In-Depth Analysis of the Thylakoid Membrane Proteome of Arabidopsis thaliana Chloroplasts: New Proteins, New Functions, and a Plastid Proteome Database

Plant Cell

Volumn 16, Issue 2, 2004, Pages 478-499

  Friso, Giulia ^a   Giacomelli, Lisa ^a   Ytterberg, A Jimmy ^a   Peltier, Jean Benoit ^a   Rudella, Andrea ^a   Sun, Qi ^a   Van Wijk, Klaas J ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; DATA REDUCTION; DATABASE SYSTEMS; HYDROPHOBICITY; ORGANIC SOLVENTS; PHOTOSYNTHESIS; PROTEINS; SEPARATION;

CLEAVAGE TECHNIQUES; CROSS-CORRELATION METHODS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; INSERTION SEQUENCES;

EID: 1042279117     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.017814     Document Type: Article

References (112)

1. Andersson, U., Heddad, M., and Adamska, I. (2003). Light stress-induced one-helix protein of the chlorophyll a/b-binding family associated with photosystem I. Plant Physiol. 132, 811-820.
2. Arabidopsis Genome Initiative. (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
3. Aro, E.-M., and Andersson, B. (2001). Regulation of Photosynthesis. (Dordrecht, The Netherlands: Kluwer Academic Publishers).
4. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S.R., Griffiths-Jones, S., Howe, K.L., Marshall, M., and Sonnhammer, E.L. (2002). The Pfam protein families database. Nucleic Acids Res. 30, 276-280.
5. Bell, E., Creelman, R.A., and Mullet, J.E. (1995). A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 92, 8675-8679.
6. Bradford, M.M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Burkhead, J.L., Abdel-Ghany, S.E., Morrill, J.M., Pilon-Smits, E.A., and Pilon, M. (2003). The Arabidopsis thaliana CUTA gene encodes an evolutionarily conserved copper binding chloroplast protein. Plant J. 34, 856-867.
8. Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P., and Nixon, P.J. (1998). Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17, 868-876.
9. Caliebe, A., Grimm, R., Kaiser, G., Lubeck, J., Soll, J., and Heins, L. (1997). The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J. 16, 7342-7350.
10. Carlberg, I., Hansson, M., Kieselbach, T., Schroder, W.P., Andersson, B., and Vener, A.V. (2003). A novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes. Proc. Natl. Acad. Sci. USA 100, 757-762.
11. Chen, M., Choi, Y., Voytas, D.F., and Rodermel, S. (2000). Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J. 22, 303-313.
12. Coligan, J.E., Dunn, B.M., Ploegh, H.L., Speicher, D.W., and Wingfield, P.T. (1995). Current Protocols in Protein Science. (New York: John Wiley & Sons).
13. Depege, N., Bellafiore, S., and Rochaix, J.D. (2003). Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299, 1572-1575.
14. Edvardsson, A., Eshaghi, S., Vener, A.V., and Andersson, B. (2003). The major peptidyl-prolyl isomerase activity in thylakoid lumen of plant chloroplasts belongs to a novel cyclophilin TLP20. FEBS Lett. 542, 137-141.
15. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
16. Ferro, M., Salvi, D., Brugiere, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J., and Rolland, N. (2003). Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2, 325-345.
17. Ferro, M., Salvi, D., Riviere-Rolland, H., Vermat, T., Seigneurin-Berny, D., Grunwald, D., Garin, J., Joyard, J., and Rolland, N. (2002). Integral membrane proteins of the chloroplast envelope: Identification and subcellular localization of new transporters. Proc. Natl. Acad. Sci. USA 99, 11487-11492.
18. Ferro, M., Seigneurin-Berny, D., Rolland, N., Chapel, A., Salvi, D., Garin, J., and Joyard, J. (2000). Organic solvent extraction as a versatile procedure to identify hydrophobic chloroplast membrane proteins. Electrophoresis 21, 3517-3526.
19. Field, H.I., Fenyo, D., and Beavis, R.C. (2002). RADARS, a bioinformatics solution that automates proteome mass spectral analysis, optimises protein identification, and archives data in a relational database. Proteomics 2, 36-47.
