The Plant Plasma Membrane pp 223-236

Part of the Plant Cell Monographs book series (CELLMONO, volume 19)

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The Role of Plasma Membrane Nitrogen Transporters in Nitrogen Acquisition and Utilization

Chapter

Abstract

Efficient nitrogen acquisition and allocation are important to enable plants to successfully compete for limited and fluctuating nitrogen sources in the soil and sustain vigorous growth. Over the past two decades, several types of nitrogen transporters, such as nitrate transporters, ammonium transporters, and amino acid transporters (Frommer et al. Proc Natl Acad Sci USA 90:5944–5948, 1993; Tsay et al. Cell 72:705–713, 1993; Ninnemann et al. EMBO J 13:3464–3471, 1994), have been identified using genetic approaches or functional complementation cloning in yeast. In this review, we focus on the physiological functions and influence of plasma membrane nitrate, ammonium, and amino acid transporters as revealed by the powerful molecular genetic tools available for investigating Arabidopsis.

References

  1. Alboresi A, Gestin C, Leydecker MT, Bedu M, Meyer C, Truong HN (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ 28:500–512PubMedCrossRefGoogle Scholar
  2. Almagro A, Lin SH, Tsay YF (2008) Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell 20:3289–3299PubMedCrossRefGoogle Scholar
  3. Andrade SL, Dickmanns A, Ficner R, Einsle O (2005) Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proc Natl Acad Sci USA 102:14994–14999PubMedCrossRefGoogle Scholar
  4. Cerezo M, Tillard P, Filleur S, Munos S, Daniel-Vedele F, Gojon A (2001) Major alterations of the regulation of root NO3 uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol 127:262–271PubMedCrossRefGoogle Scholar
  5. Chang HC, Bush DR (1997) Topology of NAT2, a prototypical example of a new family of amino acid transporters. J Biol Chem 272:30552–30557PubMedCrossRefGoogle Scholar
  6. Chopin F, Orsel M, Dorbe MF, Chardon F, Truong HN, Miller AJ, Krapp A, Daniel-Vedele F (2007) The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell 19:1590–1602PubMedCrossRefGoogle Scholar
  7. Dundar E, Bush DR (2009) BAT1, a bidirectional amino acid transporter in Arabidopsis. Planta 229:1047–1056PubMedCrossRefGoogle Scholar
  8. Fan SC, Lin CS, Hsu PK, Lin SH, Tsay YF (2009) The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21:2750–2761PubMedCrossRefGoogle Scholar
  9. Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F, Gojon A, Daniel-Vedele F (2001) An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett 489:220–224PubMedCrossRefGoogle Scholar
  10. Frommer WB, Hummel S, Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc Natl Acad Sci USA 90:5944–5948PubMedCrossRefGoogle Scholar
  11. Guo FQ, Wang R, Chen M, Crawford NM (2001) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13:1761–1777PubMedGoogle Scholar
  12. Guo FQ, Young J, Crawford NM (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117PubMedCrossRefGoogle Scholar
  13. Hammes UZ, Nielsen E, Honaas LA, Taylor CG, Schachtman DP (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J 48:414–426PubMedCrossRefGoogle Scholar
  14. Hirner A, Ludewig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946PubMedCrossRefGoogle Scholar
  15. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194PubMedCrossRefGoogle Scholar
  16. Huang NC, Chiang CS, Crawford NM, Tsay YF (1996) CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8:2183–2191PubMedGoogle Scholar
  17. Huang NC, Liu KH, Lo HJ, Tsay YF (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–1392PubMedGoogle Scholar
  18. Hunt E, Gattolin S, Newbury HJ, Bale JS, Tseng HM, Barrett DA, Pritchard J (2010) A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J Exp Bot 61:55–64PubMedCrossRefGoogle Scholar
  19. Khademi S, O’Connell J, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305:1587–1594PubMedCrossRefGoogle Scholar
  20. Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Suter Grotemeyer M, Tegeder M, Rentsch D (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol 148:856–869PubMedCrossRefGoogle Scholar
  21. Lanquar V, Loque D, Hormann F, Yuan L, Bohner A, Engelsberger WR, Lalonde S, Schulze WX, von Wiren N, Frommer WB (2009) Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis. Plant Cell 21:3610–3622PubMedCrossRefGoogle Scholar
  22. 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 40:60–74PubMedCrossRefGoogle Scholar
  23. Lee YH, Foster J, Chen J, Voll LM, Weber AP, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50:305–319PubMedCrossRefGoogle Scholar
  24. Lejay L, Tillard P, Lepetit M, Olive F, Filleur S, Daniel-Vedele F, Gojon A (1999) Molecular and functional regulation of two NO3 uptake systems by N- and C-status of Arabidopsis plants. Plant J 18:509–519PubMedCrossRefGoogle Scholar
  25. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143:425–433PubMedCrossRefGoogle Scholar
  26. Liang R, Fei YJ, Prasad PD, Ramamoorthy S, Han H, Yang-Feng TL, Hediger MA, Ganapathy V, Leibach FH (1995) Human Intestinal H+/peptide cotransporter. J Biol Chem 270:6456–6463PubMedCrossRefGoogle Scholar
  27. Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528PubMedCrossRefGoogle Scholar
  28. Little DY, Rao H, Oliva S, Daniel-Vedele F, Krapp A, Malamy JE (2005) The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc Natl Acad Sci USA 102:13693–13698PubMedCrossRefGoogle Scholar
