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SIGNALS TRANSMISSION
IN THE CHEMICAL WAY
The theory assuming the release of a chemical substance
from a damaged cell was published by Ricca (1926). From
the autor
,
s name the non-defined substance produced by
a plant wounding was called Ricca
,
s factor. Since that time
many chemical substances of different character have been
ascribed to participation in signal transmission and syste-
mic responses.
The proteinase inhibitor-inducting factor (PIIF) is a sub-
stance affecting the expression of some genes responsible
for synthesis and accumulation of proteinase inhibitors
(PIs) in tomato leaves which were directly damaged and
those being distant (Green and Ryan 1973; Ryan 1974).
Proteinase inhibitor (PI) suppressing metabolism of prote-
ins leads to their accumulation by which they become de-
fensive for the plant, and harmful for pathogenes, and viru-
ses. At present, many elicitors are attributed to the role of
PIIF in induction of gene expression in the directly dama-
ged area as well as in distant place not subject to the action
of the stress factor.
Induction of gene expression as well as synthesis of de-
fence compounds and changes in metabolism occur gene-
rally immediately after stimulation, therefore high-molecu-
lar, immobile chemical compounds cannot play a signaling
role at long distances. However, they can be one of the
first links in the signaling chain or be responsible for the
occurrence of local responses (Green and Ryan 1973; Ryan
1974).
To these compounds belong oligosaccharins such as oli-
gogalacturonids, oligoglucan, oligochitine, oligochitosan
(Wildon et al. 1989; Creelman and Mullet 1997; Ebel and
Mithöfer 1998). In damaged leaves of Arabidopsis thaliana
oligosaccharins induce expression of genes only in the place
of wounding and are recognized as the first link in the
chain of changes following the damage (Rojo et al. 1999).
Also fatty acids and their derivatives are signaling factors
in Arabidopsis (Farmer et al. 1998), as well as some oligo-
peptides are included into systemic postdamage response
in potatoes and tomatoes (Narváez-Vásquez et al. 1995).
Systemin, which induces synthesis of proteinase inhibi-
tors in damaged and distant undamaged leaves, belongs to
mobile factors playing a role in a response to wounding
Vol. 72, No. 4: 309-318, 2003 309ACTA SOCIETATIS BOTANICORUM POLONIAE
WAYS OF SIGNAL TRANSMISSION AND PHYSIOLOGICAL ROLE
OF ELECTRICAL POTENTIALS IN PLANTS
HALINA D
ZIUBIÑSKA
Department of Biophysics, Institute of Biology, Maria Curie-Sk³odowska University
Akademicka 19, 20-033 Lublin, Poland
e-mail: dziub@biotop.umcs.lublin
(Received: February 21, 2003. Accepted: July 28, 2003)
ABSTRACT
Plants are subject to stimuli from the environment on which they strongly depend and in contrast to animals,
they are unable to escape harmful influences. Therefore, being able to receive stimuli they have developed adequ-
ate responses to them. Such a reaction can occur in the area of a stimulus action or cover the whole plant or its
parts. In the latter case, it is a systemic reaction. The plant reaction is expressed by various intensity, rate and kind
of response. It is interesting to know the character of the signal informing about a stimulus, the routes of its pro-
pagation and the transmission mechanism. Three conceptions of excitation are distinguished: 1) propagation of
chemical agents formed at the site of a stimulus action with the flow of the phloem sap or through the atmosphere
(in the case of volatile substances) to other plant parts, 2) a very fast transmission by the xylem in the wave of hy-
draulic pressure formed after a plant damage. From combining the hydraulic and chemical hypothesis a con-
ception of hydraulic dispersion has been formulated which assumes that chemical substances synthetized after an
injury can be transferred very fast with the wave of hydraulic pressure changes in the whole plant, 3) a stimulus
evokes the action potential (AP), and its transmission along the whole plant, plant organ or specialized tissue, by
local circuits from cell to cell. Strong, damaging stimuli can evoke variation potentials (VPs), the character of
which differs from APs. It is postulated that transmission of VP occurs by a hydraulic dispersion and electrical
changes seem to be secondary phenomena.
KEY WORDS: action potential, variation potential, signal transmission, systemic response.
(Sticher et al. 1997; Howe and Ryan 1999).
14
C-systemin
applied to the damaged site of a tomato leaf was found to
spread in the whole leaf within 30 min (Narváez-Vásquez
et al. 1995), and after 5 hours the whole plant showed the
presence of the labelled systemin. Its transport takes place
in the phloem and in this way, as systemic signal, reaches
distant plant parts in which it activates genes of proteinase
inhibitors. The same way of transmission is proposed in the
case of other polypeptides (elicitin, cryptogein), which can
be recognized as signal substances participating in syste-
mic responses of the plant to damages (Fisher 1992; Ebel
and Mithöfer 1998).
Salicylic acid (SA) belongs also to mobile plant hormo-
nes. It participates in systemic acquired resistance (SAR)
in response to infections with pathogens. Infection of to-
bacco or cucumber leaves causes a considerable increase of
SA concentration in the phloem sap not only in damaged
place but also in uninfected, distant tissues (Dempsey et al.
1999). SA transport, however, is too slow to consider that
SA plays the role of a direct signal inducing systemic resi-
stance to stress. Induction of systemic resistance occurs
only at high SA concentrations in ultimately infected lea-
ves (Ryals et al. 1996; Birkenmeier and Ryan 1998; Ebel
and Mithöfer 1998) therefore its main role is ascribed to lo-
cal responses.