20. Fischer, K., and Weber, A. (2002). Transport of carbon in non-green plastids. Trends Plant Sci. 7, 345-351.
21. Flugge, U.I. (1998). Metabolite transporters in plastids. Curr. Opin. Plant Biol. 1, 201-206.
22. Froehlich, J.E., Wilkerson, C.G., Ray, W.K., McAndrew, R.S., Osteryoung, K.W., Gage, D.A., and Phinney, B.S. (2003). Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J. Proteome Res. 2, 413-425.
23. Fulgosi, H., Vener, A.V., Altschmied, L., Herrmann, R.G., and 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.
24. Gomez, S.M., Nishio, J.N., Faull, K.F., and Whitelegge, J.P. (2002). The chloroplast grana proteome defined by intact mass measurements from liquid chromatography mass spectrometry. Mol. Cell Proteomics 1, 46-59.
25. Gupta, R., He, Z., and Luan, S. (2002). Functional relationship of cytochrome c(6) and plastocyanin in Arabidopsis. Nature 417, 567-571.
26. Haldrup, A., Lunde, C., and Scheller, H.V. (2003). Arabidopsis thaliana plants lacking the PSI-D subunit of photosystem I suffer severe photoinhibition, have unstable photosystem I complexes, and altered redox homeostasis in the chloroplast stroma. J. Biol. Chem. 278, 33276-33283.
27. Hankamer, B., Morris, E., Nield, J., Carne, A., and Barber, J. (2001). Subunit positioning and transmembrane helix organisation in the core dimer of photosystem II. FEBS Lett. 504, 142-151.
28. Hatzfeld, Y., and Saito, K. (2000). Evidence for the existence of rhodanese (thiosulfate:cyanide sulfurtransferase) in plants: Preliminary characterization of two rhodanese cDNAs from Arabidopsis thaliana. FEBS Lett. 470, 147-150.
29. Horling, F., Lamkemeyer, P., Konig, J., Finkemeier, I., Kandlbinder, A., Baier, M., and Dietz, K.J. (2003). Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol. 131, 317-325.
30. Issakidis-Bourguet, E., Mouaheb, N., Meyer, Y., and Miginiac-Maslow, M. (2001). Heterologous complementation of yeast reveals a new putative function for chloroplast m-type thioredoxin. Plant J. 25, 127-136.
31. Itzhaki, H., Naveh, L., Lindahl, M., Cook, M., and Adam, Z. (1998). Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. J. Biol. Chem. 273, 7094-7098.
32. Jackson-Constan, D., Akita, M., and Keegstra, K. (2001). Molecular chaperones involved in chloroplast protein import. Biochim. Biophys. Acta 1541, 102-113.
33. Jackson-Constan, D., and Keegstra, K. (2001). Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol. 125, 1567-1576.
34. Jansch, L., Kruft, V., Schmitz, U.K., and Braun, H.P. (1996). New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J. 9, 357-368.
35. Jansson, S., Andersson, J., Kim, S.J., and Jackowski, G. (2000). An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Mol. Biol. 42, 345-351.
36. Jarvis, P., and Soil, J. (2002). Toe, tic, and chloroplast protein import. Biochim. Biophys. Acta 1590, 177-189.
37. Kamiya, N., and Shen, J.R. (2003). Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc. Natl. Acad. Sci. USA 100, 98-103.
38. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P. (1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657.
39. Knoetzel, J., Mant, A., Haldrup, A., Jensen, P.E., and Scheller, H.V. (2002). PSI-O, a new 10-kDa subunit of eukaryotic photosystem I. FEBS Lett. 510, 145-148.
40. Konig, J., Baier, M., Horling, F., Kahmann, U., Harris, G., Schurmann, P., and Dietz, K.J. (2002). The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc. Natl. Acad. Sci. USA 99, 5738-5743.
41. 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.
42. Kruft, V., Eubel, H., Jansch, L., Werhahn, W., and Braun, H.P. (2001). Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol. 127, 1694-1710.
43. Kyte, J., and Doolittle, R.F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
44. Leister, D. (2003). Chloroplast research in the genomic age. Trends Genet. 19, 47-56.
45. Lennartz, K., Plucken, H., Seidler, A., Westhoff, P., Bechtold, N., and Meierhoff, K. (2001). HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. Plant Cell 13, 2539-2551.
