PHOTOSYSTEM II PROTEIN33, a protein conserved in the plastid lineage, is associated with the chloroplast thylakoid membrane and provides stability to photosystem II supercomplexes in arabidopsis

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 481-492

  Fristedt, Rikard ^a   Herdean, Andrei ^b   Blaby Haas, Crysten E ^a   Mamedov, Fikret ^c   Merchant, Sabeeha S ^a   Last, Robert L ^d   Lundin, Björn ^b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

^d Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; CHLOROPHYLL; LIGHT HARVESTING SYSTEM; MEMBRANE PROTEIN; PHOTOSYSTEM II;

ARABIDOPSIS; CELL FRACTIONATION; FLUORESCENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR MEMBRANE; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOCHEMISTRY; PHOTOSYSTEM II; PLANT GENE; PROTEIN STABILITY; PROTEIN TRANSPORT; RADIATION RESPONSE; SEQUENCE ANALYSIS; THYLAKOID;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL; CONSERVED SEQUENCE; FLUORESCENCE; GENES, PLANT; INTRACELLULAR MEMBRANES; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MEMBRANE PROTEINS; MUTATION; PHENOTYPE; PHOTOCHEMICAL PROCESSES; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN STABILITY; PROTEIN TRANSPORT; SEQUENCE ANALYSIS, PROTEIN; SUBCELLULAR FRACTIONS; THYLAKOIDS;

EID: 84921956710     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.253336     Document Type: Article

References (54)

1. Ajjawi I, Lu Y, Savage LJ, Bell SM, Last RL (2010) Large-scale reverse genetics in Arabidopsis: case studies from the Chloroplast 2010 Project. Plant Physiol 152: 529-540
2. Alexeyev MF, Winkler HH (1999) Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J Mol Biol 285: 1503-1513
3. 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
4. Barber J, Ferreira KN, Maghlaoui K, Iwata S (2004) Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications. Phys Chem Chem Phys 6: 4737-4742
5. Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895
6. Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang H, Dodani SC, Pellegrini M, Huijser P, Connolly EL, et al (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/ FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24: 738-761
7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
8. Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56: 395-406
9. Cserzö M, Wallin E, Simon I, von Heijne G, Elofsson A (1997) Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10: 673-676
10. Curtis MD, Grossniklaus U (2003) A Gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
11. Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575
12. Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, Schulze WX (2010) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res 38: D828-D834
13. Edgar RC (2004)MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
14. Ellis RJ, Hartley MR (1971) The sites of synthesis of chloroplast proteins. Biochem J 124: 11P-12P
15. Fristedt R, Carlberg I, Zygadlo A, Piippo M, Nurmi M, Aro EM, Scheller HV, Vener AV (2009) Intrinsically unstructured phosphoprotein TSP9 regulates light harvesting in Arabidopsis thaliana. Biochemistry 48: 499-509
16. Fristedt R, Vener AV (2011) High light induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29. PLoS ONE 6: e24565
17. García-Cerdán JG, Kovács L, Tóth T, Kereïche S, Aseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J 65: 368-381
18. Gouet P, Courcelle E, Stuart DI, Métoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308
19. Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47: 720-734
20. Hamel PP, Dreyfuss BW, Xie Z, Gabilly ST, Merchant S (2003) Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J Biol Chem 278: 2593-2603
21. Havaux M, Bonfils JP, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124: 273-284
22. Hsieh SI, Castruita M, Malasarn D, Urzica E, Erde J, Page MD, Yamasaki H, Casero D, Pellegrini M, Merchant SS, et al (2013) The proteome of copper, iron, zinc, and manganese micronutrient deficiency in Chlamydomonas reinhardtii. Mol Cell Proteomics 12: 65-86
23. Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99: 12789-12794
24. Karamoko M, Cline S, Redding K, Ruiz N, Hamel PP (2011) Lumen Thiol Oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis. Plant Cell 23: 4462-4475
25. Karpowicz SJ, Prochnik SE, Grossman AR, Merchant SS (2011) The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J Biol Chem 286: 21427-21439
26. Lambrev PH, Nilkens M, Miloslavina Y, Jahns P, Holzwarth AR (2010) Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. Plant Physiol 152: 1611-1624
27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275
28. Lu Y, Hall DA, Last RL (2011a) A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell 23: 1861-1875
29. Lu Y, Savage LJ, Ajjawi I, Imre KM, Yoder DW, Benning C, Dellapenna D, Ohlrogge JB, Osteryoung KW, Weber AP, et al (2008) New connections across pathways and cellular processes: industrialized mutant screening reveals novel associations between diverse phenotypes in Arabidopsis. Plant Physiol 146: 1482-1500
30. Lu Y, Savage LJ, Larson MD, Wilkerson CG, Last RL (2011b) Chloroplast 2010: a database for large-scale phenotypic screening of Arabidopsis mutants. Plant Physiol 155: 1589-1600
31. Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613-615
32. Martins BM, Svetlitchnaia T, Dobbek H (2005) 2-Oxoquinoline 8-monooxygenase oxygenase component: active site modulation by Rieske-[2Fe-2S] center oxidation/reduction. Structure 13: 817-824
33. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250
34. Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161: 5-19
35. Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98: 8777-8796
36. Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134
37. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16: 307-314
38. Pagliano C, Saracco G, Barber J (2013) Structural, functional and auxiliary proteins of photosystem II. Photosynth Res 116: 167-188
39. Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, et al (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21: 2402-2423
40. Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73: 149-156
41. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301
42. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738
43. Ruban AV, Murchie EH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim Biophys Acta 1817: 977-982
44. Samol I, Shapiguzov A, Ingelsson B, Fucile G, Crèvecoeur M, Vener AV, Rochaix JD, Goldschmidt-Clermont M (2012) Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 24: 2596-2609
45. Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131: 16-26
46. Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107: 4782-4787
47. Shevchenko A, Chernushevic I, Shevchenko A, Wilm M, Mann M (2002) "De novo" sequencing of peptides recovered from in-gel digested proteins by nanoelectrospray tandem mass spectrometry. Mol Biotechnol 20: 107-118
48. 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
49. Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S, et al (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24: 2934-2948
50. Tikkanen M, Grieco M, Aro EM (2011) Novel insights into plant lightharvesting complex II phosphorylation and 'state transitions.' Trends Plant Sci 16: 126-131
51. Tóth SZ, Nagy V, Puthur JT, Kovács L, Garab G (2011) The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves. Plant Physiol 156: 382-392
52. Wang H, Gau B, Slade WO, Juergens M, Li P, Hicks LM (2014) The global phosphoproteome of Chlamydomonas reinhardtii reveals complex organellar phosphorylation in the flagella and thylakoid membrane. Mol Cell Proteomics 13: 2337-2353
53. Wegener KM, Bennewitz S, Oelmüller R, Pakrasi HB (2011) The Psb32 protein aids in repairing photodamaged photosystem II in the cyanobacterium Synechocystis 6803. Mol Plant 4: 1052-1061
54. Yin L, Fristedt R, Herdean A, Solymosi K, Bertrand M, Andersson MX, Mamedov F, Vener AV, Schoefs B, Spetea C (2012) Photosystem II function and dynamics in three widely used Arabidopsis thaliana accessions. PLoS ONE 7: e46206