Connecting the plastid: Transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism

Annual Review of Plant Biology

Volumn 62, Issue , 2011, Pages 53-77

  Weber, Andreas P M ^a   Linka, Nicole ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

chloroplast; endosymbiosis; envelope membrane; evolution; translocator

Indexed keywords

CARRIER PROTEIN; NUCLEOTIDE TRANSPORTER; PHOSPHATE TRANSPORTER; VEGETABLE PROTEIN;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CYTOSOL; INTRACELLULAR MEMBRANE; METABOLISM; PHYSIOLOGY; PLANT; PLASTID; RED ALGA;

CYTOSOL; INTRACELLULAR MEMBRANES; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; NUCLEOTIDE TRANSPORT PROTEINS; PHOSPHATE TRANSPORT PROTEINS; PLANT PROTEINS; PLANTS; PLASTIDS; RHODOPHYTA;

EUKARYOTA;

EID: 79955583888     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042110-103903     Document Type: Article

References (152)

1. Allen JF, Martin W. 2007. Evolutionary biology: out of thin air. Nature 445:610-12. (Pubitemid 46232875)
2. Aoki N, Kanai R. 1997. Reappraisal of the role of sodium in the light-dependent active transport of pyruvate into mesophyll chloroplasts of C4 plants. Plant Cell Physiol. 38:1217-25. (Pubitemid 127493249)
3. Aoki N, Ohnishi J, Kanai R. 1992. 2 different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants-a comparative study. Plant Cell Physiol. 33:805-9.
4. Ast M, Gruber A, Schmitz-Esser S, Neuhaus HE, Kroth PG, et al. 2009. Diatom plastids depend on nucleotide import from the cytosol. Proc. Natl. Acad. Sci. USA 106:3621-26.
5. Ball SG,MorellMK. 2003. From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu. Rev. Plant Biol. 54:207-33. (Pubitemid 37399993)
6. Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, et al. 2005. Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol. 137:460-74. (Pubitemid 43126677)
7. Bedhomme M, Hoffmann M, McCarthy EA, Gambonnet B, Moran RG, et al. 2005. Folate metabolism in plants: an Arabidopsis homolog of the mammalian mitochondrial folate transporter mediates folate import into chloroplasts. J. Biol. Chem. 280:34823-31. (Pubitemid 41504616)
8. Benning C. 2009. Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu. Rev. Cell Dev. Biol. 25:71-91.
9. Bjorn LO, Govindjee. 2009. The evolution of photosynthesis and chloroplasts. Curr. Sci. 96:1466-74.
10. Block MA, Douce R, Joyard J, Rolland N. 2007. Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth. Res. 92:225-44. (Pubitemid 47222261)
11. Borchert S, Harborth J, Scḧunemann D, Hoferichter P, Heldt HW. 1993. Studies of the enzymic capacities and transport properties of pea root plastids. Plant Physiol. 101:303-12.
12. Bouvier F, Linka N, Isner JC, Mutterer J,Weber APM, Camara B. 2006. Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell 18:3088-105. (Pubitemid 46013278)
13. Br̈autigam A, Hofmann-Benning S, Weber AP. 2008. 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. 148:568-79. (Pubitemid 352847591)
14. Br̈autigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, et al. 2011. An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiol. 155:43-48.
15. Br̈autigam A, Shrestha RP, Whitten D,Wilkerson CG, Carr KM, et al. 2008. Low-coverage massively parallel pyrosequencing of cDNAs enables proteomics in non-model species: comparison of a speciesspecific database generated by pyrosequencing with databases from related species for proteome analysis of pea chloroplast envelopes. J. Biotechnol. 136:44-53.
16. Br̈autigamA,WeberAPM.2009. Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Mol. Plant 2:1247-61.
17. Br̈autigam A,Weber APM. 2011. Transport processes-connecting the reactions of C4 photosynthesis. In C4 Photosynthesis and Related CO2 Concentrating Mechanisms, ed. RF Sage, AS Raghavendra, pp. 199-219 Berlin: Springer.
18. Brooks CF, Johnsen H, van Dooren GG, Muthalagi M, Lin SS, et al. 2010. The toxoplasma apicoplast phosphate translocator links cytosolic and apicoplast metabolism and is essential for parasite survival. Cell Host Microbe 7:62-73.
