ISSN 0006-2979, Biochemistry (Moscow), 2023, Vol. 88, No. 10, pp. 1467-1487 © Pleiades Publishing, Ltd., 2023.
Russian Text © The Author(s), 2023, published in Biokhimiya, 2023, Vol. 88, No. 10, pp. 1775-1799.
1467
REVIEW
Ion Channels in Electrical Signaling in Higher Plants
Maxim A. Mudrilov
1
, Maria M. Ladeynova
1
, Darya V. Kuznetsova
1
,
and Vladimir A. Vodeneev
1,a
*
1
Department of Biophysics, Lobachevsky National Research State University of Nizhny Novgorod,
603950 Nizhny Novgorod, Russia
a
e-mail: v.vodeneev@mail.ru
Received June 21, 2023
Revised September 16, 2023
Accepted September 18, 2023
Abstract— Electrical signals (ESs) appearing in plants under the action of various external factors play an important role
in adaptation to changing environmental conditions. Generation of ES in higher plant cells is associated with activation
of Ca
2+
, K
+
, and anion fluxes, as well as with changes in the activity of plasma membrane H
+
-ATPase. In the present
review, molecular nature of the ion channels contributing to ESs transmission in higher plants is analyzed based on com-
parison of the data from molecular-genetic and electrophysiological studies. Based on such characteristics of ion chan-
nels as selectivity, activation mechanism, and intracellular and tissue localization, those ion channels that meet the re-
quirements for potential participation in ES generation were selected from a wide variety of ion channels in higher plants.
Analysis of the data of experimental studies performed on mutants with suppressed or enhanced expression of a certain
channel gene revealed those channels whose activation contributes to ESs formation. The channels responsible for Ca
2+
flux during generation of ESs include channels of the GLR family, for K
+
flux– GORK, for anions– MSL. Consideration
of the prospects of further studies suggests the need to combine electrophysiological and genetic approaches along with
analysis of ion concentrations in intact plants within a single study.
DOI: 10.1134/S000629792310005X
Keywords: electrical signals in plants, long-distance signals, ion channels, action potential, variation potential
Abbreviations: AP, action potential; ES, electrical signal;
SP,system potential; VP,variation potential.
* To whom correspondence should be addressed.
INTRODUCTION
Plants in nature are subjected to the action of var-
ious adverse environmental factors. In order to develop
coordinated systemic response to the action of envi-
ronmental factors long-distance signal transmission is
required. Three types of long-distance signals are rec-
ognized in plants– chemical, hydraulic, and electrical,
which differ both in nature and in the rate of transmis-
sion. Electrical signal(ES) with propagation rates up to
tens of centimeters per second, together with hydraulic
ones, are considered as rapid long-distance signals [1-4].
Propagation of ESs triggers a wide range of func-
tional changes in the non-affected parts of the plant.
The ES-induced responses include changes in photosyn-
thesis activity and transpiration, enhancement of respi-
ration, changes in ATP content, expression of protective
genes, and others [1, 3, 5]. Such changes play an import-
ant role in the plant adaptation to the changing environ-
mental conditions. It is known that the mechanisms of
induction of ES-mediated systemic responses in plants
are based on the changes of ion concentrations during
the generation of ESs with the shifts in Ca
2+
and H
+
con-
centrations playing the most important role [5,6]. Ion
flows causing the change in concentration appear as a
result of changes in the activities of ion transport sys-
tems, primarily ion channels [2, 3, 7]. However, molec-
ular nature of such channels remains poorly understood.
Elucidation of the molecular nature of ion chan-
nels participating in generation of ESs in higher plants
is challenging. Firstly, it must be mentioned that investi-
gation of the parameters of ESs and mechanisms of their
generation was conducted with different plant species.
Inparticular, plants exhibiting locomotion comprise tra-
ditional objects in the area of plant electrophysiology.
Another model object, for which a significant amount of
data on the mechanisms of ES generation was accumu-
lated and involvement of ion channel in these processes
MUDRILOV et al.1468
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
was for the first time demonstrated, are giant cells of ch-
arophyte green algae that are very simple to work with
from methodological point of view [8-11]. At the same
time, Arabidopsis (Arabidopsis thaliana) is the main ob-
ject of molecular genetics research, but for which only
few studies devoted to investigation of ES are available.
All the facts mentioned above do not allow direct com-
parison of the electrophysiological and molecular genet-
ics data in the literature. In this review we attempted to
make such comparison: we present available information
on the nature of ion channels underlying the mecha-
nisms of ES generation and on the ion channels with
identified genetic association, as well as we suggest the
most probable participants of the process of ES gener-
ation in higher plants based on the analysis of the data.
ELECTRICAL SIGNALS IN HIGHER PLANTS
The values of membrane electric potential in the
plant cells at rest are at significantly more negative lev-
el in comparison with the animal cells, which is below
–100 mV, and for some plants and plant tissues even
below –200 mV. Such high values are due to the signif-
icant contribution of the metabolic component to the
total value of electric potential, which is created due to
the functioning of the plasmalemma H
+
-ATPase [6,8].
Electric transmembrane potential, as a component of
electrochemical gradient, is a moving force of membrane
transport, including ion flows occurring during genera-
tion of ESs. At present, three different types of ESs are
recognized in plants: action potential (AP), variation
potential (VP), and system potential (SP) [1, 3, 7, 12].
Thelatter is not considered in this review due to insuf-
ficient knowledge on the mechanisms of its generation.
Classification of the signals into different types is based
on several characteristics including direction of the po-
tential change (de-/hyperpolarization), duration of elec-
trical reaction, nature of its propagation, as well as typi-
cal stressors triggering the signal of a certain type.
Action potential (AP) comprises a transient de-
polarization with amplitude of several tens of mV that
has typical pulse shape appearing after the threshold is
reached according to the “all-or-none” principle [1, 6,
12, 13]. The mentioned properties of plant AP are similar
to those of classic nerve pulse. The main differences are
associated with the time-characteristics of the reaction:
duration of AP in plants is thousand-fold longer than the
duration of nerve pulse– from several seconds in plants
with locomotion such as mimosa and Venus flytrap, to
several tens of seconds in regular plants without locomo-
tion [1,13].
The mechanism of AP generation in plant cells
(Fig. 1) also differs from the classic Na
+
/K
+
-scheme
of the nerve pulse. Formation of depolarization phase
in plants is associated with influx of Ca
2+
and efflux of
anions, primarily Cl
–
, as well as, likely, with the tempo-
rary decrease of the H
+
-ATPase activity. In the process,
Ca
2+
ions play predominantly signaling role inducing an-
ion flow and inactivation of the H
+
-ATPase [1, 12, 13].
At the same time, the defining role of Ca
2+
in the change
of the level of electric potential during formation of de-
polarization phase was demonstrated for some plant spe-
cies [14,15], which indicates diversity of the mechanism
of AP generation in different plant species. Formation
of the repolarization phase is associated with the efflux
of K
+
mediated by depolarization and with reactivation
of H
+
-ATPase due to removal of the excess of Ca
2+
ions
[3, 8, 13].