Biochemical and molecular studies of defense reactions
of plants to the infection by pathogens and viruses allowed
identification of other signaling substances taking part in
defence against stress events: jasmonic acid (JA), methyl
ester of jasmonic acid (Me-JA), abscisic acid and ethylene
were mentioned (León et al. 2001).
Jasmonic acid solution administered to a leaf or to the
soil in which tomato seedlings (Lycopersicon esculentum)
were growing induced expression of genes of proteinase
inhibitors in the whole plant (Farmer et al. 1992). Isolation
of a single tomato leaf from the rest of the plant by cove-
ring it in a glass chamber and application of volatile Me-JA
also induced synthesis of proteinase inhibitors. Accumula-
tion of proteinase inhibitor was the highest in the leaf kept
in Me-JA atmosphere, while in the neighbour leaf the amo-
unt of proteinases inhibitor was twice smaller. In the plants
standing beside the induction of proteins synthesis was not
observed. There are reports that the above mentioned si-
gnaling volatile compounds (Me-JA and ethylene) released
after leaf infection enter to atmosphere and can induce de-
fence reactions against pathogens in other parts of the same
plant or in other plants (Enyedi et al. 1992; Koda 1997;
Baldwin and Preston 1999). This is another probable way
of signal transmission. Mechanical damage of a leaf indu-
ces identical effects as the mentioned jasmonic acid and its
ester. Expression of genes induced by jasmonates requires
cooperation with other hormones, e.g. ethylene or abscisic
acid (Wasternack and Parthier 1997; Penninckx et al. 1998;
Glazebrook 1999; Wang et al. 2002).
The most effective chemical compound carrying infor-
mation about stress could be ethylene because of its sprea-
ding ability. Ethylene as a volatile substance spreads thro-
ugh intercellular spaces and can penetrate the whole plant
in a short time. Plant tissue damage causes increased ethy-
lene production. In damaged pea leaves Phaseolus vulgaris
defence enzymes such as chitinase, gluconase are accumu-
lated (Mauch et al. 1992). However, the participation of
ethylene as a direct signal inducing expression of genes is
not unambiguous. The role of ethylene in systemic resi-
stance of plants can consist in an increase of tissue sensiti-
vity to the action of other factors, e.g. SA or jasmonates
(Lawton et al. 1994).
The main transmission route of chemical compounds
participating in signaling, besides volatile substances, is
phloem (Fisher et al. 1992; Ishiwatari et al. 1995). The im-
portant feature of the phloem transmission of the compo-
unds playing a role in signaling is that it can be directed
both basi- and acropetally.
On the other hand, the xylem tissue, is attributed to trans-
port of chemical signals by the so-called hydraulic disper-
sion. The essence of this mechanism is an interaction be-
tween two consequences of plant tissue damage: release of
PIs inducing factors, and releasing of the hydraulic signal
transporting the induction factors at high speed over a long
distance (Malone et al. 1994; Malone and Alarcon 1995).
The hydraulic signals are necessary for transmission of sy-
stemic information, but insufficient. Induction of PIs in di-
stant plant parts takes place as early as 10 min after the
wounding, only when both the inducing substance and the
hydraulic signal appear. Administration of the substance of
PIIF character, e.g. oligosaccharides onto the leaf blade
without incising does not bring any effect itself (Malone et
al. 1994). The experiments carried out by Rhodes et al.
(1999) on tomato seedlings resulted in a similar conclu-
sion. Cotyledon damage under a droplet of luciferine dye
caused the dye penetrated into the xylem and moved with
its sap along the petiole to the leaf. Luciferine distribution
in leaves depended on which of the cotyledons was dama-
ged. Examination of the connections between stimulated
cotyledons and leaves pointed to their connection through
xylem vessels. The stimuli were accompanied by systemic
induction of proteinase inhibitors. PI activities were in accord
with the dye distribution and the network of xylem vessels.
Such results indicated the appearance of some chemical
factors after damage, which were able to induce reactions.
These substances moved along xylem, because destruction
of living tissue by steam did not inhibit PI induction.
Strong damages caused a higher PI activity which, as sug-
gested by authors, was connected with penetration from
damaged cells into xylem of a larger amount of the cell sap
containing a considerable amount of inducing substances.
Large amounts of the sap passed not only into xylem but
also into phloem, because the level of PI should be lower,
assuming its distribution only by xylem. Transport of the
substance inducing PI, formed after delicate incisions,
undoubtly take place by the phloem because PIIF identified
by carboxyfluorescein was present only in this bundle.
HYDRODYNAMIC PROPAGATION
OF EXCITATION
Hydraulic pressure wave spreading by xylem tissue can
be another way of signal transmission. Mulhern et al.
(1981) studied electrical changes occurring in the leaf pe-
tiole of geranium after incision of the leaf blade. Electrical
potential changes were recorded already 10 ms after leaf
damage. It is unlikely that any substance could cover in
such a short time a distance of 50 mm from the place of da-
mage to the measurement electrode. The rate (5 m s
-1
) and
ability of the signals to pass through the cooled tissue exc-
310 Dziubiñska H.SIGNAL TRANSMISSION IN PLANTS
lude participation of action potential (AP) in signal trans-
mission after injury. Attention was thus directed to xylem
tissue and the sap present in it, which is under negative hy-
drostatic pressure. Disruption of the vessel continuity due
to injury causes a rapid increase in the xylem sap flow rate
tending to equalize the pressure with the atmospheric one.
