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Role of Chloroplast Thylakoid Lumen in Photosynthetic Regulation and Plant Cell Signaling

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Part of the book series: Progress in Botany ((BOTANY,volume 73))

Abstract

The aqueous lumen enclosed by the thylakoid membrane network of the chloroplast is the compartment where molecular oxygen is produced from water during photosynthetic light-dependent reactions. The thylakoid lumen has been thought for a long time to contain mainly plastocyanin and oxygen-evolving complex-associated proteins, playing important roles during these reactions. In the last decade, the functional characterization of thylakoid lumenal proteins from Arabidopsis thaliana has brought insights into the complex role of this subcellular compartment. The aim of this chapter is to provide an updated view of the protein composition of the thylakoid lumen and its emerging roles in photosynthetic regulation and plant cell signaling. Recent research has uncovered redox signaling and a new paradigm about the role of nucleotides in the thylakoid lumen.

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References

  • Abdel-Ghany SE (2009) Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229:767–779

    PubMed  CAS  Google Scholar 

  • Allahverdiyeva Y, Mamedov F, Holmström M, Nurmi M, Lundin B, Styring S, Spetea C, Aro EM (2009) Comparison of the electron transport properties of the psbo1 and psbo2 mutants of Arabidopsis thaliana. Biochim Biophys Acta 1787:1230–1237

    PubMed  CAS  Google Scholar 

  • Anbudurai PR, Mor TS, Ohad I, Shestakov SV, Pakrasi HB (1994) The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center complex. Proc Natl Acad Sci USA 91:8082–8086

    PubMed  CAS  Google Scholar 

  • Anderson JM, Chow WS, De Las RJ (2008) Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma. Photosynth Res 98:575–587

    PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Google Scholar 

  • Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21:2036–2044

    PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    PubMed  CAS  Google Scholar 

  • Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    PubMed  CAS  Google Scholar 

  • Baginsky S, Gruissem W (2009) The chloroplast kinase network: new insights from large-scale phosphoproteome profiling. Mol Plant 2:1141–1153

    PubMed  CAS  Google Scholar 

  • Baroli I, Niyogi KK (2000) Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos Trans R Soc Lond B Biol Sci 355:1385–1394

    PubMed  CAS  Google Scholar 

  • Bauer J, Hiltbrunner A, Kessler F (2001) Molecular biology of chloroplast biogenesis: gene expression, protein import and intraorganellar sorting. Cell Mol Life Sci 58:420–433

    PubMed  CAS  Google Scholar 

  • Buchanan BB, Luan S (2005) Redox regulation in the chloroplast thylakoid lumen: a new frontier in photosynthesis research. J Exp Bot 56:1439–1447

    PubMed  CAS  Google Scholar 

  • Chen H, Zhang D, Guo J, Wu H, Jin M, Lu Q, Lu C, Zhang L (2006) A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Mol Biol 61:567–575

    PubMed  CAS  Google Scholar 

  • Clark GB, Thompson G Jr, Roux SJ (2001) Signal transduction mechanisms in plants: an overview. Curr Sci 80:170–177

    PubMed  CAS  Google Scholar 

  • Cormann KU, Bangert JA, Ikeuchi M, Rögner M, Stoll R, Nowaczyk MM (2009) Structure of Psb27 in solution: implications for transient binding to photosystem II during biogenesis and repair. Biochemistry 48:8768–8770

    PubMed  CAS  Google Scholar 

  • Daum B, Nicastro D, Austin J 2nd, McIntosh JR, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22:1299–1312

    PubMed  CAS  Google Scholar 

  • Dietz KJ (2007) The dual function of plant peroxiredoxins in antioxidant defence and redox signaling. Subcell Biochem 44:267–294

    PubMed  Google Scholar 

  • Dilley RA (2004) On why thylakoids energize ATP formation using either delocalized or localized proton gradients – a Ca(2+) mediated role in thylakoid stress responses. Photosynth Res 80:245–263

    PubMed  CAS  Google Scholar 

  • Edvardsson A, Shapiguzov A, Petersson UA, Schröder WP, Vener AV (2007) Immunophilin AtFKBP13 sustains all peptidyl-prolyl isomerase activity in the thylakoid lumen from Arabidopsis thaliana deficient in AtCYP20-2. Biochemistry 46:9432–9442

    PubMed  CAS  Google Scholar 

  • Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1386

    PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    PubMed  CAS  Google Scholar 

  • Fu A, He Z, Cho HS, Lima A, Buchanan BB, Luan S (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:15947–15952

    PubMed  CAS  Google Scholar 

  • Fulgosi H, Vener AV, Altschmied L, Herrmann RG, Andersson B (1998) A novel multi-functional chloroplast protein: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO J 17:1577–1587

    PubMed  CAS  Google Scholar 

  • Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Héroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101:13945–51390

    PubMed  CAS  Google Scholar 

  • Gopalan G, He Z, Battaile KP, Luan S, Swaminathan K (2006) Structural comparison of oxidized and reduced FKBP13 from Arabidopsis thaliana. Proteins 65:789–795

    PubMed  CAS  Google Scholar 

  • Granlund I, Hall M, Kieselbach T, Schröder WP (2009a) Light induced changes in protein expression and uniform regulation of transcription in the thylakoid lumen of Arabidopsis thaliana. PLoS One 4:e5649

    PubMed  Google Scholar 

  • Granlund I, Storm P, Schubert M, García-Cerdán JG, Funk C, Schröder WP (2009b) The TL29 protein is lumen located, associated with PSII and not an ascorbate peroxidase. Plant Cell Physiol 50:1898–1910

    PubMed  CAS  Google Scholar 

  • Gupta R, He Z, Luan S (2002) Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis. Nature 417:567–571

    PubMed  CAS  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    PubMed  CAS  Google Scholar 

  • Hall M, Mata-Cabana A, Akerlund HE, Florencio FJ, Schröder WP, Lindahl M, Kieselbach T (2010) Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function. Proteomics 10:987–1001

    PubMed  CAS  Google Scholar 

  • Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167:176–183

    PubMed  CAS  Google Scholar 

  • Hancock JT (2009) The role of redox in signal transduction. Methods Mol Biol 476:1–9

    PubMed  Google Scholar 

  • Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256

    PubMed  CAS  Google Scholar 

  • Ido K, Ifuku K, Yamamoto Y, Ishihara S, Murakami A, Takabe K, Miyake C, Sato F (2009) Knockdown of the PsbP protein does not prevent assembly of the dimeric PSII core complex but impairs accumulation of photosystem II supercomplexes in tobacco. Biochim Biophys Acta 1787:873–881

    PubMed  CAS  Google Scholar 

  • Ifuku K, Nakatsu T, Kato H, Sato F (2004) Crystal structure of the PsbP protein of photosysem II from Nicotiana tabacum. EMBO Rep 5:362–367

    PubMed  CAS  Google Scholar 

  • Ifuku K, Yamamoto Y, Ono TA, Ishihara S, Sato F (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol 139:1175–1184

    PubMed  CAS  Google Scholar 

  • Ifuku K, Ishihara S, Sato F (2010) Molecular functions of oxygen-evolving complex family proteins in photosynthetic electron flow. J Integr Plant Biol 52:723–734

    PubMed  CAS  Google Scholar 

  • Ingelsson B, Shapiguzov A, Kieselbach T, Vener AV (2009) Peptidyl-prolyl isomerase activity in chloroplast thylakoid lumen is a dispensable function of immunophilins in Arabidopsis thaliana. Plant Cell Physiol 50:1801–1814

    PubMed  CAS  Google Scholar 

  • Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K, Sato F (2007) Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol 145:668–679

    PubMed  CAS  Google Scholar 

  • Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci USA 100:98–103

    PubMed  CAS  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    PubMed  CAS  Google Scholar 

  • Kieselbach T, Hagman Å, Andersson B, Schröder WP (1998) The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273:6710–6716

    PubMed  CAS  Google Scholar 

  • Knorpp C, Johansson M, Baird AM (2003) Plant mitochondrial nucleoside diphosphate kinase is attached to the membrane through interaction with the adenine nucleotide translocator. FEBS Lett 555:363–366

    PubMed  CAS  Google Scholar 

  • Komenda J, Nickelsen J, Tichý M, Prásil O, Eichacker LA, Nixon PJ (2008) The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 283:22390–22399

    PubMed  CAS  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    PubMed  CAS  Google Scholar 

  • Li C, Xiang Z, Ling Q, Shang K (1998) Effects of calmodulin and calmodulin binding protein BP-10 on phosphorylation of thylakoid membrane protein. Sci China C Life Sci 41:64–70

    PubMed  CAS  Google Scholar 

  • Li LH, Ma PF, Yang YJ, Zhao HJ (2010) Effects of exogenous Ca(2+) on D1 protein phosphorylation and PS II performances of wheat leaf chloroplasts under high temperature and illumination stress. Ying Yong Sheng Tai Xue Bao 21:683–688

    PubMed  CAS  Google Scholar 

  • Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci USA 103:12631–12636

    PubMed  CAS  Google Scholar 

  • Liu H, Frankel LK, Bricker TM (2008) Functional complementation of the Arabidopsis thaliana psbo1 mutant phenotype with an N-terminally His6-tagged PsbO-1 protein in photosystem II. Biochim Biophys Acta 787:1029–1038

    Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040–1044

    PubMed  CAS  Google Scholar 

  • Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, Andersson B, Spetea C (2007a) Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Biochim Biophys Acta 1767:500–508

    PubMed  CAS  Google Scholar 

  • Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C (2007b) The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 49:528–539

    PubMed  CAS  Google Scholar 

  • Lundin B, Nurmi M, Rojas-Stuetz M, Aro EM, Adamska I, Spetea C (2008) Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana – insights from phenotypic analyses of PsbO knockout mutants. Photosynth Res 98:405–414

    PubMed  CAS  Google Scholar 

  • Mabbitt PD, Rautureau GJ, Day CL, Wilbanks SM, Eaton-Rye JJ, Hinds MG (2009) Solution structure of Psb27 from cyanobacterial photosystem II. Biochemistry 48:8771–8773

    PubMed  CAS  Google Scholar 

  • Mamedov F, Nowaczyk MM, Thapper A, Rögner M, Styring S (2007) Functional characterization of monomeric photosystem II core preparations from Thermosynechococcus elongatus with or without the Psb27 protein. Biochemistry 46:5542–5551

    PubMed  CAS  Google Scholar 

  • Mattoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 156:241–246

    Google Scholar 

  • Merchant S, Sawaya MR (2005) The light reactions: a guide to recent acquisitions for the picture gallery. Plant Cell 217:648–663

    Google Scholar 

  • Meurer J, Plücken H, Kowallik KV, Westhoff P (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J 17:5286–5297

    PubMed  CAS  Google Scholar 

  • Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281:35039–35047

    PubMed  CAS  Google Scholar 

  • Mulo P, Sirpiö S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98:489–501

    PubMed  CAS  Google Scholar 

  • Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2002) Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett 523:138–142

    PubMed  CAS  Google Scholar 

  • Mustárdy L, Buttle K, Steinbach G, Garab G (2008) The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant Cell 20:2552–2557

    PubMed  Google Scholar 

  • Muthuramalingam M, Seidel T, Laxa M, Nunes de Miranda SM, Gärtner F, Ströher E, Kandlbinder A, Dietz KJ (2009) Multiple redox and non-redox interactions define 2-cys peroxiredoxin as a regulatory hub in the chloroplast. Mol Plant 2:1273–1288

    PubMed  CAS  Google Scholar 

  • Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982

    PubMed  CAS  Google Scholar 

  • Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565

    PubMed  CAS  Google Scholar 

  • Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    PubMed  CAS  Google Scholar 

  • Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rögner M (2006) Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18:3121–3131

    PubMed  CAS  Google Scholar 

  • Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481–485

    PubMed  CAS  Google Scholar 

  • Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepstorff P, von Heijne G, van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14:211–236

    PubMed  CAS  Google Scholar 

  • Pesaresi P, Scharfenberg M, Weigel M, Granlund I, Schröder WP, Finazzi G, Rappaport F, Masiero S, Furini A, Jahns P, Leister D (2009) Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state. Mol Plant 2:236–248