Propagation of AP within the plant (Fig. 1) oc-
curs without significant decrease of amplitude and rate,
which usually is from the fraction of a centimeter to
several centimeters per second, reaching 8-10 cm/s in
the plants exhibiting locomotion [1, 7, 16]. The decre-
ment-free propagation of AP indicates that this process
is active: generation of AP induces depolarization in the
neighboring cells up to threshold levels due to appear-
ance of local currents followed by generation of AP at
these sites [8, 12, 13]. In general, in can be stated that
there are fundamental similarities between the mecha-
nisms of propagation of a nerve pulse and propagation
of AP in plants, despite the lower rate of the latter (by
2-3 orders of magnitude). However, the issue of the
main pathways of AP transmission in higher plants re-
mains unresolved. Conducting bundles in higher plants
are generally recognized as a pathway of systemic trans-
mission of all types of the signals, including electrical
[1,5,7]. It has been assumed that the phloem cells both
sieve elements and phloem parenchyma are responsible
for undamped transmission of AP [1, 3]. There is also
radial propagation of AP from the conducting bundles
to the neighboring cells through plasmodesma connec-
tions, probably as a fading signal [1,12,13].
Various non-damaging stimuli such as changing of
temperature, illumination intensity, touching, and oth-
ers cause generation of AP. The mechanisms of transfor-
mation of the energy of stimulus into changes of poten-
tial and role of certain ion channels in this process are
considered in the respective reviews [3,7, 17]. It must
be emphasized that generation of AP in plants, similar
to the nerve fibers, could be also induced by the direct
electrical stimulation [15], which indicates certain role
of voltage-gated ion channels in the induction of AP.
Variation potential (VP) (Fig. 1), similar to AP, com-
prises a transient depolarization with amplitude of several
tens of mV, but it has much longer duration, up to several
minutes, and irregular shape [1, 3, 7, 13, 16]. While con-
sidering long duration of VP, which often results in its
description as a slow wave potential (SWP), it must be
emphasized that the reason for it is slow phase of repolar-
ization in VP with duration of depolarization phase usu-
ally not exceeding several seconds as in the case of AP.
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1469
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Fig. 1. Scheme for generation and propagation of action potential(AP) and variation potential(VP) along the conductive plant tissues. Non-dam-
aging stimulus, which is transmitted primarily along the phloem (sieve elements, SE) due to emergence of local currents (marked with red arrows).
Damaging stimulus induces VP, which is propagated via transmission along xylem(Xy) of the chemical (marked with green dots) or hydraulic
(marked with blue arrow) signals. Mechanisms of AP and VP generation are presented in the scheme on the right (see explanations in the text).
VP, unlike AP, does not function according to the “all-
or-none” rule, its amplitude and duration depend on the
type of stimulus [18,19] and surface area of damage [16].
Rate of propagation of VP is 0.1-10mm/s. With the in-
creasing distance form the damage site decrease of the
amplitude and rate of signal propagation are observed [1,
3, 6, 13]. Generation of VP is induced by the damaging
stimuli [1,3], such as burn [18,19], mechanical damage
[18, 20, 21], and heating [18, 19, 22].
Transient suppression of the plasmalemma H
+
-ATP-
ase activity has been considered for a long time as the
only mechanism of VP formation (Fig.1) [13,16]. Later
it was shown that the passive flows of Ca
2+
, Cl
–
, and
K
+
ions that appear, likely, during activation of corre-
sponding ion channels also contribute to generation of
VP together with the transient inactivation of the proton
pump [7, 23, 24]. Similar to the case of AP, in the initial
step of VP generation there is influx of Ca
2+
into the cell,
MUDRILOV et al.1470
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
which causes decrease of the H
+
-ATPase activity that
lasts much longer than in the case of AP. Flow of anions,
such as Cl
–
, also contributes to formation of depolariza-
tion phase [5, 12, 25, 26]. Formation of repolarization
phase occurs due to restoration of the H
+
-ATPase ac-
tivity, as well, likely, due to efflux of K
+
from the cell
[1, 26]. Despite the fact that both AP and VP involve
transport of the same set of ions (Ca
2+
, Cl
–
, K
+
, H
+
), ion
transport systems responsible for their movements are,
likely, different in both types of ESs. This is indirectly
confirmed by the fact that VP could appear in the period
of absolute refractory of AP [8,16].
Unlike AP, VP is not a self-propagating ES (Fig.1),
but comprises a local electrical reaction induced by the
hydraulic or chemical signal [1, 5, 7, 26]. The possibil-
ity of VP induction by artificially increasing pressure
[27] supports the role of hydraulic wave in its induction,
which suggests activation of mechanosensitive ion chan-
nels [1, 16, 26]. Propagation of the chemical signal from
the zone of damage is assumed to be realized through the
diffusion of the ‘wound substance’ along the conduct-
ing bundles, which induces influx of Ca
2+
into the cell.
According to the modern notion, reactive oxygen species
(ROS) produced by NADPH-oxidases, probably respi-
ratory burst oxidase homologD (RBOHD), could func-
tion as such signaling molecules [28]. Systemic spread
of H
2
O
2
has been demonstrated during the action of the
typical VP-inducing stimuli– during mechanical dam-
age, heating, and excessive illumination [28-30]. In turn,
Ca
2+
is capable of activating RBOHD causing increase
of H
2
O
2
production [7,31], which, consequently, could
facilitate self-sustaining propagation of the signal.
The abovementioned information on the mecha-
nisms of generation and propagation of ESs in higher
plants was obtained with the use of a complex of electro-
physiological methods including analysis of gradients of
electrochemical potentials for different ions, recording
the shifts of ion concentrations during excitation, vary-
ing ion composition of the medium, inhibitory analysis
using ion channel blockers, and others.
It should be mentioned, first of all, that passive
flows of ions along the concentration gradient form the
basis for generation of ESs [6, 32]. There is a significant
electrochemical gradient of Ca
2+
ions due to low Ca
2+
concentrations in cytosol and high concentrations in ap-
oplast and intracellular compartments such as vacuole
and ER [33]. Content of anions in cytosol is higher than
their content in apoplast [34], which together with the
negative intracellular electric potential creates a signif-
icant outward-directed gradient [6]. For K
+
concentra-
tion, which is close to equilibrium at rest, the outward
gradient appears during depolarization [6, 32, 35].
Contribution of certain ions to generation of ES
initially was investigated by varying ion composition of
the medium and evaluation of its effect in the param-
eters of ESs. Using this approach participation of Ca
2+
,
Cl
–
, and K
+
in generation of AP in higher plants was
revealed [8, 13]. This approach was also used to estab-
lish the source of the Ca
2+
ion concentration increases
in cytosol, which is extracellular depot, because chelat-
ing of Ca
2+
in the extracellular space results in practical-
ly complete suppression of AP, but not in the complete
suppression of VP [14, 25, 26].
Due to the long duration, generation of even a sin-
gle ES in plants, unlike in animals, causes noticeable
changes of ion concentrations. Relative changes are pro-
nounced more in those compartments, where ion con-
centration at rest is low– Ca
2+
on cytosol, K
+
and Cl
–
in
apoplast [36, 37]. Changes of ion concentrations were
recorded with the help of a number of methods such as
ion-selective electrodes [24,38], microelectrode ion flux
measurements (MIFE) [39], method of flame photom-
etry and radioactive indicators [8], as well as ion-sen-
sitive chemical or genetically encoded fluorescent sen-
sors[40]. The results indicate influx of Ca
2+
and efflux
of K
+
and Cl
–
from the cell during generation of both AP
and VP [24, 26, 38]. All aforementioned facts together
with the data on the direction of the moving force con-
firm that the flows of the indicated ions are passive mov-
ing through the ion channels along the electrochemical
potential gradient.
Classic method for evaluation of activation of ion
channels involves measuring of electric resistance of a
membrane upon excitation. Generation of AP in plants,
similar to the case of nerve pulse, is accompanied by the
decrease of membrane resistance, which serves as a proof
of activation of ion channels [26]. With regard to VP, it
has been believed for a long time that there is no drop
in resistance in this case, which served as a main argu-
ment suggesting a key role of the electrogenic H
+
pump
rather than ion channels in formation of VP [13, 16, 26].
