Advertisement

Photosynthesis Research

, Volume 82, Issue 3, pp 241–263 | Cite as

Structure, function and assembly of Photosystem II and its light-harvesting proteins

  • Jun MinagawaEmail author
  • Yuichiro Takahashi
Review

Abstract

Photosystem II (PSII) is a multisubunit chlorophyll–protein complex that drives electron transfer from water to plastoquinone using energy derived from light. In green plants, the native form of PSII is surrounded by the light-harvesting complex (LHCII complex) and thus it is called the PSII–LHCII supercomplex. Over the past several years, understanding of the structure, function, and assembly of PSII and LHCII complexes has increased considerably. The unicellular green alga Chlamydomonas reinhardtii has been an excellent model organism to study PSII and LHCII complexes, because this organism grows heterotrophically and photoautotrophically and it is amenable to biochemical, genetic, molecular biological and recombinant DNA methodology. Here, the genes encoding and regulating components of the C. reinhardtii PSII–LHCII supercomplex have been thoroughly catalogued: they include 15 chloroplast and 20 nuclear structural genes as well as 13 nuclear genes coding for regulatory factors. This review discusses these molecular genetic data and presents an overview of the structure, function and assembly of PSII and LHCII complexes.

Keywords

antenna assembly Chlamydomonas reinhardtii LHCII light-harvesting complex Photosystem II 

Abbreviations:

