Biol., 8, 1-28.
55. Rochaix, J.D. (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu. Rev. Genet., 29, 209-230.
56. Rochaix, J.-D., Mayfield, S., Goldschmidt-Clermont, M. and Erickson, J. (1988) Molecular biology of Chlamydomonas. In Shaw, C.H. (ed.), Plant Molecular Biology: A Practical Approach. IRL Press, Oxford, pp. 253-275.
57. X domain in photosystem I interacts with the subunit PsaC: site-directed changes in PsaB destabilize the subunit interaction in Chlamydomonas reinhardtii. Biochemistry, 34, 6328-6334.
58. Rutherford, A.W. and Nitschke, W. (1996) Photosystem II and the quinone-iron-containing reaction centers: comparisons and evolutionary perspectives. In Baltscheffsky, H. (ed.), Origin and Evolution of Biological Energy Conversion. VCH Publishers, New York, pp. 143-175.
59. Spreitzer, R.J. and Mets, L. (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardtii with associated light-sensitive phenotypes. Plant Physiol., 67, 565-569.
60. Studier, W., Rosenberg, A., Dunn, J. and Dubendorff, J. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Eniymol., 185, 60-89.
61. Takahashi, Y, Goldschmidt-Clermont, M., Soen, S.Y., Franzen, L.G. and Rochaix, J.D. (1991) Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I. EMBO J., 10, 2033-2040.
62. Vallon, O. and Bogorad, L. (1993) Topological study of PSI-A and PSI-B, the large subunits of the photosystem I reaction center. Eur. J. Biochem., 214, 907-915.
63. Vermaas, W.F.J. (1994) Evolution in heliobacteria: Implications for photosynthetic reaction center complexes. Photosyn. Res., 41, 285-294.
64. Webber, A.N., Gibbs, P.B., Ward, J.B. and Bingham, S.E. (1993) Site-directed mutagenesis of the photosystem I reaction center in chloroplasts. The proline-cysteine motif. J. Biol. Chem., 268, 12990-12995.
65. Webber, A.N., Su, H., Bingham, S.E., Kass, H., Krabben, L., Kuhri, M., Jordan, R., Schlodder, E. and Lubitz, W. (1996) Site-directed mutations affecting the spectroscopic characteristics and midpoint potential of the primary donor in photosystem I. Biochemistry, 35, 12857-12863.
66. Xu, Q., Yu, L., Chitnis, V.P. and Chitnis, P.R. (1994) Function and organization of photosystem I in a cyanobacterial mutant strain that lacks PsaF and PsaJ subunits. J. Biol. Chem., 269, 3205-3211.