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BAT1, a bidirectional amino acid transporter in Arabidopsis

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Abstract

The Arabidopsis thaliana At2g01170 gene is annotated as a putative gamma amino butyric acid (GABA) permease based on its sequence similarity to a yeast GABA transporting gene (UGA4). A cDNA of At2g01170 was expressed in yeast and analyzed for amino acid transport activity. Both direct measurement of amino acid transport and yeast growth experiments demonstrated that the At2g01170 encoded-protein exhibits transport activity for alanine, arginine, glutamate and lysine, but not for GABA or proline. Significantly, unlike other amino acid transporters described in plants to date, At2g01170 displayed both export and import activity. Based on that observation, it was named bidirectional amino acid transporter 1 (BAT1). Sequence comparisons show BAT1 is not a member of any previously defined amino acid transporter family. It does share, however, several conserved protein domains found in a variety of prokaryotic and eukaryotic amino acid transporters, suggesting membership in an ancient family of transporters. BAT1 is a single copy gene in the Arabidopsis genome, and its mRNA is ubiquitously expressed in all organs. A transposon—GUS gene-trap insert in the BAT1 gene displays GUS localization in the vascular tissues (Dundar in Ann Appl Biol, 2009) suggesting BAT1 may function in amino acid export from the phloem into sink tissues.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Andre B, Hein C, Grenson M, Jauniaux JC (1993) Cloning and expression of the UGA4 gene coding for the Inducible GABA-specific transport protein of Saccharomyces cerevisiae. Mol Gen Genet 237:17–25

    Article  PubMed  CAS  Google Scholar 

  • Boulland JL, Rafiki A, Levy LM, Storm-Mathisen J, Chaudhry FA (2003) Highly differential expression of SN1, a bidirectional glutamine transporter, in astroglia and endothelium in the developing rat brain. Glia 41:260–275

    Article  PubMed  Google Scholar 

  • Breitkreuz KE, Shelp BJ, Fischer WN, Schwacke R, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284

    Article  PubMed  CAS  Google Scholar 

  • Bush DR (1993) Proton-coupled sugar and amino acid transporters in plants. Ann Rev Plant Physiol Plant Mol Biol 44:513–542

    Article  CAS  Google Scholar 

  • Bush DR (1999) Amino acid transport. In: Singh BK (ed) Plant amino acids. Marcel Dekker Inc., New York, pp 305–318

    Google Scholar 

  • Bush DR, Chiou TJ, Chen LS (1996) Molecular analysis of plant sugar and amino acid transporters. J Exp Bot 47:1205–1210

    CAS  Google Scholar 

  • Chen LS, Ortiz-Lopez A, Jung A, Bush DR (2001) ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol 125:1813–1820

    Article  PubMed  CAS  Google Scholar 

  • Cimprich P, Slavik J, Kotyk A (1995) Distribution of individual cytoplasmic pH values in a population of the yeast Saccharomyces cerevisiae. FEMS Microb Lett 130:245–251

    Article  CAS  Google Scholar 

  • Claros MG, von Heijne G (1994) TopPred II: an improved software for membrane protein structure predictions. Comp Appl Biosci 10:685–686

    PubMed  CAS  Google Scholar 

  • Dundar E (2009) Multiple GUS expression patterns of a single Arabidopsis gene. Ann Appl Biol 154:33–41

    Article  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195

    Article  Google Scholar 

  • Fischer WN, Loo DDF, Koch W, Ludewig U, Boorer KJ, Tegeder M, Rentsch D, Wright EM, Frommer WB (2002) Low and high affinity amino acid H+ -cotransporters for cellular import of neutral and charged amino acids. Plant J 29:717–731

    Article  PubMed  CAS  Google Scholar 

  • Frommer WB, Hummel S, Unseld M, Ninnemann O (1995) Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis. Proc Natl Acad Sci 92:12036–12040

    Article  PubMed  CAS  Google Scholar 

  • Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7:899–906

    Article  PubMed  CAS  Google Scholar 

  • Gessler A, Weber P, Schneider S, Rennenberg H (2003) Bidirectional exchange of amino compounds between phloem and xylem during long-distance transport in Norway spruce trees (Picea abies [L.] Karst). J Exp Bot 54:1389–1397

    Article  PubMed  CAS  Google Scholar 

  • Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus J-M, Rentsch D (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137:117–126

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hsu LC, Chiou TJ, Chen LS, Bush DR (1993) Cloning a plant amino acid transporter by functional complementation of a yeast amino acid transport mutant. Proc Natl Acad Sci 90:7441–7445

    Article  PubMed  CAS  Google Scholar 

  • Hutchings H, Stahmann KP, Roels S, Espeso EA, Timberlake WE, Arst HN, Tilburn J (1999) The multiply-regulated gabA gene encoding the GABA permease of Aspergillus nidulans: a score of exons. Mol Microb 32:557–568

    Article  CAS  Google Scholar 

  • Imai T, Ohno T (1995) Measurement of yeast intracellular pH by image processing and the change it undergoes during growth phase. J Biotech 38:165–172

    Article  CAS  Google Scholar 

  • Jack DL, Paulsen IT, JrMH Saier (2000) The amino acid/polyamine/organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microb 146:1797–1814

