Activation Kinetics of the K
+
Outward Rectifying Conductance (KORC) in Xylem
Parenchyma Cells from Barley Roots
L.H. Wegner*, A.H. De Boer
Faculty of Biology, Department of Molecular Genetics, Section of Plant Physiology, Vrije Universiteit Amsterdam, De Boelelaan 1087,
1081HV Amsterdam, The Netherlands
Received: 20 November 1998/Revised: 1 April 1999
Abstract. The activation kinetics of outward currents in
protoplasts from barley root xylem parenchyma was in-
vestigated using the patch-clamp technique. The K
+
out-
ward rectifying conductance (KORC), providing the
main pathway for K
+
transport to the xylem, could be
described in terms of a Hodgkin-Huxley model with four
independent gates. Gating of KORC depended on volt-
age and the external K
+
concentration. An increase in
the external K
+
concentration resulted in a shift in the
voltage dependence of gating. This could be explained
by a K
+
dependence of the rate constant b for channel
closure, indicating binding of K
+
to a regulatory site
exposed to the bath. Occasionally, KORC was observed
to inactivate; this inactivation occurred and vanished
spontaneously. In some of the whole cell and excised
patch recordings, a stepwise increase in outward current
was observed upon a depolarizing voltage pulse, indicat-
ing that several populations of ‘sleepy’ channels existed
in the plasma membrane that activated with a certain lag
time. It is discussed whether this observation can be ex-
plained by a putative subunit, which retards channel ac-
tivation, or by a scheme of cooperative gating. A quan-
titative description of outward rectifying K
+
channels in
xylem parenchyma cells is a major step forward towards
a mathematical model of salt transport into the xylem.
Key words: Plant ion channel — Hodgkin-Huxley for-
malism — Cooperative gating — K
+
dependent gating
Introduction
Release of K
+
by xylem parenchyma cells in the root
occurs via outwardly rectifying K
+
channels (KORCs) in
the plasma membrane of these cells (Wegner & Raschke,
1994; Roberts & Tester, 1995, 1997; Wegner & De Boer,
1997). The central role of these channels for the trans-
location of potassium from the root to the shoot was first
demonstrated by Wegner and De Boer (1997). By per-
fusing the stele of young barley seedlings with the K
+
channel blocker TEA, accumulation of K
+
in the shoot
was completely inhibited. Further evidence for K
+
chan-
nels serving as major pathways for K
+
release to the
xylem sap came from the recent report by Gaymard et al.
(1998) on the cloning of a K
+
outward rectifier exclu-
sively expressed in root stelar cells of Arabidopsis
(SKOR, stelar K
+
outward rectifier). A highly homolo-
gous sequence with a similar expression pattern has also
been found in maize, (C. Alcon and H. Sentenac, per-
sonal communication), suggesting that SKOR may be
common to dicots and monocots. In knockout mutants
of Arabidopsis lacking SKOR, shoot K
+
content and xy-
lem sap concentration of K
+
were reduced significantly.
The electrophysiological properties of SKOR were stud-
ied by heterologous expression in Xenopus oocytes.
Several lines of evidence indicate that the properties of
SKOR are identical with those of KORC (Wegner & De
Boer, 1997; Gaymard et al., 1998): (i) The activation
potential of the channel shifts with a change in the ex-
ternal K
+
concentration, (ii) whole cell currents activate
with sigmoidal kinetics upon a stepwise depolarization
of the membrane, (iii) besides K
+
, the channel translo-
cates Ca
2+
, (iv) the expression of SKOR is down-
regulated by the phytohormone ABA, leading to a de-
crease of the outward K
+
currents in stelar cells when
plants were pretreated with ABA (Roberts, 1998).
*Present address: Am Lehrstuhl fu ¨ r Biotechnologie, Universita ¨t Wu ¨rz-
burg, Biozentrum, Am Hubland, D-97074 Wu ¨rzburg, Germany
Correspondence to: L.H. Wegner
J. Membrane Biol. 170, 103–119 (1999) The Journal of
Membrane
Biology
© Springer-Verlag New York Inc. 1999