ARTICLE IN PRESS
Journal of Plant Physiology 166 (2009) 290—300
www.elsevier.de/jplph
Electric signalling in fruit trees in response to
water applications and light–darkness conditions
Luis A. Gurovich, Paulo Hermosilla
Facultad de Agronomı́a e Ingenierı́a Forestal, Departamento de Fruticultura y Enologı́a, Pontificia Universidad Católica
de Chile, Av. Vicuña Mackenna 4860, Casilla, Santiago, Chile
Received 28 January 2008; received in revised form 11 June 2008; accepted 20 June 2008
KEYWORDS
Electric potential;
Light intensity;
Soil water availability;
Tree signalling
Summary
A fundamental property of all living organisms is the generation and conduction of
electrochemical impulses throughout their different tissues and organs, resulting
from abiotic and biotic changes in environmental conditions. In plants and animals,
signal transmission can occur over long and short distances, and it can correspond to
intra- and inter-cellular communication mechanisms that determine the physiological behaviour of the organism. Rapid plant and animal responses to environmental
changes are associated with electrical excitability and signalling. The same
molecules and pathways are used to drive physiological responses, which are
characterized by movement (physical displacement) in animals and by continuous
growth in plants. In the field of environmental plant electrophysiology, automatic
and continuous measurements of electrical potential differences (DEP) between
plant tissues can be effectively used to study information transport mechanisms and
physiological responses that result from external stimuli on plants. A critical mass of
data on electrical behaviour in higher plants has accumulated in the last 5 years,
establishing plant neurobiology as the most recent discipline of plant science. In this
work, electrical potential differences were monitored continuously using Ag/AgCl
microelectrodes, which were inserted 15 mm deep into sapwood at various positions
in the trunks of several fruit-bearing trees. Electrodes were referenced to an
unpolarisable Ag/AgCl microelectrode, which was installed 5 cm deep in the soil.
Systematic patterns of DEP during day–night cycles and at different conditions of soil
water availability are discussed as alternative tools to assess early plant stress
Abbreviations: AP, action potential; EP, electric potential; DVlb, electrical potential differences between the leaf zone and the
base of the trunk.
Corresponding author. Tel.: +56 2 686 4164; fax: +56 2 553 4130.
E-mail address: [email protected] (L.A. Gurovich).
0176-1617/$ - see front matter & 2008 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jplph.2008.06.004
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Electric signalling in trees
291
conditions. This research relates to the adaptive response of trees to soil water
availability and light–darkness cycles.
& 2008 Elsevier GmbH. All rights reserved.
Introduction
Two different types of electrical signals have
been reported in plants. Action potential (AP)
(Fromm, 2006) is a rapid propagating electrical
pulse that travels at a constant velocity and
maintains a constant amplitude. VP (slow wave or
‘‘variation potential’’) corresponds to a long range
of variation pulses (Stahlberg et al., 2006), which
vary with the intensity of the stimulus. Its
amplitude and speed depend on xylematic pressure
and decrease with increasing distance from its
generation site (Davies, 2004, 2006). AP is an allor-none depolarization that spreads passively from
the excited cellular membrane region to the
neighbouring non-excited region. Excitation in
plant cells depends on Ca2+ depolarization and
Cl and K+ repolarization. Both AP and VP transmit
information about local stimuli to distant cells and,
therefore, promote its physiological response
(Brenner et al., 2006).
The electrical signalling mechanism in plants has
been extensively reported; Fromm and Lautner
(2007, Table 1) summarize recent progress in the
field of electrical signalling in plants. Specifically,
they focus on the generation and propagation of
various electrical signals, the transmission pathways of these signals, and the physiological
responses in different plant tissues. In the last 20
years, numerous physiological effects of electrical
signalling in plants have been reported. Rapid
communication between living cells is considered
essential to plants and animals alike (Müller et al.,
2006). A similitude on electrical signal transmission
between animal and plant organs has been postulated by Volkov and Mwesigwa (2001).
Plants respond rather quickly to many changes in
their environment, including changes in light
intensity, osmotic pressure, temperature, mechanical damage, mechanical stimulation, water availability, chemical compounds (i.e., plant growth
stimulators or herbicides) and salt. Electrical
impulses generated at the site of stimulation can
propagate to adjacent cells. Electrical signal
velocities within woody plants range from 0.05 to
4000 cm s1 when rapid long-distance communication and the rapid response phenomena observed in
plants are considered (Volkov, 2000; Volkov et al.,
2004).