Chl

chlorophyll

Cyt

cytochrome

LHC

the light-harvesting complex

LHCII

proteins constitute major antenna complex for Photosystem II

NPQ

non-photochemical quenching

P680

primary electron donor in PSII

Pheo

pheophytin a

PheoDI

pheophytin on D1 as an intermediate electron acceptor of PSII

PSII

Photosystem II

PQ

plastoquinone

QA

the primary electron acceptor of PSII

QB

the secondary electron acceptor of PSII

RC

reaction center for Photosystem II

SRP

signal recognition particle

TMH

transmembrane helix

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersson, J, Walters, RG, Horton, P, Jansson, S 2001Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipationPlant Cell1311931204CrossRefPubMedGoogle Scholar
  2. Anbudurai, PR, Pakrasi, HB 1993Mutational analysis of the PsbL protein of Photosystem II in the cyanobacterium Synechocystis sp. PCC 6803.Z Naturforsch [C]48267274Google Scholar
  3. Anbudurai, PR, Mor, TS, Ohad, I, Shestakov, SV, Pakrasi, HB 1994ThectpA gene encodes the C-terminal processing protease for the D1 protein of the Photosystem II reaction center complexProc Natl Acad Sci USA9180828086PubMedGoogle Scholar
  4. Baena-Gonzélez, E, Aro, EM 2002Biogenesis, assembly and turnover of Photosystem II unitsPhil Trans R Soc Lond B35714511460CrossRefGoogle Scholar
  5. Baroli, I, Niyogi, KK 2000Molecular genetics of xanthophyll-dependent photoprotection in green algae and plantsPhil Trans R Soc Lond B35513851394CrossRefGoogle Scholar
  6. Bassi, R, Wollman, FA 1991The chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtiiPlanta183423433CrossRefGoogle Scholar
  7. Bassi, R, Pineau, B, Dainese, P, Marquardt, J 1993Carotenoid-binding proteins of Photosystem IIEur J Biochem212297303PubMedGoogle Scholar
  8. Bellafiore, S, Ferris, P, Naver, H, Göhre, V, Rochaix, JD 2002Loss of Albino3 leads to the specific depletion of the light-harvesting systemPlant Cell1423032314CrossRefPubMedGoogle Scholar
  9. Bennett, J 1977Phosphorylation of chloroplast membrane polypeptidesNature269344346CrossRefPubMedGoogle Scholar
  10. Bishop, CL, Purton, S, Nugent, JHA 2003Molecular analysis of the Chlamydomonas nuclear gene encoding PsbW and demonstration that PsbW is a subunit of Photosystem II, but not Photosystem IPlant Mol Biol52285289CrossRefPubMedGoogle Scholar
  11. Büchel, C, Morris, E, Orlova, E, Barber, J 2001Localisation of the PsbH subunit in Photosystem II: a new approach using labelling of His-tags with a Ni2+-NTA gold cluster and single particle analysisJ Mol Biol312371379CrossRefPubMedGoogle Scholar
  12. Burnap, RL, Sherman, LA 1991Deletion mutagenesis in Synechocystis sp. PCC6803 indicates that the Mn-stabilizing protein of Photosystem II is not essential for oxygen evolution. Biochemistry30440446Google Scholar
  13. Chua, NH, Bennoun, P 1975Thylakoid membranes of C. reinhardtii: wild type and mutant strians deficient in Photosystem II reaction centersProc Natl Acad Sci USA76111115Google Scholar
  14. Chua, NH, Gillham, NW 1977The sites of synthesis of the principal thylakoid membrane polypeptides in Chlamydomonas reinhardtiiJ Cell Biol74441452CrossRefPubMedGoogle Scholar
  15. Claros, MG, Heijne, G 1994TopPred II: an improved software For membrane protein structure predictionsCA-BIOS10685686Google Scholar
  16. Crimi, M, Dorra, D, Bosinger, CS, Giuffra, E, Holzwarth, AR, Bassi, R 2001Time-resolved fluorescence analysis of the recombinant Photosystem II antenna complex CP29: effects of zeaxanthin, pH and phosphorylationEur J Biochem268260267PubMedGoogle Scholar
  17. Debus, RJ 2001Amino acid residues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of Photosystem IIBiochim Biophys Acta1503164186PubMedGoogle Scholar
  18. Debus, RJ, Barry, BA, Babcock, GT, McIntosh, L 1988aSite-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving systemProc Natl Acad Sci USA85427430Google Scholar
  19. Debus, RJ, Barry, BA, Sithole, I, Babcock, GT, McIntosh, L 1988bDirected mutagenesis indicates that the donor to P680+ in Photosystem II is tyrosine-161 of the D1 polypeptideBiochemistry2790719074CrossRefGoogle Scholar
  20. Dedner, J, Meyer, HE, Ashton, C, Wildner, GF 1988N-terminal sequence analysis of the 8 kDa protein in Chlamydomonas reinhardtii: localization of the phosphothreonineFEBS Lett2367782CrossRefGoogle Scholar
  21. DeLille, J, Peterson, EC, Johnson, T, Moore, M, Kight, A, Henry, R 2000A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplastsProc Natl Acad Sci USA9719261931CrossRefPubMedGoogle Scholar
  22. Depège, N, Bellafiore, S, Rochaix, JD 2003Role of chloroplast protein kinase stt7 in LHCII phosphorylation and state transition in ChlamydomonasScience29915721575PubMedGoogle Scholar
