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Amino Acid Transport in Plants and Transport of Neurotransmitters in Animals: a Common Mechanism?

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Communication in Plants

Abstract

Amino acids (AA) are essential elements in animals and plants. In a genome-wide analysis in yeasts, plants and animals five AA transporter superfamilies could be identified. Transporters of one superfamily (ATF1, SLC38) which includes animal and plant members correspond to proteins involved in neurotransmitter transport in animals. Their close relation with plant genes suggests that a closely related transport mechanism could be involved in AA transport in plants. This chapter summarizes current knowledge on AA transport in animals and plants and the question of a possible common mechanism is discussed.

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References

  • Albers A, Broer A, Wagner CA, Setiawan I, Lang PA, Kranz EU, Lang F, Broer S (2001) Na+ transport by the neural glutamine transporter ATA1. Pflugers Arch Eur J Physiol 443:92–101

    Article  CAS  Google Scholar 

  • Arriza JL, Eliasof S, Kavanaugh MP, Amara SG (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94:4155–4160

    Article  PubMed  CAS  Google Scholar 

  • Atkins CA (2000) Biochemical aspects of assimilate transfers along the phloem path: N-solutes in lupins. Aust J Plant Physiol 27:531–537

    CAS  Google Scholar 

  • Bai L, Xu H, Collins JF, Ghishan FK (2001) Molecular and functional analysis of a novel neuronal vesicular glutamate transporter. J Biol Chem 276:36764–36769

    Article  PubMed  CAS  Google Scholar 

  • Bellocchio EE, Reimer RJ, Fremeau RTJ, Edwards RH (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957–960

    Article  PubMed  CAS  Google Scholar 

  • Blakely RD, Bauman AL (2000) Biogenic amine transporters: regulation in flux. Curr Opin Neurobiol 10:328–336

    Article  PubMed  CAS  Google Scholar 

  • Boll M, Daniel H, Gasnier B (2004) The SLC36 family: proton-coupled transporters for the absorption of selected amino acids from extracellular and intracellular proteolysis. Pflugers Arch Eur J Physiol 447:776–779

    Article  CAS  Google Scholar 

  • Broer A, Albers A, Setiawan I, Edwards RH, Chaudhry FA, Lang F, Wagner CA, Broer S (2002)Regulation of the glutamine transporter SN1 by extracellular pHand intracellular sodium ions. J Physiol 539:3–14

    Article  PubMed  CAS  Google Scholar 

  • Broer A, Wagner C, Lang F, Broer S (2000) Neutral amino acid transporter ASCT2 displays substrate-induced Na+ exchange and a substrate-gated anion conductance. Biochem J 346:705–710

    Article  PubMed  CAS  Google Scholar 

  • Chaudhry FA, Krizaj D, Larsson P, Reimer RJ, Wreden C, Storm-Mathisen J, Copenhagen D, Kavanaugh M, Edwards RH (2001) Coupled and uncoupled proton movement by amino acid transport system N. EMBO J 20:7041–7051

    Article  PubMed  CAS  Google Scholar 

  • Chaudhry FA, Reimer RJ, Krizaj D, Barber D, Storm-Mathisen J, Copenhagen DR, Edwards RH (1999)Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 99:769–780

    Article  PubMed  CAS  Google Scholar 

  • Chaudhry FA, Schmitz D, Reimer RJ, Larsson P, Gray AT, Nicoll R, Kavanaugh M, Edwards RH (2002) Glutamine uptake by neurons: interaction of protons with system A transporters. J Neurosci 22:62–72

    PubMed  CAS  Google Scholar 

  • Chen L, Bush DR (1997) LHT1, a lysine-and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol 115:1127–1134

    Article  PubMed  CAS  Google Scholar 

  • Chen L, 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 

  • Chen NH, Reith ME, Quick MW (2004) Synaptic uptake and beyond: the sodium-and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch Eur J Physiol 447:519–531

    Article  CAS  Google Scholar 

  • Closs EI, Lyons CR, Kelly C, Cunningham JM (1993) Characterization of the third member of the MCAT family of cationic amino acid transporters. Identification of a domain that determines the transport properties of the MCAT proteins. J Biol Chem 268:20796–20800

    PubMed  CAS  Google Scholar 

  • Fischer WN, André 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, Kwart M, Hummel S, Frommer WB (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J Biol Chem 270:16315–16320

    Article  PubMed  CAS  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 

  • Fremeau RT, Jr., Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488–14493

    Article  PubMed  CAS  Google Scholar 

  • Frommer WB, Hummel S, Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. ProcNatl Acad Sci USA 90:5944–5948

    Article  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 USA 92:12036–12040

    Article  PubMed  CAS  Google Scholar 

  • Ganapathy V, Ganapathy ME, Leibach FH (2001) Intestinal transport of peptides and amino acids. In: Barrett KE, Donowitz M (eds) Current topics in membranes, vol 50. Academic, San Diego, CA, USA, pp 379–412

    Google Scholar 

  • Gasnier B (2004) The SLC32 transporter, a key protein for the synaptic release of inhibitory amino acids. Pflugers Arch Eur J Physiol 447:756–759

