Functional organization of a plant Photosystem I: Evolution of a highly efficient photochemical machine

Plant Physiology and Biochemistry

Volumn 46, Issue 3, 2008, Pages 228-237

  Amunts, Alexey ^a   Nelson, Nathan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Electron transfer; Evolution; Light harvesting; Photosynthesis; Photosystem I; Reaction center; State transitions

Indexed keywords

CHEMISTRY; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW;

LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

CYANOBACTERIA;

EID: 40849083514     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2007.12.013     Document Type: Review

References (93)

1. Wilson T.H., and Lin E.C. Evolution of membrane bioenergetics. J. Supramol. Struct. 13 (1980) 421-446
2. Morowitz H.J., Heinz B., and Deamer D.W. The chemical logic of a minimum protocell. Orig. Life Evol. Biosph. 18 (1988) 281-287
3. Rasmussen B. Filamentous microfossils in a 3,235-million-year-old volcanogenic massive sulphide deposit. Nature 405 (2000) 676-679
4. Nisbet E.G., and Sleep N.H. The habitat and nature of early life. Nature 409 (2001) 1083-1091
5. Clausen J., and Junge W. Detection of an intermediate of photosynthetic water oxidation. Nature 430 (2004) 480-483
6. Barber J. Engine of life and big bang of evolution: a personal perspective. Photosynth. Res. 80 (2004) 137-155
7. Martin W., Rotte C., Hoffmeister M., Theissen U., Gelius-Dietrich G., Ahr S., and Henze K. Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55 (2003) 193-204
8. Cota G.F. Photoadaptation of high arctic ice algae. Nature 315 (1985) 219-222
9. Thomas D.N., and Wiencke C. Photosynthesis, dark respiration and light independent carbon fixation of endemic Antarctic macroalgae. Polar Biol. 11 (1991) 329-337
10. Sand-Jensen K. Broad-scale comparison of photosynthesis in terrestrial and aquatic plant communities. Oikos 80 (1997) 203-208
11. Ma Q., Behboudian M.H., Turner N.C., and Palta J.A. Regulation of growth. J. Exp. Bot. 52 (2001) 123-131
12. 4 plant photosynthesis. Nature 414 (2001) 543-546
13. Nelson N., and Yocum C. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57 (2006) 521-565
14. Ben-Shem A., Frolow F., and Nelson N. Evolution of Photosystem I-from symmetry through pseudosymmetry to asymmetry. FEBS Lett. 564 (2004) 274-280
15. Barber J., and Anderson B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem. Sci. 17 (1992) 61-66
16. Rochaix J.-D. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett. 581 (2007) 2768-2775
17. Mullet J.E., Burke J.J., and Arntzen C.J. Chlorophyll proteins of Photosystem I. Plant Physiol 65 (1980) 814-822
18. Mullet J.E., Burke J.J., and Arntzen C.J. A developmental study of Photosystem I peripheral chlorophyll proteins. Plant Physiol 65 (1980) 823-827
19. Nelson N., and Ben Shem A. Photosystem I reaction center: past and future. Photosynth. Res. 73 (2002) 193-206
20. Nelson N., and Ben Shem A. The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 5 (2004) 971-982
21. Fromme P., and Mathis P. Unraveling the photosystem I reaction center: a history, or the sum of many efforts. Photosynth. Res. 80 (2004) 109-124
22. Jolley C., Ben-Shem A., Nelson N., and Fromme P. Structure of plant photosystem I revealed by theoretical modeling. J. Biol. Chem. 280 (2005) 33627-33636
23. Engel G.S., Calhoun T.R., Read E.L., Ahn T.-K., Mancal T., Cheng Y.-C., Blankenship R.E., and Fleming G.R. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446 (2007) 782-786
24. Lee H., Cheng Y.-C., and Fleming G.R. Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316 (2007) 1462-1465
25. Wang H., Lin S., Allen J.P., Williams J.-A.C., Blankert S., Laser C., and Woodbury N.W. Protein dynamics control the kinetics of initial electron transfer in photosynthesis. Science 316 (2007) 747-750
26. Amunts A., Drory O., and Nelson N. The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447 (2007) 58-63