However, later drop in resistance during formation of VP
has been demonstrated, which indicated activation of
ion channels [25,26].
The types of ion channels activation of which medi-
ated the revealed ion fluxes forming ES were investigat-
ed with the help of blockers. In particular, participation
of Ca
2+
-channels in generation of ES was demonstrat-
ed by suppression of ES by the blocker of all types of
Ca
2+
-channels for both the cases of AP [15,41] and VP
[22, 25]. Use of more specific blockers, verapamil, in
particular, which blocks voltage-gated channels, as well
as neomycin and ruthenium red that block Ca
2+
efflux
from intracellular sources showed participation of corre-
sponding Ca
2+
-channels in generation of AP [15,42,43].
Gd
3+
, inhibitor of mechanosensitive Ca
2+
-channels sup-
pressed propagation of VP into unstressed tissues, but
not suppressed generation of VP in the zone of stim-
ulation [24]. The blockers of anion channels, such as
etacrynic acid, NPPB (5-nitro-2-(3-phenylpropylami-
no)-benzoic acid), and A-9-C (anthracene-9-carboxyl-
ic acid) decrease amplitude and rate of depolarization
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1471
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
in AP [15, 41, 43] and VP [24, 25, 38]. The blocker of
K
+
-channels, tetraethyl ammonium(TEA), slows down
the phase of depolarization in AP, as well as increases
amplitude of the pulse and decreases duration of depo-
larization [15, 41, 43]. The latter indicates that the ef-
flux of K
+
begins at the phase of depolarization in AP,
i.e., there is overlapping of depolarizing and repolarizing
ion flows. With regards to VP, increase of duration of
the depolarization phase under the effect of TEA was
demonstrated [24, 25, 38].
Hence, based on the results of electrophysiological
analysis it can be concluded that the generation of AP
is associated with activation of voltage-gated Ca
2+
-chan-
nels, while generation of VP is associated with activa-
tion of ligand-dependent and Ca
2+
-channels. Anion and
K
+
-channels participate in the process of generation
of both AP and VP. H
+
-ATPase of plasmalemma also
provides significant contribution to generation of ESs.
The plasmalemma channels have been considered
first during analysis of the role of ion channels in gener-
ation of ES in higher plants. At the same time, changes
of ion concentrations could be due to activation of the
channels localized on the membranes of intracellular
compartments, such as, primarily, the largest one– vac-
uole [33]. Electroexcitation of tonoplast and the role of
vacuole as a source of Ca
2+
and Cl
–
in generation of ES
was observed in charophyte algae [10, 44]. Some studies
indicate a similar role of vacuole in other plants [10,15],
in particular, electroexcitation of tonoplast and efflux
Ca
2+
from the vacuole was demonstrate in the Arabidop-
sis plants [44]. This speaks of the need to consider ion
channels of tonoplast during analysis despite the absence
of unambiguous data on their role in generation of ESs
in higher plants.
It must be mentioned that currently the exact set of
ion channels has not been identified for any types of ES,
functioning of which is associated with formation of de-
polarization and repolarization phases of ESs. Based on
the analysis of the data of electrophysiological studies,
selection of the channels potentially involved in gener-
ation of ES should be based on the following criteria:
(i) selectivity, the channels mediating Ca
2+
, K
+
, and Cl
–
transport are the most interesting; (ii) activation mech-
anism, possibility of activation during depolarization,
mechanical or chemical stimulation; (iii) localization,
predominantly on plasmalemma (probably tonoplast) of
the cells of conducting tissues.
ION CHANNELS OF HIGHER PLANTS
Currently different groups of ion channels in plants
have been characterized with the help of electrophysio-
logical methods, however, as has been mentioned in the
review by Demidchik et al. [45], majority of the genes
that encode these channels are still unknown. During
the last two decades combined analysis of molecular
genetics and electrophysiological data have been per-
formed mainly for some groups of ion channels such
a K
+
-channels [46, 47]. At the same time, the genes
encoding Ca
2+
-channels, in particular plasmalemma
Ca
2+
-channels, have not yet been revealed [45]. In this
section the data on the known groups of ion channels
that potentially could participate in formation of ESs in
plants are summarized (table).
Calcium permeable channels. Despite the widely
recognized importance of calcium for plant metabolism,
including their role as a secondary messenger, plants do
not have canonic ion channels with Ca
2+
-selective fil-
ters. Instead, plants have Ca
2+
-permeable cation chan-
nels that are capable of transporting also other two- and
monovalent cations [45,55], however, for convenience
sake this detail is omitted in the majority of publica-
tions, and we follow the suite in this review. Based on
their electrophysiological characteristics Ca
2+
-channels
are classified into three groups: depolarization-activat-
ed Ca
2+
channels (DACC), hyperpolarization-activated
Ca
2+
channels (HACC), and voltage-independent Ca
2+
channels (VICC); sometimes mechanosensitive Ca
2+
channels (MSCC) are distinguished as a subgroup in the
last group. It is worth to mention one more time that the
genes encoding DACC of plasmalemma have not been
identified yet. Ca
2+
-channels are also classified accord-
ing to kinetics of their activation: fast channels (respond-
ing within milliseconds), slow channels (responding
within seconds), and channels with pulsing conductance
(response time 1-3 milliseconds) [45,55].
Using molecular genetics approaches the following
families of Ca
2+
-channels have been identified so far:
ionotropic glutamate-like receptors (GLR), cyclic nu-
cleotide-gated channels CNGC), annexins (ANN), two-
pore channels (TPCs), Mid1-complementing activity
channels (MCA), hyperosmolality-induced [Ca
2+
]
i
in-
crease 1channel (OSCA1), and piezo channels (Piezo)
[45, 55], as well as recently discovered rapidly activated
calcium mechanosensitive channel (RMA) [95].
GLRs are integral membrane proteins localized pre-
dominantly on plasmalemma and exhibiting activity of
a non-selective ion channel, which is belongs to VICC
based on electrophysiological properties. Various amino
acids and their derivatives could serve as ligands of these
receptors, and some activators are specific for individu-
al channels of this family [45, 48, 55]. Expression of the
GLR genes is observed in the entire plant with certain
level of organ- and tissue-specificity (Table 1). Num-
ber of GLR are predominantly localized in conducting
tissues that mediate propagation of ES [48, 55, 116].