This rapid flow can bring about flows of ions in the adja-
cent cells, and in consequence, variation potential (VP) in
distant places of the plant (Malone and Stankoviæ 1991;
Malone 1992). Recently, this conception was developed
and found a broader experimental support (Stankoviæ et al.
1997). Local scorching of a tomato leaf causes a fast incre-
ase and then a long-lasting inhibition of elongation of the
petiole (Stankoviæ and Davies 1998). This damage is ac-
companied by VP. Electrical changes are preceded by pas-
sing a hydraulic pressure wave through xylem, evoked by
leaf damage. Application of external pressure mimicking
the damage induces a comparable electrical response. It is
suggested that the wave of hydraulic pressure evoked by
scorching passes by xylem and activates mechano-sensitive
ion channels or pumps in membranes of living cells adhe-
ring to the xylem. Flowing ions depolarize the membrane,
which external electrodes register as VP. VP in turn prece-
des systemic plant responses in distant tissue (Stankoviæ
and Davies 1996; Davies et al. 1997; Stankoviæ and Davies
1998). The above conception has also served to explain the
phenomena appearing after scorching leaves in the shoot of
Vitis vinifera. Such stimulus induces formation of electrical
potential changes of VP character (Mancuso 1999). Elec-
trodes attached to the stem recorded a potential change, the
amplitude of which as well as the propagation rate decrea-
sed with the distance from the scorching place. At the same
time the shoot diameter showed a transient increase. These
two phenomena, i.e. variation potential and change of the
shoot diameter did not occur simultaneously. VP appeared
when the shoot diameter reached its maximum, but chan-
ges in the shoot diameter never accompanied AP genera-
tion. Hence, it can be concluded that VP was a response to
a hydraulic wave propagated by xylem. It is further confir-
med by an experiment, in which destruction of living tissu-
es in the petiole at a length of 2.5 cm totally eliminated AP
appearance behind a steam block, but it was not an obstacle
for VP (Mancuso 1999).
PROPAGATION ROUTES OF ACTION
AND VARIATION POTENTIALS IN PLANTS
Natural stimuli (change of light or temperature) coming
from the environment, damaging stimuli (scorching, inci-
sion) and nondamaging ones (electrical and mechanical sti-
muli, illumination) induce measurable changes of electrical
potential in plants. Those induced by damaging stimuli de-
pend on their strength, cease with the distance from the sti-
mulation place, and have variable shapes. In plant electro-
physiology, they have been called variation potentials.
After non-damaging stimuli, APs appear. APs are characte-
rized by a constant amplitude, constant propagation rate
and a regular shape. They fulfil classical electrophysiologi-
cal laws: the all-or-none law, strength-duration relation-
ship, and the dependence of refractory periods on the sti-
mulus strength (Paszewski and Zawadzki 1974, 1976;
Dziubiñska et al. 1983; Zawadzki et al. 1995).
The main role in generation and propagation of AP is
played by the plasmalemma membrane. Action potentials
were recorded in unicellular algae Acetabularia, which is
excitated as a whole (Gradmann 1976). In multicellular
algae consisting of giant internodal cells connected by
small nodal cells, e.g. Chara braunii, excitation propagates
mainly along internodal cells. Cytoplasmic connections be-
tween internodal cells and nodal cells do not guarantee AP
propagation, though it occurs occasionally (Sibaoka and
Tabata 1981). On the other hand, cytoplasmic connections
of cells in fungal mycelium allow propagation of potential
changes over the whole mycelium. Electrical, chemical or
mechanical stimulation of the fungi Pleurotus ostreatus and
Armillaria bulbosa evokes a series of APs propagating in
the mycelium (Olsson and Hansson 1995).
Electrical, mechanical and light stimuli induce genera-
tion of AP and its spreading in the whole thallus of the li-
verwort Conocephalum conicum (Paszewski et al. 1982;
Dziubiñska et al. 1983; Zawadzki and Trêbacz 1985; Trê-
bacz et al. 1989). Liverworts belong evolutionary to the
oldest land plants, and their thalli are characterized by an
uncomplicated structure. In response to stimulation Cono-
cephalum generates AP or series of APs of 80-130 mV am-
plitudes. AP propagates from the stimulation place in all
directions, covering gradually the whole thallus and rhizo-
ids. Similar results were obtained by Sinyukhin (1973),
studying gametophytes of the moss Bryum pseudotrique-
trum. Short-lasting illumination of the gametophyte indu-
ces AP formation, which also propagates in the whole
plant.
APs are generated and propagated by traps of some car-
nivorous plants. The plant in which APs were recorded for
the first time was the carnivorous Venus flytrap Dionaea
muscipula (Burdon-Sanderson 1882). The active traps of
Dionaea and Aldrovanda are built of excitable cells (Sibao-
ka 1966; Iijima and Sibaoka 1981, 1982; Hodick and Sie-
vers 1988). The excitable cells have identical magnitude of
resting potential (-110 mV) and generate APs of 110-150
mV amplitudes. The propagation rate of AP in both species
approximates 10 cm s
-1
. All the cells in the trap can partici-
pate in AP transmission between the receptor (sensory
hair) and effectors (cells in the motor zone). A fast AP
transmission by the trap is guaranteed by numerous plasmo-
desmata located between the cells of the sensory hair and
those of the trap (Iijima and Sibaoka 1982).
Sundew (Drosera) possesses a passive catching device.
