The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly

Plant Cell

Volumn 22, Issue 10, 2010, Pages 3439-3460

  Armbruster, Ute ^a   Zühlke, Jessica ^a   Rengstl, Birgit ^a   Kreller, Renate ^a   Makarenko, Elina ^a   Rühle, Thilo ^a   Schünemann, Danja ^b   Jahns, Peter ^c   Weisshaar, Bernd ^d   Nickelsen, Jörg ^a   Leistera, Dario ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; CYANOBACTERIA; EUKARYOTA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 78649511035     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.077453     Document Type: Article

References (101)

1. Adir, N., Zer, H., Shochat, S., and Ohad, I. (2003). Photoinhibition - A historical perspective. Photosynth. Res. 76: 343-370.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Anbudurai, P.R., Mor, T.S., Ohad, I., Shestakov, S.V., and Pakrasi, H.B. (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.
4. Aro, E.M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N., and Rintamäki, E. (2005). Dynamics of photosystem II: A proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56: 347-356.
5. Aronsson, H., and Jarvis, P. (2002). A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett. 529: 215-220.
6. Baena-González, E., and Aro, E.M. (2002). Biogenesis, assembly and turnover of photosystem II units. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 1451-1459, discussion 1459-1460.
7. Barkan, A. (1988). Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 7: 2637-2644.
8. Bassi, R., dal Belin Peruffo, A., Barbato, R., and Ghisi, R. (1985). Differences in chlorophyll-protein complexes and composition of polypeptides between thylakoids from bundle sheaths and mesophyll cells in maize. Eur. J. Biochem. 146: 589-595.
9. Bellafiore, S., Ferris, P., Naver, H., Göhre, V., and Rochaix, J.D. (2002). Loss of Albino3 leads to the specific depletion of the lightharvesting system. Plant Cell 14: 2303-2314.
10. Blanc, G., Hokamp, K., and Wolfe, K.H. (2003). A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137-144.
11. Boekema, E.J., Hankamer, B., Bald, D., Kruip, J., Nield, J., Boonstra, A.F., Barber, J., and Rögner, M. (1995). Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc. Natl. Acad. Sci. USA 92: 175-179.
12. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G.M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P.G. (2004). Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
13. Chen, H., Zhang, D., Guo, J., Wu, H., Jin, M., Lu, Q., Lu, C., and Zhang, L. (2006). A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Mol. Biol. 61: 567-575.
14. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., and Thompson, J.D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31: 3497-3500.
15. Choquet, Y., and Wollman, F.A. (2002). Translational regulations as specific traits of chloroplast gene expression. FEBS Lett. 529: 39-42.
16. Choquet, Y., Wostrikoff, K., Rimbault, B., Zito, F., Girard-Bascou, J., Drapier, D., and Wollman, F.A. (2001). Assembly-controlled regulation of chloroplast gene translation. Biochem. Soc. Trans. 29: 421-426.
17. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
18. Diner, B.A., Ries, D.F., Cohen, B.N., and Metz, J.G. (1988). COOHterminal processing of polypeptide D1 of the photosystem II reaction center of Scenedesmus obliquus is necessary for the assembly of the oxygen-evolving complex. J. Biol. Chem. 263: 8972-8980.
19. Dewez, D., Park, S., García-Cerdán, J.G., Lindberg, P., and Melis, A. (2009). Mechanism of REP27 protein action in the D1 protein turnover and photosystem II repair from photodamage. Plant Physiol. 151: 88-99.
20. Dobáková, M., Sobotka, R., Tichý, M., and Komenda, J. (2009). Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 149: 1076-1086.
21. Dü hring, U., Irrgang, K.D., Lü nser, K., Kehr, J., and Wilde, A. (2006). Analysis of photosynthetic complexes from a cyanobacterial ycf37 mutant. Biochim. Biophys. Acta 1757: 3-11.
