Plant Biol (Stuttg) 2006; 8(4): 522-528
DOI: 10.1055/s-2006-923877
Short Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Role of AMT1;1 in NH4 + Acquisition in Arabidopsis thaliana

M. Mayer1 , U. Ludewig1
  • 1Zentrum für Molekularbiologie der Pflanzen (ZMBP), Pflanzenphysiologie, Universität Tübingen, Auf der Morgenstelle 1, 72076 Tübingen, Germany
Weitere Informationen

Publikationsverlauf

Received: September 14, 2005

Accepted: January 10, 2006

Publikationsdatum:
13. März 2006 (online)

Abstract

AtAMT1;1 was the founding member of the family of AMT/Rh ammonium transporters and accounts for about one third of the total ammonium absorption in the roots of the model plant Arabidopsis. Recent evidence suggested that at least some AMT/Rh proteins are NH3 gas channels. In order to evaluate the transported form of ammonium in AtAMT1;1, the protein was functionally expressed in Xenopus oocytes. AtAMT1;1 elicited NH4 + and methylammonium (MeA+) inward currents that saturated in a voltage-dependent manner with a half maximal concentration of 2.7 ± 1.6 µM for NH4 + and 5.0 ± 0.7 µM for the transport analogue methylammonium. AtAMT1;1 was plasma membrane localized and expressed in the root cortex and epidermis, including root hairs. The AtAMT1;1-GFP fusion construct under control of its endogenous promoter revealed additional localization of the protein in the pericycle, in the leaf epidermis, and in mesophyll cells. The functional data and its localization suggest that AtAMT1;1 participates in concentrative NH4 + acquisition in roots, in long-distance transport to the shoots, and in re-uptake of apoplastic NH4 + that derives from photorespiration in shoots.

