Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1995 Jun 15;14(12):2708–2714. doi: 10.1002/j.1460-2075.1995.tb07271.x

Gadolinium-sensitive, voltage-dependent calcium release channels in the endoplasmic reticulum of a higher plant mechanoreceptor organ.

B Klüsener 1, G Boheim 1, H Liss 1, J Engelberth 1, E W Weiler 1
PMCID: PMC398389  PMID: 7796799

Abstract

The lipid bilayer technique was adapted to the functional reconstitution of ion channels from the endoplasmic reticulum of a higher plant. This was obtained at high purity from touch-sensitive tendrils of Bryonia dioica. In this preparation, a calcium-selective strongly rectifying channel is prevailing whose single-channel properties have been characterized. The single-channel conductance is 29 pS in 50 mM CaCl2. The Ca2+: K+ selectivity was determined to be approximately 6.6. The channel is voltage-gated and, more importantly, the gating voltage is strongly shifted towards more negative voltages when a transmembrane Ca2+ gradient is applied. Thus, at physiological voltages across the endoplasmic reticulum membrane, the channel's open probability will be governed largely by the chemical potential gradient of Ca2+, generated by the Ca(2+)-ATPase in that same membrane. The calcium release channel described here is effectively blocked by Gd3+ which also completely suppresses a tendril's reaction to touch, suggesting that this channel could be a key element of calcium signaling in higher plant mechanotransduction. Its molecular characteristics and inhibitor data show it to be the first known member of a hitherto unrecognized class of calcium channels.