    Article  CAS  Google Scholar 

  • Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus JM, 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 

  • Häussinger D, Kilberg MS (1992) Amino Acid transport in the liver. In: Häussinger D, Kilberg MS (eds) Mammalian amino acid transport: mechanisms and control. Plenum, New York, pp 133–148

    Google Scholar 

  • Hirner B, Fischer WN, Rentsch D, Kwart M, Frommer WB (1998) Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. Plant J 14:535–544

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jacob R, Rosenthal N, Barrett EJ (1986) Characterization of glutamine transport by liver plasma membrane vesicles. Am J Physiol 251:E509–E514

    PubMed  CAS  Google Scholar 

  • Kanai Y, Hediger MA (2004) The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch Eur J Physiol 447:469–479

    Article  CAS  Google Scholar 

  • Karinch AM, Lin CM, Wolfgang CL, Pan M, Souba WW (2002) Regulation of expression of the SN1 transporter during renal adaptation to chronic metabolic acidosis in rats. Am J Physiol Renal Physiol 283:F1011–F1019

    PubMed  Google Scholar 

  • Kilberg MS, Handlogten ME, Christensen HN (1980) Characteristics of an amino acid transport system in rat liver for glutamine, asparagine, histidine, and closely related analogs. J Biol Chem 255:4011–4019

    PubMed  CAS  Google Scholar 

  • Kim DK, Kanai Y, Chairoungdua A, Matsuo H, Cha SH, Endou H (2001) Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. J Biol Chem 276:17221–17228

    Article  PubMed  CAS  Google Scholar 

  • Koch W, Kwart M, Laubner M, Heineke D, Stransky H, Frommer WB, Tegeder M (2003) Reduced amino acid content in transgenic potato tubers due to antisense inhibition of the leaf H+/amino acid symporter StAAP1. Plant J 33:211–220

    Article  PubMed  CAS  Google Scholar 

  • Kwart M, Hirner B, Hummel S, Frommer WB (1993) Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J 4:993–1002

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Tegeder M (2004) Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J 40:60–74

    Article  PubMed  CAS  Google Scholar 

  • Li ZC, Bush DR (1990a) ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet leaves. I. Evidence for carrier-mediated, electrogenic flux through multiple transport systems. Plant Physiol 94:268–277

    PubMed  CAS  Google Scholar 

  • Li ZC, Bush DR (1990b) ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet leaves. II. Evidence for multiple aliphatic, neutral amino acid symports. Plant Physiol 96:1338–1344

    Article  Google Scholar 

  • Lohaus G, Winter H, Riens B, Heldt HW (1995) Further studies of the phloem loading process in leaves of barley and spinach. The comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes. Bot Acta 108:270–275

    CAS  Google Scholar 

  • Lynch AM, McGivan JD (1987) Evidence for a single common Na+-dependent transport system for alanine, glutamine, leucine and phenylalanine in brush-border membrane vesicles from bovine kidney. Biochim Biophys Acta 899:176–184

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch Eur J Physiol 447:784–795

    Article  CAS  Google Scholar 

  • McGivan JD, Pastor Anglada M (1994) Regulatory and molecular aspects of mammalian amino acid transport. Biochem J 299:321–334

    PubMed  CAS  Google Scholar 

  • McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870–876

    Article  PubMed  CAS  Google Scholar 

  • Melikian HE (2004) Neurotransmitter transporter trafficking: endocytosis, recycling, and regulation. Pharmacol Therapeut 104:17–27

    Article  CAS  Google Scholar 

  • Miranda M, Borisjuk L, Tewes A, Heim U, Sauer N, Wobus U, Weber H (2001) Amino acid permeases in developing seeds of Vicia faba L.: expression precedes storage protein synthesis and is regulated by amino acid supply. Plant J 28:61–71

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi T, Kekuda R, Fei YJ, Hatanaka T, Sugawara M, Martindale RG, Leibach FH, Prasad PD, Ganapathy V (2001) Cloning and functional characterization of a new subtype of the amino acid transport system N. Am J Physiol Cell Physiol 281:C1757–C1768

    PubMed  CAS  Google Scholar 

  • Nelson N (1998) The family of Na+/Cl− neurotransmitter transporters. J Neurochem 71:1785–1803

    Article  PubMed  CAS  Google Scholar 

  • Okumoto S, Koch W, Tegeder M, Fischer WN, Biehl A, Leister D, Stierhof YD, Frommer WB (2004) Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. J Exp Bot 55:2155–2168

    Article  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 

  • Palacin M, Estevez R, Zorzano A (1998) Cystinuria calls for heteromultimeric amino acid transporters. Curr Opin Cell Biol 10:455–461

    Article  PubMed  CAS  Google Scholar 

  • Pate JS, Sharkey PJ (1975) Xylem to phloem transfer of solutes in fruiting shoots of legumes, studied by a phloem bleeding techniques. Planta 12:11–26

    Article  Google Scholar 

  • Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VP, Frommer WB (2004) Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 16:1827–1840