Cells of sensory hairs generate AP, which propagates basi-
petally twice as fast as acropetally (1.0 cm s
-1
and 0.5 cm s
-1
,
respectively). All cells of the sensory hair are excitable, but
it is possible that the longitudal internal cells of the hair
participate mainly in the conduction of AP. The terminal
walls of these cells are joined by numerous plasmodesmata
(Williams and Pickard 1972; Williams and Spanswick
1976).
The propagation routes of excitation were studied in
other plants exhibiting fast movements, e.g. in Mimosa.
The researchers
,
attention was directed to vascular bundles
as conduction routes, similar to nerves in animals. Bose
(1925) called them even plant nerves. He inserted a ca-
pillary connected with a galvanometer into the petiole of
Mimosa at different depths. Only on capillary contact with
phloem the galvanometer showed reaction. Layers of cor-
tex, xylem and pith did not give this characteristic reaction.
Vol. 72, No. 4: 309-318, 2003 311ACTA SOCIETATIS BOTANICORUM POLONIAE
By this method he found that propagated excitation (evo-
ked by mechanical or thermal stimulus) showed two maxi-
ma one at the external, the other at the internal side of
xylem. This resulted in finding that AP is propagated in the
petiole of Mimosa leaf along two phloem routes separated
by the xylem.
Using the Bose
,
s method, Sibaoka (1954) confirmed that
conduction of excitation in the Mimosa petiole takes place
by two rows of elongated cells of the phloem tissue. At the
same time he observed that stimulation could spread trans-
versely because excitable elements are not sufficiently iso-
lated one from another. Only in the case when excitation is
propagated transversely in the Mimosa petiole it can be
propagated longwise at considerable distances. Thus exci-
tation transmission is based on cooperation of many cells.
Applying microelectrode technique it was possible to de-
termine the kind of tissues, which are routes of AP propa-
gation. These proved to be phloem and elongated cells of
protoxylem (Sibaoka 1962, 1966).
Studies with
14
C labelled acrylamide (Kalinin et al.
1970), application of blocks (surgical and chemical) (Kali-
nin et al. 1970), microelectrodes (Eschrich et al. 1988) and
studies of the electrochemical gradient of ions in conduc-
ting boundless (Opritov and Retivin 1982; Retivin and
Opritov 1986) pointed to phloem cells as the most predesti-
nated to generate and transmit excitation.
Fromm and Bauer (1994), applying cut off aphid stylets,
inserted through them microelectrodes precisely into sieve
tubes of Zea mays and Mimosa pudica (Fromm and
Eschrich 1988b). Examination of transmission routes of
APs by this method allowed them to find that transmission
of bioelectrical potentials takes place along the symplasmic
route of phloem, though it does not exclude the participa-
tion of other plant tissues. Partial surgical exposure of a very
short section of the bundles did not block AP transmission
either in front or behind the block. Thus, AP is transmitted
by the bundles over long distances, but locally by other tis-
sues. The former transmission type is much faster than that
occurring through mesophyle cells.
Rhodes et al. (1996) also considered phloem tissue as the
main route of excitation transmission. They studied the
propagation route of electrical signal mediating a local da-
mage with the systemic response appearing in tomato lea-
ves. Incision of the petiole surface allowed insertion of mi-
croelectrodes into cells of various types, which were iden-
tified by ionophoretic introduction of a fluorescence dye
(Lucypherin Yellow) at the end of the experiment. No si-
gnificant differences in values of resting potentials were re-
corded in various cells, but depolarization recorded after
stimulation had the highest amplitude (80 mV) in sieve or
companion cells and was approx. 3 times higher in compa-
rison with other cells of the petiole. The shape, amplitude,
and duration of transient depolarization pointed to AP. Sie-
ve elements and companion cells are closely connected
symplasmically and isolated from cells of other kinds,
which was demonstrated by lack of dye flow to cells surro-
unding them. The presence of pores in sieve elements pro-
vides continuity of membranes of low resistance over
a long distance. Moreover, symplasmic isolation from
other tissues makes the sieve tubes an ideal route of excita-
tion propagation (Wildon et al. 1992; Rhodes et al. 1996).
Lack of propagating electrical signals evoked by weak da-
mage stimuli made researchers look for other transmission
routes. Therefore, in their later paper Rhodes et al. (1999)
did not attribute electrical potentials to their sole participa-
tion in response to stress. In the light of new evidences,
they recognized priority of chemical factors formed at place
of wounding and propagated by xylem. Propagation of these
factors is also possible by phloem.
In the paper of Paszewski and Zawadzki (1976b), a ring
of tissues outside xylem, including phloem, was removed
from lupine stem at a length of 5-10 mm to examine the route
of excitation transmission. After electrical or a weak ther-
mal stimulation AP appeared, which was recorded by an
electrode attached to the stem in front of block. Electrodes
located behind the block did not record any change, which
would account for the participation in excitation transmis-
sion of the tissues located outside xylem, including phloem
tissue. After a strong stem scorching, AP appeared in the
form of a sharp peak followed by VP with the range and
the amplitude proportional to the stimulus strength. While
AP stopped at the block, VP was transmitted and recorded
by electrodes located behind the block. This account for
participation also of other tissues in VP transmission. If VP
had sufficiently high amplitude it evoked AP behind the
block.
Events of this kind were also observed by Zawadzki and
Trêbacz (1982). By tightening a nylon threat around the lu-
pine stem its external layers were destroyed. After a strong
tightening, which destroyed cell layers including phloem,
electrically triggered AP did not pass through the block.
