Plant Physiol. (1994) 105: 875-880
Early Gravi-Electrical Responses in Bean Epicotyls
Hideki Shigematsu, Kiyoshi Toko", Tetsuya Matsuno, and Kaoru Yamafuji
Department of Electronics, Faculty of Engineering, Kyushu University 36, Fukuoka 812, Japan
auxin-movement process leading to the laterally asymmetric
auxin distribution is not yet clear. Some investigators found
electrical lateral asymmetry in plants placed horizontally
(Lund, 1947; Grahm and Hertz, 1962; Tanada and VintenJohansen, 1980). Grahm and Hertz (1962) measured the
difference in electrical potential of horizontal coleoptiles between the lower side and the upper side with a vibrating
condenser electrometer. They observed an electrical asymmetry at 15 min after gravistimulation.
Tanada and Vinten-Johansen (1980) measured the development of a positive electrical potential on the lower side in
soybean hypocotyls at 1 min after gravistimulation. Wilkins
and Woodcock (1965) and Grahm (1964) considered that the
geoelectric effect is produced by an asymmetric auxin distribution in shoots curving upward after gravistimulation.
Imagawa et al. (1991)measured surface electrical potentials
along the upper and lower sides of intact epicotyls of adzuki
bean by attaching severa1 electrodes to the surface. This
system could detect rapid changes in electrical potential
throughout the process of gravitropism. The initial component of the potential change can be divided into two stages.
One stage is the first 15 min from the beginning of gravistimulation, in which the transient positive gravitropic response
could sometimes be observed. In the later stage, the upward
curvature (negative gravitropism) was observed. During the
first 15 min, the surface electrical potentials on the lower side
increased rapidly by about 15 mV and then decreased. At the
later stage, the potentials decreased on the upper side and
increased again on the lower side. The electrical phenomenon
at the first stage corresponds to the early event observed by
Tanada and Vinten-Johansen. The phenomenon at the later
stage resembles the event observed by Grahm and Hertz.
Imagawa et al. (1991) also discovered that the potentials
on the upper side decreased transiently by about 15 mV soon
after the horizontal placement. This large, spiky potential
change is the earliest observable event reported so far to
follow horizontal placement of epicotyls. The spiky potential
may take part in graviperception or it may be a signal from
the gravireceptor. Hence, there is a possibility that it is related
to the transient positive gravitropic response. Research on
this early event requires more detailed measurements of
electrical potentials soon after the gravistimulation. Therefore, in this paper we report the results of measurements of
the surface electrical potentials on the upper side of etiolated
epicotyls of adzuki bean (Phaseolus angularis) with a fast
sampling time rate (1 s) in the initial phase after gravistimulation. Many epicotyls showed large transient change of
surface electrical potentials. It is shown that the size of the
area where the potential change was observed had a consid-
l h e relationship between gravitropism and surface electrical
potentials was studied using etiolated epicotyls of adzuki bean
(Phaseolus angularis). Early downward curvature (or transient positive gravitropic response) was observed about 1 min after gravistimulation. The downward curvature was closely related to the
speed of the subsequent upward curvature. Surface electrical potentials decreased cooperatively in a limited region on the upper
side within only 0.5 to 2 min. This is the earliest event found so far
to follow gravistimulation of intact epicotyls. l h e rapid change in
the potential had a high correlation with the early downward
curvature and also the subsequent negative gravitropism. It is
suggested that the rapid potential change plays an important role
in gravity perception.
Gravitropism in the stem of plants placed horizontally is
attributed to the migration of auxin from the upper side to
the lower side, which causes differential growth (Wilkins,
1979). Auxin is known to enhance elongation at low concentrations, whereas it inhibits elongation at high concentrations
in both shoots and roots. However, shoots are less sensitive
to auxin than roots. The classical Cholodny-Went theory,
which attributes gravitropism to the asymmetric redistribution of auxin, is applicable to both horizontally oriented
shoots and horizontally oriented roots.
The transient positive gravitropic response (the initial
downward curvature, sometimes called the wrong-way response) was observed in stems (Brauner and Zipperer, 1961).