    CAS  Google Scholar 

  • Karagiannis J, Young PG (2001) Intracellular pH homeostasis during cell-cycle progression and growth state transition in Schizosaccharomyces pombe. J Cell Sci 114:2929–2941

    PubMed  CAS  Google Scholar 

  • Kottra G, Daniel H (2001) Bidirectional electrogenic transport of peptides by the proton-coupled carrier PEPT1 in Xenopus laevis oocytes: its asymmetry and symmetry. J Phsiol London 536:495–503

    Article  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56

    Article  CAS  Google Scholar 

  • Lee YT, Duggleby RG (2001) Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40:6836–6844

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Bush DR (2006) Expression and transcriptional regulation of amino acid transporters in plants. Amino Acids 30:113–120

    Article  PubMed  Google Scholar 

  • Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese-Scott C, Gonzales NR, Gwadz M, Hao L, He S, Hurwitz DI, Jackson JD, Ke Z, Krylov D, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Thanki N, Yamashita RA, Yin JJ, Bryant SH (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33:D192–D196

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese-Scott C, Gonzales NR, Gwadz M, Hao L, He S, Hurwitz DI, Jackson JD, Ke Z, Krylov D, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Thanki N, Yamashita RA, Yin JJ, Zhang D, Bryant SH (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35:237–240

    Article  Google Scholar 

  • Marck C (1988) “DNA Strider”: a “C” program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res 16:1829–1836

    Article  PubMed  CAS  Google Scholar 

  • McCormick DA (1989) GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62:1018–1027

    PubMed  CAS  Google Scholar 

  • Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for γ-aminobutyric acid in Arabidopsis thaliana. J Biol Chem 281:7197–7204

    Article  PubMed  CAS  Google Scholar 

  • Narayan VS, Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher-plants. Phytochemistry 29:367–375

    Article  CAS  Google Scholar 

  • Nikawa J, Hosaka K, Tsukagoshi Y, Yamashita S (1990) Primary structure of the yeast choline transport gene and regulation of its expression. J Biol Chem 265:15996–16003

    PubMed  CAS  Google Scholar 

  • Okumoto S, Schmidt R, Tegeder M, Fischer WN, Rentsch D, Frommer WB, Koch W (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J Biol Chem 277:45338–45346

    Article  PubMed  CAS  Google Scholar 

  • Ortiz-Lopez A, Chang HC, Bush DR (2000) Amino acid transporters in plants. Biochim Biophys Acta 1465:275–280

    Article  PubMed  CAS  Google Scholar 

  • Patrick JW (1988) Assimilate partitioning in relation to crop productivity. Hortscience 23:33–40

    Google Scholar 

  • Pena A, Ramirez J, Rosas G, Calahorra M (1995) Proton pumping and the internal pH of yeast cells, measured with pyranine introduced by electroporation. J Bacteriol 177:1017–1022

    PubMed  CAS  Google Scholar 

  • Proteau G, Silver M (1991) Acetohydroxy acid synthetase of Thiobacillus acidophilus. Biomed Lett 46:121–128

    CAS  Google Scholar 

  • Saier MHJ (2000) Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology 146:1775–1795

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sauer N, Caspari T, Klebl F, Tanner W (1990) Functional expression of the Chlorella hexose transporter in Schizosaccharomyces pombe. Proc Natl Acad Sci 87:7949–7952

    Article  PubMed  CAS  Google Scholar 

  • Sauer N, Baier K, Gahrtz M, Stadler R, Stolz J, Truernit E (1994) Sugar transport across the plasma membranes of higher plants. Plant Mol Biol 26:1671–1679

    Article  PubMed  CAS  Google Scholar 

  • Sharkey PJ, Pate JS (1975) Selectivity in xylem to phloem transfer of amino acids in fruiting shoots of white lupin (Lupinus albus L.). Planta 127:251–262

    Article  CAS  Google Scholar 

  • Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trend Plant Sci 4:446–452

    Article  Google Scholar 

  • Solsbacher J, Maurer P, Vogel F, Schlenstedt G (2000) Nup2p, a yeast nucleoporin, functions in bidirectional transport of importin alpha. Mol Cell Biol 20:8468–8479

    Article  PubMed  CAS  Google Scholar 

  • Su HY, Frommer WB, Ludewig U (2004) Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol 136:3104–3113

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2001) PAUP* 4.0b10: phylogenetic analysis using parsimony (*and other methods). In Sinauer Associates, Sunderland

    Google Scholar 

  • Tanaka J, Fink GR (1985) The histidine permease gene (HIP1) of Saccharomyces cerevisiae. Gene 38:205–214

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Biyoloji Bölümü, Fen Edebiyat Fakültesi, Balıkesir Üniversitesi, Balıkesir, Turkey

    Ekrem Dündar

  2. Program in Physiological and Molecular Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Ekrem Dündar

  3. Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Daniel R. Bush

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  1. Ekrem Dündar
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Correspondence to Daniel R. Bush.

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Dündar, E., Bush, D.R. BAT1, a bidirectional amino acid transporter in Arabidopsis . Planta 229, 1047–1056 (2009). https://doi.org/10.1007/s00425-009-0892-8

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