Abstract
Numerous biological assays and pharmacological studies have led to the suggestion that depolarization-activated plasma membrane Ca2+ channels play prominent roles in signal perception and transduction processes during growth and development of higher plants. The recent application of patch-clamp techniques to isolated carrot protoplasts has led to direct voltage-clamp evidence for the existence of Ca2+ channels activated by physiological depolarizations in the plasma membrane of higher plant cells. However, these voltage-dependent Ca2+ channels were not stable and their activities decreased following the establishment of whole-cell recordings. We show here that large pre-depolarizing pulses positive to 0 mV induced not only the recovery of Ca2+ channel activities, but also the activation of initially quiescent voltage-dependent Ca2+ channels in the plasma membrane (recruitment). This recruitment was dependent on the intensity and duration of membrane depolarizations, i.e. the higher and longer the pre-depolarization, the greater the recruitment. Pre-depolarizing pulses to +118 mV during 30 s increased the initial calcium currents 5- to 10-fold. The recruited channels were permeable to Ba2+ and Sr2+ ions. The data suggested that voltage-dependent Ca(2+)-permeable channels are regulated by biological mechanisms which might be induced by large pre-depolarizations of the plasma membrane. In addition, this study provides evidence for the existence in the plasma membrane of higher plant cells of a large number of voltage-dependent Ca2+ channels of which a major part are inactive and quiescent. It is suggested that quiescent Ca2+ channels can be rapidly recruited for Ca(2+)-dependent signal transduction.
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Selected References
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- Artalejo C. R., Rossie S., Perlman R. L., Fox A. P. Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffin cells. Nature. 1992 Jul 2;358(6381):63–66. doi: 10.1038/358063a0. [DOI] [PubMed] [Google Scholar]
- Becker P. L., Singer J. J., Walsh J. V., Jr, Fay F. S. Regulation of calcium concentration in voltage-clamped smooth muscle cells. Science. 1989 Apr 14;244(4901):211–214. doi: 10.1126/science.2704996. [DOI] [PubMed] [Google Scholar]
- Bush D. S. Regulation of Cytosolic Calcium in Plants. Plant Physiol. 1993 Sep;103(1):7–13. doi: 10.1104/pp.103.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cosgrove D. J., Hedrich R. Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta. 1991 Dec;186(1):143–153. doi: 10.1007/BF00201510. [DOI] [PubMed] [Google Scholar]
- Ehrhardt D. W., Atkinson E. M., Long S. R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science. 1992 May 15;256(5059):998–1000. doi: 10.1126/science.10744524. [DOI] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Huang J. W., Grunes D. L., Kochian L. V. Voltage-dependent Ca2+ influx into right-side-out plasma membrane vesicles isolated from wheat roots: characterization of a putative Ca2+ channel. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3473–3477. doi: 10.1073/pnas.91.8.3473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleppisch T., Pedersen K., Strübing C., Bosse-Doenecke E., Flockerzi V., Hofmann F., Hescheler J. Double-pulse facilitation of smooth muscle alpha 1-subunit Ca2+ channels expressed in CHO cells. EMBO J. 1994 Jun 1;13(11):2502–2507. doi: 10.1002/j.1460-2075.1994.tb06538.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luan S., Li W., Rusnak F., Assmann S. M., Schreiber S. L. Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2202–2206. doi: 10.1073/pnas.90.6.2202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neher E. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 1992;207:123–131. doi: 10.1016/0076-6879(92)07008-c. [DOI] [PubMed] [Google Scholar]
- 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]
- Schroeder J. I., Thuleau P. Ca2+ Channels in Higher Plant Cells. Plant Cell. 1991 Jun;3(6):555–559. doi: 10.1105/tpc.3.6.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sculptoreanu A., Rotman E., Takahashi M., Scheuer T., Catterall W. A. Voltage-dependent potentiation of the activity of cardiac L-type calcium channel alpha 1 subunits due to phosphorylation by cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10135–10139. doi: 10.1073/pnas.90.21.10135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sculptoreanu A., Scheuer T., Catterall W. A. Voltage-dependent potentiation of L-type Ca2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature. 1993 Jul 15;364(6434):240–243. doi: 10.1038/364240a0. [DOI] [PubMed] [Google Scholar]
- Spalding E. P., Cosgrove D. J. Large plasma-membrane depolarization precedes rapid blue-light-induced growth inhibition in cucumber. Planta. 1989;178:407–410. [PubMed] [Google Scholar]
- Thuleau P., Graziana A., Canut H., Ranjeva R. A 75-kDa polypeptide, located primarily at the plasma membrane of carrot cell-suspension cultures, is photoaffinity labeled by the calcium channel blocker LU 49888. Proc Natl Acad Sci U S A. 1990 Dec 15;87(24):10000–10004. doi: 10.1073/pnas.87.24.10000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thuleau P., Graziana A., Ranjeva R., Schroeder J. I. Solubilized proteins from carrot (Daucus carota L.) membranes bind calcium channel blockers and form calcium-permeable ion channels. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):765–769. doi: 10.1073/pnas.90.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thuleau P., Graziana A., Rossignol M., Kauss H., Auriol P., Ranjeva R. Binding of the phytotoxin zinniol stimulates the entry of calcium into plant protoplasts. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5932–5935. doi: 10.1073/pnas.85.16.5932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Ullrich C. I., Novacky A. J. Electrical Membrane Properties of Leaves, Roots, and Single Root Cap Cells of Susceptible Avena sativa: Effect of Victorin C. Plant Physiol. 1991 Mar;95(3):675–681. doi: 10.1104/pp.95.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Williamson R. E., Ashley C. C. Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature. 1982 Apr 15;296(5858):647–650. doi: 10.1038/296647a0. [DOI] [PubMed] [Google Scholar]