    PubMed  CAS  Google Scholar 

  • Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807(8):887–896

    PubMed  CAS  Google Scholar 

  • Petersson UA, Kieselbach T, García-Cerdán JG, Schröder WP (2006) The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. FEBS Lett 580:6055–6061

    PubMed  CAS  Google Scholar 

  • Plücken H, Müller B, Grohmann D, Westhoff P, Eichacker LA (2002) The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett 532:85–90

    PubMed  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44

    CAS  Google Scholar 

  • Pulido P, Spínola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, González M, Cejudo FJ (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J Exp Bot 61:4043–4054

    PubMed  CAS  Google Scholar 

  • Rinalducci S, Larsen MR, Mohammed S, Zolla L (2006) Novel protein phosphorylation site identification in spinach stroma membranes by titanium dioxide microcolumns and tandem mass spectrometry. J Proteome Res 5:973–982

    PubMed  CAS  Google Scholar 

  • Rokka A, Aro EM, Herrmann RG, Andersson B, Vener AV (2000) Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiol 123:1525–1536

    PubMed  CAS  Google Scholar 

  • Romano PG, Horton P, Gray JE (2004) The Arabidopsis cyclophilin gene family. Plant Physiol 134:1268–1282

    PubMed  CAS  Google Scholar 

  • Roose JL, Pakrasi HB (2004) Evidence that D1 processing is required for manganese binding and extrinsic protein assembly into photosystem II. J Biol Chem 279:45417–45422

    PubMed  CAS  Google Scholar 

  • Roose JL, Pakrasi HB (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283:4044–4050

    PubMed  CAS  Google Scholar 

  • Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387

    PubMed  CAS  Google Scholar 

  • Ruiz Pavón L, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem 283:13520–13527

    Google Scholar 

  • Saga G, Giorgetti A, Fufezan C, Giacometti GM, Bassi R, Morosinotto T (2010) Mutation analysis of violaxanthin de-epoxidase identifies substrate-binding sites and residues involved in catalysis. J Biol Chem 285:23763–23770

    PubMed  CAS  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    PubMed  CAS  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60

    PubMed  Google Scholar 

  • Shapiguzov A, Edvardsson A, Vener AV (2006) Profound redox sensitivity of peptidyl-prolyl isomerase activity in Arabidopsis thylakoid lumen. FEBS Lett 580:3671–3676

    PubMed  CAS  Google Scholar 

  • Shen Y, Kim JI, Song PS (2005) NDPK2 as a signal transducer in the phytochrome-mediated light signaling. J Biol Chem 280:5740–5749

    PubMed  CAS  Google Scholar 

  • Shen Y, Han YJ, Kim JI, Song PS (2008) Arabidopsis nucleoside diphosphate kinase-2 as a plant GTPase activating protein. BMB Rep 41:645–650

    PubMed  CAS  Google Scholar 

  • Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17:2580–2586

    PubMed  CAS  Google Scholar 

  • Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing protein-effect of pH, calcium, and manganese. Biochemistry 44:15182–15192

    PubMed  CAS  Google Scholar 

  • Sirpiö S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM (2007) TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle. Biochem J 406:415–425

    PubMed  Google Scholar 

  • Sirpiö S, Khrouchtchova A, Allahverdiyeva Y, Hansson M, Fristedt R, Vener AV, Scheller HV, Jensen PE, Haldrup A, Aro EM (2008) AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II. Plant J 55:639–651

    PubMed  Google Scholar 

  • Sirpiö S, Holmström M, Battchikova N, Aro EM (2009) AtCYP20-2 is an auxiliary protein of the chloroplast NAD(P)H dehydrogenase complex. FEBS Lett 583:2355–2358

    PubMed  Google Scholar 

  • Spetea C, Schoefs B (2010) Solute transporters in plant thylakoid membranes: key players during photosynthesis and light stress. Commun Integr Biol 3:122–129

