Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes

Molecular Plant

Volumn 2, Issue 6, 2009, Pages 1247-1261

  Bräutigam, Andrea ^a,b   Weber, Andreas P M ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Chloroplast biology; Membrane biochemistry; Membrane proteins; Proteomics; Transcriptome analysis; Transporters

Indexed keywords

MEMBRANE PROTEIN; PROTEOME; VEGETABLE PROTEIN;

ARTICLE; BRASSICA; CHROMOSOME MAP; GENE EXPRESSION PROFILING; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; PLASTID; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; BRASSICA; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; PLANT PROTEINS; PLASTIDS; PROTEOME;

EID: 71249161231     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssp070     Document Type: Article

References (106)

1. Aldridge, C., Cain, P., and Robinson, C. (2009). Protein transport in organelles: protein transport into and across the thylakoid membrane. FEBS J. 276, 1177-1186
2. Andre, C., and Benning, C. (2007). Arabidopsis seedlings deficient in a plastidic pyruvate kinase are unable to utilize seed storage compounds for germination and establishment. Plant Physiol. 145, 1670-1680
3. Andre, C., Froehlich, J.E., Moll, M.R., and Benning, C. (2007). A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell. 19, 2006-2022
4. Aoki, N., and Kanai, R. (1997). Reappraisal of the role of sodium in the light-dependent active transport of pyruvate into mesophyll chloroplasts of C-4 plants. Plant Cell Physiol. 38, 1217-1225
5. Aoki, N., Ohnishi, J., and Kanai, R. (1992). 2 different mechanisms for transport of pyruvate into mesophyll chloroplasts of C-4 plants: a comparative-study. Plant Cell Physiol. 33, 805-809
6. Awai, K., Xu, C.C., Tamot, B., and Benning, C. (2006). A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad. Sci. U S A. 103, 10817-10822
7. Baginsky, S., Siddique, A., and Gruissem,W. (2004). Proteome analysis of tobacco bright yellow-2 (BY-2) cell culture plastids as a model for undifferentiated heterotrophic plastids. J. Proteome Res. 3, 1128-1137
8. Baud, S., Boutin, J.P., Miquel, M., Lepiniec, L., and Rochat, C. (2002). An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 40, 151-160
9. Betterle, N., Ballottari, M., Zorzan, S., de Bianchi, S., Cazzaniga, S., Dall'Osto, L., Morosinotto, T., and Bassi, R. (2009). Light-induced dissociation of an antenna hetero-oligomer is needed for nonphotochemical quenching induction. J. Biol. Chem. 284, 15255-15266
10. Bouvier, F., Linka, N., Isner, J.C., Mutterer, J., Weber, A.P.M., and Camara, B. (2006). Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell. 18, 3088-3105
11. Bräutigam, A., Hoffmann-Benning, S., and Weber, A.P.M. (2008a). Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol. 148, 568-579
12. Bräutigam, A., Shrestha, R.P., Whitten, D., Wilkerson, C.G., Carr, K.M., Froehlich, J.E., and Weber, A.P.M. (2008b). Comparison of the use of a species-specific database generated by pyrosequencing with databases from related species for proteome analysis of pea chloroplast envelopes. J. Biotechnol. 136, 44-53
13. Cheng, Z.G., Sattler, S., Maeda, H., Sakuragi, Y., Bryant, D.A., and DellaPenna, D. (2003). Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell. 15, 2343-2356
14. Cline, K., and Dabney-Smith, C. (2008). Plastid protein import and sorting: different paths to the same compartments. Curr. Opin. Plant Biol. 11, 585-592
15. Corbesier, L., Bernier, G., and Perilleux, C. (2002). C:N ratio increases in the phloem sap during floral transition of the long-day plants Sinapis alba and Arabidopsis thaliana. Plant Cell Physiol. 43, 684-688