References

  • 1 Ayling S. M.. The effect of ammonium ions on membrane potential and anion flux in roots of barley and tomato.  Plant, Cell and Environment. (1993);  16 297-303
  • 2 Bakouh N., Benjelloun F., Hulin P., Brouillard F., Edelman A., Cherif-Zahar B., Planelles G.. NH3 is involved in the NH4 + transport induced by the functional expression of the human RhC glycoprotein.  Journal of Biological Chemistry. (2004);  279 15975-15983
  • 3 Boldt M., Burckhardt G., Burckhardt B. C.. NH4 + conductance in Xenopus laevis oocytes. III. Effect of NH3.  Pflügers Archiv European Journal of Physiology. (2003);  446 652-657
  • 4 Britto D. T., Glass A. D., Kronzucker H. J., Siddiqi M. Y.. Cytosolic concentrations and transmembrane fluxes of NH4 +/NH3. An evaluation of recent proposals.  Plant Physiology. (2001);  125 523-526
  • 5 Burckhardt B. C., Burckhardt G.. NH4 + conductance in Xenopus laevis oocytes. I. Basic observations.  Pflügers Archiv European Journal of Physiology. (1997);  434 306-312
  • 6 Burckhardt B. C., Fromter E.. Pathways of NH3/NH4 + permeation across Xenopus laevis oocyte cell membrane.  Pflügers Archiv European Journal of Physiology. (1992);  420 83-86
  • 7 Burckhardt B. C., Thelen P.. Effect of primary, secondary and tertiary amines on membrane potential and intracellular pH in Xenopus laevis oocytes.  Pflügers Archiv European Journal of Physiology. (1995);  429 306-312
  • 8 Cougnon M., Benammou S., Brouillard F., Hulin P., Planelles G.. Effect of reactive oxygen species on NH4 + permeation in Xenopus laevis oocytes.  American Journal of Cellular Physiology. (2002);  282 C1445-C1453
  • 9 Cougnon M., Bouyer P., Hulin P., Anagnostpoulos T., Planelles G.. Further investigation of ionic diffusive properties and of NH4 + pathways in Xenopus laevis oocyte cell membrane.  Pflügers Archiv European Journal of Physiology. (1996);  431 658-667
  • 10 Gansel X., Munos S., Tillard P., Gojon A.. Differential regulation of the NO3 - and NH4 + transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant.  The Plant Journal. (2001);  26 143-155
  • 11 Gazzarrini S., Lejay L., Gojon A., Ninnemann O., Frommer W. B., von Wirén N.. Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots.  Plant Cell. (1999);  11 937-948
  • 12 Holm L. M., Jahn T. P., Moller A. L., Schjoerring J. K., Ferri D., Klaerke D. A., Zeuthen T.. NH3 and NH4 + permeability in aquaporin-expressing Xenopus oocytes.  Pflügers Archiv European Journal of Physiology. (2005);  450 415-428
  • 13 Husted S., Schjoerring J. K.. Apoplastic pH and ammonium concentration in leaves of Brassica napus L.  Plant Physiology. (1995);  109 1453-1460
  • 14 Ishiyama K., Inoue E., Watanabe-Takahashi A., Obara M., Yamaya T., Takahashi H.. Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. .  Journal of Biological Chemistry. (2004);  279 16598-16605
  • 15 Jahn T. P., Moller A. L., Zeuthen T., Holm L. M., Klaerke D. A., Mohsin B., Kuhlbrandt W., Schjoerring J. K.. Aquaporin homologues in plants and mammals transport ammonia.  FEBS Letters. (2004);  574 31-36
  • 16 Javelle A., Thomas G., Marini A. M., Kramer R., Merrick M.. In vivo functional characterisation of the E. coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase.  Biochemical Journal. (2005);  390 215-222
  • 17 Kaiser B. N., Rawat S. R., Siddiqi M. Y., Masle J., Glass A. D.. Functional analysis of an Arabidopsis T‐DNA “knockout” of the high-affinity NH4 + transporter AtAMT1;1.  Plant Physiology. (2002);  130 1263-1275
  • 18 Khademi S., O'Connell 3rd J., Remis J., Robles-Colmenares Y., Miercke L. J., Stroud R. M.. Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å.  Science. (2004);  305 1587-1594
  • 19 Loqué D., Ludewig U., Yuan L., von Wiren N.. Tonoplast aquaporins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole.  Plant Physiology. (2005);  137 671-680
  • 20 Loqué D., von Wiren N.. Regulatory levels for the transport of ammonium in plant roots.  Journal of Experimental Botany. (2004);  55 1293-1305
  • 21 Ludewig U.. Electroneutral ammonium transport by basolateral rhesus B glycoprotein.  Journal of Physiology. (2004);  471 751-759
  • 22 Ludewig U., von Wirén N., Frommer W. B.. Uniport of NH4 + by the root hair plasma membrane ammonium transporter LeAMT1;1.  Journal of Biological Chemistry. (2002);  277 13548-13555
  • 23 Ludewig U., Wilken S., Wu B., Jost W., Obrdlik P., El Bakkoury M., Marini A. M., Andre B., Hamacher T., Boles E., von Wiren N., Frommer W. B.. Homo- and hetero-oligomerization of ammonium transporter-1NH4 + uniporters.  Journal of Biological Chemistry. (2003);  278 45603-45610