The stimuli inducing activation of GLR are rather diverse
and include drought, cold, biotic stresses, and mechan-
ical damages [48, 51, 55, 116]. It is well known that this
set of stimuli also induces both changes of membrane
potential and intracellular Ca
2+
concentration [3], which,
MUDRILOV et al.1472
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Ca
2+
-, K
+
-, and anion channels of higher plants and their characteristics
Channel Selectivity
Cell
localization
Tissue
localization
Stimulus Regulation References
GLR1.1
leaf, root, flower
,
pods
↓Ψ
w
[48]
GLR1.2 Ca
2+
PM leaf, root, pollen cold Ser, Glu [45,48-51]
GLR1.3 PM leaf, stem, root cold [48, 49]
GLR1.4 Na
+
, K
+
, NH
4
+
, Cl
–
PM leaf, root, stem
Trp, Met,
Phe, Leu, Tyr,
Asn, Thr, Glu
,
Gly
, Arg
[45,48,52]
GLR2.1
leaf, stem, root,
flower
, pods
Glu [48]
GLR3.1 Ca
2+
PM
leaf, root, GC,
stem
↓Ψ
w
, MD Met
[20,48,51,
53]
GLR3.2 leaf, stem, root, CT NaCl, MD Ser, Met, Gly [20, 48, 53]
GLR3.3 Ca
2+
>Na
+
=K
+
leaf, root, CT BS, MD, Grv
Glu, Ala, Asn,
Gln, Cys, Gly,
Ser, GSH
[23, 48, 51]
GLR3.4 Ca
2+
>Na
+
PM, T, EM
leaf, stem, root,
GC, CT
cold, NaCl,
touch
Asn, Ser, Gly,
Ala, Glu, Gln
,
Cys
, Asp
[48, 54, 55]
GLR3.5 PM, EM ↓Ψ
w
, MD Met [48, 51, 56]
GLR3.6 Ca
2+
>Na
+
=K
+
PM leaf, stem, root, CT BS, MD Glu
[23, 48,51,
57]
GLR3.7 Ca
2+
PM leaf, stem, root NaCl [48]
CNGC1
Ca
2+
, K
+
, Pb
+
, Na
+
,
Zn
2+
, Mn
2+
, Cd
2+
root, leaf HM [58]
CNGC2 Ca
2+
, Na
+
, K
+
PM
leaf, CT, flower,
root
BS, heating cAMP, ATP [58,59]
CNGC3 K
+
, Na
+
PM, T
root, CT, LEAF,
stem
NaCl Na
+
[58,60]
CNGC4 Ca
2+
, Na
+
, K
+
BS [58]
CNGC5 Mg
2+
, Ca
2+
, Na
+
PM leaf, root, GC Hyp, cGMP [61]
CNGC6 Mg
2+
, Ca
2+
, Na
+
PM
flower > leaves >
> pods > root >
> stem, GC
BS, heating
Hyp, cAMP,
cGMP
[58,61,62]
CNGC7
CNGC8
PM pollen [63]
CNGC10 K
+
, Na
+
PM, EM
root > leaf,
mesophyll, epidermis
Grv, NaCl [58,64]
CNGC11
CNGC12
Ca
2+
, K
+
PM BS cAMP, cGMP [65]
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1473
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Table (cont.)
Channel Selectivity
Cell
localization
Tissue
localization
Stimulus Regulation References
CNGC14 Ca
2+
PM root Grv auxins, ATP [66,67]
CNGC15 Ca
2+
PM,
nucleus
NO
3
–
[67,68]
CNGC16 Ca
2+
pollen heating cGMP [69]
CNGC17 PM cGMP [70]
CNGC18 Ca
2+
PM pollen cAMP, cGMP [58]
CNGC19 Ca
2+
T, PM, EM leaf, root, CT BS, MD
Hyp, cAMP,
DAMP
[55, 58, 71]
CNGC20 T, EM
root, GC, flower,
mesophyll
NaCl [58]
ANN1 Ca
2+
:=K
+
>Na
+
PM, T,
EM, Cyt
root, epidermis
NaCl, MD,
cold, heat,
↓Ψ
w
OH
•
, H
2
O
2
,
MT
[72-77]
ANN2 Ca
2+
PM, Cyt
leaf, root, flower,
hypocotyl, pods
↓Ψ
w
, heating CRY2 [72,74]
ANN3 Ca
2+
PM, Cyt
root, hypocotyl,
cotyledons
↓Ψ
w
, heating CRY2 [74]
ANN4 Ca
2+
, K
+
PM, EM
leaf, root,
flower, stem
↓Ψ
w
, NaCl,
cold
[73,76]
ANN5 Ca
2+
?
PM,
nucleus, Cyt
flower, pods,
pollen, root
[Ca
2+
]
cyt
[78,79]
ANN8
PM,
nucleus
↓Ψ
w
, NaCl [80]
TPC1 Ca
2+
≈K
+
≈Na
+
T
leaf, CT, root,
flower, epidermis,
mesophyll
BS, NaCl
Dep, [Ca
2+
]
cyt
,
[Ca
2+
]
vac
, ↓pH
[32, 45, 55,
81]
MCA1 Ca
2+
PM, T, EM
leaf, CT, stem,
root, flower, pods,
epidermis
cold, ↓Ψ
w
,
Grv
MT [82,83]
MCA2 Ca
2+
PM, T, EM
leaf, CT, stem,
root, flower, pods
cold, Grv [82,83]
OSCA1.1
K
+
>Ba
2+
≈Ca
2+
>
>Na
+
=Mg
2+
=Cs
+
PM
leaf, root, flower,
GC
↓Ψ
w
MT [84]
OSCA1.3 Ca
2+
PM GC BS DAMP [85]
OSCA1.7 Ca
2+
? BS DAMP [85]
Piezo1 Ca
2+
?T
leaf, hypocotyl,
root, CT
BS, touch MT [86,87]
DEK1 Ca
2+
PM epidermis MT [88]
MSL1 Cl
–
≈K
+
EM, PM
heating, HM,
↓Ψ
w
, NaCl
MT [55,89]
MUDRILOV et al.1474
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Table (cont.)
Channel Selectivity
Cell
localization
Tissue
localization
Stimulus Regulation References
MSL2
MSL3
EM, PM
↓Ψ
w
[90]
MSL4
MSL5
MSL6
PM root MT [90]
MSL8 Cl
–
>Na
+
PM, ER, T pollen MT [45,91]
MSL9 Cl
–
>Ca
2+
PM, EM ↓Ψ
w
MT [90,92]
MSL10 Cl
–
>Ca
2+
≈Na
+
PM, EM CT ↓Ψ
w
MT [90, 92-96]
SLAC1 Cl
–
, NO
3
–
GC, hypocotyl
BS, ↓Ψ
w
,
dark
ABA, Ca
2+
[32, 97, 98]
SLAH1 Cl
–
, NO
3
–
root [32, 97, 98]
SLAH2 NO
3
–
root
[32, 34,
97,98]
SLAH3 NO
3
–
root, leaf, GC
Dep, pH,
ABA, NO
3
–
[32, 34,
97-99]
ALMT6
malate,
fumarate>citrate,
Cl
–
, NO
3
–
T
leaf, GC, flower,
root
Ca
2+
, pH,
malate
[100,101]
ALMT12/
QUAC1
malate and sulfate GC Dep, malate [32,98]
TMEM16A EM Ca
2+
[32,102]
DTX33
DTX35
T
root, leaf, GC,
flower, stem
pH [103]
VCCN1 Cl
–
>NO
3
–
EM leaf, flower light Dep, Ca
2+
[104]
GORK1 K
+
, NH
4
+
root, GC, leaf
BS, NaCl,
ROS
Dep, H
2
O
2
,
↓pH
, Hyp
[47, 105,
106]
SKOR K
+
>Na
+
root, CT, stem, leaf
Dep, H
2
O
2
,
[K
+
]
in
, ↓pH
[47,107]
KAT1 K
+
PM, EM GC light Hyp, ABA
[47, 108-
110]
KAT2 K
+
PM GC Hyp, ↓pH
[47,
108,109]
KC1 K
+
PM root, 3K, leaf ↓pH [47,109]
AKT1 K
+
>Na
+
PM root Hyp, ↓pH
[47,
108,109]
AKT2 K
+
PM CT
Hyp, Ca
2+
,
cAMP, ↓pH
[47,105,
109,111]
TPK1 K
+
>NH
4
+
>>Na
+
T
GC, root,
mesophyll, CT,
pollen
NaCl
[Ca
2+
]
cyt
,
ABA, CO
2
,
↓pH
, ↑pH
[47,112]
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1475
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Table (cont.)