  23. Vitry, C, Wollman, FA 1988Changes in phosphorylation of thylakoid membrane proteins in light-harvesting complex mutants from Chlamydomonas reinhardtiiBiochim Biophys Acta933444449Google Scholar
  24. Vitry, C, Olive, J, Drapier, D, Recouvreur, M, Wollman, FA 1989Posttranslational events leading to the assembly of Photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtiiJ Cell Biol1099911006CrossRefPubMedGoogle Scholar
  25. Vitry, C, Diner, BA, Popo, JL 1991Photosystem II particles from Chlamydomonas reinhardtii. Purification, molecular weight, small subunit composition, and protein phosphorylation.J Biol Chem2661661416621PubMedGoogle Scholar
  26. Diner, BA, Petrouleas, V 1987Q400, the non-heme iron of the Photosystem II iron–quinone complex. A spectroscopic probe of quinone and inhibitor binding to the reaction center.Biochim Biophys Acta895107125Google Scholar
  27. Diner, BA, Rappaport, F 2002Structure, dynamics, and energetics of the primary photochemistry of Photosystem II of oxygenic photosynthesisAnn Rev Plant Biol53551580Google Scholar
  28. Diner, BA, Schlodder, E, Nixon, PJ, Coleman, WJ, Rappaport, F, Lavergne, J, Vermaas, WF, Chisholm, DA 2001Site-directed mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilizationBiochemistry4092659281PubMedGoogle Scholar
  29. Dominici, P, Caffarri, S, Armenante, F, Ceoldo, S, Crimi, M, Bassi, R 2002Biochemical properties of the PsbS subunit of Photosystem II either purified from chloroplast or recombinantJ Biol Chem2772275022758CrossRefPubMedGoogle Scholar
  30. Durnford, DG, Deane, JA, Tan, S, McFadden, GI, Gantt, E, Green, BR 1999A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolutionJ Mol Evol485968PubMedGoogle Scholar
  31. Durnford, DG, Price, JA, McKim, SM, Sarchfield, ML 2003Light-harvesting complex gene expression is controlled by both transcriptional and post-transcriptional mechanisms during photoacclimation in Chlamydomonas reinhardtiiPhysiol Plant118193205Google Scholar
  32. Durrant, JR, Klug, DR, Kwa, SL, van, Grondelle R, Porter, G, Dekker, JP 1995A multimer model for P680, the primary electron donor of Photosystem IIProc Natl Acad Sci USA9247984802PubMedGoogle Scholar
  33. Elrad, D, Grossman, AR 2004A genome’s-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtiiCurr Genet456175CrossRefPubMedGoogle Scholar
  34. Elrad, D, Niyogi, KK, Grossman, AR 2002A major light-harvesting polypeptide of Photosystem II functions in thermal dissipationPlant Cell1418011816CrossRefPubMedGoogle Scholar
  35. Erickson, JM, Rahire, M, Malnoë, P, Girard-Bascou, J, Pierre, Y, Bennoun, P, Rochaix, JD 1986Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects Photosystem II stability and D1 expressionEMBO J517451754Google Scholar
  36. Erickson, JM 1998Assembly of Photosystem IIRochaix, JDGoldschmidt-Clermont, MMerchant, S eds. The Molecular Biology of Chloroplasts and Mitochondria in ChlamydomonasKluwer Academic PublishersDordrecht, The Netherlands255285Google Scholar
  37. Escoubas, JM, Lomas, M, LaRoche, J, Falkowski, PG 1995Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone poolProc Natl Acad Sci USA921023710241PubMedGoogle Scholar
  38. Ferreira, KN, Inverson, TM, Maghlaouli, K, Barber, J, Iwata, S 2004Architecture of the photosynthetic oxygen-evolving centerScience30318311838PubMedGoogle Scholar
  39. Fleischmann, MM, Ravanel, S, Delosme, R, Olive, J, Zito, F, Wollman, FA, Rochaix, JD 1999Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transitionJ Biol Chem2743098730994CrossRefPubMedGoogle Scholar
  40. Funk, C 2000Functional analysis of the PsbX protein by deletion of the corresponding gene in Synechocystis sp. PCC 6803.Plant Mol Biol 44815827CrossRefPubMedGoogle Scholar
  41. Gagné, G, Guertin, M 1992The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesisPlant Mol Biol18429445CrossRefPubMedGoogle Scholar
  42. Gau, AE, Thole, HH, Sokolenko, A, Altschmied, L, Herrmann, RG, Pistorius, EK 1998PsbY, a novel manganese-binding, low-molecular-mass protein associated with Photosystem IIMol Gen Genet2605668CrossRefPubMedGoogle Scholar
  43. Green, BR, Durnford, DG 1996The chlorophyll-carotenoid proteins of oxygenic photosynthesisAnn Rev Plant Physiol Plant Mol Biol47685714CrossRefGoogle Scholar
  44. Hahn, D, Kück, U 1999Identification of DNA sequences controlling light-and chloroplast-dependent expression of the lhcb1 gene from Chlamydomonas reinhardtiiCurr Genet34459466CrossRefPubMedGoogle Scholar
  45. Harrer, R, Bassi, R, Testi, MG, Schäfer, C 1998Nearest-neighbor analysis of a Photosystem II complex fromMarchantia polymorpha L. (Liverwort), which contains reaction center and antenna proteins.Eur J Biochem255196205CrossRefPubMedGoogle Scholar