Behind the block only potential changes of electrotonic
character were recorded. On weaker tightening AP passed
through the block, but its amplitude was twice lower than
that recorded in front of the block, although its transmis-
sion rate did not change. Some distance behind the block
development of AP of full amplitude was sometimes obse-
rved, it could propagate in two directions covering cells,
which were not excited before. In this experiments partici-
pation of cells of primary cortex including phloem in AP
propagation was shown.
AP propagation in Lupinus stem was studied by Hejno-
wicz et al. (1986), using an AC amplifier. The recorded si-
gnals were interpreted as originating from rows of excita-
ble cells. According to the authors, AP recorded by the tra-
ditional method (DC amplifier) resulted from averaging of
signals from excitable cells with involvement of volume
conductance of the remaining tissues.
Zawadzki et al. (1995) registered spontaneous action po-
tentials (SAPs) in sunflower, whose appearance in different
plant regions was quite nontypical. From multichannel
extracellular recording SAPs were found to appear locally,
covering larger or smaller plant region and then they disap-
pear. It is possible that SAPs propagate along limited rows
of excitable cells. This has been confirmed by studies of
APs and VPs evoked in Helianthus annuus. The plants,
which were stimulated by electrical stimuli, generated AP
which, propagating, involved the whole plant except lea-
ves. Another stimulation type, i.e. leaf scorching evoked
generation of variation potentials whose transmission diffe-
red distinctly from AP. Electrodes being at the same height
and inserted at a depth of approx. 1 mm on various stem sides
recorded VP only on the side of conducting bundles lying
in the leaf trace of the stimulated leaf. On the opposite
stem side no potential changes were recorded, or they
occurred with a low amplitude (Dziubiñska et al. 2001).
312 Dziubiñska H.SIGNAL TRANSMISSION IN PLANTS
VPs evoked by leaf scorching often entered leaves at lower
levels. Similarly, stimulation of one tomato leaf with elec-
trical stimulus induced AP, whereas after scorching VP
was observed. Stimulations of such a different character in-
duced the same events in distant leaves (Davies et al.
1997). The authors recognize two bioelectric carriers of in-
formation upon wounding: APs transmitted by the floem or
the hydraulic pressure wave propagating by the xylem in-
ducing local changes of membrane potential in adhering li-
ving cells, which is recorded as VP. They also take into ac-
count participation in signal transmission of chemical com-
pounds formed after wounding and translocated by the xylem
or the phloem.
The results obtained on Vicia faba also suggest that VP
propagation takes place by vessels (Roblin and Bonnemain
1985). Conduction of VPs takes place when the continuity
of conducting bundles between the stimulated leaf is main-
tained. Transmission of excitation occurs also transversely
because VPs were recorded in bundles isolated from the
stimulated leaf. Thus cells of other tissues participate in VP
transmission across V. faba stem. The authors also suggest
coexistence of VP transmission based on ion currents as
well as on transport of a stimulating substance formed as
a result of plant damage. Local stem cooling to 1°C inhibi-
ted bioelectrical response in this area, but it did not stop
propagation of the stimulating substance, which induced
VP behind the cooled region.
Signals evoked by a plant damage propagate systemical-
ly, reaching all plant tissues, and run distinctly along defi-
nite routes. In the latter case some regions of the plant
organism are beyond reach of electrical signals. Detailed
knowledge of propagation ways of these signals will allow
accurate interpretation of results concerning plant respon-
ses to stimuli.
PHYSIOLOGICAL ROLE
OF ELECTRICAL ACTIVITY IN PLANTS
Recognized existence of electrical responses (of AP and
VP character) in plants has resulted in attempts at connec-
ting electrical changes appearing after stimuli with changes
in physiological processes. It is important to monitor the
two phenomena simultaneously, which allows precise esti-
mation of temporal sequences of these events.
Sensitive and carnivorous plants have become objects of
studies as they exhibit motor properties.
Mimosa pudica reacts to the touch by generating AP and
subsequent leaflets folding and lowering the whole leaf. In
0.1 s after AP passing, a large amount of ions together with
water flows out from the pulvinus. The result of it is decre-
ase of turgor by motor cells and a fast leaf movement. An
identical mechanism of leaflets folding occurs in Biophy-
tum (Sibaoka 1973). Local chilling of the edge of the Mi-
mosa pudica petiole induces AP. The result of keeping ter-
minal leaflets in
14
CO
2
was that after 3-6 h labelled photo-
assymilates appeared in the phloem. Localization of the la-
belled photoassimilates was studied by the autoradiogra-
phic method before and after stimulation, i.e. before and
after AP passage. The microradiograms showed that label-
led assimilates of unstimulated plant were located only in
phloem. After stimulation, when AP reached the pulvinus,
membrane permeability undoubtedly increased and a relea-
se of labelled photoassymilates from pulvinus cells to apo-
plast took place (Fromm and Eschrich 1988a; Fromm
1991). Sudden increase of the concentration of assimilates
in apoplast causes water efflux from cells, mainly from
motor cells of the pulvinus to apoplast, and in consequence
decrease of their turgor and leaf folding. The mechanism of
rhythmical movements of Desmodium motorium leaflets also
consists in reversible changes of turgor pressure in motor
cells of the pulvinus (Antkowiak and Engelmann 1995).