Channel Selectivity
Cell
localization
Tissue
localization
Stimulus Regulation References
TPK4 K
+
>NH
4
+
>>Na
+
PM root, pollen
MT, ↓pH
cyt
,
↓ΨW
,
[Ca
2+
]
out
[47,113]
KCO3 K
+
T
leaf, stem, root,
flower, CT
↓Ψ
w
[47,114]
SPIK K
+
PM pollen Hyp, ↓pH [47,115]
Notes. Absence of the indicated selectivity, localization, etc., is marked with crossing out lines. Abbreviations: ABA, abscisic acid; PM,plas-
ma membrane; T, tonoplast; EM, endomembrane; Cyt, cytosol; GC, guard cells, CT, conducting tissues; ↓Ψ
w
, osmotic stress; BS, biotic
stress; HM,heavy metals; MD,mechanical damage; Grv,gravitation; MT,membrane tension; Dep,depolarization; Hyp,hyperpolarization;
DAMP,damage-associated molecular pattern.
in combination with localization, makes the channels
from this group potential participants in generation of
ES in higher plants.
CNGC are low-selective cation channels, which
are structurally close to the discussed below shaker-like
K
+
-channels. For some CNGC activation with cyclic
nucleotides such as cAMP and cGMP and with hyper-
polarization has been established, which allows consider-
ing them as belonging simultaneously to the HACC and
VICC groups [45, 55, 58]. CNGC are mainly located on
plasmalemma, and also are present on the nuclear mem-
brane and tonoplast. Many CNGC are tissue-specific
and are mainly present in conducting tissues, epider-
mis, and guard cells [55, 58, 116]. Response to different
stimuli and/or protective response to stressors including
those inducing changes in electrical activity [3] due to
salinization, drought, temperature change, pathogens,
heavy metals, and others (table) was demonstrated for
the channels from this group [55, 58, 67, 116]. Local-
ization of CNGC on the plasma membrane of the cells
in conducting tissues allows suggesting participation of
some of the members of this family of channels in gener-
ation of ES in higher plants.
Annexins represent a group of cytoplasmic pro-
teins capable of binding to phospholipids of plasmalem-
ma, tonoplast, and ER membrane, they play a role of
low-selective cation channels, probably belonging to the
VICC group [45,55]. The stimuli inducing activation of
the channels from this family include drought, saliniza-
tion, temperature change. ROS could play a role of an-
nexin regulators (table), which, as have been mentioned
above, could be inducers of VP [45, 55, 72-74].
TPCs are represented in Arabidopsis by a single
gene TPC1, which is expressed in all plant tissues on the
vacuolar membrane. TPC1 is a cation channel with low
selectivity and slow activation kinetics with slight advan-
tage for Ca
2+
[55,116]. It is known that TPC1 is activat-
ed by depolarization and cytosolic Ca
2+
[45, 55]. TPC1
participates in the protective response to various stress-
ors such as salinization, flooding, attacks of pests, etc.,
is associated with stomatal closure, hormonal regula-
tion, and production of ROS through NADPH-oxidase
[45, 55, 116], i.e., physiological processes regulation of
which is realized through transmission of ESs [1, 2, 4,
5, 7]. Taking into account selectivity, localization on to-
noplast, and mechanism of activation, TPC1 could be
considered as a promising participant in ES generation.
Consideration of mechanosensitive Ca
2+
-channels
should begin with the MCA family [45,55], which are lo-
calized on plasmalemma and expressed at especially high
level in conducting tissues [55, 82, 90]. MCA are acti-
vated by the changes in membrane tension caused by os-
motic stress, mechanical actions, cold, and other stimuli
[82, 90,116-118]. Permeability for Ca
2+
and localization
in conducting bundles allows considering this family of
channels as the most probable participants in generation
of ES among the mechanosensitive Ca
2+
-channels.
OSCA1 are plasmalemma cation channels with low
selectivity localized predominantly in the stomata guard
cells [45,55]. Their activation occurs during changes in
membrane tension, they play a role of osmosensors and
regulate stomatal closure, although some members of
this family are, likely, activated by the damage-associ-
ated molecular patterns (DAMP), and indirectly partic-
ipate in the protective response to attack of pathogens
[55,85]. Rather specific localization and functional role
of the OSCA1 channels make them unlikely participants
in electrical signaling.
Other mechanosensitive channels discovered in
plants include the plant piezo channel Piezo1 and not
related, but with electrophysiological characteristics
similar to the mouse piezo channel, the RMA channel
encoded by the DEK1 (DEFECTIVE KERNEL1) gene
from the family of phytocalpains. Both channels are fast
activated and inactivated cation channels with low con-
ductance [45, 55]. RMA is located predominantly on
plasmalemma of epidermal cells and, most likely, is re-
sponsible for correct formation of epidermis and tissues
underneath [95]. Piezo1 is localized primarily in the root
cap, in conducting tissues, pollen, and in the pollen tube,
MUDRILOV et al.1476
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
where it mostly detected on tonoplast. Its main func-
tions are associated with mechanosensitivity of the
roots in the solid substrate and antiviral immunity [86,
87, 119]. Limited amount of information on the chan-
nels Piezo1 and RMA available at present does not allow
univocal conclusion on their possible role in generation
of ES in plants.
In conclusion, it can be stated that the representa-
tives from a number of Ca
2+
-channels families potential-
ly could participate in generation of ES in plants. Based
on such criteria as localization, mechanism of activa-
tion, and functional role, the most probable candidates
are the members of the GLR, CNGC, TPC1, MCA,
and ANN families of channels.
Anion channels. Many anion channels in plants
transmit not only chloride ions, but also other anions in-
cluding nitrates, sulfates, and some organic anions. One
important feature is the fact that under normal condi-
tions intracellular concentration of anions are higher
than extracellular, hence, concentration gradient is di-
rected outward. Based on electrophysiological charac-
teristics anion channels are commonly divided into two
types: rapid, R-type, and slow, S-type. The former ones,
R-type, are voltage-dependent, exhibit fast activation/
deactivation (within milliseconds), and predominant-
ly transport chlorides, nitrates, and sulfates, while the
S-type channels are voltage-independent with activa-
tion/deactivation times around 10s, exhibit high perme-
ability for nitrates and lower permeability for all other
anions [32, 34, 97, 98]. It is worth mentioning that such
classification was suggested during investigation of an-
ion channels in guard cells; later another types of anion
channels have been discovered such as separately recog-
nized aluminum-sensitive channels, mechanosensitive
anion channels, and endomembrane anion channels
[32,34].
Mechanosensitive-like channels (MSL) exhibit,
predominantly, anion permeability in higher plants, de-
spite the traditional for many reviews attribution of MSL
to Ca
2+
-channels [45,55]. Representatives of this fami-
ly are localized mainly on plasmalemma and ER mem-
brane (table). Many plasmalemma MSL channels have
high tissue- and organ-specificity, and are expressed
predominantly in roots, with exception of MSL8, which
is expressed in pollen, and MSL10, which is strongly ex-
pressed in conducting tissues along with roots [45, 90,
94, 96]. MSLs are activated by changes in membrane
tensions including during osmotic stress, and are charac-
terized with relatively high conductance in comparison
with other mechanosensitive channels [45, 55, 90, 94].
Majority of the members of MSL family, likely, cannot
be assigned to the participants in ES generation due to
their specific role and localization in roots. However,
one of the members of the family, MSL10, required
more detailed consideration as a potential participant in
the mechanism of ES generation, because it meets the
criteria: in addition to mechanosensitivity, selectivity to
Cl
–
, and localization on the plasma membrane of con-
ducting cells, it is also capable of activating production
of ROS with participation of NADPH-oxidase, opera-
tion of which, as mentioned above, could provide con-
tribution to propagation of VP [55, 90, 94, 96, 116, 117].