19. Brownell PF, Crossland CJ. 1972. Requirement for sodium as a micronutrient by species having C4 dicarboxylic photosynthetic pathway. Plant Physiol. 49:794-97.
20. Butowt R, Granot D, Rodriguez-Garcia MI. 2003. A putative plastidic glucose translocator is expressed in heterotrophic tissues that do not contain starch, during olive (Olea europea L.) fruit ripening. Plant Cell Physiol. 44:1152-61. (Pubitemid 37519072)
21. Cavalier-Smith T. 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5:174-82. (Pubitemid 30192275)
22. ColleoniC, Linka M, Deschamps P,HandfordMG, Dupree P, et al. 2010. Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol. Biol. Evol. 27:2691-701.
23. Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, et al. 2008. Metabolic symbiosis and the birth of the plant kingdom. Mol. Biol. Evol. 25:536-48. (Pubitemid 351301909)
24. Deschamps P, Haferkamp I, Dauvillee D, Haebel S, Steup M, et al. 2006. Nature of the periplastidial pathway of starch synthesis in the cryptophyte Guillardia theta. Eukaryot. Cell 5:954-63. (Pubitemid 43895025)
25. Deschamps P,Haferkamp I, d'HulstC,Neuhaus HE, Ball SG. 2008. The relocation of starchmetabolism to chloroplasts: when, why and how. Trends Plant Sci. 13:574-82.
26. Deschamps P, Moreau H, Worden AZ, Dauvillee D, Ball SG. 2008. Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 178:2373-87.
27. Douce R, Joyard J. 1981. Does the plastid envelope derive from the endoplasmic reticulum? Trends Biochem. Sci. 6:237-39.
28. Duy D, Soll J, Philippar K. 2007. Solute channels of the outer membrane: from bacteria to chloroplasts. Biol. Chem. 388:879-89. (Pubitemid 47258542)
29. EicksM,Maurino V, Knappe S, Fl̈ugge UI, FischerK. 2002. The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 128:512-22. (Pubitemid 34190866)
30. Embley TM, MartinW. 2006. Eukaryotic evolution, changes and challenges. Nature 440:623-30.
31. Falkowski PG, Godfrey LV. 2008. Electrons, life and the evolution of Earth's oxygen cycle. Philos. Trans. R. Soc. Lond. B. 363:2705-16. (Pubitemid 351989775)
32. Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, et al. 2003. Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell Proteomics 2:325-45.
33. Ferro M, Salvi D, Riviere-Rolland H, Vermat T, Seigneurin-Berny D, et al. 2002. Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc. Natl. Acad. Sci. USA 99:11487-92. (Pubitemid 34924952)
34. Fischer K, Kammerer N, Gutensohn M, Arbinger B, Weber A, et al. 1997. A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9:453-62. (Pubitemid 27176830)
35. Fleige T, FischerK, Ferguson DJ, GrossU, Bohne W. 2007. Carbohydrate metabolism in the Toxoplasma gondii apicoplast: localization of three glycolytic isoenzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryot. Cell 6:984-96. (Pubitemid 46983298)
36. Fliege R, Fl̈ugge UI, Werdan K, Heldt HW. 1978. Specific transport of inorganic phosphate, 3- phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim. Biophys. Acta 502:232-47. (Pubitemid 8326466)
37. Fl̈ugge UI. 1995. Phosphate translocation in the regulation of photosynthesis. J. Exp. Bot. 46:1317-23.
38. Fl̈ugge UI. 1999. Phosphate translocators in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:27-45.
39. Fl̈ugge UI, GaoW. 2005. Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol. 7:91-97.
40. Fl̈ugge UI,Ḧausler RE, Ludewig F, Fischer K. 2003. Functional genomics of phosphate antiport systems of plastids. Physiol. Plant. 118:475-82. (Pubitemid 36990441)
41. Fl̈ugge UI, Heldt HW. 1984. The phosphate-triose phosphate- phosphoglycerate translocator of the chloroplast. Trends Biochem. Sci. 9:530-33.
42. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, et al. 2008. ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Res. 36:D553-56. (Pubitemid 351149784)
43. Garcia O, Bouige P, ForestierC,Dassa E. 2004. Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J. Mol. Biol. 343:249-65. (Pubitemid 39277462)
44. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
45. Gigolashvili T, Yatusevich R, Rollwitz I, Humphry M, Gershenzon J, Fl̈ugge UI. 2009. The plastidic bile acid transporter 5 is required for the biosynthesis ofmethionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21:1813-29.
46. Haferkamp I. 2007. The diverse members of the mitochondrial carrier family in plants. FEBS Lett. 581:2375-79. (Pubitemid 46726294)
47. Haferkamp I, Deschamps P, Ast M, Jeblick W, Maier U, et al. 2006. Molecular and biochemical analysis of periplastidial starch metabolism in the cryptophyte Guillardia theta. Eukaryot. Cell 5:964-71. (Pubitemid 43895026)
48. Hanson AD, Gage DA, Shachar-Hill Y. 2000. Plant one-carbon metabolism and its engineering. Trends Plant Sci. 5:206-13. (Pubitemid 30300844)
49. Hanson AD, Gregory JF III. 2002. Synthesis and turnover of folates in plants. Curr. Opin. Plant Biol. 5:244-49. (Pubitemid 34452072)
50. Hattenbach A, Muller-Rober B, Nast G, Heineke D. 1997. Antisense repression of both ADP-glucose pyrophosphorylase and triose phosphate translocator modifies carbohydrate partitioning in potato leaves. Plant Physiol. 115:471-75. (Pubitemid 28395294)
51. Ḧausler RE, Baur B, Scharte J, Teichmann T, Eicks M, et al. 2000. Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum. Plant J. 24:285-96.
52. Ḧausler RE, Geimer S, Kunz HH, Schmitz J, D̈ormann P, et al. 2009. Chlororespiration and grana hyperstacking: how an Arabidopsis double mutant can survive despite defects in starch biosynthesis and daily carbon export from chloroplasts. Plant Physiol. 149:515-33.
53. Ḧausler RE, Schlieben NH, Fl̈ugge UI. 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 210:383-90.
54. Ḧausler RE, Schlieben NH, Nicolay P, Fischer K, Fischer KL, Fl̈ugge UI. 2000. Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants (Nicotiana tabacum L.). I. Comparative physiological analysis of tobacco plants with antisense repression and overexpression of the triose phosphate/phosphate translocator. Planta 210:371-82.
55. HeinekeD, Kruse A, Fl̈ugge UI, FrommerWB, Riesmeier JW, et al. 1994. Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 193:174-80. (Pubitemid 2053636)
56. Herrmann KM. 1995. The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7:907-19.
57. Herrmann KM, Weaver LM. 1999. The shikimate pathway. Annu. Rev. Plant Phys. 50:473-503. (Pubitemid 129491971)
58. Imamura S, Terashita M, Ohnuma M, Maruyama S, Minoda A, et al. 2010. Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga Cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Plant Cell Physiol. 51:707-17.
59. Joyard J, Teyssier E, MiegeC, Berny-SeigneurinD,Marechal E, et al. 1998. The biochemical machinery of plastid envelope membranes. Plant Physiol. 118:715-23. (Pubitemid 128652996)
60. Kammerer B, Fischer K, Hilpert B, Schubert S, GutensohnM, et al. 1998. Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10:105-17. (Pubitemid 28309817)
61. Keeling PJ. 2010. The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. Lond. B 365:729-48.
62. Kirchberger S, Leroch M, Huynen MA, Wahl M, Neuhaus HE, Tjaden J. 2007. Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays. J. Biol. Chem. 282:22481-91. (Pubitemid 47267347)