46. Lew, S., and London, E. (1997). Simple procedure for reversed-phase high-performance liquid chromatographic purification of long hydrophobic peptides that form transmembrane helices. Anal. Biochem. 251, 113-116.
47. Lindahl, M., Spetea, C., Hundal, T., Oppenheim, A.B., Adam, Z., and Andersson, B. (2000). The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12, 419-432.
48. Meurer, J., Plucken, 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.
49. Miernyk, J.A. (2001). The J-domain proteins of Arabidopsis thaliana: An unexpectedly large and diverse family of chaperones. Cell Stress Chaperones 6, 209-218.
50. Millar, A.H., Sweetlove, L.J., Giege, P., and Leaver, C.J. (2001). Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127, 1711-1727.
51. Molloy, M.P., Herbert, B.R., Williams, K.L., and Gooley, A.A. (1999). Extraction of Escherichia coli proteins with organic solvents prior to two-dimensional electrophoresis. Electrophoresis 20, 701-704.
52. Monde, R.A., Schuster, G., and Stern, D.B. (2000). Processing and degradation of chloroplast mRNA. Biochimie 82, 573-582.
53. Mori, H., and Cline, K. (2001). Post-translational protein translocation into thylakoids by the Sec and DeltapH-dependent pathways. Biochim. Biophys. Acta 1541, 80-90.
54. Mou, Z., He, Y., Dai, Y., Liu, X., and Li, J. (2000). Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12, 405-418.
55. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and Shikanai, T. (2002). PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361-371.
56. Naithani, S., Saracco, S.A., Butler, C.A., and Fox, T.D. (2003). Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell 14, 324-333.
57. Nield, J., Orlova, E.V., Morris, E.P., Gowen, B., van Heel, M., and Barber, J. (2000). 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat. Struct. Biol. 7, 44-47.
58. Ohtsu, K., Nakazono, M., Tsutsumi, N., and Hirai, A. (2001). Characterization and expression of the genes for cytochrome c oxidase subunit VIb (COX6b) from rice and Arabidopsis thaliana. Gene 264, 233-239.
59. Oliver, D.J., and Raman, R. (1995). Glycine decarboxylase: Protein chemistry and molecular biology of the major protein in leaf mitochondria. J. Bioenerg. Biomembr. 27, 407-414.
60. Onda, Y., Matsumura, T., Kimata-Ariga, Y., Sakakibara, H., Sugiyama, T., and Hase, T. (2000). Differential interaction of maize root ferredoxin:NADP(+) oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins. Plant Physiol. 123, 1037-1045.
61. Ort, D.R., and Yocum, C.F. 1996. Oxygenic Photosynthesis: The Light Reactions. (Dordrecht, The Netherlands: Kluwer Academic Publishers).
62. Peltier, G., and Coumac, L. (2002). Chlororespiration. Annu. Rev. Plant Biol. 53, 523-550.
63. Peltier, J.B., Emanuelsson, O., Kalume, D.E., Ytterberg, J., Friso, G., Rudella, A., Liberles, D.A., Soderberg, L., Roepstorff, P., von Heijne, G., and van Wijk, K.J. (2002). Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14, 211-236.
64. Peltier, J.B., Friso, G., Kalume, D.E., Roepstorff, P., Nilsson, F., Adamska, I., and van Wijk, K.J. (2000). Proteomics of the chloroplast: Systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12, 319-342.
65. Peltier, J.B., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Ytterberg, A.J., Giacomelli, L., Pillardy, J., and van Wijk, K.J. (2004). Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted 3-D structures and functional implications. J. Biol. Chem., in press.
66. Peltier, J.B., Ytterberg, J., Liberles, D.A., Roepstorff, P., and van Wijk, K.J. (2001). Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J. Biol. Chem. 276, 16318-16327.
67. Porra, R.J., Thompson, W.A., and Kriedemann, P.E. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394.
68. Portnoy, M.E., Rosenzweig, A.C., Rae, T., Huffman, D.L., O'Halloran, T.V., and Culotta, V.C. (1999). Structure-function analyses of the ATX1 metallochaperone. J. Biol. Chem. 274, 15041-15045.
