Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues

References

• Sharkey TD. Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Revwalk 1985; 51:53 - 105
   Web of Science ®Google Scholar
• Walker DA, Sivak MN. Photosynthesis and phosphate: a cellular affair?. Trends Biochem Sci 1986; 11:176 - 179
   Web of Science ®Google Scholar
• Preiss J. Regulation of the biosynthesis and degradation of starch. Annu Rev Plant Physiol Plant Mol Biol 1982; 33:431 - 454
   Web of Science ®Google Scholar
• RuizPavón LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C. Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem 2008; 283:13520 - 13527
   PubMed Web of Science ®Google Scholar
• Knappe S, Flügge UI, Fischer K. Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol 2003; 131:1178 - 1190
   PubMed Web of Science ®Google Scholar
• Flügge UI, Fischer K, Gross A, Sebald W, Lottspeich F, Eckerskorn C. The triose phosphate-3-phosphoglycerate-phosphate translocator from spinach chloroplasts: nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO J 1989; 8:39 - 46
   PubMed Web of Science ®Google Scholar
• Eicks M, Maurino V, Knappe S, Flügge UI, Fischer K. The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol 2002; 128:512 - 522
   PubMed Web of Science ®Google Scholar
• Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Häusler RE, et al. A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 1997; 9:453 - 462
   PubMed Web of Science ®Google Scholar
• Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, et al. Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 1998; 10:105 - 117
   PubMed Web of Science ®Google Scholar
• Flügge UI. Functional genomics of phosphate antiport systems in plastids. Physiol Plantarum 2003; 118:475 - 482
   Web of Science ®Google Scholar
• Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M. Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 1999; 11:2153 - 2166
   PubMed Web of Science ®Google Scholar
• Versaw WK, Harrison MJ. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 2002; 14:1751 - 1766
   PubMed Web of Science ®Google Scholar
• Zhao L, Versaw WK, Liu J, Harrison MJ. A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and is located in the chloroplast envelope. New Phytol 2003; 157:291 - 302
   PubMed Web of Science ®Google Scholar
• Ferro M, Salvi D, Riviere-Rolland H, Vermat T, Seigneurin-Berny D, Grunwald D, et al. Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc Natl Acad Sci USA 2002; 99:11487 - 11492
   PubMed Web of Science ®Google Scholar
• Rausch C, Zimmermann P, Amrhein N, Bucher M. Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis. Plant J 2004; 39:13 - 28
   PubMed Web of Science ®Google Scholar
• Guo B, Jin Y, Wussler C, Blacaflor EB, Motes CM, Versaw WK. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 2008; 177:889 - 898
   PubMed Web of Science ®Google Scholar
• Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, et al. Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2003; 2:325 - 345
   PubMed Web of Science ®Google Scholar
• Roth C, Menzel G, Petetot JM, Rochat-Hacker S, Poirier Y. Characterization of a protein of the plastid inner envelope having homology to animal inorganic phosphate, chloride and organic-anion transporters. Planta 2004; 218:406 - 416
   PubMed Web of Science ®Google Scholar
• Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 1962; 15:473 - 497
   Web of Science ®Google Scholar
• Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998; 16:735 - 743
   PubMed Web of Science ®Google Scholar
• Jefferson RA, Kavanaugh TA, Bevan MW. GUS fusions: β-glucuronidase as a sensitive and versitile gene fusion marker in higher plants. EMBO J 1987; 6:3901 - 3907
   PubMed Web of Science ®Google Scholar
• Vitha S, Benes K, Phillips JP, Gartland KMA. Gartland KMA, Davey MR. Histochemical GUS analysis. Agrobacterium Protocols 1995; Totowa, NJ, USA Humana Press 185 - 193
   Google Scholar
• Steedman HF. Polyester wax; a new ribboning embedding medium for histology. Nature 1957; 179:1345
   PubMed Web of Science ®Google Scholar
• Schulz B, Frommer WB, Flügge UI, Hummel S, Fischer K, Willmitzer L. Expression of the triose phosphate translocator gene from potato is light dependent and restricted to green tissues. Mol Gen Genet 1993; 238:357 - 361
   PubMedGoogle Scholar
• Michael TP, McClung CR. Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiol 2002; 130:627 - 638
   PubMed Web of Science ®Google Scholar
• Wang Z-Y, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 1997; 9:491 - 507
