Advertisement

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

  • Cornelia SpeteaEmail author
Chapter
Part of the Progress in Botany book series (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.

Keywords

Thylakoid Membrane PSII Activity PSII Complex Thylakoid Lumen Photosynthetic Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abdel-Ghany SE (2009) Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229:767–779PubMedGoogle Scholar
  2. 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 1787:1230–1237PubMedGoogle Scholar
  3. 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 91:8082–8086PubMedGoogle Scholar
  4. 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 98:575–587PubMedGoogle Scholar
  5. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  6. 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 21:2036–2044PubMedGoogle Scholar
  7. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedGoogle Scholar
  8. 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 56:347–356PubMedGoogle Scholar
  9. Baginsky S, Gruissem W (2009) The chloroplast kinase network: new insights from large-scale phosphoproteome profiling. Mol Plant 2:1141–1153PubMedGoogle Scholar
  10. Baroli I, Niyogi KK (2000) Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos Trans R Soc Lond B Biol Sci 355:1385–1394PubMedGoogle Scholar
  11. Bauer J, Hiltbrunner A, Kessler F (2001) Molecular biology of chloroplast biogenesis: gene expression, protein import and intraorganellar sorting. Cell Mol Life Sci 58:420–433PubMedGoogle Scholar
  12. Buchanan BB, Luan S (2005) Redox regulation in the chloroplast thylakoid lumen: a new frontier in photosynthesis research. J Exp Bot 56:1439–1447PubMedGoogle Scholar
  13. 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 61:567–575PubMedGoogle Scholar
  14. Clark GB, Thompson G Jr, Roux SJ (2001) Signal transduction mechanisms in plants: an overview. Curr Sci 80:170–177PubMedGoogle Scholar
  15. 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 48:8768–8770PubMedGoogle Scholar
  16. 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 22:1299–1312PubMedGoogle Scholar
  17. Dietz KJ (2007) The dual function of plant peroxiredoxins in antioxidant defence and redox signaling. Subcell Biochem 44:267–294PubMedGoogle Scholar
  18. 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 80:245–263PubMedGoogle Scholar
  19. 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 46:9432–9442PubMedGoogle Scholar
  20. Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1386PubMedGoogle Scholar
  21. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedGoogle Scholar
  22. 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 104:15947–15952PubMedGoogle Scholar
  23. 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 17:1577–1587PubMedGoogle Scholar
  24. 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 101:13945–51390PubMedGoogle Scholar
  25. Gopalan G, He Z, Battaile KP, Luan S, Swaminathan K (2006) Structural comparison of oxidized and reduced FKBP13 from Arabidopsis thaliana. Proteins 65:789–795PubMedGoogle Scholar
  26. 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:e5649PubMedGoogle Scholar
  27. 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 50:1898–1910PubMedGoogle Scholar
  28. Gupta R, He Z, Luan S (2002) Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis. Nature 417:567–571PubMedGoogle Scholar
  29. 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 16:334–342PubMedGoogle Scholar
  30. 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 10:987–1001PubMedGoogle Scholar
  31. 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 167:176–183PubMedGoogle Scholar
  32. Hancock JT (2009) The role of redox in signal transduction. Methods Mol Biol 476:1–9PubMedGoogle Scholar
  33. 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 16:241–256PubMedGoogle Scholar
  34. 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 1787:873–881PubMedGoogle Scholar
  35. Ifuku K, Nakatsu T, Kato H, Sato F (2004) Crystal structure of the PsbP protein of photosysem II from Nicotiana tabacum. EMBO Rep 5:362–367PubMedGoogle Scholar
  36. 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 139:1175–1184PubMedGoogle Scholar
  37. Ifuku K, Ishihara S, Sato F (2010) Molecular functions of oxygen-evolving complex family proteins in photosynthetic electron flow. J Integr Plant Biol 52:723–734PubMedGoogle Scholar
  38. 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 50:1801–1814PubMedGoogle Scholar
  39. 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 145:668–679PubMedGoogle Scholar
  40. 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 100:98–103PubMedGoogle Scholar
  41. 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 19:1039–1047PubMedGoogle Scholar
  42. Kieselbach T, Hagman Å, Andersson B, Schröder WP (1998) The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273:6710–6716PubMedGoogle Scholar
  43. 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 555:363–366PubMedGoogle Scholar
  44. 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 283:22390–22399PubMedGoogle Scholar
  45. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563PubMedGoogle Scholar
  46. 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 41:64–70PubMedGoogle Scholar
  47. 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 21:683–688PubMedGoogle Scholar
  48. 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 103:12631–12636PubMedGoogle Scholar
  49. 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 787:1029–1038Google Scholar
  50. 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 438:1040–1044PubMedGoogle Scholar
  51. 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 1767:500–508PubMedGoogle Scholar
  52. 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 49:528–539PubMedGoogle Scholar
  53. 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 98:405–414PubMedGoogle Scholar
  54. Mabbitt PD, Rautureau GJ, Day CL, Wilbanks SM, Eaton-Rye JJ, Hinds MG (2009) Solution structure of Psb27 from cyanobacterial photosystem II. Biochemistry 48:8771–8773PubMedGoogle Scholar
  55. 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 46:5542–5551PubMedGoogle Scholar
