Abstract
Numerous biological assays and pharmacological studies on various higher plant tissues have led to the suggestion that voltage-dependent plasma membrane Ca2+ channels play prominent roles in initiating signal transduction processes during plant growth and development. However, to date no direct evidence has been obtained for the existence of such depolarization-activated Ca2+ channels in the plasma membrane of higher plant cells. Carrot suspension cells (Daucus carota L.) provide a well-suited system to determine whether voltage-dependent Ca2+ channels are present in the plasma membrane of higher plants and to characterize the properties of putative Ca2+ channels. It is known that both depolarization, caused by raising extracellular K+, and exposure to fungal toxins or oligogalacturonides induce Ca2+ influx into carrot cells. By direct application of patch-clamp techniques to isolated carrot protoplasts, we show here that depolarization of the plasma membrane positive to -135 mV activates Ca(2+)-permeable channels. These voltage-dependent ion channels were more permeable to Ca2+ than K+, while displaying large permeabilities to Ba2+ and Mg2+ ions. Ca(2+)-permeable channels showed slow and reversible inactivation. The single-channel conductance was 13 pS in 40 mM CaCl2. These data provide direct evidence for the existence of voltage-dependent Ca2+ channels in the plasma membrane of a higher plant cell and point to physiological mechanisms for plant Ca2+ channel regulation. The depolarization-activated Ca(2+)-permeable channels identified here could constitute a regulated pathway for Ca2+ influx in response to physiologically occurring stimulus-induced depolarizations in higher plant cells.
MeSH Terms
Calcium Channels/metabolism
Cations, Divalent/metabolism
Cell Membrane/metabolism
Cell Membrane Permeability/physiology
Membrane Potentials/physiology
Protoplasts/metabolism
Signal Transduction/physiology
Vegetables/cytology,metabolism
Chemicals
Calcium Channels
Cations, Divalent
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Thuleau P
Department of Biology, University of California, San Diego, La Jolla 92093-0116.
Ward J M
Ranjeva R
Schroeder J I
References (26)
26 references, click to expand
-
Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
Pflugers Arch. 1981 Aug;391(2):85-100
PMID: 6270629
-
Calcium channels in vertebrate cells.
Annu Rev Neurosci. 1990;13:337-56
PMID: 2158265
-
Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts.
Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3591-5
PMID: 1533046
-
Large plasma-membrane depolarization precedes rapid blue-light-induced growth inhibition in cucumber.
Planta. 1989;178:407-10
PMID: 11537725
-
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
PMID: 12244253
-
Regulation of calcium concentration in voltage-clamped smooth muscle cells.
Science. 1989 Apr 14;244(4901):211-4
PMID: 2704996
-
Calcium channel antagonists induce direct inhibition of the outward rectifying potassium channel in tobacco protoplasts.
FEBS Lett. 1994 Feb 28;340(1-2):45-50
PMID: 8119406
-
Free calcium increases during anaphase in stamen hair cells of Tradescantia.
J Cell Biol. 1987 Nov;105(5):2137-43
PMID: 3680374
-
Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors.
Science. 1992 May 15;256(5059):998-1000
PMID: 10744524
-
Sodium and calcium channels in bovine chromaffin cells.
J Physiol. 1982 Oct;331:599-635
PMID: 6296372
-
Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L.
Planta. 1991 Dec;186(1):143-53
PMID: 11538499
-
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):10000-4
PMID: 11607139
-
Rhythmic and phytochrome-regulated changes in transmembrane potential in samanea pulvini.
Nature. 1975 May 29;255(5507):408-10
PMID: 165432
-
Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells.
Trends Biochem Sci. 1989 May;14(5):187-92
PMID: 2475930
-
Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells.
EMBO J. 1990 Dec;9(12):3889-92
PMID: 1701140
-
Correction for liquid junction potentials in patch clamp experiments.
Methods Enzymol. 1992;207:123-31
PMID: 1528115
-
Binding of the phytotoxin zinniol stimulates the entry of calcium into plant protoplasts.
Proc Natl Acad Sci U S A. 1988 Aug;85(16):5932-5
PMID: 16593970
-
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):9305-9
PMID: 2174559
-
Intercellular communication in plants: Evidence for a rapidly generated, bidirectionally transmitted wound signal.
Proc Natl Acad Sci U S A. 1981 Apr;78(4):2422-6
PMID: 16593006
-
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):675-81
PMID: 16668038
-
Free Ca2+ and cytoplasmic streaming in the alga Chara.
Nature. 1982 Apr 15;296(5858):647-50
PMID: 7070508
-
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):765-9
PMID: 11607356
-
Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum-sensitive wheat cultivars.
Plant Physiol. 1992 Jan;98(1):230-7
PMID: 16668619
-
Voltage dependence of K channels in guard-cell protoplasts.
Proc Natl Acad Sci U S A. 1987 Jun;84(12):4108-12
PMID: 16593851
-
Three types of neuronal calcium channel with different calcium agonist sensitivity.
Nature. 1985 Aug 1-7;316(6027):440-3
PMID: 2410796
-
Calcium channels, stores, and oscillations.
Annu Rev Cell Biol. 1990;6:715-60
PMID: 2177344