Phloem, which represents a continuum of plant
plasma membranes, might play a significant role for
electric signal transmission between plant organs.
When the phloem is stimulated, the AP propagates
over the entire length of the cell membrane and
along the phloem with a constant voltage. The
phloem’s structure largely determines the movement of the AP. Each phloem vessel is similar to an
animal axon in that it is a hollow tube filled with
electrolyte solutions. The length of a phloem vessel
varies from several mm to several m, with
diameters in the range from 1 to 100 mm (Davies,
2004; Lautner et al., 2005; van Bel and Ehlers,
2005; Fromm, 2006).
Extracellular electrical measurements in plants
were pioneered by Burdon-Sanderson (1873), Darwin
(1875) and Bose (1926). Only recently, however,
have these measurements been used as a phytomonitoring technique for their potential application to fruit tree production (Gil et al., 2008).
Evidence exists for a role of electrical signals in
many processes of plant life, including respiration
(Dziubinska et al., 1989; Filek and Koscielniak,
1997), water uptake (Davies et al., 1991), phloem
unloading (Fromm, 1991), phloem translocation
(Fromm and Bauer, 1994), photosynthesis (Koziolek
et al., 2004) and responses to wounds (Roblin,
1985; Rhodes et al., 1996; Mancuso, 1999).
The following two techniques for the measurement of electrical currents in plant tissues are
under study: non-invasive surface measurements
and measurements using inserted thin metal
electrodes (Fromm and Lautner, 2007). At different
positions within the plant, from roots to fruits,
electrodes are connected by insulated cables to a
high-input impedance multi-channel electrometer.
In addition, a reference electrode is inserted in the
soil. When all channels are electrically stabilized,
the following treatments can be evaluated: light–
darkness sequences, drought – irrigation cycles,
heat pulses at a specific leaf, localized chemical
product applications, wind speed, relative air
humidity, and mechanical wounding of plant organs
(trunk girdling, pruning, leaf and fruit removal, and
root excision).
The main goal of this work is to detect plant
electrical activity in trees exposed to different soil
water availabilities and light–darkness periods. To
do this, Ag/AgCl microelectrodes were used as
ARTICLE IN PRESS
292
L.A. Gurovich, P. Hermosilla
alternative phytomonitoring sensors of early plant
stress detection.
Material and methods
The extracellular plant bio-potential measurement
installation for electrophysiological computer-assisted
measurements of electrical potential (EP) is compartmented between two rooms (Figure 1). Room A is a
Faraday cage (3.5 m 1.25 m 3.0 m), which prevents
external electromagnetic signals from interfering with
measurements of internal plant voltages. The soilgrounded Faraday cage is located in an environmentally
controlled greenhouse; the cage contains eight 25 L sandy
soil containers, which are each planted with 3-year-old
trees grafted in commercial rootstocks. The trees used in
this study were the following: two avocado plants (Persea
americana Mill.) cv. Hass, grafted on Mexicola rootstock,
two Southern Highbush blueberry plants (Vaccinium spp.)
of cultivar O’Neal, two lemon plants (Citrus limon (L.)
Burm. f) of cultivar Fino 49 grafted on Citrus macrophylla
Wester, and two olive plants (Olea europaea L.) of
cultivar Azapa grafted on Manzanillo rootstock.
All the trees used in these experiments had a
5.0–7.0 cm diameter lignified trunk, 5–7 branches and
75–100 leaves. Air temperature and relative humidity
during the experiments were kept between 23 and 25 1C
and 85% and 88%, respectively. The photosynthetic
photon flux, which was measured with a quantum sensor
(QSS-01 light meter, Lehle Seeds, Round Rock, Texas,
USA) at the top of the canopy, ranged from
0 mmol photons m 2 s1 (night) to 630 mmol photons m2 s1
(noon).