  46. Hatano-Iwasaki, A, Minagawa, J, Inoue, Y, Takahashi, Y 2000Characterization of chloroplast psbA transformants of Chlamydomonas reinhardtii with impaired processing of a precursor of a Photosystem II reaction center protein, D1Plant Mol Biol42353363CrossRefPubMedGoogle Scholar
  47. Haußühl, K, Andersson, B, Adamska, I 2001A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant Photosystem IIEMBO J20713722PubMedGoogle Scholar
  48. Herrin, D, Michaels, A, Hickey, E 1981Synthesis of a chloroplast membrane polypeptide on thylakoid-bound ribosomes during the cell cycle of Chlamydomonas reinhardtiiBiochim Biophys Acta655136145Google Scholar
  49. Hippler, M, Klein, J, Fink, A, Allinger, T, Hoerth, P 2001Towards functional proteomics of membrane protein complexes: analysis of thylakoid membranes from Chlamydomonas reinhardtiiPlant J28595606CrossRefPubMedGoogle Scholar
  50. Hippler, M, Rimbault, B, Takahashi, Y 2002Photosynthetic complex assembly in Chlamydomonas reinhardtiiProtist153197220CrossRefPubMedGoogle Scholar
  51. Hirokawa, T, Boon-Chieng, S, Mitaku, S 1998SOSUI: classification and secondary structure prediction system for membrane proteinsBioinformatics14378379CrossRefPubMedGoogle Scholar
  52. Hiyama, T, Yumoto, K, Satoh, A, Takahashi, M, Nishikido, T, Nakamoto, H, Suzuki, K, Hiraide, T 2000Chromatographic separation of a small subunit (PsbW/PsaY) and its assignment to Photosystem I reaction centerBiochim Biophys Acta1459117124PubMedGoogle Scholar
  53. Hobe, S, Foster, R, Klingler, J, Paulsen, H 1995N-proximal sequence motif in light-harvesting chlorophyll a/b -binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complexBiochemistry341022410228CrossRefPubMedGoogle Scholar
  54. Hoober, JK, Park, H, Wolfe, GR, Komine, Y, Eggink, LL 1998Assembly of light harvesting systemsRochaix, JDGoldschmidt-Clermont, MMerchant, S eds. The Molecular Biology of Chloroplasts and Mitochondria in ChlamydomonasKluwer Academic PublishersDordrecht, The Netherlands363376Google Scholar
  55. Hoshida, H, Sugiyama, R, Nakano, Y, Shiina, T, Toyoshima, Y 1997Electron paramagnetic resonance and mutational analyses revealed the involvement of Photosystem II-L subunit in the oxidation step of Tyr-Z by P680+ to form the Tyr-Z+P680Pheo state in Photosystem IIBiochemistry361205312061CrossRefPubMedGoogle Scholar
  56. Ikeuchi, M, Inoue, Y 1988A new Photosystem II reaction center component (4.8 kDa protein) encoded by chloroplast genomeFEBS Lett2499104CrossRefGoogle Scholar
  57. Ikeuchi, M, Takio, K, Inoue, Y 1989N-terminal sequencing of Photosystem II low-molecular-mass proteins 5 and 4.1 kDa components of the O2-evolving core complex from higher plantsFEBS Lett242263269CrossRefPubMedGoogle Scholar
  58. Ikeuchi, M, Eggers, B, Shen, GZ, Webber, A, Yu, JJ, Hirano, A, Inoue, Y, Vermaas, W 1991Cloning of the psbK gene from Synechocystis sp. PCC 6803 and characterization of Photosystem II in mutants lacking PSII-K.J Biol Chem2661111111115PubMedGoogle Scholar
  59. Ikeuchi, M, Shukla, VK, Pakrasi, HB, Inoue, Y 1995Directed inactivation of the psbI gene does not affect Photosystem II in the cyanobacterium Synechocystis sp. PCC 6803.Mol Gen Genet249622628CrossRefPubMedGoogle Scholar
  60. Im, CS, Grossman, AR 2001Identification and regulation of high light-induced genes in Chlamydomonas reinhardtiiPlant J30301313CrossRefGoogle Scholar
  61. Imbault, P, Wittemer, C, Johanningmeier, U, Jacobs, JD, Howell, SH 1988Structure of the Chlamydomonas reinhardtii cabII-1 gene encoding a chlorophyll a/b-binding proteinGene73397407CrossRefPubMedGoogle Scholar
  62. Irrgang, KD, Shi, LX, Funk, C, Schröder, WP 1995A nuclear-encoded subunit of the Photosystem II reaction centerJ Biol Chem2701758817593CrossRefPubMedGoogle Scholar
  63. Jansson, S 1999A guide to the Lhc genes and their relatives in ArabidopsisTrends Plant Sci4236240CrossRefPubMedGoogle Scholar
  64. Johanningmeier, U, Howell, SH 1984Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii : possible involvement of chlorophyll synthesis precursorsJ Biol Chem2591354113549PubMedGoogle Scholar
  65. Kamiya, N, Shen, JR 2003Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7-A resolutionProc Natl Acad Sci USA10098103PubMedGoogle Scholar
  66. Kanervo, E, Spetea, C, Nishiyama, Y, Murata, N, Andersson, B, Aro, EM 2003Dissecting a cyanobacterial proteolytic system: efficiency in inducing degradation of the D1 protein of Photosystem II in cyanobacteria and plantsBiochimi Biophys Acta1607131140CrossRefGoogle Scholar
  67. Kapazoglou, A, Sagliocco, F, Dure, L 1995PSII-T, a new nuclear encoded lumenal protein from Photosystem IIJ Biol Chem2701219712202CrossRefPubMedGoogle Scholar