22. Eaton-Rye, J.J. (2004). The construction of gene knockouts in the cyanobacterium Synechocystis sp. PCC 6803. Methods Mol. Biol. 274: 309-324.
23. Edelman, M., and Mattoo, A.K. (2008). D1-protein dynamics in photosystem II: The lingering enigma. Photosynth. Res. 98: 609-620.
24. Emanuelsson, O., Nielsen, H., and von Heijne, G. (1999). ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8: 978-984.
25. Enami, I., Okumura, A., Nagao, R., Suzuki, T., Iwai, M., and Shen, J.R. (2008). Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth. Res. 98: 349-363.
26. Ermakova-Gerdes, S., and Vermaas, W. (1999). Inactivation of the open reading frame slr0399 in Synechocystis sp. PCC 6803 functionally complements mutations near the Q(A) niche of photosystem II. A possible role of Slr0399 as a chaperone for quinone binding. J. Biol. Chem. 274: 30540-30549.
27. Färber, A., Young, A.J., Ruban, A.V., Horton, P., and Jahns, P. (1997). Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants. The relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching. Plant Physiol. 115: 1609-1618.
28. Ferreira, K.N., Iverson, T.M., Maghlaoui, K., Barber, J., and Iwata, S. (2004). Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831-1838.
29. Frey, M., Stettner, C., and Gierl, A. (1998). A general method for gene isolation in tagging approaches: amplification of insertion mutagenised sites (AIMS). Plant J. 13: 717-721.
30. Göhre, V., Ossenbühl, F., Crèvecoeur, M., Eichacker, L.A., and Rochaix, J.D. (2006). One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 18: 1454-1466.
31. Granvogl, B., Reisinger, V., and Eichacker, L.A. (2006). Mapping the proteome of thylakoid membranes by de novo sequencing of intermembrane peptide domains. Proteomics 6: 3681-3695.
32. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and 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.
33. Hankamer, B., Nield, J., Zheleva, D., Boekema, E., Jansson, S., and Barber, J. (1997). Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur. J. Biochem. 243: 422-429.
34. Hatano-Iwasaki, A., Minagawa, J., Inoue, Y., and Takahashi, Y. (2000). Characterization of chloroplast psbA transformants of Chlamydomonas reinhardtii with impaired processing of a precursor of a photosystem II reaction center protein, D1. Plant Mol. Biol. 42: 353-363.
35. Ihnatowicz, A., Pesaresi, P., Lohrig, K., Wolters, D., Müller, B., and Leister, D. (2008). Impaired photosystem I oxidation induces STN7- dependent phosphorylation of the light-harvesting complex I protein Lhca4 in Arabidopsis thaliana. Planta 227: 717-722.
36. Ihnatowicz, A., Pesaresi, P., Varotto, C., Richly, E., Schneider, A., Jahns, P., Salamini, F., and Leister, D. (2004). Mutants for photosystem I subunit D of Arabidopsis thaliana: Effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J. 37: 839-852.
37. Iwata, S., and Barber, J. (2004). Structure of photosystem II and molecular architecture of the oxygen-evolving centre. Curr. Opin. Struct. Biol. 14: 447-453.
38. Kapri-Pardes, E., Naveh, L., and 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.
39. Karimi, M., de Oliveira Manes, C.L., Van Montagu, M., and Gheysen, G. (2002). Activation of a pollenin promoter upon nematode infection. J. Nematol. 34: 75-79.
40. Karnauchov, I., Herrmann, R.G., and Klösg en, R.B. (1997). Transmembranetopology of the Rieske Fe/S protein of the cytochrome b6/f complex from spinach chloroplasts. FEBS Lett. 408: 206-210.
41. Kashino, Y., Lauber, W.M., Carroll, J.A., Wang, Q., Whitmarsh, J., Satoh, K., and Pakrasi, H.B. (2002). Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41: 8004-8012.
42. Kato, Y., and Sakamoto, W. (2009). Protein quality control in chloroplasts: A current model of D1 protein degradation in the photosystem II repair cycle. J. Biochem. 146: 463-469.