69. Quinn, J.M., and Merchant, S. (1998). Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol. 297, 263-279.
70. Rabilloud, T., Vuillard, L., Gilly, C., and Lawrence, J.J. (1994). Silver-staining of proteins in polyacrylamide gels: A general overview. Cell Mol. Biol. (Noisy-le-grand) 40, 57-75.
71. Rey, P., Gillet, B., Romer, S., Eymery, F., Massimino, J., Peltier, G., and Kuntz, M. (2000). Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress. Plant J. 21, 483-494.
72. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277.
73. Rochaix, J.-D., Goldschmidt-Clermont, M., and Merchant, S. (1998). The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, Advances in Photosynthesis and Respiration, Vol. 7. (Dordrecht, The Netherlands: Kluwer Academic Publishers).
74. Rosenzweig, A.C., Huffman, D.L., Hou, M.Y., Wemimont, A.K., Pufahl, R.A., and O'Halloran, T.V. (1999). Crystal structure of the Atx1 metallochaperone protein at 1.02 A resolution. Structure Fold. Des. 7, 605-617.
75. Sakamoto, W., Tamura, T., Hanba-Tomita, Y., and Murata, M. (2002). The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7, 769-780.
76. 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. 168, 368-379.
77. Scheller, H.V., Jensen, P.E., Haldrup, A., Lunde, C., and Knoetzel, J. (2001). Role of subunits in eukaryotic Photosystem I. Biochim. Biophys. Acta 1507, 41-60.
78. Schneider, A., Hausler, R.E., Kolukisaoglu, U., Kunze, R., van der Graaff, E., Schwacke, R., Catoni, E., Desimone, M., and Flugge, U.I. (2002). An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J. 32, 685-699.
79. Schroda, M., Vallon, O., Whitelegge, J.P., Beck, C.F., and Wollman, F.A. (2001). The chloroplastic GrpE homolog of Chlamydomonas: Two isoforms generated by differential splicing. Plant Cell 13, 2823-2839.
80. Schubert, M., Petersson, U.A., Haas, B.J., Funk, C., Schroder, W.P., and Kieselbach, T. (2002). Proteome map of the chloroplast lumen of Arabidopsis thaliana. J. Biol. Chem. 277, 8354-8365.
81. Schuenemann, D., Amin, P., Hartmann, E., and Hoffman, N.E. (1999). Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J. Biol. Chem. 274, 12177-12182.
82. Seigneurin-Berny, D., Rolland, N., Garin, J., and Joyard, J. (1999). Technical Advance: Differential extraction of hydrophobic proteins from chloroplast envelope membranes: A subcellular-specific proteomic approach to identify rare intrinsic membrane proteins. Plant J. 19, 217-228.
83. Shen, G., Antonkine, M.L., van der Est, A., Vassiliev, I.R., Brettel, K., Bittl, R., Zech, S.G., Zhao, J., Stehlik, D., Bryant, D.A., and Golbeck, J.H. (2002a). Assembly of photosystem I. II. Rubredoxin is required for the in vivo assembly of F(X) in Synechococcus sp. PCC 7002 as shown by optical and EPR spectroscopy. J. Biol. Chem. 277, 20355-20366.
84. Shen, G., Zhao, J., Reimer, S.K., Antonkine, M.L, Cai, Q., Weiland, S.M., Golbeck, J.H., and Bryant, DA. (2002b). Assembly of photosystem I. I. Inactivation of the rubA gene encoding a membrane-associated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of photosystem I activity. J. Biol. Chem. 277, 20343-20354.
85. Shevchenko, A., Loboda, A., Ens, W., and Standing, K.G. (2000). MALDI quadrupole time-of-flight mass spectrometry: A powerful tool for proteomic research. Anal. Chem. 72, 2132-2141.
86. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
87. Shikanai, T., Muller-Moule, P., Munekage, Y., Niyogi, K.K., and Pilon, M. (2003). PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15, 1333-1346.
88. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J., and Klenk, D.C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
89. Snyders, S., and Kohorn, B.D. (1999). TAKs, thylakoid membrane protein kinases associated with energy transduction. J. Biol. Chem. 274, 9137-9140.
90. Srinivasan, R., and Oliver, D.J. (1995). Light-dependent and tissue-specific expression of the H-protein of the glycine decarboxylase complex. Plant Physiol. 109, 161-168.