In the second independent room (B, Figure 1), Ag/AgCl
non-polarisable microelectrodes (Figure 2) were inserted
into the soil and into the sapwood of trees. These
A
microelectrodes were connected to a Keithley 20 channel
Differential Multiplexer model 7700, with an electromechanical latching system. Actuation time was less than
3 ms, contact resistance was less than 1 O, potential was
7500 nV and the offset current was less than 100 pA. The
multiplexer was operated using a Keithley Multimeter/
Data Acquisition System (model 2701) and ExceLINX-1A
software. This software is an add-in utility provided by
Microsoft& Excel. The multimeter operates within the
following ranges: DC and AC voltage from 100 nV to
1000 V, frequency from 3 Hz to 500 kHz and resistance
from 10 mO to 120 MO. The multimeter was connected
through the internet to a PC computer.
Ag/AgCl reference microelectrodes were designed,
constructed and calibrated according to techniques
described by Sawyer et al. (1995). These microelectrodes
were a 0.3 mm diameter Ag wire (99.99% Ag) and coated
with an AgCl film, which was obtained by immersion in a
0.1 N HCl solution for 10 s under a 5 V electric field. The
wire was inserted inside a 0.6 mm diameter stainlesssteel needle, which was filled with a 3.5 M KCl solution.
The needle was sealed with a heat-fused PE coating
insulation at both ends (Figure 2).
Polyethylene heat
fused insulation
4 mm stainless steel
hypodermic needle
Polyethylene heat
fused insulation
0.1 mm 99.99% Ag wire,
AgCl electro-coated
3.5 M KCI filling solution
Figure 2. Ag/AgCl reference microeletrode.
B
20 CHANNEL
KEITHLEY 7700
MULTIPLEXER
LEAF AREA
ELECTRODE
BASE
ELECTRODE
25 L
soil
INTERNET
KEITHLEY 2701
MULTIMETER
REFERENCE
ELECTRODE
EXCELINK
SOFTWARE
FARADAY CAGE
PC DATA
RECORDING
Figure 1. Schematic diagram of the digital acquisition system for recording voltage differences between the base of
the trunk and the leaf zone (DVlb). (Vb and Vl: electrode position at the trunk base and at the leaf area, respectively).
ARTICLE IN PRESS
Electric signalling in trees
Two measuring microelectrodes were inserted by
drilling the tree trunk with a 0.5 mm stainless-steel drill.
Microelectrode tips were firmly introduced into the
phloem. The first tip was placed 5 cm above the
rootstock–scion interface (i.e., the ‘‘base electrode),
and the second tip was placed at the leaf area (i.e., the
‘‘leaf area’’ electrode, Figure 1). Microelectrodes were
45 cm apart and were referred to the same symmetrical
reference electrode, which was positioned 5 cm below
the soil surface on each container (Figure 1). Thus, the
non-isolated metallic part of electrodes was fully stuck in
the wood so that meteorological influences, such as rain
or fast temperature changes, were reduced.
Measurements of the EP were made at all the
microelectrodes with a sampling interval of 0.01–10 s,
depending on the specific soil water availability and the
light–dark conditions explained below. The computer and
the multimeter were powered with a backup generator,
which prevents breaks caused by short failures of the
electrical power line. As shown by Petiau (2000), the
temperature sensitivity of the grounded electrochemical
electrode used as a reference was negligible (i.e.,
smaller than 0.73 mV/1C). Thus, a direct effect of
temperature on the measured electrode potential can be
ruled out. The microelectrode array explained above
enabled the recording of EP differences between the leaf
zone and the base of the trunk (DVlb).
Results
The experimental setup was used for several
experiments. We selected a few specific examples
to present in this paper. Figure 3 presents the
absolute DVlb values for an 83 h experiment
(25–29 October 2007). These data correspond to
30,000 samplings from each microelectrode, which
were measured every 10 s. The experiment is
designed to examine tree electrical behaviour
during day and night cycles. One litre of water
was applied on October 26 at 16:00 P.M. Thus, the
effect of a single irrigation event on tree electrical
behaviour was also determined.
Sunset, daybreak and water application in
avocado resulted in fast changes of the EP between
the base and leaf area electrodes in the trunk
(Figure 3(1)). EP fluctuations during light and dark
periods were strikingly different, probably due to
different sap flow velocities (Gibert et al., 2006).