  68. Kashino, Y, Lauber, WM, Carroll, JA, Wang, Q, Whitmarsh, J, Satoh, K, Pakrasi, HB 2002Proteomic analysis of a highly active Photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides.Biochemistry4180048012PubMedGoogle Scholar
  69. Katoh, H, Ikeuchi, M 2001Targeted disruption of psbX and biochemical characterization of Photosystem II complex in the thermophilic cyanobacterium Synechococcus elongatusPlant Cell Physiol42179188CrossRefPubMedGoogle Scholar
  70. Kim, SJ, Robinson, D, Robinson, C 1996An Arabidopsis thaliana cDNA encoding PS II-X, a 4.1 kDa component of Photosystem II: a bipartite presequence mediates SecA/ΔpH-independent targeting into thylakoidsFEBS Lett390175178CrossRefPubMedGoogle Scholar
  71. Kindle, KL 1987Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii : effect of light and acetatePlant Mol Biol9547563CrossRefGoogle Scholar
  72. Kruse, O 2001Light-induced short-term adaptation mechanisms under redox control in the PS II–LHC II supercomplex: LHCII state transitions and PSII repair cycleNaturwissenschaften88284292CrossRefPubMedGoogle Scholar
  73. Künstner, P, Guardiola, A, Takahashi, Y, Rochaix, JD 1995A mutant strain of Chlamydomonas reinhardtii lacking the chloroplast Photosystem II psbI gene grows photoautotrophicallyJ Biol Chem27096519654CrossRefPubMedGoogle Scholar
  74. Lautner, A, Klein, R, Ljungberg, U, Reilander, H, Bartling, D, Andersson, B, Reinke, H, Beyreuther, K, Herrmann, RG 1988Nucleotide sequence of cDNA clones encoding the complete precursor for the ‘10-kDa’ polypeptide of Photosystem II from spinachJ Biol Chem2631007710081PubMedGoogle Scholar
  75. Li, XP, Björkman, O, Shih, C, Grossman, AR, Rosenquist, M, Jansson, S, Niyogi, KK 2000A pigment-binding protein essential for regulation of photosynthetic light harvestingNature403391395PubMedGoogle Scholar
  76. Li, XP, Phippard, A, Pasari, J, Niyogi, KK 2002Structure–function analysis of Photosystem II subunit S (PsbS) in vivoFunct Plant Biol1911311139Google Scholar
  77. Li, XP, Gilmore, AM, Caffarri, S, Bassi, R, Golan, T, Kramer, D, Niyogi, K 2004Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS proteinJ Biol Chem2792286622874CrossRefPubMedGoogle Scholar
  78. Lind, LK, Shukla, VK, Nyhus, K, Pakrasi, HB 1993Genetic and immunological analyses of the cyanobacterium Synechocystis sp. PCC 6803 show that the protein encoded by the psbJ gene regulates the number of Photosystem II centers in thylakoid membranes.J Biol Chem26815751579PubMedGoogle Scholar
  79. Lindahl, M, Spetea, C, Hundal, T, Oppenheim, AB, Adam, Z, Andersson, B 2000The thylakoid FtsH protease plays a role in the light-induced turnover of the Photosystem II D1 proteinPlant Cell12419431CrossRefPubMedGoogle Scholar
  80. Liu, Z, Yan, H, Wang, K, Kyang, T, Zhang, J, Gui, L, An, X, Chang, W 2004Crystal structure of spinach major light-harvesting complex at 2.72 Å resolutionNature428287292PubMedGoogle Scholar
  81. Malnöe, P, Mayfield, SP, Rochaix, JD 1988Comparative analysis of the biogenesis of Photosystem II in the wild- type and Y-1 mutant of Chlamydomonas reinhardtiiJ Cell Biol106609616CrossRefPubMedGoogle Scholar
  82. Masuda, T, Tanaka, A, Melis, A 2003Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expressPlant Mol Biol51757771CrossRefPubMedGoogle Scholar
  83. Maul, JE, Lilly, JW, dePamphilis, CW, Cui, L, Miller, W, Harris, EH, Stern, DB 2002The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeatsPlant Cell1426592679CrossRefPubMedGoogle Scholar
  84. Mayes, SR, Barber, J 1991Primary structure of the psbN–psbH–petC–petA gene cluster of the cyanobacterium Synechocystis PCC 6803Plant Mol Biol17289293CrossRefPubMedGoogle Scholar
  85. Mayes, SR, Dubbs, JM, Vass, I, Hideg, E, Nagy, L, Barber, J 1993Further characterization of the psbH locus of Synechocystis sp. PCC 6803: inactivation of psbH impairs QA to QB electron transport in Photosystem 2.Biochemistry3214541465CrossRefPubMedGoogle Scholar
  86. Mayfield, SP, Bennoun, P, Rochaix, JD 1987aExpression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of Photosystem II particles in Chlamydomonas reinhardtiiEMBO J6313318Google Scholar
  87. Mayfield, SP, Rahire, M, Frank, G, Zuber, H, Rochaix, JD 1987bExpression of the nuclear gene encoding oxygen-evolving enhancer protein 2 is required for high levels of photosynthetic oxygen evolution in Chlamydomonas reinhardtiiProc Natl Acad Sci USA84749753Google Scholar
  88. Meetam M, Keren Nir, Ohad I and Pakrasi HB (1999) The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC6803.Google Scholar
  89. Meurer, J, Plücken, H, Kowallik, KV, Westhoff, P 1998A nuclear-encoded protein of prokaryotic origin is essential for the stability of Photosystem II in Arabidopsis thalianaEMBO J1752865297CrossRefPubMedGoogle Scholar