Hanison and Pickard (1989) showed that the transient positive gravitropic response is active, not passive, in tomato
hypocotyls on a 3-rpm clinostat. Hild and Hertel (1972)
studed gravitropism using two types of pre-gravistimulated
corn coleoptiles with regard to auxin transport. The transient
positive gravitropic response was observed in one group of
samples, whereas only a small response was observed in the
other group. In the former group, there was considerable
upward auxin transport at about 10 min after gravistimulation, i.e. after sudden resetting of the plant from vertical to
horizontal. In the latter group, there was a downward auxin
transport at the same time. These facts indicate that the
transient positive gravitropic response is induced by the
upward auxin transport. Other workers also observed an
upward auxin transport at about 10 min after gravistimulation in corn coleoptiles (Filner and Hertel, 1970) and in Zea
mays roots (Young et al., 1990). These experiments indicate
that the Cholodny-Went theory needs to be modified.
In spite of many reports on auxin transport, the detailed
* Corresponding author; fax 81-92-641-5866.
875
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Plant Physiol. Vol. 105, 1994
Shigematsu et al.
876
erable relationship with the transient positive gravitropic
response and also the subsequent negative gravitropism.
MATERIALS AND METHODS
Plant Material
Etiolated epicotyls of adzuki bean (Phaseolus angularis)
were used. The seeds were allowed to imbibe water kept 40
f l0C for 4 h and were arranged on a filter paper previously
moistened with 0.1 m~ KC1 and 0.05 mM CaC12solution. The
seeds germinated and were grown for 4 to 5 d in the dark
box (30.0 f 0.1OC with full humidity). Each seedling was
moved to an acrylic case filled with 0.01 mM KCl, 0.05 mM
CaC12and 1%agar solution, in which the root with cotyledon
was fixed. The epicotyls were maintained upright for 1 d in
the same dark box. The epicotyls that were straight and 40
to 130 mm long were selected for experiments.
Measurement System
The measurement system is the same as reported previously (Imagawa et al., 1991). The plant was placed on a stage
that was able to rotate the whole plant body from vertical to
horizontal. The surface electrical potentials became stable
after about 1 h, but they fluctuated for the 1st h because of
the mechanical perturbation of the pIant that accompanied
setting and application of the paste to the plant surface, etc.
Thus, gravistimulation was applied at 2 h after the plant was
set. The temperature and the humidity around the plant were
controlled at 31 f 2OC and 60 f 5%, respectively. A coupled
charged device camera (Hitachi KP-140) was used to observe
the epicotyl movement induced by gravistimulation. A dim
(60 lux at the plant surface) red light, which has a slight
effect of phototropism, was used for the observation. Although effects of red light on the gravitropism of hypocotyls
and roots of some plant species have been reported (Kelly
and Leopold, 1992; Liscum and Hangarter, 1993), gravitropism was not affected in the present species. The tip movements of epicotyls were recorded on video tape with I-min
intervals for 40 min after gravistimulation.
Measurements of Surface Electrical Potential
An electrical conductive paste, which is a mixture of 4.5 g
of starch, 7.5 mg of KCl, 20 mL of distilled water, and 10 mL
of glycerin, was used to connect electrically and physically
the surface of the epicotyl and Ag/AgCl wire electrodes, each
of which was 0.3 mm in radius and 7 mm in length with a
rounded tip. The paste did not affect the growth of the
epicotyl (Imagawa et al., 1991). The paste was applied carefully to a small area; if two regions were connected casually
by the paste, their electrical potentials showed similar behavior. Thus, we always checked whether the paste was applied
correctly or not. The electrodes were connected to a measurement circuit through narrow enamel-coated copper wires (50
pm in radius) that were sufficiently soft to prevent mechanical
stress to the epicotyl.
The Ag/AgC1 wire electrodes were arranged at about 5mm intervals on the upper side of the epicotyl. The measured
surface potentials of the epicotyl were loaded into a personal
computer through high-input impedance (1O” a)amplifiers
and analog-to-digital converters. A glass pipet electrode containing am Ag/AgCl wire, filled with 100 m~ KCl and 1%
agar, was used as a reference. The electrode was placed in
the mediiim in the stage in which the seedling was set.
The measurement of the surface electrical potential of the
epicotyl at I-s intervals started at 1 min before the gravistimulation and continued through 4 min.