Pressure changes and leaflets movements appeared follo-
wing AP. Oscillations of K
+
activity measured in the pulvi-
nus apoplast were correlated with changes of the membra-
ne potential. Apoplastic K
+
activity increased when the
membrane of pulvinus cells depolarized and leaflets moved
downwards. Upward leaflet movement was accompanied
by K
+
concentration decrease in apoplast.
APs appearing in carnivorous plants are important ele-
ments of the uptake mechanism of nitrogen rich compo-
unds. The fly-trap Dionaea muscipula has a leaf-trap,
which closes along the central nerve. The trap edges are
supplied with thorny processes, which make the impression
of a trap. On the leaf surface Dionaea possesses glands being
an attraction for insects, as well as multicellular sensory
hairs. Bending such a hair by an insect evokes a graded
electrical response in sensory cells within hairs depending
on the intensity and a rate of bending (Sibaoka 1969).
After exceeding a certain value of depolarization, AP appe-
ars which at a rate of 10 cm min
-1
propagates all over the
trap. The first stimulation does not make the trap close, but
it is memorized. If within 20 s the second stimulation
takes place the AP propagates over the trap at approx. 3
times higher rate and the trap is closed. The motor cells are
supposed to act on the same principle as in Mimosa (Sibao-
ka 1969; Jacobson 1974; Sibaoka 1979). Basing on the hy-
pothesis of acid growth, a different mechanism was propo-
sed by Williams and Bennet (1982). AP evoked after sti-
mulation causes a fast H
+
efflux into the cell walls of the
lower side of the trap, in the area of the main nerve. Pro-
tons cause cell wall loosening, which leads to fast water
absorption by cells and their volume increase. Asymmetri-
cal volume change of the lower and upper trap sides causes
its closing.
The physiological significance of AP was shown also in
other carnivorous plants, e.g. Aldrovanda, Drosera (Sibao-
ka 1979; Iijima and Sibaoka 1981, 1982, 1983, 1985). In
these plants the mechanism of stimulus perception by the
hair receptor cells, excitation transmission, trap closure on
the basis of turgor decrease by motor cells are similar to
that in Dionaea.
Water loss by sieve cells that causes leaf movement di-
sturbs phloem transport. Electrical stimulation of the Pha-
seolus vulgaris stem and stimulation of Zea mays leaf with
thermal shock stops (totally or partially) the translocation
of the phloem sap (Fromm and Bauer 1994; Pickard and
Minchin 1990, 1992). Transport inhibition is the result of
opening of ion channels in the plasmalemma and an efflux
of K
+
, and Cl
-
ions together with water from phloem cells
into apoplast. These ions together with Ca
2+
are the main
ions taking part in AP generation.
APs participate in the first stage of fertilization of the
moss Bryum pseudotriquetrum and the fern Asplenium tri-
chomanes, and thereby in the process of reproduction.
A short-lasting illumination of the gametophyte of these
Vol. 72, No. 4: 309-318, 2003 313ACTA SOCIETATIS BOTANICORUM POLONIAE
plants induced electrical changes propagating over the
whole thallus (Sinuykhin 1973). Within 2 s after passing of
depolarization wave water efflux (guttation) so indispensa-
ble in fertilization of these plants begins. AP regulates also
other aspect of plant preparation for fertilization as is the
case in Lilium martagon, Lilium longiflorum and Incarvil-
lea grandiflora (Sinuykhin and Britikov 1967; Spanjers
1981). In Incarvillea, stimulation of the stigma by an insect
induces AP, which, propagating at a rate of 1.8 cm s
-1
rea-
ches the place of connection of the bilobal stigma. The
stigma closes within 6-10 s. AP does not pass below the
stigma. If mechanical stimulation is not accompanied by
pollination, the stigma opens again after several minutes.
In case the deposited pollen begins to germinate on the
stigma, chemical processes lead to depolarization of the
stigma cells and the induction of subsequent AP, which, at
a higher rate than the preceding, propagates along the style
reaching the ovary after several dozens of seconds. Meta-
bolic processes are activated in the ovary, respiration incre-
ase is observed. In this way the ovary is preparing for ac-
ceptance of the pollen-tube with sperm cells and for fertili-
zation. Such two-stage AP transmission is very advantage-
ous for Incarvillea, because it eliminates accidental mecha-
nical stimulation of the stigma for instance by insects
which have not brought any pollen. The stigma of Lilium
martagon does not show motor properties as Incarvillea,
but germinating pollen induces similar electrical and meta-
bolic reaction as in Incarvillea. A mechanism of protection
against fertilization with improper pollen was found in Li-
lium (Spanjers 1981). Electrical potentials generated after
depositing an improper pollen on the stigma differed from
those induced by a proper pollen. Similar preparation of
the ovary for acceptance of the male cell was demonstrated
in Hibiscus (Fromm et al. 1995). Stimulation of the plant
stigma with a compatible pollen induced series of APs,
which are propagated along the style to the ovary. The ova-
ry response (after 3-5 min since stimulation) was in the
form of increased respiration rate by approx. 12%, levels of
ATP, and sugars (glucose, fructose and saccharose). Scor-
ching of Hibiscus stigma induced electrical response diffe-
ring from AP. It was shown that different physiological
and non-physiological stimuli applied to Hibiscus stigma
induced specific electrical responses, which, propagating
along the pistil, carry information to the ovary. Depen-
ding on the kind of the signal the ovary is preparing for fer-
tilization, changing its metabolism or not. The biochemical
responses of the ovary to pollination are so fast that only
APs can take part in signal transmission. Preparation for
plant fertilization based on generation of electrical poten-
tials can be a phenomenon commonly occurring. It is even
supposed that AP but not florigen (flowering hormone) is
responsible for plant flowering (Davies 1987).