63. Kirchberger S, Tjaden J, Neuhaus HE. 2008. Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J. 56:51-63.
64. Klaus SM, Kunji ER, Bozzo GG, Noiriel A, de la Garza RD, et al. 2005. Higher plant plastids and cyanobacteria have folate carriers related to those of trypanosomatids. J. Biol. Chem. 280:38457-63. (Pubitemid 43853743)
65. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, et al. 2001. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126:811-25. (Pubitemid 32566630)
66. Kloos K, Schlichting R, ZimmerW, Bothe H. 1993. Glutamine and glutamate transport in Cyanophora paradoxa. Bot. Acta 106: 435-40. (Pubitemid 2006120)
67. Kromer S, Scheibe R. 1996. Function of the chloroplastic malate valve for respiration during photosynthesis. Biochem. Soc. Trans. 24:761-66. (Pubitemid 26306294)
68. KrugerNJ, von SchaewenA. 2003. The oxidative pentose phosphate pathway: structure and organisation. Curr. Opin. Plant Biol. 6:236-46. (Pubitemid 36704509)
69. Li HM, Chiu CC. 2010. Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61:157-80.
70. Lim L, Linka M, Mullin KA, Weber AP, McFadden GI. 2010. The carbon and energy sources of the non-photosynthetic plastid in the malaria parasite. FEBS Lett. 584:549-54.
71. Lim L, McFadden GI. 2010. The evolution, metabolism and functions of the apicoplast. Philos. Trans. R. Soc. Lond. B 365:749-63.
72. Linka M, Jamai A, Weber AP. 2008. Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae. Plant Physiol. 148:1487-96. (Pubitemid 352847513)
73. Linka N, Hurka H, Lang BF, Burger G, Winkler HH, et al. 2003. Phylogenetic relationships of nonmitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306:27-35. (Pubitemid 36351392)
74. Linka N, Theodoulou FL, Haslam RP, Linka M, Napier JA, et al. 2008. Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20:3241-57.
75. Linka N,Weber APM. 2010. Intracellular metabolite transporters in plants. Mol. Plant 3:21-53.
76. Loddenk̈otter B, Kammerer B, Fischer K, Fl̈ugge UI. 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. USA 90:2155-59.
77. Ma Y, Jakowitsch J, Maier TL, BayerMG,M̈uller NE, et al. 2001. ATP citrate lyase in the glaucocystophyte alga Cyanophora paradoxa is a cytosolic enzyme: characterisation of the gene for the large subunit at the cDNA and genomic levels. Mol. Genet. Genomics 266:231-38. (Pubitemid 32938417)
78. MajeranW, Cai Y, SunQ, van Wijk KJ. 2005. Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17:3111-40.
79. Majeran W, van Wijk KJ. 2009. Cell-type-specific differentiation of chloroplasts in C4 plants. Trends Plant Sci. 14:100-9.
80. Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ. 2008. Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol. Cell Proteomics 7:1609-38.
81. Mangelsdorf PC. 1926. The genetics and morphology of some endosperm characters in maize. Conn. Agric. Exp. Stn. Bull. 279:509-614.
82. Martin W, Koonin EV. 2006. Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41-45. (Pubitemid 43336261)
83. Meierhoff K, Westhoff P. 1993. Differential biogenesis of photosystem-II in mesophyll and bundlesheath cells of monocotyledonous NADP-malic enzyme-type C4 plants-the nonstoichiometric abundance of the subunits of photosystem-II in the bundle-sheath chloroplasts and the translational activity of the plastome-encoded genes. Planta 191:23-33.
84. Moustafa A, Reyes-Prieto A, Bhattacharya D. 2008. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE 3:e2205.
85. Mullin KA, Lim L, Ralph SA, Spurck TP, Handman E, McFadden GI. 2006. Membrane transporters in the relict plastid of malaria parasites. Proc. Natl. Acad. Sci. USA 103:9572-77. (Pubitemid 43955866)
86. Neuhaus HE, Wagner R. 2000. Solute pores, ion channels, and metabolite transporters in the outer and inner envelope membranes of higher plant plastids. Biochim. Biophys. Acta 1465:307-23. (Pubitemid 30169076)
87. NiewiadomskiP,Knappe S, Geimer S, FischerK, SchulzB, et al. 2005.TheArabidopsis plastidic glucose 6- phosphate/phosphate translocator GPT1 is essential for pollenmaturation and embryo sac development. Plant Cell 17:760-75. (Pubitemid 43138219)
88. Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC. 2004. A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87-89. (Pubitemid 38055776)
89. Oesterhelt C, Klocke S, Holtgrefe S, Linke V, Weber AP, Scheibe R. 2007. Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell Physiol. 48:1359-73. (Pubitemid 47428927)
90. Palmieri F, Rieder B, Ventrella A, Blanco E, Do PT, et al. 2009. Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD+ carrier proteins. J. Biol. Chem. 284:31249-59.