EP values were reduced during the initial hours
after daybreak, but they started to increase after
mid-day as a result of transient water stress
conditions. This explanation is partially confirmed
by EP data for October 28, which show a second
reduction in EP around 17:30 P.M. due to the
increase in water stress on plants that were not
irrigated after October 26 at 16:00. Also, the
EP ¼ f(t) tendency shows a linear increase during
the first night and a linear decrease during the
293
second and third nights. These results are consistent with the steady reduction of soil water
availability over time.
Immediately following sunset, there was a rapid
increase in EP values. After midnight, the rate of
this increase slowed down. Also, small but consistent increases in EP values were detected about
1–2 h before daybreak. Explanations of this behaviour may be related to circadian rhythms in plants;
however, this needs further study (Dodd et al.,
2005; Hotta et al., 2007).
Similar results were obtained for blueberry,
lemon and olive (Figures 3(2)–(4), respectively).
EP night fluctuations were larger in blueberry than
in avocado (Figure 3(1)). Measurements ranged
from 38 to 150 mV in blueberry vs. 295–325 mV in
avocado. Also, the EP response to irrigation is less
intense in blueberry compared to avocado.
During the night hours, EP values were reduced,
and EP fluctuation continuously increased in lemon
(Figure 3(3)). At daybreak, EP increased sharply
(about 25 mV) for 1 or 2 min and then steadily
decreased during the morning hours. Around midday, EP started to increase for 3–4 h, which is
coincident with a high evapo-transpiration rate. In
the last 3 h before sunset, EP values were nearly
constant.
The following differences in EP responses to soil
water availability and to light and dark conditions
were observed in olive (Figure 3(4)): a short-lived
(2–5 min) decrease in EP values at daybreak and a
very strong signal (55 mV) pulse at the irrigation
event. Variation in all EP measurements, except
those taken during the irrigation event, was only
30 mV.
These results are similar to data provided by
Davies (2004, 2006) and Fromm and Lautner (2007).
These authors indicate that EP behaviour is related
to plant species characteristics and are probably
associated with anatomical differences in conductive tissues. EP variations, however, follow a
common pattern with respect to its amplitude both
during the day and night. For example, the
amplitude of EP was significantly more stable
during the light hours. At sunset, EP changed
almost immediately. At daybreak, a refractory
period lasted 5–30 min where no changes in EP
were detected. On cloudy days, the refractory
period was extended (data not shown).
The effect of a single water application on the EP
behaviour of trees was determined using the
information of the same experiment on a different
time scale (Figures 4(1)–(4)). EP values, which were
measured every 10 s for 2 consecutive days October
26 (* - - - - - - *) and October 27 (- - - - - -), are plotted
against time (i.e., between 16:00:00 and
ARTICLE IN PRESS
294
L.A. Gurovich, P. Hermosilla
AVOCADO
mV
330
IRRIGATION EVENT
320
310
300
290
Sunset
Daybreak
Sunset
Daybreak
Sunset
Daybreak
Sunset
280
270
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
BLUEBERRY
160
mV
IRRIGATION EVENT
140
120
100
80
60
40
Sunset
Daybreak
20
Sunset
Sunset
0
15:36:00
3:36:00
15:36:00
Daybreak
Sunset
Daybreak
3:36:00
15:36:00
3:36:00
15:36:00
LEMON
200
mV
IRRIGATION EVENT
180
160
140
120
100
80
60
40
Sunset
Daybreak
Sunset
Daybreak
Sunset
Daybreak
Sunset
20
0
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
OLIVE
mV
200
IRRIGATION EVENT
180
160
140
120
100
80
60
40
Sunset
Daybreak
Sunset
Daybreak
Sunset
Daybreak
Sunset
20
0
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
3:36:00
15:36:00
Figure 3. (1) Electrical potential responses of avocado. (hours are given in local time). (2) Electrical potential
responses of Southern Highbush blueberry (hours are given in local time). (3) Electrical potential responses of lemon
(hours are given in local time). (4) Electrical potential responses of olive (hours are given in local time).