    PubMed  Google Scholar 

  • Spetea C, Hundal T, Lohmann F, Andersson B (1999) GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the photosystem II D1 protein. Proc Natl Acad Sci USA 96:6547–6552

    PubMed  CAS  Google Scholar 

  • Spetea C, Keren N, Hundal T, Doan JM, Ohad I, Andersson B (2000) GTP enhances the degradation of the photosystem II D1 protein irrespective of its conformational heterogeneity at the Q(B) site. J Biol Chem 275:7205–7211

    PubMed  CAS  Google Scholar 

  • Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B (2004) Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101:1409–1414

    PubMed  CAS  Google Scholar 

  • Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19:1347–1361

    PubMed  CAS  Google Scholar 

  • Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010) The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J 62:240–249

    PubMed  CAS  Google Scholar 

  • Suorsa M, Aro EM (2007) Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res 93:89–100

    PubMed  CAS  Google Scholar 

  • Suorsa M, Sirpiö S, Paakkarinen V, Kumari N, Holmström M, Aro EM (2010) Two proteins homologous to PsbQ are novel subunits of the chloroplast NAD(P)H dehydrogenase. Plant Cell Physiol 51:877–883

    PubMed  CAS  Google Scholar 

  • Sweetlove LJ, Mowday B, Hebestreit HF, Leaver CJ, Millar AH (2001) Nucleoside diphosphate kinase III is localized to the inter-membrane space in plant mitochondria. FEBS Lett 508:272–276

    PubMed  CAS  Google Scholar 

  • TAIR: The Arabidopsis information resource. http://www.tair.org. Accessed 30 Sept 2010

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    PubMed  CAS  Google Scholar 

  • Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16:2164–2175

    PubMed  CAS  Google Scholar 

  • Thuswaldner S, Lagerstedt JO, Rojas-Stütz M, Bouhidel K, Der C, Leborgne-Castel N, Mishra A, Marty F, Schoefs B, Adamska I, Persson BL, Spetea C (2007) Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J Biol Chem 282:8848–8859

    PubMed  CAS  Google Scholar 

  • Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275:1767–1777

    PubMed  CAS  Google Scholar 

  • Vener AV, Rokka A, Fulgosi H, Andersson B, Herrmann RG (1999) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38:14955–14965

    PubMed  CAS  Google Scholar 

  • Wagner V, Gessner G, Heiland I, Kaminski M, Hawat S, Scheffler K, Mittag M (2006) Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot Cell 5:457–468

    PubMed  CAS  Google Scholar 

  • Wei L, Guo J, Ouyang M, Sun X, Ma J, Chi W, Lu C, Zhang L (2010) LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J Biol Chem 285:21391–21398

    PubMed  CAS  Google Scholar 

  • Weinl S, Held K, Schlücking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686

    PubMed  CAS  Google Scholar 

  • Yabuta S, Ifuku K, Takabayashi A, Ishihara S, Ido K, Ishikawa N, Endo T, Sato F (2010) Three PsbQ-like proteins are required for the function of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell Physiol 51:866–876

    PubMed  CAS  Google Scholar 

  • Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 280:16170–16174

    PubMed  CAS  Google Scholar 

  • Yi X, Hargett SR, Frankel LK, Bricker TM (2006) The PsbQ protein is required in Arabidopsis for photosystem II assembly/stability and photoautotrophy under low light conditions. J Biol Chem 281:26260–26267

    PubMed  CAS  Google Scholar 

  • Yi X, Hargett SR, Frankel LK, Bricker TM (2009) The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Lett 583:2142–2147

    PubMed  CAS  Google Scholar 

  • Yin L, Lundin B, Bertrand M, Nurmi M, Solymosi K, Kangasjärvi S, Aro EM, Schoefs B, Spetea C (2010) Role of thylakoid ATP/ADP carrier in photoinhibition and photoprotection of photosystem II in Arabidopsis. Plant Physiol 153:666–677

    PubMed  CAS  Google Scholar 

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Correspondence to Cornelia Spetea .

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Spetea, C. (2012). Role of Chloroplast Thylakoid Lumen in Photosynthetic Regulation and Plant Cell Signaling. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 73. Progress in Botany, vol 73. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22746-2_8

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