91. Palmieri L, Arrigoni R, Blanco E, Carrari F, Zanor MI, et al. 2006. Molecular identification of an Arabidopsis S-adenosylmethionine transporter. Analysis of organ distribution, bacterial expression, reconstitution into liposomes, and functional characterization. Plant Physiol. 142:855-65. (Pubitemid 44764614)
92. Picault N, Hodges M, Palmieri L, Palmieri F. 2004. The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci. 9:138-46. (Pubitemid 38300260)
93. Plancke C, Colleoni C, Deschamps P, Dauvillee D,Nakamura Y, et al. 2008. Pathway of cytosolic starch synthesis in the model glaucophyte Cyanophora paradoxa. Eukaryot. Cell 7:247-57. (Pubitemid 351959691)
94. Prabhakar V, LottgertT,Gigolashvili T, Bell K, Fl̈ugge UI, Hausler RE. 2009. Molecular and functional characterization of the plastid-localized Phosphoenolpyruvate enolase (ENO1) from Arabidopsis thaliana. FEBS Lett. 583:983-91.
95. Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, et al. 2004. Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J. Biol. Chem. 279:22548-57. (Pubitemid 38679455)
96. Reichert A, Dennes A, Vetter S, Scheibe R. 2003. Chloroplast fructose 1,6-bisphosphatase with changed redox modulation: comparison of the Galdieria enzyme with cysteine mutants from spinach. Biochim. Biophys. Acta 1645:212-17. (Pubitemid 38229280)
97. Reinhold T, Alawady A, Grimm B, Beran KC, Jahns P, et al. 2007. Limited nocturnal ATP import into Arabidopsis chloroplasts causes photooxidative damage. Plant J. 50:293-304. (Pubitemid 46624137)
98. Reiser J, Linka N, Lemke L, Jeblick W, Neuhaus HE. 2004. Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis. Plant Physiol. 136:3524-36. (Pubitemid 41075792)
99. Renne P, DressenU,HebbekerU,Hille D, Fl̈ugge UI, et al. 2003. The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J. 35:316-31. (Pubitemid 36990635)
100. Reumann S,Weber APM. 2006. Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled-others remain. Biochim. Biophys. Acta 1763:1496-510. (Pubitemid 44880482)
101. Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, et al. 2006. Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot. Cell 5:1517-31. (Pubitemid 44423648)
102. Riebeseel E, Hausler RE, Radchuk R,Meitzel T, HajirezaeiMR, et al. 2010. The 2-oxoglutarate/malate translocator mediates amino acid and storage protein biosynthesis in pea embryos. Plant J. 61:350-63.
103. Riesmeier JW, Fl̈ugge UI, Schulz B, Heineke D, Heldt HW, et al. 1993. Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc. Natl. Acad. Sci. USA 90:6160-64. (Pubitemid 23191474)
104. Roje S. 2006. S-adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686-98. (Pubitemid 44233619)
105. Rolletschek H, Nguyen TH, Hausler RE, Rutten T, Gobel C, et al. 2007. Antisense inhibition of the plastidial glucose-6-phosphate/phosphate translocator in Vicia seeds shifts cellular differentiation and promotes protein storage. Plant J. 51:468-84. (Pubitemid 47106548)
106. Ruuska SA, Schwender J, Ohlrogge JB. 2004. The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 136:2700-9. (Pubitemid 41071309)
107. Sahr T, Ravanel S, Basset G, Nichols BP, Hanson AD, Rebeille F. 2006. Folate synthesis in plants: purification, kinetic properties, and inhibition of aminodeoxychorismate synthase. Biochem. J. 396:157-62. (Pubitemid 43764507)
108. Sato N, Moriyama T. 2007. Genomic and biochemical analysis of lipid biosynthesis in the unicellular rhodophyte Cyanidioschyzon merolae: lack of a plastidic desaturation pathway results in the coupled pathway of galactolipid synthesis. Eukaryot. Cell 6:1006-17. (Pubitemid 46983300)
109. Sawada Y, Toyooka K, Kuwahara A, Sakata A, Nagano M, et al. 2009. Arabidopsis bile acid:sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol. 50:1579-86.