ARTICLE IN PRESS
Electric signalling in trees
295
mV
325
AVOCADO
322.5
320
317.5
*
315
*
*
312.5
IRRIGATED: 26.10.07
NO IRRIGATION: 27.10.07
310
307.5
1 L water is
applied in 5 s
305
302.5
*
A
300
15:50:24 15:57:36 16:04:48 16:12:00 16:19:12 16:26:24 16:33:36 16:40:48 16:48:00 16:55:12 17:02:24 17:09:36
mV
90
BLUEBERRY
80
70
60
50
*
*
40
*
30
20
*
1 L water is
applied in 5 s
IRRIGATED: 26.10.07
NO IRRIGATION: 27.10.07
10
0
15:50:24 15:57:36 16:04:48 16:12:00 16:19:12 16:26:24 16:33:36 16:40:48 16:48:00 16:55:12 17:02:24 17:09:36
mV
175
LEMON
170
*
165
160
155
150
1 L water is
applied in 5 s
*
*
*
145
IRRIGATED: 26.10.07
NO IRRIGATION: 27.10.07
140
135
130
15:50:24 15:57:36 16:04:48 16:12:00 16:19:12 16:26:24 16:33:36 16:40:48 16:48:00 16:55:12 17:02:24 17:09:36
mV
175
OLIVE
165
155
145
135
*
125
*
IRRIGATED: 26.10.07
NO IRRIGATION: 27.10.07
115
1 L water is
applied in 5 s
105
95
*
*
85
75
15:50:24 15:57:36 16:04:48 16:12:00 16:19:12 16:26:24 16:33:36 16:40:48 16:48:00 16:55:12 17:02:24 17:09:36
Figure 4. (1) The effect of irrigation on EP behaviour of avocado (hours are given in local time). (2) The effect of
irrigation on EP behaviour of Southern Highbush blueberry (hours are given in local time). (3) The effect of irrigation on
EP behaviour of lemon (hours are given in local time). (4) The effect of irrigation on EP behaviour of olive (hours are
given in local time).
ARTICLE IN PRESS
296
17:00:00 h). One litre of water was applied in 5 s to
each plant on October 26. In avocado, a sharp EP
differential of 20 mV was observed almost immediately after irrigation and was followed by a slow
decrease in EP in the minutes that followed.
Nevertheless, plants did not completely recover
to their pre-irrigation EP after 1 h. The next day, at
16:00:00, the EP value was still 6 mV EP higher than
the value measured the previous day at the same
hour. This indicates that the apparent AP that
results from irrigation has a long-term effect on the
EP response of the plant. Point A in Figure 4(1)
cannot be adequately explained with the available
data.
In blueberry (Figure 4(2)), irrigation resulted in a
sharp, almost instantaneous reduction of EP
(17 mV). In the following hour, there was an
asymptotic and incomplete slow recovery, which
corresponds to a classic AP wave (Fromm and
Spanswick, 2007). The following day at 16:00 P.M.,
EP values remained 25 mV higher than they were
the previous day.
In lemon (Figure 4(3)), EP fluctuated rapidly, with
an almost instantaneous and short-lived increment
of 7 mV. This was followed by an immediate
reduction of 10 mV with respect to the EP value
that was measured prior to irrigation. Then, there
was a new increment, lasting about 4 min. This was
then followed by a second sharp and rapid 16 mV
fluctuation. After this initial instability, EP slowly
increased during the following hour. The next day,
at 16:00:00, EP was still 11 mV higher than it was
the previous day, before the irrigation event. The
AP response to irrigation was related to species
characteristics. Specifically, the response was more
intense and short-lived in olive (50 mV, 30 min in
Figure 4(4)) than it was in blueberry (17 mV, over
24 h in Figure 4(2)).
The effect of light on EP behaviour was studied in
another short-term experiment, which lasted
70 min. After an initial period of 5–15 min in the
sun at noon, plants were introduced into a dark
wooden box for 30 min before being exposed
again to sunlight. Results, which are presented in
Figure 5(1)–(4), show significant differences in
plant EP behaviour. In avocado plants, the response
curve resembles an AP, lasting about 5 s after the
onset of the darkness period. It peaks at 280 mV and
shows a significant instability for about 2 min.
Then, a recovery stage (EP exponential reduction)
follows for 10 min, until it reaches an almost
constant EP value. When full sunlight is again
allowed, a small EP instability is detected. After
10 min, however, the EP stabilizes near the values
measured before the onset of the experiment
(Figure 5(1)).