16. Crisp, P., Walkey, D.G.A., Bellman, E., and Roberts, E. (1975). Mutation affecting curd color in cauliflower (Brassica oleracea L Var Botrytis Dc). Euphytica. 24, 173-176
17. Di Cola, A., Bailey, S., and Robinson, C. (2005). The thylakoid Delta pH/Delta Psi are not required for the initial stages of Tatdependent protein transport in tobacco protoplasts. J. Biol. Chem. 280, 41165-41170
18. Dietz, K.J., Horling, F., Konig, J., and Baier, M. (2002). The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. J. Exp. Bot. 53, 1321-1329
19. Douce, R., and Joyard, J. (1979). Isolation and properties of the envelope of spinach chloroplasts. In Plant Organelles, Vol.9, Reid, G., ed. (Chichester, UK: Ellis Horwood), pp. 47-59
20. Eichacker, L.A., Granvogl, B., Mirus, O., Muller, B.C., Miess, C., and Schleiff, E. (2004). Hiding behind hydrophobicity: transmembrane segments in mass spectrometry. J. Biol. Chem. 279, 50915-50922
21. Eicks, M., Maurino, V., Knappe, S., Flügge, U.I., and Fischer, K. (2002). The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 128, 512-522
22. Emes, M.J., and Neuhaus, H.E. (1997). Metabolism and transport in non-photosynthetic plastids. J. Exp. Bot. 48, 1995-2005
23. Ferro, M., Salvi, D., Bugiere, S., Miras, S., Kowalski, D., 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
24. 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. U S A. 99, 11487-11492
25. Finazzi, G., Chasen, C., Wollman, F.A., and De Vitry, C. (2003). Thylakoid targeting of Tat passenger proteins shows no Delta pH dependence in vivo. EMBO J. 22, 807-815
26. Fischer, K., and Weber, A. (2002). Transport of carbon in non-green plastids. Trends Plant Sci. 7, 345-351
27. Fischer, K., Kämmerer, B., Gutensohn, M., Arbinger, B., Weber, A., Häusler, R.E., and Flügge, U.I. (1997). A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell. 9, 453-462
28. Flügge,U.I., andHeldt,H.W. (1984). The phosphate-triose phosphatephosphoglycerate translocator of the chloroplast. Trends Biochem. Sci. 9, 530-533
29. Flügge, U.I., Häusler, R.E., Ludewig, F., and Fischer, K. (2003). Functional genomics of phosphate antiport systems of plastids. Physiol. Plant. 118, 475-482
30. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q., and Van Wijk, K.J. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell. 16, 478-499 (Pubitemid 38192704)
31. 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. Prot. Res. 2, 413-425
32. Goetze, T.A., Philippar, K., Ilkavets, I., Soll, J., andWagner, R. (2006). OEP37 is a new member of the chloroplast outer membrane ion channels. J. Biol. Chem. 281, 17989-17998
33. Guo, B., Jin, Y., Wussler, C., Blancaflor, E.B., Motes, C.M., and Versaw, W.K. (2008). Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177, 889-898
34. Häusler, R.E., Schlieben, N.H., and Flügge, U.I. (2000). Control of carbon partitioning and photosynthesis by the triose phosphate/ phosphate translocator in transgenic tobacco plants (Nicotiana tabacum). II. Assessment of control coefficients of the triose phosphate/phosphate translocator. Planta. 210, 383-390
35. Heineke, D., Riens, B., Grosse, H., Hoferichter, P., Peter, U., Flügge, U.I., and Heldt, H.W. (1991). Redox transfer across the inner chloroplast envelope membrane. Plant Physiol. 95, 1131-1137
36. 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
37. Ishihara, S., Takabayashi, A., Ido, K., Endo, T., Ifuku, K., and 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
38. Ivanova, Y., Smith, M.D., Chen, K.H., and Schnell, D.J. (2004). Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell. 15, 3379-3392
39. Jackson-Constan, D., and Keegstra, K. (2001). Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol. 125, 1567-1576