43. Keren, N., Ohkawa, H., Welsh, E.A., Liberton, M., and Pakrasi, H.B. (2005). Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. PlantCell 17: 2768-2781.
44. Klinkert, B., Ossenbühl, F., Sikorski, M., Berry, S., Eichacker, L., and Nickelsen, J. (2004). PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of photosystem II in Synechocystis sp. PCC 6803. J. Biol. Chem. 279: 44639-44644.
45. Kogata, N., Nishio, K., Hirohashi, T., Kikuchi, S., and Nakai, M. (1999). Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids. FEBS Lett. 447: 329-333.
46. Komenda, J., Nickelsen, J., Tichý, M., Prásil, O., Eichacker, L.A., and Nixon, P.J. (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.
47. Komenda, J., Tichý, M., and Eichacker, L.A. (2005). The PsbH protein is associated with the inner antenna CP47 and facilitates D1 processing and incorporation into PSII in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol. 46: 1477-1483.
48. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567-580.
49. Kufryk, G.I., and Vermaas, W.F. (2001). A novel protein involved in the functional assembly of the oxygen-evolving complex of photosystem II in Synechocystis sp. PCC 6803. Biochemistry 40: 9247-9255.
50. Kufryk, G.I., and Vermaas, W.F. (2003). Slr2013 is a novel protein regulating functional assembly of photosystem II in Synechocystis sp. strain PCC 6803. J. Bacteriol. 185: 6615-6623.
51. Laidler, V., Chaddock, A.M., Knott, T.G., Walker, D., and Robinson, C. (1995). A SecY homolog in Arabidopsis thaliana. Sequence of a fulllength cDNA clone and import of the precursor protein into chloroplasts. J. Biol. Chem. 270: 17664-17667.
52. Leister, D., Varotto, C., Pesaresi, P., Niwergall, A., and Salamini, F. (1999). Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiol. Biochem. 37: 671-678.
53. Ma, J., Peng, L., Guo, J., Lu, Q., Lu, C., and Zhang, L. (2007). LPA2 is required for efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 19: 1980-1993.
54. Martienssen, R.A. (1998). Functional genomics: Probing plant gene function and expression with transposons. Proc. Natl. Acad. Sci. USA 95: 2021-2026.
55. Martínez-García, J.F., Monte, E., and Quail, P.H. (1999). A simple rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J. 20: 251-257.
56. Meurer, J., Plücken, H., Kowallik, K.V., and 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.
57. Minagawa, J., and Takahashi, Y. (2004). Structure, function and assembly of photosystem II and its light-harvesting proteins. Photosynth. Res. 82: 241-263.
58. Mulo, P., Sirpiö, S., Suorsa, M., and Aro, E.M. (2008). Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth. Res. 98: 489-501.
59. Nelson, N., and Yocum, C.F. (2006). Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57: 521-565.
60. Nixon, P.J., Barker, M., Boehm, M., de Vries, R., and Komenda, J. (2005). FtsH-mediated repair of the photosystem II complex in response to light stress. J. Exp. Bot. 56: 357-363.
61. Nixon, P.J., Michoux, F., Yu, J., Boehm, M., and Komenda, J. (2010). Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. (Lond.) 106: 1-16.
62. Nixon, P.J., Trost, J.T., and Diner, B.A. (1992). Role of the carboxy terminus of polypeptide D1 in the assembly of a functional wateroxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31: 10859-10871.
63. Nowaczyk, M.M., Hebeler, R., Schlodder, E., Meyer, H.E., Warscheid, B., and Rögner, M. (2006). Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18: 3121-3131.
64. Ossenbühl, F., Göhre, V., Meurer, J., Krieger-Liszkay, A., Rochaix, J.D., and Eichacker, L.A. (2004). Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell 16: 1790-1800.