110. Scḧafer G, Heber U, Heldt HW. 1977. Glucose transport into intact spinach chloroplasts. Plant Physiol. 60:286-89.
111. Schlichting R, BotheH. 1993. The cyanelles (organelles of a low evolutionary scale) possess a phosphatetranslocator and a glucose-carrier in Cyanophora paradoxa. Bot. Acta 106:428-34. (Pubitemid 2006117)
112. Schlichting R, Zimmer W, Bothe H. 1990. Exchange of metabolites in Cyanophora paradoxa and its cyanelles. Bot. Acta 103: 392-98.
113. Schmid J, Amrhein N. 1995. Molecular organization of the shikimate pathway in higher plants. Phytochemistry 39:737-49.
114. Schmitz-Esser S, Linka N, Collingro A, Beier CL, Neuhaus HE, et al. 2004. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 186:683-91. (Pubitemid 38129645)
115. Schneider A,Ḧausler RE, KolukisaogluU, Kunze R, van der Graaff E, et al. 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. 32:685-99. (Pubitemid 36010874)
116. Schneidereit J, Ḧausler RE, Fiene G, Kaiser WM, Weber APM. 2006. Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator DiT1 at the interface between carbon and nitrogen metabolism. Plant J. 45:206-24. (Pubitemid 43382055)
117. Schulz B, FrommerWB, Fl̈ugge UI, Hummel S, Fischer K, Willmitzer L. 1993. Expression of the triose phosphate translocator gene from potato is light dependent and restricted to green tissues. Mol. Gen. Genet. 238:357-61. (Pubitemid 23134997)
118. Schwender J,Goffman F, Ohlrogge JB, Shachar-Hill Y. 2004. Rubisco without theCalvin cycle improves the carbon efficiency of developing green seeds. Nature 432:779-82. (Pubitemid 39656300)
119. Sharkey TD, Laporte M, Lu Y, Weise S, Weber APM. 2004. Engineering plants for elevated CO2: a relationship between starch degradation and sugar sensing. Plant Biol. 6:280-88. (Pubitemid 38708666)
120. Shen J, Ren X, Cao R, Liu J, Gong Z. 2009. Transcriptional gene silencing mediated by a plastid inner envelope phosphoenolpyruvate/phosphate translocator CUE1 in Arabidopsis. Plant Physiol. 150:1990-96.
121. Smith AM, Zeeman SC, Smith SM. 2005. Starch degradation. Annu. Rev. Plant Biol. 56:73-98.
122. 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 101:1409-14. (Pubitemid 38182702)
123. Stitt M, Ap Rees T. 1979. Capacities of pea chloroplasts to catalyse the oxidative pentose phosphate and glycolysis. Phytochemistry 18:1905-11.
124. Streatfield SJ, Weber A, Kinsman EA, Ḧausler RE, Li JM, et al. 1999. The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastiddependent nuclear gene expression. Plant Cell 11:1609-21.
125. Strittmatter P, Soll J, B̈olter B. 2010. The chloroplast protein import machinery: a review. Methods Mol. Biol. 619:307-21.
126. Sullivan TD, Strelow LI, Illingworth CA, Phillips RL, Nelson OEJ. 1991. Analysis of the maize brittle-1 alleles and a defective suppressor-mutator induced mutable allele. Plant Cell 3:1337-48. (Pubitemid 21913677)
127. Taniguchi M, Taniguchi Y, Kawasaki M, Takeda S, Kato T, et al. 2002. Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant Cell Physiol. 43:706-17. (Pubitemid 34877885)
128. Taniguchi Y, Nagasaki J, Kawasaki M, Miyake H, Sugiyama T, Taniguchi M. 2004. Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. Plant Cell Physiol. 45:187-200. (Pubitemid 38318824)
129. Thuswaldner S, Lagerstedt JO, Rojas-St ̈utzM, Bouhidel K, DerC, et al. 2007. Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J. Biol. Chem. 282:8848-59. (Pubitemid 47093511)
130. Tjaden J, M̈ohlmann T, Kampfenkel K, Henrich G, Neuhaus HE. 1998. Altered plastidic ATP/ADPtransporter activity influences potato (Solanum tuberosum L.) tuber morphology, yield and composition of tuber starch. Plant J. 16:531-40.