Full text

PDF
2708

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen G. J., Sanders D. Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells. Plant Cell. 1994 May;6(5):685–694. doi: 10.1105/tpc.6.5.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boheim G., Hanke W., Barrantes F. J., Eibl H., Sakmann B., Fels G., Maelicke A. Agonist-activated ionic channels in acetylcholine receptor reconstituted into planar lipid bilayers. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3586–3590. doi: 10.1073/pnas.78.6.3586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Braam J., Davis R. W. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell. 1990 Feb 9;60(3):357–364. doi: 10.1016/0092-8674(90)90587-5. [DOI] [PubMed] [Google Scholar]
  4. Ding J. P., Pickard B. G. Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J. 1993 May;3(5):713–720. [PubMed] [Google Scholar]
  5. Elinder F., Arhem P. Effects of gadolinium on ion channels in the myelinated axon of Xenopus laevis: four sites of action. Biophys J. 1994 Jul;67(1):71–83. doi: 10.1016/S0006-3495(94)80456-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gilroy S., Fricker M. D., Read N. D., Trewavas A. J. Role of Calcium in Signal Transduction of Commelina Guard Cells. Plant Cell. 1991 Apr;3(4):333–344. doi: 10.1105/tpc.3.4.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hanke W., Boheim G., Barhanin J., Pauron D., Lazdunski M. Reconstitution of highly purified saxitoxin-sensitive Na+-channels into planar lipid bilayers. EMBO J. 1984 Mar;3(3):509–515. doi: 10.1002/j.1460-2075.1984.tb01839.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jafri M. S., Gillo B. A membrane potential model with counterions for cytosolic calcium oscillations. Cell Calcium. 1994 Jul;16(1):9–19. doi: 10.1016/s0143-4160(05)80003-x. [DOI] [PubMed] [Google Scholar]
  9. Kendall J. M., Dormer R. L., Campbell A. K. Targeting aequorin to the endoplasmic reticulum of living cells. Biochem Biophys Res Commun. 1992 Dec 15;189(2):1008–1016. doi: 10.1016/0006-291x(92)92304-g. [DOI] [PubMed] [Google Scholar]
  10. Knight M. R., Campbell A. K., Smith S. M., Trewavas A. J. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature. 1991 Aug 8;352(6335):524–526. doi: 10.1038/352524a0. [DOI] [PubMed] [Google Scholar]
  11. Knight M. R., Smith S. M., Trewavas A. J. Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4967–4971. doi: 10.1073/pnas.89.11.4967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lacampagne A., Gannier F., Argibay J., Garnier D., Le Guennec J. Y. The stretch-activated ion channel blocker gadolinium also blocks L-type calcium channels in isolated ventricular myocytes of the guinea-pig. Biochim Biophys Acta. 1994 Apr 20;1191(1):205–208. doi: 10.1016/0005-2736(94)90250-x. [DOI] [PubMed] [Google Scholar]
  13. Lee K. S., Tsien R. W. High selectivity of calcium channels in single dialysed heart cells of the guinea-pig. J Physiol. 1984 Sep;354:253–272. doi: 10.1113/jphysiol.1984.sp015374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Meissner G. Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum. Mol Cell Biochem. 1983;55(1):65–82. doi: 10.1007/BF00229243. [DOI] [PubMed] [Google Scholar]
  15. Pantoja O., Gelli A., Blumwald E. Voltage-dependent calcium channels in plant vacuoles. Science. 1992 Mar 20;255(5051):1567–1570. doi: 10.1126/science.255.5051.1567. [DOI] [PubMed] [Google Scholar]
  16. Petersen C. C., Petersen O. H., Berridge M. J. The role of endoplasmic reticulum calcium pumps during cytosolic calcium spiking in pancreatic acinar cells. J Biol Chem. 1993 Oct 25;268(30):22262–22264. [PubMed] [Google Scholar]
  17. Ping Z., Yabe I., Muto S. Voltage-dependent Ca2+ channels in the plasma membrane and the vacuolar membrane of Arabidopsis thaliana. Biochim Biophys Acta. 1992 Dec 9;1112(2):287–290. doi: 10.1016/0005-2736(92)90404-a. [DOI] [PubMed] [Google Scholar]
  18. Rink T., Bartel H., Jung G., Bannwarth W., Boheim G. Effects of polycations on ion channels formed by neutral and negatively charged alamethicins. Eur Biophys J. 1994;23(3):155–165. doi: 10.1007/BF01007607. [DOI] [PubMed] [Google Scholar]
  19. Schroeder J. I., Hagiwara S. Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9305–9309. doi: 10.1073/pnas.87.23.9305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stephenson D. G., Wendt I. R., Forrest Q. G. Non-uniform ion distributions and electrical potentials in sarcoplasmic regions of skeletal muscle fibres. Nature. 1981 Feb 19;289(5799):690–692. doi: 10.1038/289690a0. [DOI] [PubMed] [Google Scholar]
  21. Thuleau P., Ward J. M., Ranjeva R., Schroeder J. I. Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell. EMBO J. 1994 Jul 1;13(13):2970–2975. doi: 10.1002/j.1460-2075.1994.tb06595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tsien R. W., Tsien R. Y. Calcium channels, stores, and oscillations. Annu Rev Cell Biol. 1990;6:715–760. doi: 10.1146/annurev.cb.06.110190.003435. [DOI] [PubMed] [Google Scholar]
  23. Ward J. M., Schroeder J. I. Calcium-Activated K+ Channels and Calcium-Induced Calcium Release by Slow Vacuolar Ion Channels in Guard Cell Vacuoles Implicated in the Control of Stomatal Closure. Plant Cell. 1994 May;6(5):669–683. doi: 10.1105/tpc.6.5.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Weiler E. W., Kutchan T. M., Gorba T., Brodschelm W., Niesel U., Bublitz F. The Pseudomonas phytotoxin coronatine mimics octadecanoid signalling molecules of higher plants. FEBS Lett. 1994 May 23;345(1):9–13. doi: 10.1016/0014-5793(94)00411-0. [DOI] [PubMed] [Google Scholar]
  25. Yang X. C., Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 1989 Feb 24;243(4894 Pt 1):1068–1071. doi: 10.1126/science.2466333. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES