Plant Science 132 (1998) 203 – 213
Electrical signaling and gas exchange in maize plants of drying
soil
Jörg Fromm a,*, Houman Fei b
a
Institute for Wood Research, Uni6ersity of Munich, Winzererstrasse 45, 80797 Munich, Germany
b
Department of Biology, Uni6ersity of Saskatchewan, Saskatoon S7N 5E2, Canada
Received 11 February 1997; received in revised form 12 January 1998; accepted 13 January 1998
Abstract
The involvement of electrical signaling in the regulation of gas exchange was checked with maize plants subjected
to a drying cycle of 5 days in a controlled environment. Gas exchange and extracellular electrical potential
measurements were made on attached leaves. The CO2 uptake and transpiration rate decreased in drying soil and
increased to their original values after irrigation. Continuous records of the electrical potential difference between two
surface points were made on the same leaf on which the gas measurements were performed. A daily rhythm was
clearly visible and seemed to be correlated with the soil water status. After soil drying the plants were watered and
increases in CO2 and H2O exchange have been demonstrated to follow the arrival of an electrical signal in the leaves.
When a dye solution was applied to the roots its uptake and movement to the leaves was observed continuously by
microscopy showing that the increase of gas exchange 12 – 15 min after irrigation could not be triggered by water
ascent. By using severed aphid stylets it was shown that sieve tubes served as a pathway for electrical signal
transmission. Furthermore, roots were water-stressed by addition of non-penetrating osmolyte to the root medium.
The gas exchange of the leaves decreased clearly 6 min after application of polyethylene glycol 6000 (PEG, − 0.5
MPa water potential). Comparative measurements of the sieve tube electrical potential indicated that PEG-induced
water stress evoked a propagating depolarization of the potential. Other osmolytes (100 mM NaCl) caused similar
results showing that the leaf responses are not related to any specific toxic effect of PEG. Thus, the results strongly
support the view that electrical signaling plays an important role in root to shoot communication of water-stressed
plants. © 1998 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Electrical surface potential; Gas exchange (drought effect); Sieve tube membrane potential; Water stress;
Zea mays L
* Corresponding author. Tel.: +49 89 3063090; fax: +49 89 30630911; e-mail: [email protected]
0168-9452/98/$19.00 © 1998 Elsevier Science Ireland Ltd. All rights reserved.
PII S0168-9452(98)00010-7
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J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
1. Introduction
In recent years non-hydraulic signaling between
roots and shoots of plants growing in drying soil
has evoked considerable interest. Based on observations that plants subjected to soil drying exhibited stomatal closure and leaf growth inhibition
before reductions in leaf turgor were measured, it
is discussed that non-hydraulic signals from roots
may serve as a sensitive link between soil water
changes and responses of the shoot [1]. The purpose of the present study is to demonstrate that
large shifts in gas exchange also rapidly follow the
transmission of electrical signals from the roots to
the leaves. Our data clearly show that a rapid
increase of gas exchange after irrigation can not
be triggered by water ascent in the xylem. Evidence for electrical signaling was obtained by
both,
extraand
intracellular
potential
measurements.
Extracellular potential measurements on the
surface of higher plants have been widely performed in the past. By this method action potentials and slow waves of depolarization were
studied in a number of species, among them Mimosa pudica [2–4], Helianthus annuus [5], Bidens
pilosa [6] and Salix 6iminalis [7]. In contrast to
intracellular measurements with penetrating glass
microelectrodes, extracellular recordings have the
advantage of detecting electrical potential differences over long periods like several days. Up to
now, such continuous records have been made in
the cambial region of various tree species, showing daily and yearly rhythms as well as 5 min
oscillations related to cambial growth [8]. However, cambial measurements cause wound reactions by electrode insertion. Therefore, surface
measurements seem to be more suitable, at least
for measurements up to periods of 1 week. They
are non-invasive, physical stable and can be performed simultaneously with gas exchange measurements. This seems to be worthwhile because
stomatal size provides information on the soil
water content [9] and wetting dry roots is known
to be an extremely effective way to produce action
potentials [10].
In addition, by using severed aphid stylets the
electrical potential of sieve tubes was measured as
firstly described by Wright and Fisher [11]. These
experiments were carried out to compare the extracellularly measured signals with intracellular
recordings and also to check a role of the phloem
in long-distance transmission of electrical signals.
Finally the effect of PEG-induced water stress on
the gas exchange and sieve tube potential was
investigated. The results clearly show that electrical signaling is involved in root to shoot communication of plants under water stress.
2. Material and methods
2.1. Plant material
Maize plants (Zea mays L.) were grown in
growth chambers under a light intensity of 300
mmol m − 2 s − 1 provided by mercury halide lamps
in a 14/10 h light/dark period at a temperature of
25°C and 50–60% rel. humidity. The soil contained all nutrients essential for plant growth and
was composed of 50% peat, 35% clay and 15%
humus (pH 6.0). A second group of plants was
grown in nutrient solution, composed of 5 mM
KNO3, 5 mM Ca(NO3)2, 2 mM MgSO4, 1 mM
KH2PO4, 50 mM KCl, 40 mM Fe-EDTA, 25 mM
H3BO3, 5 mM MnSO4, 2 mM ZnSO4 and 0.5 mM
CuSO4 (pH 6.0).
2.2. Experimental set-up
When maize plants grown in soil had about ten
leaves they were placed in a Faraday cage on a
digital balance to determine changes of the soil
water content during the experiment (Fig. 1). The
growth conditions were the same as in the climate
chambers. Four different plants of each species
were investigated. After irrigation the weight of
the plant-soil-system was determined from the
beginning to the end of the 5 day-long experiment. Then the shoot was cut off and the soil was
dried in an oven at 80°C to determine its dry
weight which was added to the shoot weight. The
difference between this sum and the weight measured before is the weight (%) of the soil water
which was multiplied by the soil density to determine the soil water content (Vol.%).
J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
2.3. Surface electrode technique
After a plant was placed in the Faraday cage
the measuring electrode was attached to the upper
surface of a mature leaf at a distance of 10 – 20 cm
to the reference electrode attached to the shoot
surface (Fig. 1). Both electrodes consisted of Ag/
AgCl-wire 0.4 mm in diameter, moistened with
0.1% (w/v) KCl in agar and wrapped in cotton to
provide the appropriate contact with the plant
surface. They were connected to a differential
amplifier (Model 750, WPI, Sarasota, FL) and the
outputs were displayed on a chart recorder. Before an experiment started both electrodes were
calibrated (0 mV) together in 0.1% KCl solution.
2.4. Measurement of electric potential differences
in the phloem
The electric potential of sieve tubes was mea-
205
sured via severed aphid stylets. Briefly, aphids
(Rhopalosiphum padi ) were applied to a mature
leaf and allowed to settle overnight. On the following day they were severed from their stylets by
using a laser beam generator (Beck, Neu-Isenburg, FRG) connected to a Zeiss microscope.
When the stylet stump exuded sieve tube sap, the
droplet on the stylet was brought into contact
with the tip of a microelectrode by using a Leitz
micromanipulator. The glass microelectrodes had
tip diameters of approximately 1 mm and were
fabricated from microcapillaries (WPI, Sarasota)
by using a vertical electrode puller (Getra, Munich, FRG). They were backfilled with 100 mM
KCl, clamped in an Ag-AgCl pellet holder (WPI)
and connected to a microelectrode preamplifier
(input impedance \ 1012 ohms) to which a WPI
amplifier (Model 750) was attached. The resistance for an electric current inside the stylet is
relatively low (around 109 ohms according to
Wright and Fisher [11]) compared with the high
input impedance of the electric equipment used.
In all plants the reference electrode was brought
into contact with the stem surface via 100 mM
KCl in agar.
2.5. Gas exchange measurements
As shown in Fig. 1 the gas exchange was measured on the same leaf on which the measuring
electrode was fixed. Changes in CO2 concentration were detected with a porometer (Li-Cor Li
6000, Lincoln, WA) that simultaneously measured
the rate of transpiration. Series of measurements
were made 3–5 times per day during the whole
experiment, each starting at a CO2 concentration
of 400 ppm and a relative humidity of 50%. The
temperature in the leaf chamber was 25°C and the
light intensity 300 mmol photons m − 2 s − 1. The
analyzer was calibrated prior to each series of
measurements; the stability of the zero point was
checked by means of an air line that bypassed the
chamber with the leaf.
Fig. 1. Measurement of the electrical potential difference and
gas exchange on an attached leaf during a drying cycle of 5
days. To determine changes in the soil water status the plants
were placed on a balance.
2.6. Determination of water mo6ement
Water uptake by roots and movement to the
shoot was observed with 0.6% (w/v) amidoblack
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J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
solution in water by using a light microscope
(Zeiss Axioskop 20, Oberkochen, FRG). Photographs were taken with Kodak Ektachrome 64 T
artificial light films.
3. Results
3.1. Electric surface potential and gas exchange
Plants were irrigated at the beginning of a 5
day-long experiment and after 4 days when the
soil water content was strongly reduced. After
initial irrigation an electrical potential between
− 200 and − 250 mV was measured on the surface (Fig. 2(a), upper curve), showing a daily
rhythm with a negative maximum during the
light period and a minimum in the early morning before the light was switched on. Every
change from darkness to light and vice versa
caused a transient hyperpolarization with an average amplitude of 50 mV and a duration of
20 – 30 min. This rhythm diminished after 48 h
when the electrical potential remained low during the day (Fig. 2(a), upper curve). At this time
the soil water content was reduced to 32 Vol%,
in comparison to 43% at the beginning (Fig.
2(a), lower curve). In the following 2 days the
soil dried out to a water content of 15 Vol.%;
simultaneously the electrical potential decreased
to − 94 mV (after 96 h) and the amplitude of
the transient hyperpolarizations at dark/light
changes was reduced (25 mV). After watering
the roots (Fig. 2(a), arrow), the soil water content increased to 44 Vol.% and an action potential (ap) with an average amplitude of 50 mV
was evoked and measured on the leaf surface.
After transmission the electrical potential hyperpolarized to −265 mV, showing the same daily
rhythm during dark/light changes as in the beginning.
By using intracellular microelectrodes we also
measured the transmembrane electrical potential
difference in cells close to the two extracellular
electrodes and found mean values of − 102 mV
at the epidermal cells of the shoot and − 128
mV at cells of the leaf. Thus, large extracellular
potentials are not due to the difference between
the mean transmembrane potentials at the measured points. Obviously the potential difference
between the extracellular electrodes involves ion
diffusion potentials in the apoplast. It is known
that guard cells extrude protons when the stomata open, i.e. they give rise to an electric current
which is proportional to the degree of stomatal
opening and can be measured with a porometer
[12].
However, in Fig. 3 it is shown that alterations
in gas exchange following irrigation occured after electrical signaling, indicating no contribution
of stomatal currents to the rapid potential
changes.
In combination to the measurements of the
electric surface potential the gas exchange was
detected several times per day on the same
plants (Fig. 2(b)). CO2 uptake and transpiration
remained on a stable level until 72 h without
irrigation, then both rates decreased 2–3-fold in
drying soil to a minimum after 96 h. After watering the soil (arrow) a steep increase to the
original values was measured; at the same time
the electrical surface potential hyperpolarized.
The plant response upon irrigation was further
investigated by measuring the gas exchange rate
every 3 min. Fig. 3 shows the sequence of the
measured parameters in the first 24 min after
watering. At first the electrical surface potential
depolarized transiently to − 50 mV (action potential), followed by a hyperpolarization to −
150 mV about 10 min after irrigation (Fig. 3(a)).
At the same time the CO2 uptake rate began to
increase (Fig. 3( c)) while the transpiration rate
increased 15 min after watering (Fig. 3(b)).
To determine if the water ascent in the xylem
had reached the measured leaf at this time, a dye
solution (0.6% amidoblack) was applied to the
roots and its uptake and movement to the leaves
was observed continously by light microscopy. As
shown in Fig. 4(A) which was taken from a
section 4 mm behind the tip 15 min after dye
application, uptake of the solution by the roots
occurred at the outer cells of the cortex (left) from
which the solution moves to the protoxylem vessels (white arrow) of the central cylinder. At
higher magnification it becomes clear that only
Fig. 2. (a) Typical example of the daily rhythm of the electrical potential difference (voltage) in maize plants during soil drying and irrigation after 96 h. Continuous
soil drought causes depolarization while soil watering (arrow) generates an action potential (ap) followed by hyperpolarization. Black bars indicate dark periods. (b)
Measurement of CO2 uptake and transpiration (H2O) in maize plants during soil drying and irrigation after 96 h. Gas records were made five times per day, the data
are mean values from four plants.
J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
207
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J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
Fig. 3. Correlations between electrical potential changes and the rates of CO2 uptake and transpiration shortly after irrigation. (a)
Typical response of the electrical potential (voltage) in response to root watering. After 1 min an action potential is measured
followed by hyperpolarization. (b) Transpiration measurement on the same leaf as in a. every 3 min. Data are mean values 9 S.D.
from four plants. ( c) Simultaneous measurement of CO2 uptake. Both CO2 uptake and transpiration increase shortly after
measuring the action potential. Data are mean values9 S.D. from four plants. (d) Comparison of the speed of the transpiration
stream by using a dye solution with the speed of the propagated potential change after root watering. The measuring technique was
applied at a plant height of 60 cm.
Fig. 4. Uptake and movement of 0.6% amidoblack solution in maize: (A) Light micrograph of a cross section of the root 4 mm behind the tip. Outer cortex cells (left)
as well as the cells of the protoxylem (white arrow) appear blue-stained. Endodermis (E), cortex C, metaxylem vessel MV. Bar 50 mm. (B) At higher magnification
it is clearly shown that 15 min after dye application only the vessels of the protoxylem (white arrow) are blue-stained, indicating water transport towards the shoot.
Phloem (P), pericycle (Pe), endodermis (E), metaxylem vessel (MV), protoxylem vessel (PV). Bar 20 mm. (C) Cross section of the shoot showing transport of the dye
in the xylem (X) towards the leaves. Phloem P. Bar 50 mm. (D) Cross section of a vascular bundle of the measured leaf. Xylem vessels are blue-stained (white arrows)
indicating arrival of the dye solution in the leaf. Bundle sheath (BS), Phloem (P), Xylem (X). Bar 30 mm.
J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
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J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
the walls of the protoxylem vessels are stained
(Fig. 4(B), white arrow), but not those of the large
metaxylem vessels (Fig. 4(B), MV) which are located more central than the protoxylem vessels
(PV). The walls of the phloem (P), the pericycle
(Pe) and the endodermis (E) are less stained.
Thus, after 15 min the dye is present in the
protoxylem and moving acropetally. However, we
have no information about differences between
the diffusion rates of the dye and water from the
soil to the shoot. Since the dye must be transported across the different apoplastic territories
and endodermal cell membranes to the xylem
vessels, its movement could be slower than that of
water.
Cross sections from the shoot made 20 min
after dye application also clearly show bluestained xylem vessels indicating dye transport
with the transpiration stream (Fig. 4(C)). The dye
solution arrived after 24 min in the metaxylem
vessels of the measured leaf located 60 cm above
the roots (Fig. 4(D), white arrows), indicating a
speed of 2.5 cm min − 1. Thus, the increase of gas
exchange 12–15 min after irrigation was not likely
to be triggered by water ascent. Although water
from the soil may lead to an increase in the water
flux arriving at the leaves, such an increase can
not occur immediately over a distance of 60 cm.
In Fig. 3(d) the movement of the dye solution is
compared with the propagation of the electric
potential change from roots to leaves, which occured with a speed of 1 cm s − 1.
3.2. Action potentials in sie6e tubes during
changes of the root water status
As shown recently on maize, action potentials
caused by leaf cooling and electric shock are
transmitted in sieve tubes [13]. To check if the
extracellularly measured potential changes after
irrigation (Fig. 2(a), Fig. 3(a)) were also transmitted in the sieve tube system, we measured the
electric potential via severed aphid stylets during
watering the roots. The reference electrode contacted the stem surface while the measuring electrode was brought into contact with sieve tube
exudate. A resting potential of −145 912 mV
was measured in ten different plants (Fig. 5).
Fig. 5. Typical recording of the sieve tube electrical potential
via severed aphid stylets. Watering the roots (arrow) after a
drought period of 4 days induced a rapidly transmitted action
potential.
Following soil drought the plants were watered
and an action potential with the same amplitude,
transmission velocity and duration (Fig. 5) as
measured extracellularly (Fig. 3(a)) was detected.
Another group of plants was grown hydroponically and water stress was caused by addition of
polyethylene glycol 6000 (PEG) to the root nutrient solution. Addition of PEG to the root
medium evoked a rapidly propagating depolarization of the potential in the phloem (Fig. 6, above),
showing an amplitude of 50 mV. Thus, amplitude
and form of this signal are different in comparison to the signal induced by irrigation (Fig. 5).
After addition of PEG the gas exchange of the
leaves responded with a significant decrease of the
transpiration and CO2 uptake rate (Fig. 6). Similar results were obtained after treatment of the
root system with 100 mM NaCl (data not shown).
Therefore, the leaf responses are not related to
any specific toxic effect of PEG.
4. Discussion
It is well-known that plants respond to external
stimuli through processes that lead to morphological or physiological changes. According to Millet
[14] the classical steps of such processes are signal
reception, transduction, transmission and re-
J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
sponse. The latter raises the problem of long-distance communication in plants and emphasizes
the question of messengers.
With regard to water stress it is also known
that the physiology of the plant is changed upon
soil drying [1,9], even in the absence of any detectable changes of leaf water status. Thus, modifications in shoot physiology can mostly result
more closely from decrease in soil water availability than to changes in leaf water status [15].
Additionally, in pressurized plants where the leaf
water potential can be maintained at a high value,
the stomata showed a restricted conduction as the
soil dried [16]. Therefore stomata should be able
to receive information on the soil water status
independently from the leaf water potential. Evidence that the nature of this information is chemical was obtained by analyzing the xylem sap
from unwatered plants, indicating a contribution
of ion content, pH, amino acids and hormones
Fig. 6. Measurement of CO2 uptake (CO2) and transpiration
(H2O) during application of polyethylene glycol 6000 (PEG,
−0.5 Mpa water potential) to the root medium. The addition
evoked a depolarization of the phloem potential which is
transmitted with a velocity of 1 cm s − 1 to the leaves (above).
The time of PEG-addition is indicated by an arrow. Gas
records were made every 6 min after stimulation. Data are
mean values from ten experiments.
211
[17]. Especially the concentration of abscisic acid
increases in roots growing in drying soil [1]. The
hormone can be synthesized in roots [18,19] and
moves from roots to shoots primarily through the
xylem stream to restrict stomatal conductance.