Passing AP wave influences the intensity of gas exchan-
ge in angiosperm plants: Cucurbita pepo, Phaseolus vulga-
ris (Gunar and Sinuykhin 1963; Sinuykhin and Gorchakov
1968), Lycopersicon esculentum (Van Sambeek and Pic-
kard 1976), Salix viminalis (Fromm and Eschrich 1993),
Vicia faba (Filek and Kocielniak 1997), Zea mays
(Fromm and Fei 1998). In evolutionary distant plants, be-
longing to the oldest land plants as the liverwort Conoce-
phalum, electrical or mechanical stimulation (incision of
the thallus edge) induces AP or VP, and in several seconds
later the respiration intensity increases by up to 100%
(Dziubiñska et al. 1989). In the case of APs series, the res-
piration increase is correlated with subsequently appearing
APs. In unexcitable thalli stimulation does not induce either
AP or VP and does not cause a change in respiration rate,
either. Such a fast plant reaction to stress can appear only
when a fast propagating signal is involved. In this case
only electrical potentials satisfy the condition. They can
play an informative role and coordinate physiological pro-
cesses in the whole plant regardless of the place where
a stimulus acts.
Fast electrical signalization guarantees communication
of the whole mycelium in the fungi Pleurotus ostreatus and
Armillaria bulbosa (Olsson and Hansson 1995) carrying in-
formation about damages, pathogens and locally changing
conditions. Similarly, the electrical change appearing in se-
veral seconds after illumination by red light in a caulone-
mal filament of the moss Physcomitrella patens precedes
the initial stage of gametophyte development (Ermolayeva
et al. 1996).
Application of abscisic acid to willow roots induces acro-
petally propagating APs. After reaching leaves (in 2-3 s)
they cause instantaneous closing of stomata (Fromm 1991).
The ionic mechanism of AP and the closing mechanism of
stomata show a great similarity (Schroeder 1992).
Preparation of tissues for defence against various stres-
ses, among other things against effects of low temperature,
belongs to the physiological phenomena controlled by AP
(Retivin et al. 1997; Pyatygin et al. 1999). Moreover, AP
causes a reduction of the growth rate of stem internodes in
Luffa cylindrica (Shiina and Tazawa 1986), inhibits water
uptake and stem growth of Helianthus annuus (Davies et
al. 1991). Chemical stimuli induce changes of electrical
potential, which in turn stimulate growth of etiolated see-
dlings and affect nutation and phototropic movements
(Spalding and Cosgrove 1993). Touch and gravitation are
stimuli, which affect growth of Arabidopsis seedlings, and
APs, besides other candidates, are recognized as factors
mediating between stimulus and reaction (Fasano 2002).
In response to changes occurring in the environment
plant cells are able to synthetize various protective substan-
ces. Addition to the soil, in which 3-week-old soybean see-
dlings (Glycine max (L) Merrill) grow, of pentachlorofenol
(PCP), carbonyl cyanide 4-trifluoromethoxyphenylhydra-
zone (FCCP), carbonyl cyanide 3-chlorophenylhydrazone
(CCCP) solution induces AP formation, which propagates
along the stem at a rate of 30 m s
-1
(Volkov et al. 2000;
Shvetsova at al. 2001; Volkov and Mwesigwa 2001; Laba-
dy et al. 2002). Such fast AP transmission seems to be ne-
cessary for the plant to react quickly to the presence of
extremely harmful chemical compounds in the medium, by
producing phytoalexins or stress proteins. Neverthless it
should be stressed that these are the first reports presenting
such a fast AP transmission. As yet the highest rate of AP
transmission (7.0-25.0 cm s
-1
) has been recorded in carni-
vorous plants (Sibaoka 1966, 1969; Iijima and Sibaoka
1982).
Furthermore, measurements of APs and VPs can be used
as environmental biosensors for studying the influence of
external stimuli on plants, i.e. acid rain (Shvetsova et al.
2002).
Participation of AP in regulation of peroxidase activity in
Conocephalum thallus has been shown (Dziubiñska et al.
1999). After local incision of thallus APs were generated.
314 Dziubiñska H.SIGNAL TRANSMISSION IN PLANTS
Soon after that a doubling (approx.) of peroxidase activity
was recorded. AP absence despite stimulation or appearan-
ce of only local responses of small amplitudes had no in-
fluence on peroxidases activity. The results of these studies
distinctly point to participation of APs in formation of sys-
temic response to stress.
Owing to application of rapidly developing techniques of
molecular biology attempts could be made to determine
stress influence on gene expression. Mechanical injury of
tomato leaf results in expression of gene pin2 encoding
protective substance proteinase inhibitor (Stankoviæ and
Davies 1996; Vian et al. 1996; Davies at al. 1997; Stanko-
viæ and Davies 1997, 1998; Herde et al. 1999) as well as
calmodulin (cal) encoding gene (Davies et al. 1997). The
activity of pin2 is correlated with the electrical signal,
which appears after injury and passes along the stem to the
leaf (Wildon et al. 1992). Blocking of phloem transport by
chilling the cotyledonary petiole of wounded cotyledon did
not stop transmission of electrical signal and did not inhibit
PI activity in the stem and leaf. Cutting off the wounded
cotyledon just after the damage so that the electrical signal
had not enough time to reach the stem did not cause chan-
ges in the PI expression. Thus, the function of electrical si-
gnals propagating in plants was unambiguously demonstra-
ted (Roberts 1992; Wildon et al. 1992; Thain and Wildon
1993). Later, more detailed studies resulted in the conclu-
sion that other signaling processes could also lead to syste-
mic gene expression (Stankoviæ and Davies 1997; Rhodes
at al. 1999). In the light of these results the participation of
both electrical and hydraulic signals and chemical substan-
ces could be accepted in PIs induction after wounding.