   PubMed Web of Science ®Google Scholar
• Yuan Q, Ouyang S, Wang A, Zhu W, Maiti R, Lin H, et al. The institute for genomic research Osa1 rice genome annotation database. Plant Physiol 2005; 138:18 - 26
   PubMed Web of Science ®Google Scholar
• Moretti S, Armougom F, Wallace IM, Higgins DG, Jongeneel CV, Notredame C. The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res 2007; 35:W645 - W648
   PubMed Web of Science ®Google Scholar
• Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2007; 2:953 971
   PubMed Web of Science ®Google Scholar
• Chaw SM, Chang CC, Chen HL, Li WH. Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 2004; 58:424 - 441
   PubMed Web of Science ®Google Scholar
• Paterson AH, Bowers JE, Chapman BA. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 2004; 101:9903 - 9908
   PubMed Web of Science ®Google Scholar
• Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y. The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 2002; 99:13627 - 13632
   PubMed Web of Science ®Google Scholar
• Paszkowski U, Kroken S, Roux C, Briggs SP. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 2002; 99:13324 - 13329
   PubMed Web of Science ®Google Scholar
• Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C. The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 2007; 49:528 - 539
   PubMed Web of Science ®Google Scholar
• Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, et al. Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Bioch Biophys Acta 2007; 1767:500 - 508
   PubMed Web of Science ®Google Scholar
• Booij-James IS, Swegle WM, Edelman M, Mattoo AK. Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiol 2002; 130:2069 - 2075
   PubMed Web of Science ®Google Scholar
• Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, et al. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 2005; 309:630 - 633
   PubMed Web of Science ®Google Scholar
• Takizawa K, Kanazawa A, Kramer DM. Depletion of stromal Pi induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFo-CF1 ATP synthase. Plant Cell Environ 2008; 31:235 - 243
   PubMed Web of Science ®Google Scholar
• Usami T, Mochizuki N, Kondo M, Nishimura M, Nagatani A. Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light. Plant Cell Physiol 2004; 45:1798 - 1808
   PubMed Web of Science ®Google Scholar
• Fliege R, Flügge UI, Werdan K, Heldt HW. Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Bioch Biophys Acta 1978; 502:232 - 247
   PubMed Web of Science ®Google Scholar
• Barnes SA, Knight JS, Gray JC. Alteration of the amount of the chloroplast phosphate translocator in transgenic tobacco affects the distribution of assimilate between starch and sugar. Plant Physiol 1994; 106:1123 - 1129
   PubMed Web of Science ®Google Scholar
• Häusler RE, Schlieben NH, Schultz B, Flügge U. Compensation of the decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 1998; 204:366 - 376
   PubMed Web of Science ®Google Scholar
• Heineke D, Kruse A, Flügge U, Frommer WB, Riesmeier JW, Willmitzer L, et al. Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 1994; 193:174 - 180
   Web of Science ®Google Scholar
• Riesmeier JW, Flügge UI, Schulz B, Heineke D, Heldt HW, Willmitzer L, et al. Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 1993; 90:6160 - 6164
   PubMed Web of Science ®Google Scholar
• Schneider A, Häusler RE, Kolukisaoglu Ü, Kunze R, van der Graaff E, Schwacke R, et al. 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 2002; 32:685 - 699
   PubMed Web of Science ®Google Scholar
• Walters RG, Ibrahim DG, Horton P, Kruger NJ. A mutant of Arabidopsis lacking the triosephosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 2004; 135:891 - 906
   PubMed Web of Science ®Google Scholar
• Neuhaus HE, Emes MJ. Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 2000; 51:111 - 140
   PubMed Web of Science ®Google Scholar
• Neuhaus HE, Maass U. Unidirectional transport of orthophosphate across the envelope of isolated cauliflower-bud amyloplasts. Planta 1996; 198:542 - 548
   Web of Science ®Google Scholar
• Behnke HD. Plastids in sieve elements and their companion cells. Planta 1973; 110:321 - 328
   PubMed Web of Science ®Google Scholar
• Behnke HD. Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 1991; 3:167 - 182
   Google Scholar
• Lu H, McKnight TD. Tissue-specific expression of the beta-subunit of tryptophan synthase in Camptotheca acuminata, an indole alkaloid-producing plant. Plant Physiol 1999; 120:43 - 52
   PubMed Web of Science ®Google Scholar