Correlation Coefficient
Correlation coefficients between various quantities obtained in this experiment were calculated. The correlation
coefficierit Y between the dispersive data X and Y is given by
Bendat and Piersol(l971)
r = ((Xnyn)- (Xn)(Yn)1/{((Xn2)- (Xn)’)((Yn’) - (Yn)2))1’2
where X,, and Yn are the quantities of nth sample that characterize $i-avitropism,and (Z) is the mean value of Z (= X,,
Yn,etc.).
RESULTS
Figure 1 shows the time course of the deflection of the tip
after gravistimulation averaged over 28 epicotyls. ‘rhe tip was
defined as the basal position of the first leaves of epicotyls.
We can see that the etiolated epicotyl of adzuki bi2an moved
downward at the initial stage of gravitropism; it is a transient
positive gravitropic response.
Figure 2 shows the relationship between the “downward
deflection,” which is the maximum of the deflection, and the
“upward speed,” which is the average speed of thrt tip move-
.A
-I
O
B I
-
6-
E
E
3-
0I
I
I
20
O
40
Time (min)
Figure 1. A, Definition of deflection. Deflection meanj movement
of the tip (the basal position of the first leaves). 6, Average over
time sequences of deflections of 28 epicotyls. Vertical Iiars indicate
the SD.
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Copyright © 1994 American Society of Plant Biologists. All rights reserved.
Early Gravi-Electrical Responses in Epicotyls
A
O min
::i::::.
..
loweal pasilion
O
0.4 -
O
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8
0.2-
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30
0
877
other (b) at the first stage for 10 min. The upward speed of
epicotyl a at the second stage (i.e. over 10 min after gravistimulation) was faster than that of b. The spatio-temporal
pattems of the surface electrical potentials of samples a and
b are shown in Figure 4, a and b, respectively. The surface
potentials scarcely fluctuated in sample b, whereas the rapid
transient responses in surface potentials were observed in
sample a. From the data on sample a, we can see that the
surface potentials change coherently along the epicotyl surface and that the response-generating part forms a cluster
(localized pattem; see also Fig. 5) of severa1 millimeters in
length.
This experiment suggests a high correlation between the
epicotyl curvature and the rapid change in the surface electrical potentials at the initial phase. To confirm the correla-
O
oO%
0-
O
I
O
1
2
Downward deflection (mm)
Figure 2. A, Definition of downward deflection (left side) and
upward speed (right side). The downward deflection is t h e lowest
position of the tip movement. The upward speed is the average
speed of the tip movement between 20 and 40 min after gravistimulation. 6, Relationship between the downward deflection and
the upward speed.
76
80
ment between 20 and 40 min after gravistimulation. The
result indicates that the epicotyl exhibiting the larger downward deflection has the higher upward speed. Therefore, the
transient positive gravitropic response is related to the upward gravitropic response; this relation is also important
as the earliest observable morphogenetic phenomena of
gravitropism.
Figure 3 shows two typical sets of data on the course of
the upward and downward deflections of the tips of epicotyls.
One epicotyl (a) had a larger downward deflection than the
--'-;;---
105
I
I
I
I
O
I
2
I
Time (min)
13
17
28
22
833
E
E
38
4-
0-
I
I
I
I
I
I
I
O
I
2
I
Time (min)
O
10
20
30
Time (min)
Figure 3. Time course of the deflection of t h e tip. Two typical sets
of data are illustrated.
Surface electrical potentials along the epicotyl o n the
upper side. The numbers o n t h e left refer to the distance (mm)
from the base of the tip. Data in a and b correspond to a and b in
Figure 3, respectively, for epicotyl lengths of 117 and 67 mm.
Figure 4.
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Shigematsu et al.
878
I
3-3
Electrode
u
f
4-11-
6
3
Domain
o
Plant Physiol. Vol. 105, 1994
placed epicotyls, which were not tumed but were stimulated
by pulling in the horizontal direction with a string (Fig. 8).
The potential change in pulled epicotyls was similar to that
in gravistimulated epicotyls, but there are three differences
between the two cases. First, the electrical potential propagation along the axis of the epicotyl was not observed in
gravistimulated epicotyls (Fig. 4), but it was obseived in the
pulled epicotyls. Second, the narrow area in which the po-
1
2
Time (min)
Figure 5. Definition of a domain. Electrodes 1 through 6 are arranged along the epicotyl o n the upper side. The shaded portion is
the domain, because electrodes 2 through 5 show the potential
drop.
3
(a)
O
O
2-
O
O
O
tion, we characterized the change in the surface electrical
potentials quantitatively.