    Article  PubMed  CAS  Google Scholar 

  • Pohlmeyer K, Soll J, Grimm R, Hill K, Wagner R (1998) A high-conductance solute channel in the chloroplastic outer envelope from Pea. Plant Cell 10:1207–1216

    Article  PubMed  CAS  Google Scholar 

  • Pohlmeyer K, Soll J, Steinkamp T, Hinnah S, Wagner R (1997) Isolation and characterization of an a mino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proc Natl Acad Sci USA 94:9504–9509

    Article  PubMed  CAS  Google Scholar 

  • Reimer RJ, Edwards RH (2004) Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch Eur J Physiol 447:629–635

    Article  CAS  Google Scholar 

  • Rentsch D, Frommer WB (1996) Molecular approaches towards an understanding of loading and unloading of assimilates in higher plants. J Exp Bot 47:1199–1204

    CAS  Google Scholar 

  • Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446

    Article  PubMed  CAS  Google Scholar 

  • Rolletschek H, Hosein F, Miranda M, Heim U, Gotz KP, Schlereth A, Borisjuk L, Saalbach I, Wobus U, Weber H (2005) Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and Pea increases storage proteins. Plant Physiol 137:1236–1249

    Article  PubMed  CAS  Google Scholar 

  • Sagne C, Agulhon C, Ravassard P, Darmon M, Hamon M, El Mestikawy S, Gasnier B, Giros B (2001) Identification and characterization of a lysosomal transporter for small neutral amino acids. Proc Natl Acad Sci USA 98:7206–7211

    Article  PubMed  CAS  Google Scholar 

  • Saier MH Jr (1999) A functional-phylogenetic system for the classification of transport proteins. J Cell Biochem (Suppl 32–33):84–94

    Article  PubMed  Google Scholar 

  • Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11:377–392

    Article  PubMed  CAS  Google Scholar 

  • Shotwell MA, Jayme DW, Kilberg MS, Oxender DL (1981) Neutral amino acid transport systems in Chinese hamster ovary cells. J Biol Chem 256:5422–5427

    PubMed  CAS  Google Scholar 

  • Su YH, 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 (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, MA, USA

    Google Scholar 

  • Tegeder M, Offler CE, Frommer WB, Patrick JW (2000) Amino acid transporters are localized to transfer cells of developing Pea seeds. Plant Physiol 122:319–325

    Article  PubMed  CAS  Google Scholar 

  • Thwaites DT, McEwan GTA, Simmons NL (1995) The role of the proton electrochemical gradient in the transepithelial absorption of amino acids by human intestinal Caco-2 cell monolayers. J Membr Biol 145:245–256

    PubMed  CAS  Google Scholar 

  • Vadgama JV, Christensen HN (1984) Wide distribution of pH-dependent service of transport system ASC for both anionic and zwitterionic amino acids. J Biol Chem 259:3648–3652

    PubMed  CAS  Google Scholar 

  • Velasco I, Tenreiro S, Calderon IL, Andre B (2004) Saccharomyces cerevisiae Aqr1 is an internal-membrane transporter involved in excretion of amino acids. Eukaryot Cell 3:1492–1503

    Article  PubMed  CAS  Google Scholar 

  • Verrey F, Closs EI, Wagner CA, Palacin M, Endou H, Kanai Y (2004) CATs and HATs: the SLC7 family of amino acid transporters. Pflugers Arch Eur J Physiol 447:532–542

    Article  CAS  Google Scholar 

  • Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, Hayakawa S, Suzuki S, Futsuhara Y, Kawamitsu Y, Takabe T (2002) Functional characterization of betaine/praline transporters in betaine-accumulating mangrove. J Biol Chem 277:18373–18382

    Article  PubMed  CAS  Google Scholar 

  • Wipf D, Ludewig U, Tegeder M, Rentsch D, Koch W, Frommer WB (2002) Conservation of amino acid transporters in fungi, plants and animals. Trends Biochem Sci 27:139–147

    Article  PubMed  CAS  Google Scholar 

  • Zerangue N, Kavanaugh MP (1996) Flux coupling in a neuronal glutamate transporter. Nature 383:634–637

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. NGW Transport in Mycorrhiza, IZMB — Institut für Zelluläre und Molekulare Botanik Bonn, University of Bonn, Kirschallee 1, 53115, Bonn, Germany

    Tobias Müller & Daniel Wipf

  2. Plant Physiology, ZMBP, Auf derMorgenstelle 1, 72076, Tübingen, Germany

    Wolfgang Koch

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  1. Tobias Müller
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  2. Wolfgang Koch
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  3. Daniel Wipf
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Editors and Affiliations

  1. Institute of Cellular and Molecular Botany, University of Bonn, Kirschallee 1, 53115, Bonn, Germany

    František Baluška  & Dieter Volkmann  & 

  2. Department of Horticulture Electrophysiology Laboratory, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino, Italy

    Stefano Mancuso

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Müller, T., Koch, W., Wipf, D. (2006). Amino Acid Transport in Plants and Transport of Neurotransmitters in Animals: a Common Mechanism?. In: Baluška, F., Mancuso, S., Volkmann, D. (eds) Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-28516-8_11

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