Furthermore, a drought-induced pH increase of
the xylem sap was suggested [17,20], based on a
transmission of the pH change from roots to
shoots. Under drought stress pH shifts occur in
different leaf cell compartments, apparently
caused by an inhibition of proton-motive forces,
e.g. of the proton pumping ATPase at the plasmalemma [21]. Slovik and Hartung [22–24] described a model which predicts that the
drought-induced increase in apoplastic pH can
cause rapid stomatal closure through the symplastic release of ABA. As a weak acid ABA will
preferentially accumulate in the more alkaline
compartments of the unstressed leaf, i.e. in the
alkaline cytoplasm of mesophyll or epidermal
cells. Under drought stress the apoplastic pH
increases followed by ABA increase and stomatal
closure. Hartung [25] as well as Hornberg and
Weiler [26] showed that a group of ABA receptors
is located at the external surface of the plasmalemma. After binding ABA the receptors cause
changes in membrane ion transport, leading to a
reduction of turgor pressure and guard cell closure. Since stomatal closure starts a few minutes
after the onset of drought stress and differentiated
guard cells have no plasmodesmata, their apoplast
is the most relevant compartment for an ABAstress signal.
The still open question is how the leaf apoplast
will be alkalized rapidly after water-stressing the
roots. Following addition of PEG to the root
medium we measured a propagating depolarization in sieve tubes (Fig. 6), correlating to the
slowly occuring depolarization of the surface potential during soil drought (Fig. 2(a)). The PEGevoked signal propagates with a velocity of 1 cm
s − 1 towards the leaves which may be more rapid
than an alkalization of the transpiration stream.
In a former study it was shown that electrically
induced action potentials in maize leaves are generated by chloride, potassium and calcium fluxes
[13]. So far, it is unknown which ion fluxes build
up the PEG-induced depolarization at the roots.
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J. Fromm, H. Fei / Plant Science 132 (1998) 203–213
A H + -ATPase, hyperpolarizing the membrane
potential often more negative than − 150 mV,
was identified in maize coleoptile cells by Hedrich
et al. [27]. By using the patch clamp technique [28]
further experiments with phloem protoplasts have
to show if PEG-induced water stress inhibits the
proton pump transiently, leading to an alkalization of the apoplast.
Concerning the electric signal observed in response to irrigation, the potential change of sieve
tubes (Fig. 5) shows a close correlation to the
surface recordings (Fig. 3(a)), indicating that the
electric signals may be the primary responses of
the plant to the changes of the soil water content.
However, there is still another possible way in
which root water status could be signalled rapidly
to the shoot. This is by hydraulic means via the
xylem. Hydraulic signals have been the subject of
recent debate in the literature [29 – 31]. When the
soil of a dry plant is watered, leaf water status
must rise because the pressure of water in the
xylem will increase markedly from the time of
irrigation of the soil. Raschke [32] showed that
changes in xylem pressure can markedly affect
stomatal aperture throughout the leaf. On the
other hand it is well-known that roots are able to
sense the drying of the soil and send signals to the
leaves independently of the turgor. A propagation
of a pressure front in the xylem of course can be
orders of magnitude faster than the flow rate of
the water, but roots are able to send signals to the
leaves independent of the turgor. Indeed, Passioura [33] showed by using pressure chambers
that leaves can be kept highly turgid even when
the soil dried. From this evidence it is unlikely
that hydraulic signals are responsible for the rapid
changes of the gas exchange measured in the
present study.
However, to argue that the electric signals directly regulate gas exchange is unwarrented at the
present time. Therefore, more experiments are
required showing e.g. that exogenous electrical
treatments cause indeed a change of the photosynthesis and transpiration rate.
In studies with Mimosa [34,35] it was also
shown that action potentials propagate in sieve
elements over long distances. With regard to a
physiological function it was found that they can
affect elongation growth [36], respiration [37], water uptake [38], gas exchange [39,40] and phloem
transport [13]. Concerning plants in drying soil,
our results suggest that electrical root to shoot
communication could play an essential role in the
coordination of processes between roots and
leaves, especially in large trees with long transport
pathways and slow water transport rates.
Acknowledgements
This work was supported by Deutsche
Forschungsgemeinschaft (Grant Fr 955/1-2). We
thank Volker Stiller for helpful advice and stimulating discussions.
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