  90. Minagawa, J, Kramer, DM, Kanazawa, A, Crofts, AR 1996Donor-side photoinhibition in Photosystem II from Chlamydomonas reinhardtii upon mutation of tyrosine-Z in the D1 polypeptide to phenylalanineFEBS Lett389199202CrossRefPubMedGoogle Scholar
  91. Minagawa, J, Han, KC, Dohmae, N, Takio, K, Inoue, Y 2001Molecular characterization and gene expression of lhcb5 gene encoding CP26 in the light-harvesting complex II of Chlamydomonas reinhardtiiPlant Mol Biol46277287CrossRefPubMedGoogle Scholar
  92. Miyao, M, Murata, N 1989The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the Photosystem II complex of spinachBiochim Biophys Acta977315321Google Scholar
  93. Monod, C, Takahashi, Y, Goldschmidt-Clermont, M, Rochaix, JD 1994The chloroplast ycf8 opne reading frame encodes a Photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditionsEMBO J1327242754Google Scholar
  94. Morais, F, Barber, J, Nixon, PJ 1998The chloroplast-encoded alpha subunit of cytochrome b-559 is required for assembly of the Photosystem two complex in both the light and the dark in Chlamydomonas reinhardtiiJ Biol Chem2732931529320CrossRefPubMedGoogle Scholar
  95. Müller, B, Eichcker, LA 1999Assembly of the D1 precursor in monomeric Photosystem II reaction center precomplexes precedes chlorophyll a-triggered accumulation of reaction center II in barley etioplastPlant Cell1123652377CrossRefPubMedGoogle Scholar
  96. Mullet, JE, Klein, PG, Klein, RR 1990Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stabilityProc Natl Acad Sci USA8740384042PubMedGoogle Scholar
  97. Murata, N, Miyao, M, Hayashida, N, Hidaka, T, Sugiura, M 1988Identification of a new gene in the chloroplast genome encoding a low-molecular-mass polypeptide of Photosystem II complexFEBS Lett235283288CrossRefGoogle Scholar
  98. Nanba, O, Satoh, K 1987Isolation of a Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559Proc Natl Acad Sci USA84109112Google Scholar
  99. Nield, J, Funk, C, Barber, J 2000aSupermolecular structure of Photosystem II and location of the PsbS proteinPhil Trans R Soc Lond B35513371344CrossRefGoogle Scholar
  100. Nield, J, Kruse, O, Ruprecht, J, Fonseca, P, Buchel, C, Barber, J 2000bThree-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus Photosystem II complexes allows for comparison of their oxygen-evolving complex organizationJ Biol Chem2752794027946Google Scholar
  101. Nilsson, R, Brunner, J, Hoffman, NE, Wijk, KJ 1999Interaction of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54EMBO J18733742CrossRefPubMedGoogle Scholar
  102. Nixon, PJ, Trost, JT, Diner, BA 1992Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in Photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: assembly requires a free carboxyl group at C-terminal position 344.Biochemistry311085910871CrossRefPubMedGoogle Scholar
  103. Niyogi, KK, Björkman, O, Grossman, AR 1997Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenchingPlant Cell913691380CrossRefPubMedGoogle Scholar
  104. Noguchi, T 2002Dual role of triplet localization on the accessory chlorophyll in the Photosystem II reaction center: photoprotection and photodamage of the D1 proteinPlant Cell Physiol4311121116CrossRefPubMedGoogle Scholar
  105. O’Connor, HE, Ruffle, SV, Cain, AJ, Deak, Z, Vass, I, Nugent, JH, Purton, S 1998The 9-kDa phosphoprotein of Photosystem II. Generation and characterisation of Chlamydomonas mutants lacking PSII-H and a site-directed mutant lacking the phosphorylation site.Biochim Biophys Acta13646372PubMedGoogle Scholar
  106. Ohnishi, N, Takahashi, Y 2001PsbT polypeptide is required for efficient repair of photodamaged Photosystem II reaction centerJ Biol Chem2763379833804CrossRefPubMedGoogle Scholar
  107. Ossenbühl, F, Göhre, V, Meure, J, Liszkay-Krieger, A, Rochaix, JD, Eichacker, L 2004Efficient assembly of Photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3Plant Cell1617901800CrossRefPubMedGoogle Scholar
  108. Pakrasi, HB, Williams, JG, Arntzen, CJ 1988Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b559 in Photosystem IIEMBO J7325332PubMedGoogle Scholar
  109. Plücken, H, Müller, B, Grohmann, D, Westhoff, P, Eichacker, L 2002The HCF136 protein is essential for assembly of the Photosystem II reaction center in Arabidopsis thalianaFEBS Lett5328590CrossRefPubMedGoogle Scholar
  110. Rova, EM, McEwen, B, Fredriksson, P-O, Styring, S 1996Photoactivation and photoinhibition are competing in a mutant of Chlamydomonas reinhardtii lacking the 23-kDa extrinsic subunit of Photosystem IIJ Biol Chem2712891828924CrossRefPubMedGoogle Scholar