27. Ben-Shem A., Frolow F., and Nelson N. Crystal structure of plant photosystem I. Nature 426 (2003) 630-635
28. Amunts A., Ben-Shem A., and Nelson N. Solving the structure of plant photosystem I-biochemistry is vital. Photochem. Photobiol. Sci. 4 (2005) 1011-1015
29. Scheller H.V., Jensen P.E., Haldrup A., Lunde C., and Knoetzel J. Role of subunits in eukaryotic Photosystem I. Biochim. Biophys. Acta 1507 (2001) 41-60
30. Jensen P.E., Haldrup A., Rosgaard L., and Scheller H.V. Molecular dissection of photosystem I in higher plants: topology, structure and function. Physiol. Plant 119 (2003) 313-321
31. Jensen P.E., Bassi R., Boekema E.J., Dekker J.P., Jansson S., Leister D., Robinson C., and Scheller H.V. Structure, function and regulation of plant photosystem I. Biochim. Biophys. Acta 1767 (2007) 335-352
32. Bengis C., and Nelson N. Subunit structure of chloroplast photosystem I reaction center. J. Biol. Chem. 250 (1977) 4564-4569
33. Chitnis P.R., Purvis D., and Nelson N. Molecular cloning and targeted mutagenesis of the gene PsaF encoding subunit III of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 266 (1991) 20146-20151
34. Farah J., Rappaport F., Choquet Y., Joliot P., and Rochaix J.D. 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 (1995) 4976-4984
35. Boekema E.J., Jensen P.E., van Breemen J.F.L., van Roon H., Scheller H.V., and Dekker J.P. Green plant photosystem I binds Light-harvesting complex I on one side of the complex. Biochemistry 40 (2001) 1029-1036
36. Ben-Shem A., Frolow F., and Nelson N. Light-harvesting features revealed by the structure of plant photosystem I. Photosynth. Res. 81 (2004) 239-250
37. Fischer N., Boudreau E., Hippler M., Drepper F., Haehnel W., and Rochaix J.D. A large fraction of PsaF is nonfunctional in photosystem I complexes lacking the PsaJ subunit. Biochemistry 38 (1999) 5546-5552
38. Hansson A., Amann K., Zygadlo A., Meurer J., Scheller H.V., and Jensen P.E. Knock-out of the chloroplast encoded PSI-J Subunit of Photosystem I in Nicotiana tabacum: PSI-J is required for efficient electron transfer and stable accumulation of photosystem I. FEBS J 274 (2007) 1734-1746
39. Lunde C., Jensen P.E., Haldrup A., Knoetzel J., and Scheller H.V. The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408 (2000) 613-615
40. Jensen P.E., Haldrup A., Zhang S., and Scheller H.V. The PSI-O subunit of plant photosystem I is involved in balancing the excitation pressure between the two photosystems. J. Biol. Chem. 279 (2004) 24212-24217
41. Zhang S., and Scheller H.V. Light-harvesting complex II binds to several small subunits of photosystem I. J. Biol. Chem. 279 (2004) 3180-3187
42. Khrouchtchova A., Hansson M., Paakkarinen V., Vainonen J.P., Zhang S.P., Jensen P.E., Scheller H.V., Vener A.V., Aro E.M., and Haldrup A. A previously found thylakoid membrane protein of 14(kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett. 579 (2005) 4808-4812
43. Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4 (1999) 236-240
44. Jansson S., Andersen B., and Scheller H.V. Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol 112 (1996) 409-420
45. Haldrup A., Naver H., and Scheller H.V. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J 17 (1999) 689-698
46. Jordan P., Fromme P., Witt H.T., Klukas O., Saenger W., and Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution. Nature 411 (2001) 909-917
47. Fromme P., Jordan P., and Krauss N. Structure of photosystem I. Biochim. Biophys. Acta 1507 (2001) 5-31
48. Nelson N., and Ben-Shem A. The structure of photosystem I and evolution of photosynthesis. BioEssays 27 (2005) 914-922
49. Sener M.K., Park S., Lu D., Damjanovic A., Ritz T., Fromme P., and Schulten K. Excitation migration in trimeric cyanobacterial photosystem I. J. Chem. Phys. 120 (2004) 11183-11195
50. Fromme P., and Grotjohann I. Structural Analysis of Cyanobacterial Photosystem I (2006), Springer, Dordrecht 47-69