65. Ossenbühl, F., Inaba-Sulpice, M., Meurer, J., Soll, J., and Eichacker, L.A. (2006). The synechocystis sp PCC 6803 oxa1 homolog is essential for membrane integration of reaction center precursor protein pD1. Plant Cell 18: 2236-2246.
66. Park, S., Khamai, P., Garcia-Cerdan, J.G., and Melis, A. (2007). REP27, a tetratricopeptide repeat nuclear-encoded and chloroplast-localized protein, functions in D1/32-kD reaction center protein turnover and photosystem II repair from photodamage. Plant Physiol. 143: 1547-1560.
67. Pasch, J.C., Nickelsen, J., and Schünemann, D. (2005). The yeast split-ubiquitin system to study chloroplast membrane protein interactions. Appl. Microbiol. Biotechnol. 69: 440-447.
68. Peng, L., Ma, J., Chi, W., Guo, J., Zhu, S., Lu, Q., Lu, C., and Zhang, L. (2006). LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18: 955-969.
69. Peng, L., Shimizu, H., and Shikanai, T. (2008). The chloroplast NAD(P) H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283: 34873-34879.
70. Pesaresi, P., Hertle, A., Pribil, M., Kleine, T., Wagner, R., Strissel, H., Ihnatowicz, A., Bonardi, V., Scharfenberg, M., Schneider, A., Pfannschmidt, T., and Leister, D. (2009). Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21: 2402-2423.
71. Pesaresi, P., Lunde, C., Jahns, P., Tarantino, D., Meurer, J., Varotto, C., Hirtz, R.D., Soave, C., Scheller, H.V., Salamini, F., and Leister, D. (2002). A stable LHCII-PSI aggregate and suppression of photosynthetic state transitions in the psae1-1 mutant of Arabidopsis thaliana. Planta 215: 940-948.
72. Pesaresi, P., Masiero, S., Eubel, H., Braun, H.P., Bhushan, S., Glaser, E., Salamini, F., and Leister, D. (2006). Nuclear photosynthetic gene expression is synergistically modulated by rates of rotein synthesis in chloroplasts and mitochondria. Plant Cell 18: 970-991.
73. Plücken, H., Müller, B., Grohmann, D., Westhoff, P., and Eichacker, L.A. (2002). The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett. 532: 85-90.
74. Rokka, A., Suorsa, M., Saleem, A., Battchikova, N., and Aro, E.M. (2005). Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem. J. 388: 159-168.
75. Roose, J.L., and Pakrasi, H.B. (2004). Evidence that D1 processing is required for manganese binding and extrinsic protein assembly into photosystem II. J. Biol. Chem. 279: 45417-45422.
76. Roose, J.L., Wegener, K.M., and Pakrasi, H.B. (2007). The extrinsic proteins of photosystem II. Photosynth. Res. 92: 369-387.
77. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and Weisshaar, B. (2003). An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53: 247-259.
78. Roy, L.M., and Barkan, A. (1998). A SecY homologue is required for theelaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J. Cell Biol. 141: 385-395.
79. Schägger, H., Aquila, H., and Von Jagow, G. (1988). Coomassie bluesodium dodecyl sulfate-polyacrylamide gel electrophoresis for direct visualization of polypeptides during electrophoresis. Anal. Biochem. 173: 201-205.
80. Schägger, H., and von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
81. Schottkowski, M., Gkalympoudis, S., Tzekova, N., Stelljes, C., Schünemann, D., Ankele, E., and Nickelsen, J. (2009a). Interaction of the periplasmic PratA factor and the PsbA (D1) protein during biogenesis of photosystem II in Synechocystis sp. PCC 6803. J. Biol. Chem. 284: 1813-1819.
82. Schottkowski, M., Ratke, J., Oster, U., Nowaczyk, M., and Nickelsen, J. (2009b). Pitt, a novel tetratricopeptide repeat protein involved in lightdependent chlorophyll biosynthesis and thylakoid membrane biogenesis in Synechocystis sp. PCC 6803. Mol. Plant 2: 1289-1297.