  111. Ruban, AV, Wentworth, M, Yakushevska, AE, Andersson, J, Lee, PJ, Keegstra, W, Dekker, JP, Boekema, EJ, Jansson, S, Horton, P 2003Plants lacking the main light-harvesting complex retain Photosystem II macro-organizationNature421648652CrossRefPubMedGoogle Scholar
  112. Ruf, S, Biehler, K, Bock, R 2000A small chloroplast-encoded protein as a novel architectural component of the light-harvesting antennaJ Cell Biol149369378CrossRefPubMedGoogle Scholar
  113. Ruffle, SV, Sayre, RT 1998Functional analysis of Photosystem IIRochaix, JDGoldschmidt-Clermont, MMerchant, S eds. The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, pp 287–322Kluwer Academic PublishersDordrecht, The NetherlandsGoogle Scholar
  114. Ruffle, SV, Wang, J, Johnston, HG, Gustafson, TL, Hutchison, RS, Minagawa, J, Crofts, A, Sayre, RT 2001Photosystem II peripheral accessory chlorophyll mutants in Chlamydomonas reinhardtii. Biochemical characterization and sensitivity to photo-inhibition. Plant Physiol127633644CrossRefPubMedGoogle Scholar
  115. Sakamoto, W, Zaltsman, A, Adam, Z, Takahashi, Y 2003Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH met alloproteases involved in the repair cycle of Photosystem II in Arabidopsis thylakoid membranesPlant Cell1528432855CrossRefPubMedGoogle Scholar
  116. Savard, F, Richard, C, Guertin, M 1996The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illuminationPlant Mol Biol32461473CrossRefPubMedGoogle Scholar
  117. Silva, P, Thompson, E, Bailey, S, Kruse, O, Mullineaux, C, Robinson, C, Mann, NH, Nixon, PJ 2003FtsH is involved in the early stages of repair of Photosystem II in Synechocystis sp. PCC 6803.Plant Cell1521522164CrossRefPubMedGoogle Scholar
  118. Schrager, J, Chang, C-W, Davies, J, McDermott, J, Harris, E, Hauser, C, Tamse, R, Surzycki, R, Gurjal, M, Zhang, Z 2001Chlamydomonas cDNAs: assembly and potential role in understanding metabolic processes Commonwealth Scientific and industrial Research Organization PublishingCollingwood, AustraliaArticle no. S41-001. In: Proceedings of the 12th International Congress on Photosynthesis.Google Scholar
  119. Schroda, M, Vallon, O, Wollman, FA, Beck, CF 1999A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of Photosystem II during and after photoinhibitionPlant Cell1111651178CrossRefPubMedGoogle Scholar
  120. Shi, LX, Lorkovic, ZJ, Öelmuller, R, Schröder, WP 2000The low molecular mass PsbW protein is involved in the stabilization of the dimeric Photosystem II complex in Arabidopsis thalianaJ Biol Chem2753794537950CrossRefPubMedGoogle Scholar
  121. Snyder, S, Kohorn, BD 1999TAKs, thylakoid membrane protein kinases associated with energy transductionJ Biol Chem27491379140CrossRefPubMedGoogle Scholar
  122. Snyder, S, Kohorn, BD 2001Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in ArabidopsisJ Biol Chem2763216932176CrossRefPubMedGoogle Scholar
  123. Stauber, EJ, Fink, A, Markert, C, Kruse, O, Johanningmeier, U, Hippler, M 2003Proteomics of Chlamydomonas reinhardtii light-harvesting proteinsEukaryot Cell2978994CrossRefPubMedGoogle Scholar
  124. Stockhaus, J, Höfer, M, Renger, G, Westhoff, P, Wydrzynski, T, Willmitzer, L 1990Anti-sense RNA efficiently inhibits formation of the 10 kD polypeptide of Photosystem II in transgenic potato plants: analysis of the role of the 10 kD proteinEMBO J930133021PubMedGoogle Scholar
  125. Sugimoto, I, Takahashi, Y 2003Evidence that the PsbK polypeptide is associated with the Photosystem II core antenna complex CP43J Biol Chem2784500445010CrossRefPubMedGoogle Scholar
  126. Sugiura, M, Inoue, Y, Minagawa, J 1998Rapid and discrete isolation of oxygen-evolving His-tagged Photosystem II core complex from Chlamydomonas reinhardtii by Ni2+ affinity column chromatographyFEBS Lett426140144CrossRefPubMedGoogle Scholar
  127. Suzuki, T, Minagawa, J, Tomo, T, Sonoike, K, Ohta, H, Enami, I 2003Binding and functional properties of the extrinsic proteins in oxygen-evolving Photosystem II particle from a green alga, Chlamydomonas reinhardtii having His-tagged CP47Plant Cell Physiol447684PubMedGoogle Scholar
  128. Summer, EJ, Schmid, VH, Bruns, BU, Schmidt, GW 1997Requirement for the H phosphoprotein in Photosystem II of Chlamydomonas reinhardtiiPlant Physiol11313591368CrossRefPubMedGoogle Scholar
  129. Suorsa, M, Regel, RE, Paakkarinen, V, Battchikova, N, Hermann, RG, Aro, EM 2004Protein assembly of Photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJEur J Biochem27196107CrossRefPubMedGoogle Scholar
  130. Swiatek, M, Kuras, R, Sokolenko, A, Higgs, D, Olive, J, Cinque, G, Muller, B, Eichacker, LA, Stern, DB, Bassi, R, Herrmann, RG, Wollman, FA 2001The chloroplast gene ycf9 encodes a Photosystem II (PS II) core subunit, PsbZ, that participates in PS II supramolecular architecturePlant Cell1313471367CrossRefPubMedGoogle Scholar