40. Jarvis, P., and Robinson, C. (2004). Mechanisms of protein import and routing in chloroplasts. Curr. Biol. 14, R1064-R1077
41. Journet, E.P., and Douce, R. (1985). Enzymic capacities of purified cauliflower bud plastids for lipid-synthesis and carbohydratemetabolism. Plant Physiol. 79, 458-467
42. Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A., and Flügge, U.I. (1998). Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell. 10, 105-117
43. Kanervo, E., Singh, M., Suorsa, M., Paakkarinen, V., Aro, E., Battchikova, N., and Aro, E.M. (2008). Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49, 396-410
44. Keegstra, K., and Yousif, A.E. (1986). Isolation and characterization of chloroplast envelope membranes. Meth. Enzymol. 118, 316-325
45. Keller, A., Nesvizhskii, A.I., Kolker, E., and Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
46. Kessler, F., and Schnell, D.J. (2006). The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic. 7, 248-257
47. Kieffer, M., Fuller, M.P., and Jellings, A.J. (1998). Explaining curd and spear geometry in broccoli, cauliflower and 'romanesco': quantitative variation in activity of primary meristems. Planta. 206, 34-43
48. Kirchberger, S., Tjaden, J.H., and Neuhaus, E. (2008). Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J. 56, 51-63
49. Kirk, J.T.O., and Tilney-Bassett, R.A.E. (1978). The Plastids: Their Chemistry, Structure, Growth and Inheritance, revised 2nd edn (Amsterdam,NewYork,Oxford: Elsevier/North-Holland Biomedical Press)
50. Kleffmann, T., Hirsch-Hoffmann, M., Gruissem,W., and Baginsky, S. (2006). plprot: a comprehensive proteome database for different plastid types. Plant Cell Physiol. 47, 432-436
51. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354-362
52. Kleffmann, T., von Zychlinski, A., Russenberger, D., Hirsch- Hoffmann, M., Gehrig, P., Gruissem, W., and Baginsky, S. (2007). Proteome dynamics during plastid differentiation in rice. Plant Physiol. 143, 912-923
53. Knappe, S., Löttgert, T., Schneider, A., Voll, L., Flügge, U.I., and Fischer, K. (2003). Characterization of two functional phosphoenolpyruvate/ phosphate translocator (PPT) genes in Arabidopsis- AtPPT1 may be involved in the provision of signals for correct mesophyll development. Plant J. 36, 411-420
54. Kubis, S., et al. (2004). Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell. 16, 2059-2077
55. Küchler, M., Decker, S., Hormann, F., Soll, J., and Heins, L. (2002). Protein import into chloroplasts involves redox-regulated proteins. EMBO J. 21, 6136-6145 (Pubitemid 35415330)
56. Labate, J.A., Robertson, L.D., Baldo, A.M., and Bjorkman, T. (2006). Inflorescence identity gene alleles are poor predictors of inflorescence type in broccoli and cauliflower. J. Am. Soc. Hortic. Sci. 131, 667-673
57. Li, L.G., Tutone, A.F., Drummond, R.S.M., Gardner, R.C., and Luan, S. (2001). A novel family of magnesium transport genes in Arabidopsis. Plant Cell. 13, 2761-2775
58. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and Niyogi, K.K. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature. 403, 391-395
59. Loddenkötter, B., Kämmerer, B., Fischer, K., and Flügge, U.I. (1993). Expression of the functional mature chloroplast triose phosphate translocator in yeast internal membranes and purification of the histidine-tagged protein by a single metal-affinity chromatography step. Proc. Natl Acad. Sci. U S A. 90, 2155-2159
60. Lonosky, P.M., Zhang, X.S., Honavar, V.G., Dobbs, D.L., Fu, A., and Rodermel, S.R. (2004). A proteomic analysis of maize chloroplast biogenesis. Plant Physiol. 134, 560-574
61. Lu, B.B., Xu, C.C., Awai, K., Jones, A.D., and Benning, C. (2007). A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J. Biol. Chem. 282, 35945-35953