According to the above presented results electrical po-
tentials should be recognized as important, multifunctional
signals occurring in plants. APs can initiate both non-spe-
cific and specific adaptational responses in plants. Plants
belonging to different systematic groups respond to various
stimuli coming from environment with movements, chan-
ges of gene expression, the level of respiration, transpira-
tion, photosynthesis, stem growth and water uptake as well
as with changes in activity of enzymes.
Regardless of which transmission routes the excitation of
a plant chooses, it always induces changes in ion flow.
This occurs due to opening ion channels in the membrane.
It concerns not only plasmalemma but also the endomem-
branes as ER, and particularly the tonoplast. The vacuole is
a reservoir of Ca
2+
ions, which are the main second mes-
senger in signalling. Therefore, it is very important to study
the ion channels of the tonoplast and other endomembranes,
their influence on generation of electrical potential and, in
consequence, on physiological responses of plants subject
to the action of pathogens, viruses or other kinds of stress.
There are different ways Ca
2+
ions can participate in in-
tracellular signalling:
1) Ca
2+
influx to the cytoplasm after a stimulus, activates
Ca
2+
-dependent Cl
-
channels and in consequence depolari-
zation of the membrane spreads. 2) A stimulus opens Cl
-
channels and depolarization follows which opens Ca
2+
channels in the vacuole and Ca
2+
concentration in cyto-
plasm increases. 3) A stimulus induces opening of cation
channels and through them Ca
2+
flow into the cytoplasm,
which causes activation of Cl
-
channels depending on Ca
2+
and depolarization and opening of vacuolar Ca
2+
channels
and Ca
2+
concentration increase in the cytoplasm.
It is possible that plants can take advantage of various si-
gnals differing in mechanism of propagating and their ac-
tion. They can be APs, VPs, chemical factors and signals
resulting from hydraulic pressure change. Such a variety of
mechanisms and ways of signal transmission protects
plants in the environment.
ACKNOWLEDGEMENTS
This paper was financially supported by the State Com-
mittee for Scientific Researches (KBN).
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DROGI TRANSMISJI SYGNA£ÓW
I FIZJOLOGICZNA ROLA POTENCJA£ÓW ELEKTRYCZNYCH U ROLIN
STRESZCZENIE
Roliny podlegaj¹ wp³ywom bodców pochodz¹cych ze rodowiska. S¹ one od niego bardzo zale¿ne i w prze-
ciwieñstwie do zwierz¹t nie s¹ w stanie aktywnie unikn¹æ jego wp³ywom, czêsto szkodliwym. Dlatego posiadaj¹c
zdolnoæ odbierania bodców wykszta³ci³y te¿ adekwatne odpowiedzi na nie. Reakcja taka mo¿e pojawiæ siê tyl-
ko w obszarze dzia³ania bodca, obj¹æ czêæ roliny lub ca³¹. W tym ostatnim przypadku jest to odpowied syste-
miczna. Reakcja roliny wyra¿ona jest ró¿n¹ si³¹ i szybkoci¹ i rodzajem odpowiedzi. Powstaje pytanie o naturê
sygna³u nios¹cego informacje o bodcu, drogi jego rozprzestrzeniania siê i mechanizmu transmisji. Wyró¿nia siê
trzy koncepcje transmisji pobudzenia: 1) rozchodzenie siê czynników chemicznych powsta³ych w miejscu dzia³a-
nia bodca z pr¹dem soku floemowego (lub poprzez atmosferê jeli s¹ to substancje lotne) do innych czêci roli-
ny, 2) bardzo szybka transmisja ksylemem fali cinienia hydraulicznego powsta³ego po uszkodzeniu roliny. £¹-
cz¹c hipotezê hydrauliczn¹ z chemiczn¹ powstaje koncepcja hydraulicznej dyspersji. Zak³ada ona, ¿e sub-
stancje chemiczne powsta³e po zranieniu mog¹ bardzo szybko przemieszczaæ siê po ca³ej rolinie z fal¹ zmian ci-
nienia hydraulicznego, 3) bodziec wywo³uje zmianê potencja³u o charakterze czynnociowym (action potential
AP) a jego transmisja, odbywaj¹ca siê na zasadzie obwodów lokalnych od komórki do komórki, mo¿e wyst¹piæ
wzd³u¿ ca³ej roliny, jej organu lub wyspecjalizowanej tkanki. Po silnych, uszkadzaj¹cych bodcach mog¹ poja-
wiæ siê variation potentials (VPs), których natura ró¿ni siê od APs. Postuluje siê, ¿e transmisja VP pojawia siê
dziêki hydraulicznej dyspersji za elektryczne zmiany s¹ zjawiskiem wtórnym.
S£OWA KLUCZOWE: potencja³ czynnociowy, potencja³ wariacyjny, transmisja sygna³u, odpo-
wied systemiczna.
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318 Dziubiñska H.SIGNAL TRANSMISSION IN PLANTS