  29. Liu X, Bush DR (2006) Expression and transcriptional regulation of amino acid transporters in plants. Amino Acids 30:113–120PubMedCrossRefGoogle Scholar
  30. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013PubMedCrossRefGoogle Scholar
  31. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874PubMedGoogle Scholar
  32. Loque D, Ludewig U, Yuan L, von Wiren N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680PubMedCrossRefGoogle Scholar
  33. Loque D, Lalonde S, Looger LL, von Wiren N, Frommer WB (2007) A cytosolic trans-activation domain essential for ammonium uptake. Nature 446:195–198PubMedCrossRefGoogle Scholar
  34. Ludewig U, Wilken S, Wu B, Jost W, Obrdlik P, El Bakkoury M, Marini AM, Andre B, Hamacher T, Boles E, von Wiren N, Frommer WB (2003) Homo- and hetero-oligomerization of ammonium transporter-1 NH4 uniporters. J Biol Chem 278:45603–45610PubMedCrossRefGoogle Scholar
  35. Ludewig U, Neuhauser B, Dynowski M (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581:2301–2308PubMedCrossRefGoogle Scholar
  36. Marini AM, Vissers S, Urrestarazu A, Andre B (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13:3456–3463PubMedGoogle Scholar
  37. Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I, Tillard P, Zhuo D, Glass AD, Touraine B (2003) Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol Biol 52:689–703PubMedCrossRefGoogle Scholar
  38. Neuhauser B, Dynowski M, Mayer M, Ludewig U (2007) Regulation of NH4+ transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiol 143:1651–1659PubMedCrossRefGoogle Scholar
  39. Ninnemann O, Jauniaux JC, Frommer WB (1994) Identification of a high affinity NH4+ transporter from plants. EMBO J 13:3464–3471PubMedGoogle Scholar
  40. 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 277:45338–45346PubMedCrossRefGoogle Scholar
  41. Oostindier-Braaksma FJ, Feenstra WJ (1973) Isolation and characterization of chlorate-resistant mutants of Arabidopsis thaliana. Mutat Res 19:175–185CrossRefGoogle Scholar
  42. Orsel M, Chopin F, Leleu O, Smith SJ, Krapp A, Daniel-Vedele F, Miller AJ (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein–protein interaction. Plant Physiol 142:1304–1317PubMedCrossRefGoogle Scholar
  43. Quesada A, Galvan A, Fernandez E (1994) Identification of nitrate transporter genes in Chlamydomonas reinhardtii. Plant J 5:407–419PubMedCrossRefGoogle Scholar
  44. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211PubMedCrossRefGoogle Scholar
  45. Rentsch D, Laloi M, Rouhara I, Schmelzer E, Delrot S, Frommer WB (1995) NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS Lett 370:264–268PubMedCrossRefGoogle Scholar
  46. Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581:2281–2289PubMedCrossRefGoogle Scholar
  47. 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 137:1236–1249PubMedCrossRefGoogle Scholar
  48. Sanders A, Collier R, Trethewy A, Gould G, Sieker R, Tegeder M (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J 59:540–552PubMedCrossRefGoogle Scholar
  49. Schmidt R, Stransky H, Koch W (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226:805–813PubMedCrossRefGoogle Scholar
  50. Segonzac C, Boyer JC, Ipotesi E, Szponarski W, Tillard P, Touraine B, Sommerer N, Rossignol M, Gibrat R (2007) Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell 19:3760–3777PubMedCrossRefGoogle Scholar
  51. Sohlenkamp C, Wood CC, Roeb GW, Udvardi MK (2002) Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiol 130:1788–1796PubMedCrossRefGoogle Scholar
  52. Song W, Steiner H-Y, Zhang L, Naider F, Stacey G, Becker JM (1996) Cloning of a second Arabidopsis peptide transport gene. Plant Physiol 110:171–178PubMedCrossRefGoogle Scholar
  53. Tong Y, Zhou JJ, Li Z, Miller AJ (2005) A two-component high-affinity nitrate uptake system in barley. Plant J 41:442–450PubMedCrossRefGoogle Scholar
  54. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713PubMedCrossRefGoogle Scholar
  55. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300PubMedCrossRefGoogle Scholar
  56. Unkles SE, Hawker KL, Grieve C, Campbell EI, Montague P, Kinghorn JR (1991) crnA encodes a nitrate transporter in Aspergillus nidulans. Proc Natl Acad Sci USA 88:204–208PubMedCrossRefGoogle Scholar
  57. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95:15134–15139PubMedCrossRefGoogle Scholar
  58. 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 27:139–147PubMedCrossRefGoogle Scholar
  59. Wirth J, Chopin F, Santoni V, Viennois G, Tillard P, Krapp A, Lejay L, Daniel-Vedele F, Gojon A (2007) Regulation of root nitrate uptake at the NRT2.1 protein level in Arabidopsis thaliana. J Biol Chem 282:23541–23552PubMedCrossRefGoogle Scholar
  60. Yuan L, Loque D, Ye F, Frommer WB, von Wiren N (2007a) Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol 143:732–744PubMedCrossRefGoogle Scholar
  61. Yuan L, Loque D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wiren N (2007b) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652PubMedCrossRefGoogle Scholar
  62. Zhou JJ, Trueman LJ, Boorer KJ, Theodoulou FL, Forde BG, Miller AJ (2000) A high affinity fungal nitrate carrier with two transport mechanisms. J Biol Chem 275:39894–39899PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Academia SinicaInstitute of Molecular BiologyTaipeiTaiwan

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