62. Lu, S., et al. (2006). The cauliflower or gene encodes a DnaJ cysteinerich domain-containing protein that mediates high levels of betacarotene accumulation. Plant Cell. 18, 3594-3605
63. Martens, L., Hermjakob, H., Jones, P., Adamski, M., Taylor, C., States, D., Gevaert, K., Vandekerckhove, J., and Apweiler, R. (2005). PRIDE: the proteomics identifications database. Proteomics. 5, 3537-3545
64. Maser, P., et al. (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126, 1646-1667
65. Murcha, M.W., Elhafez, D., Lister, R., Tonti-Filippini, J., Baumgartner, M., Philippar, K., Carrie, C., Mokranjac, D., Soll, J., and Whelan, J. (2007). Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol. 143, 199-212
66. Neuhaus, H.E., and Emes, M.J. (2000). Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 111-140
67. Neuhaus, H.E., Thom, E., Möhlmann, T., Steup, M., and Kampfenkel, K. (1997). Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J. 11, 73-82
68. Peltier, J.B., et al. (2002). Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell. 14, 211-236
69. 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, 319-341
70. Peltier, J.B., Ytterberg, A.J., Sun, Q., and Van Wijk, K.J. (2004). New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J. Biol. Chem. 279, 49367-49383 (Pubitemid 39625823)
71. Picault, N., Hodges, M., Paimieri, L., and Palmieri, F. (2004). The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci. 9, 138-146
72. Picault, N., Palmieri, L., Pisano, I., Hodges, M., and Palmieri, F. (2002). Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria: bacterial expression, reconstitution, functional characterization, and tissue distribution. J. Biol. Chem. 277, 24204-24211 (Pubitemid 34951936)
73. Pohlmeyer, K., Soll, J., Grimm, R., Hill, K., and Wagner, R. (1998). A high-conductance solute channel in the chloroplastic outer envelope from pea. Plant Cell. 10, 1207-1216
74. Pohlmeyer, K., Soll, J., Steinkamp, T., Hinnah, S., and Wagner, R. (1997). Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proc. Natl Acad. Sci U S A. 94, 9504-9509
75. Reinhold, T., et al. (2007). Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage. Plant J. 50, 293-304
76. Reiser, J., Linka, N., Lemke, L., Jeblick,W., and Neuhaus, H.E. (2004). Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis. Plant Physiol. 136, 3524-3536
77. Renne, P., Dressen, U., Hebbeker, U., Hille, D., Flügge, U.I., Westhoff, P., and Weber, A.P.M. (2003). The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J. 35, 316-331
78. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506
79. Schnell, D.J. (2000). Functions and origins of the chloroplast protein-import machinery. In Molecular Trafficking, Bernstein P., ed. (New York: Portland Press) Vol.36 47-59
80. Schünemann, D. (2007). Mechanisms of protein import into thylakoids of chloroplasts. Biol. Chem. 388, 907-915
81. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flügge, U.I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26
82. Seigneurin-Berny, D., Rolland, N., Garin, J., and Joyard, J. (1999). Technical Advance: Differential extraction of hydrophobic proteins fromchloroplast envelopemembranes: a subcellular-specific proteomic approach to identify rare intrinsic membrane proteins. Plant J. 19, 217-228
83. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
84. Smith, L.B., and King, G.J. (2000). The distribution of BoCAL-a alleles in Brassica oleracea is consistent with a genetic model for curd development and domestication of the cauliflower. Mol. Breed. 6, 603-613
85. Soll, J., and Schleiff, E. (2004). Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198-208
