Skip to main content
SpringerLink
Log in

AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold

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

Abstract

The Arabidopsis genome encodes for 20 members of putative ligand-gated channels, termed glutamate receptors (GLR). Despite the fact that initial studies suggested a role for GLRs in various aspects of photomorphogenesis, calcium homeostasis or aluminium toxicity, their functional properties and physiological role in plants remain elusive. Here, we have focussed on AtGLR3.4, which is ubiquitously expressed in Arabidopsis including roots, vascular bundles, mesophyll cells and guard cells. AtGLR3.4 encodes a glutamate-, touch-, and cold-sensitive member of this gene family. Abiotic stress stimuli such as touch, osmotic stress or cold stimulated AtGLR3.4 expression in an abscisic acid-independent, but calcium-dependent manner. In plants expressing the Ca2+ -reporter apoaequorin, glutamate as well as cold elicited cytosolic calcium elevations. Upon glutamate treatment of mesophyll cells, the plasma membrane depolarised by about 120 mV. Both glutamate responses were transient in nature, sensitive to glutamate receptor antagonists, and were subject to desensitisation. One hour after eliciting the first calcium signal, a 50% recovery from desensitisation was observed, reflecting the stimulus-induced fast activation of AtGLR3.4 transcription. We thus conclude that AtGLR3.4 in particular and GLRs in general could play an important role in the Ca2+ -based, fast transmission of environmental stress.

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
Fig. 6

Similar content being viewed by others

Abbreviations

GLR:

Glutamate receptor

DNQX:

6,7-dinitroquinoxaline-2,3-dione

CNQX:

6-cyano-7-nitro-quinoxaline-2,3-dione

MNQX:

5,7-Dinitro-1,4-dihydro-2,3-quinoxalinedione

GABA:

γ-aminobutyrate

CHX:

Cycloheximide

References

  • Baum G, Long JC, Jenkins GI, Trewavas AJ (1999) Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc Natl Acad Sci USA 96:13554–13559

    Article  CAS  PubMed  Google Scholar 

  • Becker D, Geiger D, Dunkel M, Roller A, Bertl A, Latz A, Carpaneto A, Dietrich P, Roelfsema MRG, Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K, Hedrich R (2004) AtTPK4, an Arabidopsis “open-rectifying” K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+ dependent manner. Proc Natl Acad Sci USA 101:15621–15626

    Article  CAS  PubMed  Google Scholar 

  • Bouche N, Lacombe B, Fromm H (2003) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol 13:607–610

    Article  CAS  PubMed  Google Scholar 

  • Braam J, Sistrunk ML, Polisensky DH, Xu W, Purugganan MM, Antosiewicz DM, Campbell P, Johnson KA (1997) Plant responses to environmental stress: regulation and functions of the Arabidopsis TCH genes. Planta 203(Suppl):S35–S41

    Article  CAS  PubMed  Google Scholar 

  • Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000) Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol 124:1615–1624

    Article  CAS  PubMed  Google Scholar 

  • Chiu JC, Brenner ED, DeSalle R, Nitabach MN, Holmes TC, Coruzzi GM (2002) Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Mol Biol Evol 19:1066–1082

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Davenport R (2002) Glutamate receptors in plants. Ann Bot (Lond) 90:549–557

    Article  CAS  Google Scholar 

  • Dennison KL, Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124:1511–1514

    Article  CAS  PubMed  Google Scholar 

  • Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM (2003) A role for glycine in the gating of plant NMDA-like receptors. Plant J 35:800–810

    Article  CAS  PubMed  Google Scholar 

  • Elzenga JT, Van Volkenburgh E (1997) Kinetics of Ca(2+)- and ATP-dependent, voltage-controlled anion conductance in the plasma membrane of mesophyll cells of Pisum sativum. Planta 201:415–423

    Article  CAS  PubMed  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Turano FJ (2003) The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6872–6877

    Article  CAS  PubMed  Google Scholar 

  • Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 42:74–84

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Knight MR (1995) Recombinant aequorin methods for intracellular calcium measurement in plants. Methods Cell Biol 49:201–216

    CAS  PubMed  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503

    Article  CAS  PubMed  Google Scholar 

  • Lacombe B, Becker D, Hedrich R, DeSalle R, Hollmann M, Kwak JM, Schroeder JI, Le Novere N, Nam HG, Spalding EP, Tester M, Turano FJ, Chiu J, Coruzzi G (2001) The identity of plant glutamate receptors. Science 292:1486–1487

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Madden DR (2002) The structure and function of glutamate receptor ion channels. Nat Rev Neurosci 3:91–101

    Article  CAS  PubMed  Google Scholar 

  • Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–675

    Article  CAS  PubMed  Google Scholar 

  • Stitt M, Muller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970

    Article  CAS  PubMed  Google Scholar 

  • Tazawa M, Kikuyama M (2003) Is Ca2+ release from internal stores involved in membrane excitation in characean cells? Plant Cell Physiol 44:518–526

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Biskup B, Elzenga JTM, Homann U, Thiel G, Wissing F, Maathuis FJM (1999) Advanced patch-clamp techniques and single-channel analysis. J Exp Bot 50:1037–1054

    Article  CAS  Google Scholar 

  • White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM (2002) Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim Biophys Acta 1564:299–309

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank K. Neuwinger and D. Giehl (University of Würzburg, Ger) for assistance during the Ca2+ measurements. We are grateful to A. Trewavas (University of Edinburgh, UK) for supplying us with seeds of apoaequorin-expressing Arabidopsis plants. This work was funded by DFG grants and Körber European Science Award to RH, and by a DFG grant (SPP1108) to PD and DB.

Author information

Authors and Affiliations

  1. Molecular Plant Physiology and Biophysics, University of Wuerzburg, Julius-von-Sachs-Platz 2, 97082, Wuerzburg, Germany

    Oliver Meyerhoff, Katharina Müller, M. Rob G. Roelfsema, Andreas Latz, Rainer Hedrich & Dirk Becker

  2. Biochimie et Physiologie Moleculaires des Plantes, UMR 5004, Agro-M/CNRS/INRA/UM2, 34060, Montpellier Cedex 1, France

    Benoit Lacombe

  3. Institut für Molekulare Pflanzenphysiologie, University of Erlangen, Staudtstr. 5, 91058, Erlangen, Germany

    Petra Dietrich

Authors
  1. Oliver Meyerhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katharina Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Rob G. Roelfsema
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andreas Latz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Benoit Lacombe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rainer Hedrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Petra Dietrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dirk Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Becker.

Additional information

Data deposition: The sequences referred to in this paper have been deposited in the GenBank database (accession no. AF167355.1 [AtGLR3.4])

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyerhoff, O., Müller, K., Roelfsema, M.R.G. et al. AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta 222, 418–427 (2005). https://doi.org/10.1007/s00425-005-1551-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-1551-3

Keywords

Search

Navigation