Members of the family of slow anion channels
(SLAC/SLAH, slow anion channel associated) belong
to the S-type of channels localized on plasmalemma.
There are differences between the members of the fami-
ly: SLAH2 and SLAH3 predominantly transport nitrates
and do not transport significant amounts of chlorides,
while rest of the channels of the family transport both
chlorides and nitrates [32, 34, 98]. There are also some
differences in localization: SLAH1 and SLAH2 are
predominantly expressed in roots, while expression of
SLAC1 and SLAH3 is wider including in guard cells.
Activation of SLAC1 could be triggered by various stim-
uli, and some of them cause changes in electrical activity
such as attack of pathogens, increase of CO
2
concen-
tration, drought, darkness, etc., likely via the Ca
2+
-de-
pendent pathway. SLAH3, in addition to Ca
2+
-depen-
dent regulation, could be activated by depolarization
and acidification of cytosol [32, 34, 97-99]. Among the
members of this family, SLAC1 and SLAH3 could be as-
signed to the group of potential participants in ES gen-
eration, because they meet all the criteria in selectivity
and regulation.
Representative of the family of aluminum-activated
malate transporters (ALMT) encoded by the ALMT12
gene was identified as an R-type channel. Another
name of ALMT12– quickly activating anion channel1
(QUAC1) has been given to this channel due to the ab-
sence of activation of this channel by aluminum typical
for other members of this family [32,34]. The QUAC1
channel is localized on plasmalemma of guard cells and
participates in stomatal closure, it is activated by depo-
larization, exhibits activation/deactivation times char-
acteristic for R-type of channels, and transports malate
and sulfate. Another member of the family, ALMT6,
which is localized on tonoplast, exhibits predominant-
ly malate and fumarate permeability, but also transports
chloride, it is activated by Ca
2+
and acidic pH in vacuole
[100, 101]. Other well investigated at present representa-
tives of ALMTs are localized mainly in roots, and, most
likely, are activated through the aluminum-dependent
pathway [32, 34, 98]. Based on the electrophysiological
characteristics, among the members of ALMT family only
QUAC1 could be considered as a potential participant in
ES generation, however, available at the moment infor-
mation on its localization contradicts this assumption.
Among the other anion channels, representatives
of the family of detoxification efflux carriers (DTX),
DTX33 and DTX35, localized on tonoplast in many
plant tissues should be mentioned. These channels are
responsible for the voltage-dependent influx of chloride
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1477
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
and other anions to vacuole controlled by pH changes
[103]. The protein localized on the ER membrane and
encoded by the TMEM16 gene could, potentially, func-
tion as a Ca
2+
-activated anion channel [32,102]. There
is also information on the voltage-dependent Cl
–
chan-
nel1 (VCCN1) in thylakoids, which is activated by de-
polarization and light, but not by Ca
2+
, and participates
in regulation of photosynthesis [104].
Hence, from the point of view of potential partic-
ipation in generation of ES, most attention should be
paid to the following anion channels: MSL10, QUAC1,
SLAC1, and SLAH3.
Potassium channels. The most detailed analysis of
electrophysiological characteristics of the channels and
the genes coding for these channels has been performed
for the K
+
-channels. The main principle of classifica-
tion of K
+
-channels is based on the mechanism of ac-
tivation and type of observed permeability [35, 46, 47].
Based on the mechanisms of activation the channels are
divided into voltage-dependent and voltage-independent
channels. The voltage-dependent K
+
-channels are local-
ized on plasmalemma, while the voltage-independent,
with some exception, are endomembrane K
+
-chan-
nels [46, 47]. The voltage-dependent K
+
-channels are
sub-divided into the channels mediating potassium ef-
flux (K
+
out
) and influx (K
+
in
), and sometimes the channels
with weak permeability (K
+
weak
) are identified among the
latter [35,46,120].
Currently two families of the K
+
-channel genes
have been recognized: Shaker-type K
+
-channels and
two-pore K
+
channels (TPK). All members of the Shak-
er-type K
+
-channel family belong to the voltage-depen-
dent channel, and, in turn, are subdivided into efflux
channels (GORK, SKOR) and influx channels (AKT,
KAT) [46]. Sometimes among the genes of K
+
in
-channel
the KC1 gene (KAT3), which codes for the regulatory
subunit not capable of forming the channel on its own,
but capable of affecting the K
+
in
-channel characteristics
by binding to them, is considered separately [46,109].
All other genes of the Shaker-type K
+
in
-channels [KAT1,
KAT2, AKT1, AKT2, AKT5, and SPIK (AKT6)] code
for the subunits that form channels; these channels are
formed by either homomers or heteromers, and have
slightly different electrophysiological characteristics [47,
108]. All channels in this subgroup are activated by
hyperpolarization and generate inward K
+
flows with
exception of AKT2, which is also capable to perform
function of efflux channel [109,111], and which is often
assigned to the separate subgroup K
+
weak
[46,47,120].
Two types of K
+
out
-channels of the Shaker type have
been identified in plants: GORK (guard cell K
+
outward
rectifying channel) and SKOR (Shaker-type K
+
outward
rectifying channel), both are activated by depolarization.
Moreover, their activation could occur also with par-
ticipation of Ca
2+
-dependent protein kinases, as well as
of ROS, which indicates possible involvement of these
channels in generation of ES. However, it should be
mentioned that SKOR is practically not expressed out-
side of roots (table), hence, the possibility of its partici-
pation in generation of ES in shoots is rather low, unlike
for the widely expressed GORK [46, 47, 120].
TPK (KCO K
+
channel, outward rectifying) include
voltage independent channels localized on tonoplast with
exception of TPK4 localized predominantly on the pol-
len plasmalemma [46,47]. Activation by Ca
2+
and acidi-
fication of cytosol (pH6.7 with normal pH level 7.5-7.8)
was demonstrated for TPK1, this channel is responsible
for release of vacuolar K
+
during, for example, stomatal
closure. There is also data that these channels could be
mechanosensitive responding to the changes of tonoplast
curvature as osmosensors. As to plasmalemma-localized
TPK4, it is pH-insensitive and can be blocked by the ex-
tracellular Ca
2+
[47, 90, 112, 117].
Hence, among the currently known K
+
-channels,
only GORK and TPK1 could be considered as potential
participants in ES formation in higher plants.
PARTICIPATION OF ION CHANNELS
IN ELECTRICAL SIGNALING
Before starting discussion of the currently avail-
able proofs of participation of the genetically identified
ion channels in generation of ES, some methodological
limitations of such studies should be briefly considered.
The main approach in such studies is the use of mutant
plants deficient in the gene of interest or with its overex-
pression. Parameters of ES in these plants (amplitude,
duration, peculiarities of propagation, and others) are
next compared with the ES parameters determined for
the wild type plants (Fig. 2). Presence of differences is
considered as an indication of participation of this ion
channel in the processes of generation and propagation
of ES [20, 53, 93, 121]. In addition to the direct compar-
ison of the ES parameters, simultaneous monitoring of
the changes in concentrations of ions mediated by these
channels could be also used, which could be followed
by comparison of the type of these changes between the
plant variants and with the ES parameters [23, 53, 122].