51. Amunts A., Drory O., and Nelson N. A glimpse into the atomic structure of plant Photosystem I. In: Fromme P. (Ed). Structures of Photosynthetic Proteins (2008), Wiley-VCH
52. Heinemeyer J., Eubel H., Wehmhoner D., Jansch L., and Braun H.P. Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry 65 (2004) 1683-1692
53. Kouril R., van Oosterwijk N., Yakushevska A.E., and Boekema E.J. Photosystem I: a search for green plant trimers Photochem. Photobiol. Sci. 4 (2005) 1091-1094
54. Morosinotto T., Ballottari M., Klimmek F., Jansson S., and Bassi R. The association of the antenna system to photosystem I in higher plants. Cooperative interactions stabilize the supramolecular complex and enhance red-shifted spectral forms. J. Biol. Chem. 280 (2005) 31050-31058
55. Mozzo M., Morosinotto T., Bassi R., and Croce R. Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta 1757 (2006) 1607-1613
56. Jensen P.E., Gilpin M., Knoetzel J., and Scheller H.V. The PSI-K subunit of photosystem I is involved in the interaction between light-harvesting complex I and the photosystem I reaction center core. J. Biol. Chem. 275 (2000) 24701-24708
57. Ballottari M., Dall'Osto L., Morosinotto T., and Bassi R. Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282 (2007) 8947-8958
58. Pichersky E., and Jansson S. Oxygenic Photosynthesis: The Light Reactions (1996), Kluwer Academic Publishers, Dordrecht 507-521
59. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., and Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428 (2004) 287-292
60. Standfuss J., Terwisscha van Scheltinga A.C., Lamborghini M., and Kuhlbrandt W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24 (2005) 919-928
61. Melkozernov A.N., Kargul J., Lin S., Barber J., and Blankenship R.E. Structural and functional organization of the peripheral light-harvesting system in photosystem I. Photosynth. Res. 85 (2005) 33-50
62. Melkozernov A.N., Barber J., and Blankenship R.E. Light harvesting in photosystem I supercomplexes. Biochemistry 45 (2006) 331-345
63. Schmid V.H., Paulsen H., and Rupprecht J. Identification of N- and C-terminal amino acids of Lhca1 and Lhca4 required for formation of the heterodimeric peripheral photosystem I antenna LHCI-730. Biochemistry 41 (2002) 9126-9131
64. Corbet D., Schweikardt T., Paulsen H., and Schmid V.H. Amino acids in the second transmembrane helix of the Lhca4 subunit are important for formation of stable heterodimeric light-harvesting complex LHCI-730. J. Mol. Biol. 370 (2007) 170-182
65. Schmid V.H., Cammarata K.V., Bruns B.U., and Schmidt G.W. In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: Heterodimerization is required for antenna pigment organization. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7667-7672
66. Castelletti S., Morosinotto T., Robert B., Caffarri S., Bassi R., and Croce R. Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42 (2003) 4226-4234
67. Ihalainen J.A., Croce R., Morosinotto T., van Stokkum I.H., Bassi R., Dekker J.P., and van Grondelle R. Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study. J. Phys. Chem. B. 109 (2005) 21150-21158
68. Croce R., Mozzo M., Morosinotto T., Romeo A., Hienerwadel R., and Bassi R. Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I. Biochemistry 46 (2007) 3846-3855
69. Croce R., Chojnicka A., Morosinotto T., Ihalainen J.A., van Mourik F., Dekker J.P., Bassi R., and van Grondelle R. The low-energy forms of photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys. J. 93 (2007) 2418-2428
70. Ganeteg U., Klimmek F., and Jansson S. Lhca5-an LHC-type protein associated with photosystem I. Plant Mol. Biol. 54 (2004) 641-651
71. Storf S., Jansson S., and Schmid V.H. Pigment binding, fluorescence properties, and oligomerization behavior of Lhca5, a novel light-harvesting protein. J. Biol. Chem. 280 (2005) 5163-5168