  131. Takahashi, Y, Matsumoto, H, Goldschmidt-Clermont, M, Rochaix, JD 1994Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the Photosystem II reaction center complexPlant Mol Biol24779788CrossRefPubMedGoogle Scholar
  132. Teramoto, H, Ono, T, Minagawa, J 2001Identification of Lhcb gene family encoding the light-harvesting chlorophyll- a/b proteins of Photosystem II in Chlamydomonas reinhardtiiPlant Cell Physiol42849856CrossRefPubMedGoogle Scholar
  133. Teramoto, H, Nakamori, A, Minagawa, J, Ono, T 2002Light-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll- a/b proteins of Photosystem II in Chlamydomonas reinhardtiiPlant Physiol130325333CrossRefPubMedGoogle Scholar
  134. Terzaghi, WB, Cashmore, AR 1995Light-regulated transcriptionAnnu Rev Plant Physiol Plant Mol Biol46445474CrossRefGoogle Scholar
  135. Thidholm, E, Lindstrom, V, Tissier, C, Robinson, C, Schröder, WP, Funk, C 2002Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the Photosystem II dimerFEBS Lett513217222CrossRefPubMedGoogle Scholar
  136. Thompson, JD, Higgins, DG, Gibson, TJ 1994CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choiceNucleic Acids Res2246734680PubMedGoogle Scholar
  137. Thompson, S, Robinson, C, Mant, A 1999Dualsignal peptides mediate the signal recognition particle/Sec-independent insertion of a thylakoid membrane polyprotein, PsbYJ Biol Chem27440594066CrossRefPubMedGoogle Scholar
  138. Tokutsu, R, Teramoto, H, Takahashi, Y, Ono, T, Minagawa, J 2003The light-harvesting complex of Photosystem I in Chlamydomonas reinhardtii: protein composition, gene structures and phylogenic implicationsPlant Cell Physiol45138145CrossRefGoogle Scholar
  139. Wijk, KJ, Nilsson, LO, Styring, S 1994Synthesis of reaction center proteins and reactivation of redox components during repair of Photosystem II after light-induced inactivationJ Biol Chem2692838228392PubMedGoogle Scholar
  140. Vasil’ev, S, Orth, P, Zouni, A, Owens, TG, Bruce, D 2001Excited-state dynamics in Photosystem II: insights from the X-ray crystal structureProc Natl Acad Sci USA9886028607PubMedGoogle Scholar
  141. Vener, AV, Kan, PJM, Rich, PR, Ohad, I, Andersson, B 1997Plastoquinol at the quinol oxidation site of reduced Cyt by mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flashProc Natl Acad Sci USA9415851590PubMedGoogle Scholar
  142. Vermaas, WFJ, Rutherford, AW, Hansson, Ö 1988Site-directed mutagenesis in Photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: donor D is a tyrosine residue in the D2 protein.Proc Natl Acad Sci USA8584778481Google Scholar
  143. Wang, J, Gosztola, D, Ruffle, SV, Hemann, C, Seibert, M, Wasielewski, MR, Hille, R, Gustafson, TL, Sayre, RT 2002Functional asymmetry of Photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtiiProc Natl Acad Sci USA9940914096CrossRefPubMedGoogle Scholar
  144. Woolhead, CA, Thompson, SJ, Moore, M, Tissier, C, Mant, A, Rodger, A, Henry, R, Robinson, C 2001Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertionJ Biol Chem2764084140846CrossRefPubMedGoogle Scholar
  145. Wollman, FA, Delepelaire, P 1984Correlation between changes in light energy distribution and changes in thylakoid membrane polypeptide phosphorylation in C. reinhardtii.J Cell Biol9817CrossRefPubMedGoogle Scholar
  146. Xiong, L, Sayre, RT 2004Engineering the chloroplast encoded proteins of ChlamydomonasPhotosynth Res80411419CrossRefGoogle Scholar
  147. Yakushevska, AE, Keegstra, W, Boekema, EJ, Dekker, JP, Andersson, J, Jansson, S, Ruban, AV, Horton, P 2003The structure of Photosystem II in Arabidopsis : localization of the CP26 and CP29 antenna complexesBiochemistry42608613CrossRefPubMedGoogle Scholar
  148. Zerges, W, Rochaix, JD 1998Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtiiJ Cell Biol140101110CrossRefPubMedGoogle Scholar
  149. Zhang, L, Paakkarinen, , Wijk, KJ, Aro, EM 1999Co-translational assembly of the D1 protein into Photosystem IIJ Biol Chem2741606216067CrossRefPubMedGoogle Scholar
  150. Zhang, L, Paakkarinen, , Wijk, KJ, Aro, EM 2000Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into Photosystem IIPlant Cell1217691781PubMedGoogle Scholar
  151. Zhang, L, Paakkarinen, V, Suorsa, M, Aro, EM 2001A SecY homologue is involved in chloroplast-encoded D1 protein biogenesisJ Biol Chem2763780937814PubMedGoogle Scholar
  152. Zouni, A, Witt, HT, Kern, J, Fromme, P, Krauss, N, Saenger, W, Orth, P 2001Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolutionNature409739743PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  1. 1.Institute of Low Temperature ScienceHokkaido UniversitySapporoJapan
  2. 2.Department of Biology, Faculty of ScienceOkayama UniversityOkayamaJapan

Personalised recommendations