91. Sussman, M.R. (1988). Purification of integral plasma membrane proteins by reverse-phase high performance liquid chromatography. Anal. Biochem. 169, 395-399.
92. Swiatek, M., Kuras, R., Sokolenko, A., Higgs, D., Olive, J., Cinque, G., Muller, B., Eichacker, L.A., Stern, D.B., Bassi, R., Herrmann, R.G., and Wollman, F.A. (2001). The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell 13, 1347-1367.
93. Tarr, G.E., and Crabb, J.W. (1983). Reverse-phase high-performance liquid chromatography of hydrophobic proteins and fragments thereof. Anal. Biochem. 131, 99-107.
94. Teramoto, H., Nakamori, A., Minagawa, J., and Ono, T.A. (2002). Light-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. Plant Physiol. 130, 325-333.
95. Tyers, M., and Mann, M. (2003). From genomics to proteomics. Nature 422, 193-197.
96. van Montfort, B.A., Canas, B., Duurkens, R., Godovac-Zimmermann, J., and Robillard, G.T. (2002). Improved in-gel approaches to generate peptide maps of integral membrane proteins with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Mass Spectrom. 37, 322-330.
97. van Wijk, K.J. (2001a). Proteins involved in biogenesis of the thylakoid membrane. In Regulatory Aspects of Photosynthesis, Advances in Photosynthesis and Respiration, Vol. 11. E.-M. Aro and B. Andersson, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 153-175.
98. van Wijk, K.J. (2001b). Challenges and prospects of plant proteomics. Plant Physiol. 126, 501-508.
99. Varotto, C., Pesaresi, P., Jahns, P., Lessnick, A., Tizzano, M., Schiavon, F., Salamini, F., and Leister, D. (2002). Single and double knockouts of the genes for photosystem I subunits G, K, and H of Arabioopsis. Effects on photosystem I composition, photosynthetic electron flow, and state transitions. Plant Physiol. 129, 616-624.
100. Varotto, C., Pesaresi, P., Meurer, J., Oelmuller, R., Steiner-Lange, S., Salamini, F., and Leister, D. (2000). Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J. 22, 115-124.
101. Watson, B.S., Asirvatham, V.S., Wang, L., and Sumner, L.W. (2003). Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol. 131, 1104-1123.
102. Weigel, M., Varotto, C., Pesaresi, P., Finazzi, G., Rappaport, F., Salamini, F., and Leister, D. (2003). Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J. Biol. Chem. 278, 31286-31289.
103. Wernimont, A.K., Huffman, D.L., Lamb, A.L., O'Halloran, T.V., and Rosenzweig, A.C. (2000). Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat. Struct. Biol. 7, 766-771.
104. Westerlund, I., Von Heijne, G., and Emanuelsson, O. (2003). LumenP - a neural network predictor for protein localization in the thylakoid lumen. Protein Sci. 12, 2360-2366.
105. Whitelegge, J.P., Zhang, H., Aguilera, R., Taylor, R.M., and Cramer, W.A. (2002). Full subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein: Cytochrome b(6)f complex from spinach and the cyanobacterium Mastigocladus laminosus. Mol. Cell Proteomics 1, 816-827.
106. 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.
107. Yabuta, Y., Motoki, T., Yoshimura, K., Takeda, T., Ishikawa, T., and Shigeoka, S. (2002). Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photooxidative stress. Plant J. 32, 915-925.
108. Yamaguchi, K., and Subramanian, A.R. (2000). The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28466-28482.
109. Yamaguchi, K., and Subramanian, A.R. (2003). Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur. J. Biochem. 270, 190-205.
110. Yu, Z., Friso, G., Miranda, J.J., Patel, M.J., Lo-Tseng, T., Moore, E.G., and Burlingame, A.L. (1997). Structural characterization of human hemoglobin crosslinked by bis(3,5-dibromosalicyl) fumarate using mass spectrometric techniques. Protein Sci. 6, 2568-2577.
111. Zhang, H., Whitelegge, J.P., and Cramer, W.A. (2001). Ferredoxin: NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J. Biol. Chem. 276, 38159-38165.
112. Zhang, W., and Chait, B.T. (2000). ProFound: An expert system for protein Identification using mass spectrometric peptide mapping information. Anal. Chem. 72, 2482-2489.