131. Tjaden J, WinklerHH,Schẅoppe C, van der Laan M,M̈ohlmannT, Neuhaus HE. 1999.Twonucleotide transport proteins from Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181:1196-202. (Pubitemid 29119558)
132. Trentmann O, Horn M, van Scheltinga AC, Neuhaus HE, Haferkamp I. 2007. Enlightening energy parasitism by analysis of an ATP/ADP transporter from Chlamydiae. PLoS Biol. 5:e231.
133. Trentmann O, Jung B, Neuhaus HE, Haferkamp I. 2008. Nonmitochondrial ATP/ADP transporters accept phosphate as third substrate. J. Biol. Chem. 283:36486-93.
134. Tyra HM, Linka M,Weber AP, Bhattacharya D. 2007. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 8:R212.
135. Viola R, Nyvall P, Pedersen M. 2001. The unique features of starch metabolism in red algae. Proc. R. Soc. Lond. B 268:1417-22. (Pubitemid 32625608)
136. Voll L, Ḧausler RE, Hecker R,Weber A, Weissenbock G, et al. 2003. The phenotype of the Arabidopsis cue1 mutant is not simply caused by a general restriction of the shikimate pathway. Plant J. 36:301-17. (Pubitemid 37436055)
137. von Caemmerer S, Furbank RT. 2003. The C4 pathway: an efficient CO2 pump. Photosynth. Res. 77:191-207.
138. Waller JC, Dhanoa PK, SchumannU,MullenRT, SneddenWA. 2010. Subcellular and tissue localization ofNADkinases from Arabidopsis: compartmentalization of de novoNADP biosynthesis. Planta 231:305-17.
139. Weber A, Fl̈ugge UI. 2002. Interaction of cytosolic and plastidic nitrogen metabolism in plants. J. Exp. Bot. 53:865-74. (Pubitemid 34287170)
140. Weber A, Menzlaff E, Arbinger B, Gutensohn M, Eckerskorn C, Fl̈ugge UI. 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 34:2621-27.
141. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, et al. 2000. Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12:787-801. (Pubitemid 30343588)
142. Weber APM, Linka M, Bhattacharya D. 2006. Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot. Cell 5:609-12.
143. Weber APM, Schwacke R, Fl̈ugge UI. 2005. Solute transporters of the plastid envelope membrane. Annu. Rev. Plant Biol. 56:133-64. (Pubitemid 40802406)
144. Weber APM, von Caemmerer S. 2010. Plastid transport and metabolism of C3 and C4 plants- comparative analysis and possible biotechnological exploitation. Curr. Opin. Plant Biol. 13:257-65.
145. Weber APM, Oesterhelt C, Gross W, Br̈autigam A, Imboden LA, et al. 2004. EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol. Biol. 55:17-32.
146. Weber APM, Schneidereit J, Voll LM. 2004. Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. J. Exp. Bot. 55:1231-44. (Pubitemid 38751756)
147. Wentz JB. 1926. Heritable characters of maize. XXVI. Concave. J. Hered. 17:327-29.
148. Winkler HH, Neuhaus HE. 1999. Non-mitochondrial ATP transport. Trends Biochem. Sci. 24:64-68. (Pubitemid 29346575)
149. Wolf YI, Aravind L, Koonin EV. 1999. Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 15:173-75. (Pubitemid 29217064)
150. Xiong J, Bauer CE. 2002. Complex evolution of photosynthesis. Annu. Rev. Plant Biol. 53:503-21. (Pubitemid 36257505)
151. Zhang L, Hausler RE, Greiten C, Hajirezaei MR, Haferkamp I, et al. 2008. Overriding the co-limiting import of carbon and energy into tuber amyloplasts increases the starch content and yield of transgenic potato plants. Plant Biotechnol. J. 6:453-64. (Pubitemid 351670272)
152. Zrenner R, Stitt M, Sonnewald U, Boldt R. 2006. Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57:805-36 (Pubitemid 44061046)