First, we use two criteria related to the magnitude and
duration of this rapid electrical change occurring at the earliest stage after gravistimulation. One criterion is that the
surface potential must decrease more than 3 mV, which is
sufficiently larger than the noise. The other is that it transiently keeps a constant value larger than 3 mV at least for a
few seconds between 30 and 120 s after gravistimulation. In
this paper, we cal1 the change satisfying the above criteria a
'potential drop." In 20 epicotyls (i.e. about 70% of 28 epicotyls), the potential drop was observed.
Second, we will use the term "domain" to refer to the
region where the potential drop was observed, as shown in
Figure 5. The electrodes were arranged at about 5-mm intervals, which corresponds to the spatial resolution in the measurement of the domain size. We defined the domain size as
the length between the most distant pair of points where
potential drops were observed.
The relationships between the domain size and the other
three kinds of data are shown in Figure 6, a to c. The domain
size correlates well with the other quantities. It is clear that
the epicotyl in which a larger domain size was observed had
a larger downward deflection. This type of epicotyl was
longer and exhibited the upward curvature with higher
speed. It is apparent that the domain size is an important
quantity for negative gravitropism, where the size is estimated from the changes in surface potentials for 3 min soon
after gravistimulation.
Figure 7,a and b, shows the dependence of the downward
deflection and the upward speed, respectively, on the epicotyl
length. These two quantities increased with increase in the
epicotyl length. The correlation coefficients among the four
quantities, i.e. the domain size, the downward deflection, the
upward speed, and the epicotyl length, are shown in the
legends of Figures 6 and 7. The 20 samples that exhibited the
potential drop were used to calculate the correlations. Because
a11 the correlation coefficients are larger than 0.6, the four
quantities have large correlations with each other.
The potential drop at the initial phase is not caused by the
gravitation-induced distortion of the epicotyl but by a gravitation-induced event such as sedimentation of amyloplasts,
as confirmed in Figure 8.
The surface electrical potentials were measured in vertically
O 0
O
I
I
O
20
Domain size (mm)
O
O
O
O
O
O
0
O
1
O
O
0.2
O.1
O
I
oo
8
o
o
O
I
I
I
O
20
Domain size (mm)
O
O
120-
O
O
0
8
O
@O
80O
I
1
O
o
O
0
20
Domain size (mm)
Figure 6. Relationships between t h e domain size and the other
three kinds of data, i.e. the downward deflection (a),the upward
speed (b),,and t h e epicotyl length (c). T h e correlation coefficients,
r, were 0.74 (a), 0.74 (b),and 0.66 (c).
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879
Early Gravi-Electrical Responses in Epicotyls
-
O
E
E
I
v
c
2
O
ü=
al
U
E
Q
B
C
3
O
n
40
80
120
Epicotyl length (mm)
.
h
.-c
E
E
E
v
O
O
8
O
O
U
O
W
n
v)
O
O'(I
0.2
6J0
em
3
5
40
80
120
Epicotyl length (mm)
Figure 7. Relationships between the epicotyl length and the down-
had no correlation with the upward speed, downward deflection, or domain size (data not shown). The epicotyl exhibiting a larger downward deflection showed a higher upward
speed in the subsequent phase of negative gravitropism
(Fig. 2).
The early surface potential change suggests the importance
of electrical phenomena in perception and/or transmission of
the information about gravity. Behrens et al. (1982) measured
the electric current around a root tip of Lepidium sativum L.
They observed the current flowing in the acropetal direction
on the upper side of the root cap and in the basipetal direction
on the lower side about 30 s after gravistimulation. Membrane potentials in statocytes were measured in roots after
gravistimulation (Behrens et al., 1985). The changes in the
membrane potentials were consistent with the observed extracellular electric currents, which strongly indicates that
there is an asymmetric surface potential. The surface electrical
potentials observed in epicotyls in the present study may
correspond to electric phenomena observed in roots. The
surface electrical potential may reflect the H+ concentration
or the H+ pump (or channel) activity. Accumulation of H+
and the electrical potential are closely related through electrical current loops inside and outside the stem (Toko et al.,
1989, 1990).