  56. Mattoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 156:241–246Google Scholar
  57. Merchant S, Sawaya MR (2005) The light reactions: a guide to recent acquisitions for the picture gallery. Plant Cell 217:648–663Google Scholar
  58. 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 17:5286–5297PubMedGoogle Scholar
  59. 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 281:35039–35047PubMedGoogle Scholar
  60. Mulo P, Sirpiö S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98:489–501PubMedGoogle Scholar
  61. 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 523:138–142PubMedGoogle Scholar
  62. 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 20:2552–2557PubMedGoogle Scholar
  63. 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 2:1273–1288PubMedGoogle Scholar
  64. Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982PubMedGoogle Scholar
  65. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565PubMedGoogle Scholar
  66. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16PubMedGoogle Scholar
  67. 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 18:3121–3131PubMedGoogle Scholar
  68. 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 99:481–485PubMedGoogle Scholar
  69. 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 14:211–236PubMedGoogle Scholar
  70. 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 2:236–248PubMedGoogle Scholar
  71. 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):887–896PubMedGoogle Scholar
  72. 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 580:6055–6061PubMedGoogle Scholar
  73. 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 532:85–90PubMedGoogle Scholar
  74. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44Google Scholar
  75. 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 61:4043–4054PubMedGoogle Scholar
  76. 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 5:973–982PubMedGoogle Scholar
  77. 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 123:1525–1536PubMedGoogle Scholar
  78. Romano PG, Horton P, Gray JE (2004) The Arabidopsis cyclophilin gene family. Plant Physiol 134:1268–1282PubMedGoogle Scholar
  79. Roose JL, Pakrasi HB (2004) Evidence that D1 processing is required for manganese binding and extrinsic protein assembly into photosystem II. J Biol Chem 279:45417–45422PubMedGoogle Scholar
  80. Roose JL, Pakrasi HB (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283:4044–4050PubMedGoogle Scholar
  81. Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387PubMedGoogle Scholar
  82. 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 283:13520–13527Google Scholar
  83. 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 285:23763–23770PubMedGoogle Scholar
  84. 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 277:8354–8365PubMedGoogle Scholar
  85. Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60PubMedGoogle Scholar
  86. Shapiguzov A, Edvardsson A, Vener AV (2006) Profound redox sensitivity of peptidyl-prolyl isomerase activity in Arabidopsis thylakoid lumen. FEBS Lett 580:3671–3676PubMedGoogle Scholar
  87. Shen Y, Kim JI, Song PS (2005) NDPK2 as a signal transducer in the phytochrome-mediated light signaling. J Biol Chem 280:5740–5749PubMedGoogle Scholar
  88. Shen Y, Han YJ, Kim JI, Song PS (2008) Arabidopsis nucleoside diphosphate kinase-2 as a plant GTPase activating protein. BMB Rep 41:645–650PubMedGoogle Scholar
  89. 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 17:2580–2586PubMedGoogle Scholar
  90. 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 44:15182–15192PubMedGoogle Scholar
  91. 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 406:415–425PubMedGoogle Scholar
  92. 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 55:639–651PubMedGoogle Scholar
  93. 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 583:2355–2358PubMedGoogle Scholar
  94. Spetea C, Schoefs B (2010) Solute transporters in plant thylakoid membranes: key players during photosynthesis and light stress. Commun Integr Biol 3:122–129PubMedGoogle Scholar
  95. 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 96:6547–6552PubMedGoogle Scholar
  96. 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 275:7205–7211PubMedGoogle Scholar
  97. 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 101:1409–1414PubMedGoogle Scholar
  98. 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 19:1347–1361PubMedGoogle Scholar
  99. 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 62:240–249PubMedGoogle Scholar
  100. Suorsa M, Aro EM (2007) Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res 93:89–100PubMedGoogle Scholar
  101. 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 51:877–883PubMedGoogle Scholar
  102. 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 508:272–276PubMedGoogle Scholar
  103. TAIR: The Arabidopsis information resource. http://www.tair.org. Accessed 30 Sept 2010
  104. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182PubMedGoogle Scholar
  105. 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 16:2164–2175PubMedGoogle Scholar
  106. 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 282:8848–8859PubMedGoogle Scholar
  107. 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 275:1767–1777PubMedGoogle Scholar
  108. 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 38:14955–14965PubMedGoogle Scholar
  109. 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 5:457–468PubMedGoogle Scholar
  110. 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 285:21391–21398PubMedGoogle Scholar
  111. 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 179:675–686PubMedGoogle Scholar
  112. 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 51:866–876PubMedGoogle Scholar
  113. 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 280:16170–16174PubMedGoogle Scholar
  114. 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 281:26260–26267PubMedGoogle Scholar
  115. 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 583:2142–2147PubMedGoogle Scholar
  116. 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 153:666–677PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Plant and Environmental SciencesUniversity of GothenburgGothenburgSweden

Personalised recommendations