72. Klimmek F., Ganeteg U., Ihalainen J.A., van Roon H., Jensen P.E., Scheller H.V., Dekker J.P., and Jansson S. Structure of the higher plant light harvesting complex I: in vivo characterization and structural interdependence of the Lhca proteins. Biochemistry 44 (2005) 3065-3073
73. Lucinski R., Schmid V.H., Jansson S., and Klimmek F. Lhca5 interaction with plant photosystem I. FEBS Lett. 580 (2006) 6485-6488
74. Hippler M., Reichert J., Sutter M., Zak E., Altschmied L., Schroer U., Herrmann R.G., and Haehnel W. The plastocyanin binding domain of photosystem I. EMBO J 15 (1996) 6374-6384
75. Hippler M., Drepper F., Haehnel W., and Rochaix J.-D. The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 7339-7344
76. Hippler M., Drepper F., Rochaix J.-D., and Muhlenhoff U. Insertion of the N-terminal part of PsaF from Chlamydomonas reinhardtii into photosystem I from Synechococcus elongatus enables efficient binding of algal plastocyanin and cytochrome c6. J. Biol. Chem. 274 (1999) 4180-4188
77. Sommer F., Drepper F., and Hippler M. The luminal helix l of PsaB is essential for recognition of plastocyanin or cytochrome c6 and fast electron transfer to photosystem I in Chlamydomonas reinhardtii. J. Biol. Chem. 277 (2002) 6573-6581
78. Sommer F., Drepper F., Haehnel W., and Hippler M. The hydrophobic recognition site formed by residues PsaA-Trp651 and PsaB-Trp627 of photosystem I in Chlamydomonas reinhardtii confers distinct selectivity for binding of plastocyanin and cytochrome c6. J. Biol. Chem. 279 (2004) 20009-20017
79. Setif P.Q., and Bottin H. Laser flash absorption spectroscopy study of ferredoxin reduction by photosystem I: spectral and kinetic evidence for the existence of several photosystem I-ferredoxin complexes. Biochemistry 34 (1995) 9059-9070
80. Fischer N., Setif P., and Rochaix J.-D. Site-directed mutagenesis of the PsaC subunit of photosystem I. F(b) is the cluster interacting with soluble ferredoxin. J. Biol. Chem. 274 (1999) 23333-23340
81. Fischer N., Hippler M., Setif P., Jacquot J.P., and Rochaix J.-D. The PsaC subunit of photosystem I provides an essential lysine residue for fast electron transfer to ferredoxin. EMBO J. 17 (1998) 849-858
82. Setif P., Fischer N., Lagoutte B., Bottin H., and Rochaix J.-D. The ferredoxin docking site of photosystem I. Biochim. Biophys. Acta 1555 (2002) 204-209
83. Bottin H., Hanley J., and Lagoutte B. Role of acidic amino acid residues of PsaD subunit on limiting the affinity of photosystem I for ferredoxin. Biochem. Biophys. Res. Commun. 287 (2001) 833-836
84. Hanley J., Setif P., Bottin H., and Lagoutte B. Mutagenesis of photosystem I in the region of the ferredoxin cross-linking site: modifications of positively charged amino acids. Biochemistry 35 (1996) 8563-8571
85. Andersen B., Scheller H.V., and Moller B.L. The PSI-E subunit of photosystem I binds ferredoxin:NADP+ oxidoreductase. FEBS Lett. 311 (1992) 169-173
86. Murata N. Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim. Biophys. Acta 172 (1969) 242-251
87. Murata N. Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim. Biophys. Acta 189 (1969) 171-181
88. Forsberg J., and Allen J.F. Protein tyrosine phosphorylation in the transition to light state 2 of chloroplast thylakoids. Photosynth. Res. 68 (2001) 71-79
89. Allen J.F., Bennett J., Steinback K.E., and Arntzen C.G. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291 (1981) 25-29
90. Kyle D.J., Staehelin L.A., and Arntzen C.J. Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch. Biochem. Biophys. 222 (1983) 527-541
91. Kouril R., Zygadlo A., Arteni A.A., de Wit C.D., Dekker J.P., Jensen P.E., Scheller H.V., and Boekema E.J. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44 (2005) 10935-10940
92. Kargul J., Turkina M.V., Nield J., Benson S., Vener A.V., and Barber J. Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J 272 (2005) 4797-4806
93. Takahashi H., Iwai M., Takahashi Y., and Minagawa J. Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 477-482