Moreover, artificial activation or deactivation of the
particular channels by their specific ligands that cause
typical changes of membrane potential could also be
considered as a proof of participation in electrical sig-
naling, however, such approach is applicable only to
the ligand-activated channels [23,123]. The abovemen-
tioned methods also have drawbacks. One of such draw-
backs is possible interaction of the subunits encoded by
different genes leading to formation of fully functional
heteromeric channel, while the possibility of formation
of homomeric channels also exists. Characteristics and
functional roles of homo- and heteromeric channels
could be different [47, 109, 124]. Investigation of the
MUDRILOV et al.1478
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
Fig. 2. Schematic representation of the effects of knockout mutations of the genes of ion channels on parameters of electrical signals and Ca
2+
wave
in higher plants. Membrane potential is shown as a black line, and Ca
2+
wave– as a red line. Color of symbols indicated type of knockout mutation
(see explanations in the text).
double- and more mutants also could not provide as un-
ambiguous answer whether the change of ES parameters
is associated with the fact that certain heteromeric chan-
nels are not formed, or some of the homomeric chan-
nels participating in generation of ES are suppressed
[20, 53, 122].
Existence of a compensatory mechanism in the case
of participation of several channels in generation of ES,
when dysfunction of the suppressed gene is compensat-
ed by overexpression of another gene that perform the
same or similar role, also could complicate interpre-
tation of the results [77]. And finally, it was shown for
some channels that they are capable to perform some of
their functions, such as regulation of cell death, through
their non-channel subunits [125]. Hence, the use of mu-
tants does not provide an unambiguous answer, but at
present there is no other approach for analysis of elec-
trophysiological and molecular genetics data at the level
of whole organism.
The most investigated participants of ES generation
in plants are Ca
2+
-channels, primarily from the GLR
family (Fig.2) [51]. Complete suppression of VP propa-
gation outside of the region of the leaf subjected to me-
chanical damage [20, 21, 53, 56, 122], attack of chew-
ing insects [20], excessive light [122], and laser-initiate
damage [53] was observed in the glr3.3glr3.6 double mu-
tant of Arabidopsis. In the process, amplitude of elec-
trical response decreases in the damaged leaf, but is not
completely suppressed [20, 21, 56]. Mechanical damage
of roots also causes decrease of amplitude and duration
of ES in the leaves of the glr3.3glr3.6 plants in compar-
ison with the wild type plant [23]. In the case of sin-
gle mutants, glr3.3 or glr3.6, decrease of amplitude and
duration of the propagated VP is observed [20, 53, 122].
It is worth mentioning that while in the case when in
the VP induced by the leaf cutting there is a fast AP-
like component in addition to the slow wave of depo-
larization, in the glr3.6 mutant only the latter is sup-
pressed[56]. With regards to the GLR3.3 channel, this
channel in comparison with the GLR3.6, likely, provides
larger contribution to the response to thermal stress, be-
cause in the glr3.1glr3.3 double mutant the response to
laser-induced burn is also completely suppressed, but
not the response to mechanical damage [53]. It is im-
portant to note that during comparison of the glr mu-
tant with the wild type coordinated changes were ob-
served during simultaneous recording of the dynamics of
Ca
2+
concentration and dynamics of electric potential:
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1479
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
in the mutant forms with GLR deficit both Ca
2+
-wave
and VP were suppressed [23, 53, 122]. This indicates direct
association between the changes of Ca
2+
concentration
mediated by the GLR channels and generation of VP.
In a number of studies artificial activation of GLR
channels by addition of glutamate have been performed,
which resulted in both increase of Ca
2+
concentration
in cytosol [57] and generation of ES [23]. Moreover,
addition of glutamate to the mutant plants glr3.3 and
glr3.6 practically did not induce either increase of Ca
2+
or generation of ES [23,57]. These data together with
consideration of the temporal-spatial dynamics of Ca
2+
concentration allow suggesting potential participation of
GLR3.3 and GLR3.6 in the long-distance reaction to
touch [126] and attack of aphids [121], and participation
of GLR3.3 in the reaction to salt stress [127].
The data obtained for the tomato plants (Solanum
lycopersicum L.) also indicate that GLRs play a role in
generation of ES: complete suppression of VP trans-
mission into the neighboring leaves was observed in
the SlGLR3.3 and SlGLR3.5 (homologs of GLR3.3 and
GLR3.6 in Arabidopsis) double mutants, while in the
stressed leaf itself there was only reduction of ampli-
tude[128].
Predominant expression of GLR3.3 and GLR3.6 in
conducting bundles provides additional support to the
suggestion that these channels participate in the system-
ic propagation of ESs. In particular, pronounced expres-
sion has been detected in the primary, secondary, as well
as tertiary bundles in the Arabidopsis leaves. It must be
mentioned that GLR3.3 is expressed mainly in the pri-
mary conducting bundles of phloem, while GLR3.6–
in xylem [53,57].
It was shown for other potential candidates from
this family, that decrease of amplitude and duration of
ES induced in response to mechanical or laser damage
occurs in the GLR3.1 and GLR3.2 mutants [20, 53],
however, even in double mutants, with exception of the
previously mentioned glr3.1glr3.3, neither systemic reac-
tion nor local reaction were suppressed completely [53].
It has been suggested that GLR3.1 participates in propa-
gation of ES outside the limits of conducting bundles due
to disruption of the ES-associated radial propagation of
the Ca
2+
signal [53]. The channels encoded by GLR3.5
could be responsible for formation of the AP-like shape
of ES in response to mechanical damage, however, the
issue could be more complicated. In particular, in the
mutant plants no AP-like shape of ES was observed in
the non-stressed leaves, which have direct connection
with the stressed leaf, unlike in the wild type plants, but
it was present in the non-stressed leaves with indirect
connections with the stressed leaf, in which the AP-like
shape was absent in the wild type plant [56]. This pro-
vides another indication of complexity and versatility
of the processes of generation and propagation of ESs
in plants, which remain to be elucidated.
The DmGLR3.6 channel of the Venus flytrap, ho-
molog of the Arabidopsis GLR3.1/3.3, potentially could
participate in propagation of AP induced by touch from
the trigger hair to the leaf of the trap, as evidenced by the
specific pattern of expression of this gene and possibility
of AP induction by glutamate in the leaf-trap [129,130].
In monocots, such as rice (Oryza sativa L.), the gene
OsGLR3.4, which encodes Ca
2+
-channel with functions
similar to the functions of GLR3.3 and GLR3.6 of Ara-
bidopsis could be highlighted among the GLRs: system-
ic propagation of VP induced by mechanical damage
is partially suppressed in the rice mutants deficient in
this channel, while the local electrical response is not
suppressed [123]. It is also worth mentioning that the
channel OsGLR3.4 could be activated by several ami-
no acids [123], unlike the glutamate-specific GLR3.3
and GLR3.6 in Arabidopsis [23], which could be due to
the fact that from phylogenetic point of view OsGLR3.4
is located at a relatively long distance from GLR3.3
and GLR3.6 [131].
Another type of channels for which their participa-
tion in formation of ES was determined using molecu-
lar genetics approach, are anion channels belonging to
the family of mechanosensitive channels MSL (Fig.2).
In the msl10 mutant plants reduction of the duration of
the systemically transmitted VP induced by mechani-
cal damage has been observed, which occurred due to
disappearance of the phase of “slow depolarization” in
VP, as indicated by the authors. VP in the msl10 mu-
tant plants demonstrated similarity of its characteristics
with the VP in the glr3.3 and glr3.6 single-mutant plants.
At the same time, no changes in the VP parameters have
been revealed for the other mutants of MSL family, msl4,
msl5, msl6, and msl9 [93]. As has been mentioned above,
expression of MSL10 is observed in the conducting bun-
dles including both phloem and xylem. The MSL10
channel demonstrates anion conductance, but not cal-
cium conductance [93,132]. Nevertheless, functioning
of MSL10, most likely, activates influx of Ca
2+
into the
cell during mechanical damage through GLR3.3 and
GLR3.6. It was demonstrated also that the initial depo-
larization phase occurs before the start of the changes
in Ca
2+
concentration [93], which raises the question re-
garding the accepted mechanism of VP generation.