  • 24 Marini A. M., Vissers S., Urrestarazu A., André B.. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae.  EMBO Journal. (1994);  13 3456-3463
  • 25 Miller A. J., Cookson S. J., Smith S. J., Wells D. M.. The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants.  Journal of Experimental Botany. (2001);  52 541-549
  • 26 Nielsen K. H., Schjoerring J. K.. Regulation of apoplastic NH4 + concentration in leaves of oilseed rape.  Plant Physiology. (1998);  118 1361-1368
  • 27 Ninnemann O., Jauniaux J. C., Frommer W. B.. Identification of a high affinity NH4 + transporter from plants.  EMBO Journal. (1994);  13 3464-3471
  • 28 Raven J. A., Farquhar G. D.. Methylammonium transport in Phaseolus vulgaris leaf slices.  Plant Physiology. (1981);  67 859-863
  • 29 Rawat S. R., Silim S. N., Kronzucker H. J., Siddiqi M. Y., Glass A. D.. AtAMT1 gene expression and NH4 + uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels.  The Plant Journal. (1999);  19 143-152
  • 30 Ripoche P., Bertrand O., Gane P., Birkenmeier C., Colin Y., Cartron J. P.. The human Rhesus-associated RhAG protein mediates facilitated transport of NH3 into red blood cells.  Proceedings of the National Acadamy of Sciences of the USA. (2004);  101 17222-17227
  • 31 Roberts D. M., Tyerman S. D.. Voltage-dependent cation channels permeable to NH4 +, K+, and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. .  Plant Physiology. (2002);  128 370-378
  • 32 Shelden M. C., Dong B., de Bruxelles G. L., Trevaskis B., Whelan J., Ryan P. R., Howitt S. M., Udvardi M. K.. Arabidopsis ammonium transporters, AtAMT1;1 and AtAMT1;2, have different biochemical properties and functional roles.  Plant and Soil. (2001);  321 151-160
  • 33 Sohlenkamp C., Wood C. C., Roeb G. W., Udvardi M. K.. Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane.  Plant Physiology. (2002);  130 1788-1796
  • 34 Sonoda Y., Ikeda A., Saiki S., von Wiren N., Yamaya T., Yamaguchi J.. Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice.  Plant and Cell Physiology. (2003);  44 726-734
  • 35 Su Y. H., Frommer W. B., Ludewig U.. Molecular and functional characterization of a family of amino acid transporters from Arabidopsis.  Plant Physiology. (2004);  136 3104-3113
  • 36 Suding K. N., Collins S. L., Gough L., Clark C., Cleland E. E., Gross K. L., Milchunas D. G., Pennings S.. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization.  Proceedings of the National Acadamy of Sciences of the USA. (2005);  102 4387-4392
  • 37 Suenaga A., Moriya K., Sonoda Y., Ikeda A., Von Wiren N., Hayakawa T., Yamaguchi J., Yamaya T.. Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants.  Plant and Cell Physiology. (2003);  44 206-211
  • 38 Tyerman S. D., Niemietz C. M., Bramley H.. Plant aquaporins: multifunctional water and solute channels with expanding roles.  Plant, Cell and Environment. (2002);  25 173-194
  • 39 Ullrich W. R., Larsson M., Larsson C. M., Lesch S., Novacky A.. Ammonium uptake in Lemna-Gibba G‐1, related membrane-potential changes, and inhibition of anion uptake.  Physiologia Plantarum. (1984);  61 369-376
  • 40 Walker N. A., Smith F. A., Beilby M. J.. Amine uniport at the plasmalemma of charophyte cells. II. Ratio of matter to charge transported and permeability of free base.  Journal of Membrane Biology. (1979);  49 238-296
  • 41 Wang M. Y., Glass A. D. M., Shaff J. E., Kochian L. V.. Ammonium uptake by rice roots. III. Electrophysiology.  Plant Physiology. (1994);  104 899-906
  • 42 Westhoff C. M., Ferreri-Jacobia M., Mak D. O., Foskett J. K.. Identification of the erythrocyte Rh blood group glycoprotein as a mammalian ammonium transporter.  Journal of Biological Chemistry. (2002);  277 12499-12502
  • 43 Yu J., Wo K. C.. Correlation between the development of photorespiration and the change in activities of NH3 assimilation enzymes in greening oat leaves.  Australian Journal of Plant Physiology. (1991);  18 583-588
  • 44 Zheng L., Kostrewa D., Berneche S., Winkler F. K., Li X. D.. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. .  Proceedings of the National Acadamy of Sciences of the USA. (2004);  101 17090-17095

U. Ludewig

Zentrum für Molekularbiologie der Pflanzen (ZMBP)
Pflanzenphysiologie
Universität Tübingen

Auf der Morgenstelle 1

72076 Tübingen

Germany

eMail: uwe.ludewig@zmbp.uni-tuebingen.de

Editor: M. Hawkesford

    >