Skip to main content
SpringerLink
Log in

Regulation of amino acid uptake by carbon and nitrogen in Pinus sylvestris

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The simultaneous uptake of 13 different amino acids by Scots pine (Pinus sylvestris L.) was characterized and its regulation investigated after pre-treatments with a range of C and N metabolites. The uptake system exhibited a broad substrate specificity, acquiring all tested amino acids at similar uptake rates. Uptake of all tested amino acids by excised roots was linear over a time period of 150 min and exhibited pH-dependency, showing a peak at pH 4.0–5.0. Uptake was increased following pre-treatments with glucose and sucrose, while ammonium pre-treatments had a negative effect on amino acid acquisition. Pre-treatments with the important Krebs cycle intermediates oxaloacetate or 2-oxoglutarate did not result in altered amino acid uptake. It is speculated that the up-regulation of uptake may be due to an increased flow of glucose through a sensor mechanism, such as hexokinase. The regulation of transport by N and C suggests a function for amino acid uptake in the N nutrition of the plant, thus further highlighting the importance of organic nitrogen for plant N nutrition suggested by an increasing amount of research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

Abbreviations

BA:

6-benzylaminopurine

NAA:

1-naphthaleneacetic acid

References

  • Bernard F, André B (2001) Ubiquitin and the SCFGrr1 ubiquitin ligase complex are involved in the signalling pathway activated by external amino acids in Saccharomyces cerevisiae. FEBS Lett 496:81–85

    PubMed  Google Scholar 

  • Borstlap AC, Meenks JLD, van Eck WF, Bicker JTE (1986) Kinetics and specificity of amino acid uptake by the duckweed Spirodela polyrhiza (L.) Schleiden. J Exp Bot 37:1020–1035

    CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Chiou T-J, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 95:4784–4788

    Article  CAS  PubMed  Google Scholar 

  • Cho B-H, Sauer N, Komor E, Tanner W (1981) Glucose induces two amino acid transport systems in Chlorella. Proc Natl Acad Sci USA 78:3591–3594

    CAS  Google Scholar 

  • Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signalling in plants: emerging "matrix effects". Curr Opin Plant Biol 4:247–253

    Article  CAS  PubMed  Google Scholar 

  • Fischer W-N, André B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz KE, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195

    Article  Google Scholar 

  • Fischer W-N, 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  CAS  PubMed  Google Scholar 

  • Gibson SI (2000) Plant sugar-response pathways. Part of a complex regulatory web. Plant Physiol 124:1532–1539

    Article  CAS  PubMed  Google Scholar 

  • Glass ADM, Britto DT, Kaiser BN, Kronzucker HJ, Kumar A, Okamoto M, Rawat SR, Siddiqi MY, Silim SN, Vidmar JJ, Zhou D (2001) Nitrogen transport in plants, with an emphasis on the regulation of fluxes to match plant demand. J Plant Nutr Soil Sci 164:199–207

    Google Scholar 

  • Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat SR, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  CAS  PubMed  Google Scholar 

  • Guo FQ, Wang RC, Crawford NM (2002) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J Exp Bot 53:835–844

    Article  CAS  PubMed  Google Scholar 

  • Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219

    Article  CAS  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Google Scholar 

  • Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98

    CAS  Google Scholar 

  • Lam H-M, Chiu J, Hsieh MH, Meisel L, Oliveira IC, Shin M, Coruzzi GM (1998) Glutamate-receptor genes in plants. Nature 396:125–126

    Article  CAS  PubMed  Google Scholar 

  • Lejay L, Tillard P, Lepetit M, Olive FD, 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 18:509–519

    Article  CAS  PubMed  Google Scholar 

  • Montamat F, Maurosset L, Tegeder M, Frommer WB, Delrot S (1999) Cloning and expression of amino acid transporters from broad bean. Plant Mol Biol 41:259–268

    Google Scholar 

  • Morcuende R, Krapp A, Hurry V, Stitt M (1998) Sucrose-feeding leads to increased rates of nitrate assimilation, increased rates of alpha-oxoglutarate synthesis, and increased synthesis of a wide spectrum of amino acids in tobacco leaves. Planta 206:394–409

    Article  CAS  Google Scholar 

  • Persson J, Näsholm T (2001a) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4:434–438

    Article  Google Scholar 

  • Persson J, Näsholm T (2001b) A GC–MS method for determination of amino acid uptake by plants. Physiol Plant 113:352–358

    CAS  Google Scholar 

  • Persson J, Näsholm T (2002) Regulation of amino acid uptake in conifers by exogenous and endogenous nitrogen. Planta 215:639–644

    CAS  PubMed  Google Scholar 

  • Rawat SR, Silim SN, Kronzucker HJ, Siddiqi MY, Glass ADM (1999) AtAMT1 gene expression and NH4 + uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant J 19:143–152

    CAS  PubMed  Google Scholar 

  • Scheible W-R, González-Fontez A, Lauerer M, Müller-Röber B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    Article  CAS  PubMed  Google Scholar 

  • Schmidt SK, Stewart GR (1999) Glycine metabolism by plant roots and its occurrence in Australian plant communities. Aust J Plant Physiol 26:253–264

    CAS  Google Scholar 

  • Schmülling T, Schäfer S, Romanov G (1997) Cytokinins as regulators of gene expression. Physiol Plant 100:505–519

    Article  Google Scholar 

  • Silverman FP, Assiamah AA, Bush DR (1998) Membrane transport and cytokinin action in root hairs of Medicago sativa. Planta 205:23–31

    Article  CAS  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81

    Google Scholar 

  • Takei K, Sakakibara H, Tanigushi M, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93

    Article  CAS  PubMed  Google Scholar 

  • Thornton B (2001) Uptake of glycine by non-mycorrhizal Lolium perenne. J Exp Bot 52:1315–1322

    Article  CAS  PubMed  Google Scholar 

  • Ueda A, Shi W, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289

    Article  CAS  PubMed  Google Scholar 

  • Vidmar JJ, Zhou D, Siddiqi MY, Schjoerring JK, Touraine B, Glass ADM (2000) Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol 123:307–318

    Google Scholar 

  • von Wirén N, Lauter F-R, Ninnemann O, Gillissen B, Walch-Liu P, Engels C, Jost W, Frommer WB (2000) Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J 21:167–175

    PubMed  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  CAS  PubMed  Google Scholar 

  • Young GB, Jack DL, Smith DW, Saier Jr MH (1999) The amino acid/auxin: proton symport permease family. Biochim Biophys Acta 1415:306–322

    CAS  Google Scholar 

  • Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Jonas Gullberg for helpful comments on multivariate analysis, and Karin Ljung and Roger Granbom for skillful analyses. In addition, two anonymous reviewers contributed significantly to this work with valuable comments and criticism. This work was financed by grants to T.N. from The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and the program for Abatement Strategies for Transboundary Air Pollution (ASTA) under the Foundation for Strategic Environmental Research (MISTRA).

Author information

Authors and Affiliations

  1. Umeå Plant Science Center, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden

    Jörgen Persson & Torgny Näsholm

Authors
  1. Jörgen Persson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Torgny Näsholm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jörgen Persson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Persson, J., Näsholm, T. Regulation of amino acid uptake by carbon and nitrogen in Pinus sylvestris . Planta 217, 309–315 (2003). https://doi.org/10.1007/s00425-003-0991-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-0991-x

Keywords

Search

Navigation