86. Stengel, A., Benz, P., Balsera, M., Soll, J., and Bölter, B. (2008). TIC62 redox-regulated translocon composition and dynamics. J. Biol. Chem. 283, 6656-6667
87. Stengel, A., Soll, J., and Bölter, B. (2007). Protein import into chloroplasts: new aspects of a well-known topic. Biol. Chem. 388, 765-772
88. Sugiyama, N., Nakagami, H., Mochida, K., Daudi, A., Tomita, M., Shirasu, K., and Ishihama, Y. (2008). Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol. Syst. Biol. 4
89. Swarbreck, D., et al. (2008). The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucl. Acids. Res. 36, D1009-D1014
90. Takabatake, R., Hata, S., Taniguchi, M., Kouchi, H., Sugiyama, T., and Izui, K. (1999). Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice, and Arabidopsis. Plant Mol. Biol. 40, 479-486
91. Taniguchi, M., Taniguchi, Y., Kawasaki, M., Takeda, S., Kato, T., Sato, S., Tahata, S., Miyake, H., and Sugiyama, T. (2002). Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant Cell Physiol. 43, 706-717
92. Theg, S.M., Cline, K., Finazzi, G., and Wollman, F.A. (2005). The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10, 153-154
93. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., and Stitt, M. (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939
94. Thuswaldner, S., et al. (2007). Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J. Biol. Chem. 282, 8848-8859
95. Voll, L.M., Häusler, R.E., Hecker, R., Weber, A.P.M., Weissenböck, G., Fiene, G., Waffenschmidt, S., and Flügge, U.I. (2003). The phenotype of the Arabidopsis cue1 mutant is not simply caused by a general restriction of the shikimate pathway. Plant J. 36, 301
96. von Zychlinski, A., Kleffmann, T., Krishnamurthy, N., Sjolander, K., Baginsky, S., and Gruissem,W. (2005). Proteome analysis of the rice etioplast: metabolic and regulatory networks and novel protein functions. Mol. Cell. Proteomics. 4, 1072-1084
97. Wakao, S., and Benning, C. (2005).Genome-wide analysis of glucose- 6-phosphate dehydrogenases in Arabidopsis. Plant J. 41, 243-256
98. Wakao, S., Andre, C., and Benning, C. (2008). Functional analyses of cytosolic glucose-6-phosphate dehydrogenases and their contribution to seed oil accumulation in Arabidopsis. Plant Physiol. 146, 277-288
99. Weber, A., and Flügge, U.I. (2002). Interaction of cytosolic and plastidic nitrogen metabolism in plants. J. Exp. Bot. 53, 865-874
100. Weber, A., Menzlaff, E., Arbinger, B., Gutensohn, M., Eckerskorn, C., and Flügge, U.I. (1995). The 2-oxoglutarate/ malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry. 34, 2621-2627
101. Weber, A.P.M., Schwacke, R., and Flügge, U.I. (2005). Solute transporters of the plastid envelope membrane. Ann. Rev. Plant Biol. 56, 133-164
102. Weibull, J., and Melin, G. (1990). Free amino-acid content of phloem sap from brassica plants in relation to performance of Lipaphis erysimi (Hemiptera, Aphididae). Ann. Appl. Biol. 116, 417-423
103. Xu, C.C., Fan, J., Froehlich, J.E., Awai, K., and Benning, C. (2005). Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell. 17, 3094-3110
104. Zhu, X.L., Shaw, P.N., Pritchard, J., Newbury, J., Hunt, E.J., and Barrett, D.A. (2005). Amino acid analysis by micellar electrokinetic chromatography with laser-induced fluorescence detection: application to nanolitre-volume biological samples from Arabidopsis thaliana and Myzus persicae. Electrophoresis. 26, 911-919
105. Zrenner, R., Stitt, M., Sonnewald, U., and Boldt, R. (2006). Pyrimidine and purine biosynthesis and degradation in plants. Ann. Rev. Plant Biol. 57, 805-836
106. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and Van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE. 3, e1994