L.A. Gurovich, P. Hermosilla
Variation in EP was completely different in
blueberry (Figure 5(2)). Before the darkness period, EP values changed in small, almost linear
increments of 8 mV. This lasted for 8 min after the
initiation of the dark period. Then, a 10 mV
continuous and linear reduction of EP values was
measured until plants were exposed again to
sunlight. EP reduction continued during the following 5 min and eventually stabilized at 107.5 mV,
which was about 5 mV bellow the pre-experimental
EP value.
The response in lemon trees was similar to that
of an AP. When a sudden dark period was
imposed at noon (Figure 5(3)), a sharp and
unstable EP pulse was detected. It lasted
about 50 s and was in the range of 75 mV. It was
followed by an 8 min recovery period, with EP
values similar to those measured before the dark
period. When sunlight was allowed to reach the
plants, a new EP modification was detected. It
lasted about 30 s and ranged 50 mV. For the last
30 min of measurements, EP values incremented
exponentially.
For olive trees (Figure 5(4)), both the start and
the end of the 30 min darkness period were
detected by EP modifications. The curve resembled
an AP. During the dark period, EP values were
almost constant and were 10 mV higher than the
pre-experimental measurements. After sunlight
was allowed to reach the plants, a linear, continuous reduction in EP values was detected. Twentyfive minutes later, it reached the pre-darkness EP
value.
Species-specific responses to the sudden dark
period that was imposed at noon are probably
related to the species’ evolutionary adaptations.
Blueberries are forest under-story plants and
respond rather slowly to light intensity
fluctuations. In contrast, avocado and lemon are
more sensitive to light fluctuations. In olive,
leaf anatomical characteristics are expected to
buffer its sensitivity to light (Trebacz et al., 1997,
2006).
Discussion
Mechanisms that generate trunk polarizations
that were measured in this paper remain unclear.
As mentioned in the introduction, the observed EP
may reflect a combination of physical, chemical
and physiological responses to sap flow, plant
growth, photosynthesis and adaptive feedback
controls of the tree (Fensom, 1963; Morat et al.,
1994; Koppan et al., 2002). The order of magnitude
of the observed EP variation in this work is
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Electric signalling in trees
297
mV
450
AVOCADO 3 October 2007
400
350
300
250
200
LIGHT (L)
DARKNESS
L
150
0
300
600
900
1200 1500 1800 2100 2400 2700 3000 3300 3600 3900
sec
BLUEBERRY 3 October 2007
mV
122.5
120
117.5
115
112.5
110
107.5
105
102.5
DARKNESS
LIGHT
LIGHT
100
0
300
600
900
mV
250
1200 1500 1800 2100 2400 2700 3000 3300 3600 3900 sec
LEMON 3 October 2007
225
200
175
150
125
100
75
LIGHT
DARKNESS
LIGHT
50
0
300
600
900
mV
85
1200 1500 1800 2100 2400 2700 3000 3300 3600 3900 sec
OLIVE 3 October 2007
80
75
70
65
60
55
LIGHT
DARKNESS
LIGHT
50
0
300
600
900
1200 1500 1800 2100 2400 2700 3000 3300 3600 3900 sec
Figure 5. (1) The effect of a 30 min dark period induced at noon on the EP behaviour of avocado. (2) The effect of a
30 min dark period induced at noon on the EP behaviour of Southern Highbush blueberry. (3) The effect of a 30 min dark
period induced at noon on the EP behaviour of lemon. (4) The effect of a 30 min dark period induced at noon on the EP
behaviour of olive.
ARTICLE IN PRESS
298
consistent with other studies (Davies, 2004;
Fromm, 2006; Gil et al., 2008).
Data presented in this work provide experimental
evidence of specific daily variations of the EP in
tree trunks. In addition, the effect of light intensity
and soil water availability on the EP in fruit-bearing
trees was examined. Based on these data, the
continuous measurements of tree electrical behaviour under field conditions may be used to detect
incipient conditions of water stress. Microelectrodes designed for this work can be coupled with
phytomonitoring devices, automatic agro-meteorological weather stations and soil water content
recording devices to provide a more precise
irrigation schedule.
Electrical activity in the dark fluctuated on a
wider range (over one order of magnitude) compared to the electrical activity in the light. This
observation, which was detected for each species
under study, may be associated with sap flow
intensity (Gibert et al., 2006). The effect of light
and dark on electrical activity may be related to
membrane polarization, which occurs in the leaf
due to photosynthesis (Whitmarsh, 2004). Also,
Bulychev and Kamzolkina (2006) reported an effect
of light and dark on the plasma membrane electric
excitation on H+ fluxes and photosynthesis in
Characean cells.
Several physiological mechanisms that explain
resting potential periods and electric responses to
irrigation have been postulated. AP and VP lead to a
physiological reaction by informing distant cells
about local stimuli (Lautner et al., 2005; Fromm,
2006; Fromm and Lautner, 2007). Additional
signalling mechanisms in plants have been reported, including modifications of cytoplasmatic pH
(Wilkinson and Davies, 1997; Felle, 2001), coupling
hydraulic waves (Malone, 1993; Mancuso, 1999),
rapid ethylene gas diffusion in the xylem (Guo and
Ecker, 2004) and abscisic acid signal transduction
(Leung and Giraudat, 1998; Himmelbach et al.,
1998). Most of the chemistry of the neuromotoric
system of animals has been recently found in
plants, including neurotransmitters (i.e., acetylcholine), cellular messengers (i.e., calmodulin) and
cellular motors (i.e., actin) (Baluška et al., 2006;
Brenner et al., 2006; Roshchina, 2001; Murch,
2006).
Apart from short-distance signalling, long-distance transmission via the phloem pathway is a
well-known mechanism in many plants. APs generated by re-watering maize plants in drying soil
causes an increase in CO2 and H2O gas exchange
within leaves. The involved ion fluxes and/or the
amplitude and duration of the electrical signal play
a key role in the generation of the photosynthetic
L.A. Gurovich, P. Hermosilla
response (Fromm and Fei, 1998). APs triggered by
the cold shock of leaf tips can reduce phloem
transport to distant leaf parts (Fromm and Bauer,
1994). The flaming of a leaf on a poplar tree also
evokes electrical signals that travel across the
shoot to adjacent leaves where the rate of CO2
uptake and the quantum yield of electron transport
are temporarily reduced (Lautner et al., 2005).
Different EP fluctuations during the day and night
may be related to a sap flow that varies sporadically in space and time (Gibert et al., 2006).
Understanding the effect of sap flow on the
electrical response of trees may help to better
explain transfer processes between the soil and the
atmosphere.
Conclusions
This work reports specific daily variations of the
electric potential (EP) distribution in trunks of four
species of fruit-bearing trees. Results in previous
studies are from measurements within a single
poplar tree (Fensom, 1963), a single chestnut tree
(Morat et al., 1994) and a single oak tree (Koppan
et al., 2000, 2002). Daily variations relate to the
simultaneous sap flow during light hours. The
electric signal amplitude was one order of magnitude larger during the night hours than it was
during the day hours.
Results reported in this work indicate that the
electrical monitoring of a living tree can reveal new
mechanisms of charge exchange in xylem elements.
Communication within plants may occur as signals
between plant organs that sense natural or mangenerated environmental modifications or as plant
organs showing a physiological response. According
to this work, continuous measurements of EP can
be used to assess the nature of information
exchange within plant cells and organs as well as
its control mechanism and the link between ion
fluxes, plant physiological responses and environmental change. These results should raise a
renewed interest in electrical measurements in
trees as they relate to signalling control mechanism, the interlink between ion fluxes and physiological responses and the molecular identity of
different channel types that participate in electrical signals.
Experiments with continuous long-term (seasonal) (VP) and short-term (EP) monitoring are
currently underway. Moreover, these experiments
use a large number of distributed electrodes and
include a very high frequency (ms) of EP measurements. Results are expected to quantitatively
define the following agronomic issues: the early
ARTICLE IN PRESS
Electric signalling in trees
detection and precise extension of water stress,
the adaptive response of trees to transient soil
water availability, the use of woody plants as
environmental bio-sensors by monitoring EP variations, the modelling of water and carbon balance in
relation to climate change and the contribution of
trees to the fate of contaminants in the biosphere.
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