The electric current densities flowing at the stem surface
and out of the surface can be estimated easily from Figure
4a. The electric current of 0.9 pA/cm2 flows from a point at
60 mm to a point at 67 mm, and 4.8 pA/cm2 flows from a
point at 67 mm to a point at 71 mm, assuming 10' O/cm as
a typical value of electric resistance of the cell wall (Behrens
et al., 1985; Toko et al., 1989). Therefore, the electric current
out of the plant surface at the 67-mm point is estimated at
ward deflection (a) and the upward speed (b). The correlation
coefficients, r, were 0.72 (a) and 0.69 (b).
tential scarcely changed appeared inside the domain in 25%
of the gravistimulated epicotyls that showed the potential
drop. However, this type of area did not appear in the pulled
epicotyls. Third, the magnitude of potential change was about
10 mV in gravistimulated epicotyls, which was much smaller
than the potential change of about 100 mV found in pulled
epicotyls. Therefore, it is concluded that the potential changes
in these two situations may arise from different mechanisms.
40
DISCUSSION
The following facts were obtained in the present study: (a)
Downward curvature (transient positive gravitropic response)
was observed with etiolated epicotyls of adzuki bean about
1 min after gravistimulation. (b) The surface electrical potentials decreased simultaneously in a limited region on the
upper side of the epicotyl soon after gravistimulation.This is
the earliest event observed in intact epicotyls after gravistimulation. (c) Each pair of the four quantities measured, i.e.
the domain size, the downward deflection, the speed of
upward curvature (upward speed), and the epicotyl length,
had a close relationship with each other. The term "domain"
refers to the region where the early potential decrease (potential drop) was observed. The magnitude of potential drop
73
3
t
I
I
1
I
I
O
2
4
I
I
Time (min)
Figure 8. Surface electrical potentials at various distances (mm)
from the base of the tip in epicotyls pulled in the horizontal
direction. The sampling time interval was 15 s. The bidirectional
propagation can be seen from the 50-mm point. The propagation
speed is about 40 mm/min.
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880
Shigematsu et al.
3.9 pA/cm2. This value is of an order comparable to that
reported for roots under gravistimulation (Behrens et ,aL,
1982; Weisenseel et al., 1992).
The surface potentials on the lower side of epicotyls
scarcely changed for about 1 min after gravistimulation, as
previously indicated (Imagawa et al., 1991). The relative
potential of the upper side measured from the lower side
decreased both at the surface of epicotyls in the present study
and in the statocytes of roots (Behrens et al., 1985) soon after
gravistimulation. This fact can be reasonably explained. The
maximum value of the potential change at the surface of
epicotyls had the same order of magnitude as that in the
statocytes of roots. The fact that a similar potential change
was observed in different organs after gravistimulation implies a common mechanism underlying gravistimulation in
stems and roots.
The potential change found here is the earliest observable
event so far reported in intact epicotyls after gravistimulation.
It intimately correlates with the downward curvature and
also with the subsequent negative gravitropism. Sequential
processes may occur at the early stage after gravistimulation:
gravi-perceptible cells respond to gravistimulation by sedimentation of amyloplasts. A cooperative electrochemical
process (e.g. opening of ion channels) extending over many
cells causes a coherent change of the surface electrical potentia1 along the epicotyl surface. The domain is formed. The
cooperative electrical field induces redistribution of some ions
and some growth hormones (Jaffe, 1979; Desrosiers and
Bandurski, 1988), as observed: the concentration of auxin
changed in the upper half at about 10 min after gravistimulation (Filner and Hertel, 1970; Hild and Hertel, 1972; Young
et al., 1990). Then each cell elongates to an extent that is
dependent on its capacity for elongation and the quantity of
growth hormones. In fact, the curving of the epicotyl was
observed within less than 50 mm from the tip (Imagawa et
al., 1991), whereas the potential drop appeared in the region
where curvature was scarcely observed (Fig. 4). Gravitropism
(transient positive gravitropic response) occurs as a result of
asymmetric growth triggered by the above chemical process.
Although we do not know the causal relationship between
the transient positive gravitropic response and the subsequent
negative gravitropism, this transient response may be a key
to important information on the mechanism of gravitropism.
ACKNOWLEDCMENT
We thank Mr. Hideo Adachi for assistance with the experimental
work.
Received December 13, 1993; accepted March 21, 1994.
Copyright Clearance Center: 0032-0889/94/105/0875/06.
Plant Physiol. Vol. '105, 1994
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