83. Schult, K., Meierhoff, K., Paradies, S., Töller, T., Wolff, P., and Westhoff, P. (2007). The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19: 1329-1346.
84. Schwenkert, S., Umate, P., Dal Bosco, C., Volz, S., Mlçochová, L., Zoryan, M., Eichacker, L.A., Ohad, I., Herrmann, R.G., and Meurer, J. (2006). PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J. Biol. Chem. 281: 34227-34238.
85. Shestakov, S.V., Anbudurai, P.R., Stanbekova, G.E., Gadzhiev, A., Lind, L.K., and Pakrasi, H.B. (1994). Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 269: 19354-19359.
86. Shi, L.X., and Schröder, W.P. (2004). The low molec lar mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta 1608: 75-96.
87. Sirpiö, S., Khrouchtchova, A., Allahverdiyeva, Y., Hansson, M., Fristedt, R., Vener, A.V., Scheller, H.V., Jensen, P.E., Haldrup, A., and Aro, E.M. (2008). AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II. Plant J. 55: 639-651.
88. Spence, E., Bailey, S., Nenninger, A., Møller, S.G., and Robinson, C. (2004). A homolog of Albino3/OxaI is essential for thylakoid biogenesis in the cyanobacterium Synechocystis sp. PCC6803. J. Biol. Chem. 279: 55792-55800.
89. Sun, X., Ouyang, M., Guo, J., Ma, J., Lu, C., Adam, Z., and Zhang, L. (2010). The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J. 62: 240-249.
90. Sundberg, E., Slagter, J.G., Fridborg, I., Cleary, S.P., Robinson, C., and Coupland, G. (1997). ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717-730.
91. Tatusova, T.A., and Madden, T.L. (1999). BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174: 247-250.
92. Taylor, M.A., Packer, J.C.L., and Bowyer, J.R. (1988). Processing of the D1 polypeptide of the photosystem II reaction centre and photoactivation of a low fluorescence mutant (LF-1) of Scenedesmus obliquus. FEBS Lett. 237: 229-233.
93. van Wijk, K.J., Andersson, B., and Aro, E.M. (1996). Kinetic resolution of the incorporation of the D1 protein into photosystem II and localization of assembly intermediates in thylakoid membranes of spinach chloroplasts. J. Biol. Chem. 271: 9627-9636.
94. van Wijk, K.J., Bingsmark, S., Aro, E.M., and Andersson, B. (1995). In vitro synthesis and assembly of photosystem II core proteins. The D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids. J. Biol. Chem. 270: 25685-25695.
95. van Wijk, K.J., Roobol-Boza, M., Kettunen, R., Andersson, B., and Aro, E.M. (1997). Synthesis and assembly of the D1 protein into photosystem II: Processing of the C-terminus and identification of the initial assembly partners and complexes during photosystem II repair. Biochemistry 36: 6178-6186.
96. Varotto, C., Pesaresi, P., Maiwald, D., Kurth, J., Salamini, F., and Leister, D. (2000a). Identification of photosynthetic mutants of Arabidopsis by automatic screening for altered effective quantum yield of photosystem 2. Photosynthetica 38: 497-504.
97. Varotto, C., Pesaresi, P., Meurer, J., Oelmüller, R., Steiner-Lange, S., Salamini, F., and Leister, D. (2000b). Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J. 22: 115-124.
98. Wei, L., Guo, J., Ouyang, M., Sun, X., Ma, J., Chi, W., Lu, C., and Zhang, L. (2010). LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J. Biol. Chem. 285: 21391-21398.
99. Wessel, D., and Flügge, U.I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138: 141-143.
100. Wollman, F.A., Minai, L., and Nechushtai, R. (1999). The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1. Biochim. Biophys. Acta 1411: 21-85.
101. Zaltsman, A., Feder, A., and Adam, Z. (2005). Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts- Implications for thylakoid formation and photosystem II maintenance. Plant J. 42: 609-617.