And, finally, a channel has been identified ensur-
ing K
+
flow in the course of AP depolarization phase–
GORK1. Amplitude and rate of depolarization induced
by the AP electric current in the gork1 mutants was high-
er in comparison with the wild type, while repolarization
was significantly slower (Fig.2). The following mathe-
matical modeling confirmed participation of this chan-
nel in generation of AP. It was also shown that GORK1
is activated already at the phase of depolarization de-
creasing its rate and amplitude under normal conditions
[105]. It was also demonstrated in this study that anoth-
er K
+
-channel, AKT2, could affect generation of AP,
MUDRILOV et al.1480
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
but not directly through regulation of the plasmalemma
excitability [105].
Participation of two K
+
-channels, DmSKOR be-
longing to the same group as the previously considered
GORK1and KDM1, homolog of the KAT1 of Arabi-
dopsis, was demonstrated in the recent studies on Venus
flytrap [37, 129]. Suppression of the DmSKOR expres-
sion by coronatine, which suppresses expression of the
genes associated with excitability in Venus flytrap, re-
sulted in the increase of the time of repolarization during
generation of the mechanically induced AP in the trap
leaf, which could indicate participation of DmSKOR
in formation of depolarization phase in AP [129, 130].
KDM1 is a channel activated by hyperpolarization and
acidic pH of apoplast, which is localized exclusively in
the mechanosensitive hairs and responsible for the K
+
influx into the cell. Mathematical modeling and com-
parison with the experimental data showed that the role
of this channel involves restoration of K
+
concentration
during generation of a series of APs resulting in the trap
closing in Venus flytrap and initiation of the release of
digestive enzymes [37].
Potential contribution of certain channels to gener-
ation of ES could be suggested not only based on the
effects of mutation on parameters of ES pre se, but also
based on their effects on parameters of Ca
2+
-signals,
because there is close similarity between the dynamics
of Ca
2+
concentration and dynamics of the changes of
electric potential during excitation [53, 129]. In partic-
ular, decrease of amplitude and of the rate of Ca
2+
wave
in response to salinization [81, 133] and mechanical
damage [134] was observed in the vacuolar channel
TPC1 mutants. In the case of attack of aphids, overex-
pression of TPC1 results in systemic increase of Ca
2+
,
which is not observed in the wild type [121]. Neverthe-
less, the authors suggested only auxiliary role of TPC1
in initiating response to salinization and mechanical
damage involving enhancement of the Ca
2+
concen-
tration shift initiated by other channels [133, 134].
The demonstrated role of TPC1 in formation of Ca
2+
-
wave induced by different stimuli together with the pre-
sumed role of tonoplast in ES generation [44], and taking
into consideration the data of inhibitory analysis [15,42]
allows suggesting direct involvement of TPC1 in genera-
tion of ES. Contribution to formation of Ca
2+
-signal was
also demonstrated for the channel from a different fam-
ily, CNGC19, localized on the plasmalemma of phlo-
em cells: participation of the channel in the increase of
Ca
2+
concentration in response to the attack of chewing
insect was revealed, moreover, activation of CNGC19
could be mediated by either Pep1 (Protein elicitor pep-
tide1, one of the DAMP released during the cell dam-
age) or directly by cAMP, content of which also increas-
es during the damage [71].
Fig. 3. Ion channels participating in generation and propagation of electrical signals(ES) in a cell of higher plants. Location of ion channels
corresponds to particular phase of the process of ES generation to which their contribute, which exception of Ca
2+
-channels, which could be ac-
tivated at different stages of the process of ES formation. Ion channels with experimentally proved participation in ES generation are underlined.
Ion channels, which, potentially, could participate in generation of ES are shown in regular font. The H
+
-ATPase, AHA1, that also provides contri-
bution to generation of ES is shown in the figure [2,7].
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1481
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
In addition to the results of investigating propagat-
ing Ca
2+
-signal, data on the changes of Ca
2+
concentra-
tion in the zone of stimulus action exemplified, in par-
ticular, by the well investigated stimuli such as heating
and cooling, could be also used. The studies with MCA1
and MCA2 [118], ANN1 and ANN4 [73], OsCNGC14 and
OsCNGC16 (homologs of CNGC2 and CNGC4 in Ara-
bidopsis) [135] mutants demonstrated decrease of the
amplitude of Ca
2+
increase in cytosol induced by cold
in comparison with the wild type plants. Moreover, the
amplitude also decreases under the action of inhibitors
suppressing AP, which together with the characteristic
shape of Ca
2+
-signal allows suggesting participation of
these channels in generation of electrical response in the
zone of cooling [73, 118, 135]. It should be mentioned
that the increase of Ca
2+
concentration
was not com-
pletely suppressed in any of the mutants including the
double ones [118]. Moreover, if the degrees of reduction
of calcium concentration observed for different mutants
are summarized, the resulting degree is much higher
than 100%, which, obviously, indicates either compen-
satory expression of other genes, or existence of different
participants in the processes of changing Ca
2+
levels in
different plant species [73, 118, 135]. Suppression of the
Ca
2+
wave in cytosol induced by another well investigat-
ed stimulus, heating, was shown in the CNGC2, CNGC6,
OsCNGC14, OsCNGC16, ANN1, and ANN2 mutant
plants; furthermore, the heating-induced increase of
Ca
2+
level in the wild type plants is similar to the VP in
shape and duration [62, 72, 135, 136]. The abovemen-
tioned information implies that the discussed channels
could provide contribution to generation of electrical re-
sponse in the zone of the corresponding stimulus action.
In general, it could be stated with confidence that
the following Ca
2+
-channels in higher plants are involved
in generation of propagating ES: GLR3.1, GLR3.2,
GLR3.3, GLR3.5, and GLR3.6, as well as anion channel
MSL10 and K
+
-channel GORK1 (Fig. 3). The Ca
2+
-
channels ANN1, ANN2, ANN4, CNGC2, CNGC4,
CNGC6, CNGC19 could be also considered as potential
participants in generation of ES, as well as the vacuolar
channel TPC1 and mechanosensitive channels MCA1
and MCA2. There are no experimental data supporting
participation of anion channels QUAC1, SLAC1, and
SLAH3 in this, but their properties indicate the possi-
bility of their potential involvement in generation of ES.
CONCLUSIONS
In conclusion of our analysis of molecular mecha-
nisms of electrical signaling in higher plants, it must be
mentioned that further detailed investigations are nec-
essary. Most significant results could be expected if the
efforts are concentrated on the following issues: (i)iden-
tification of molecular nature of the voltage-dependent
Ca
2+
-channels of plasmalemma responsible for initiation
of AP appearing in plants when the threshold level of de-
polarization is reached [8]; (ii)search for the genes en-
coding ion channels in different species of plants includ-
ing the ones with locomotion and carnivorous plant, for
which electrophysiological examinations are common.
At the same time, investigation of the whole complexity
of electrical signaling in plants is necessary, both from
the point of view of different types of ES, and from the
point of view of peculiarities of electrical signaling in
different plant species. Best results could be achieved by
combining electrophysiological and genetic approaches
in a single study supplementing them with analysis of ion
concentration in intact plants using, for example, geneti-
cally encoded fluorescent sensors.
Identification and characterization of ion channels
participating in generation of ES could provide signifi-
cant contribution not only to elucidation of mechanisms
of excitation in plants but also to the general picture of
the functional role of ES, because induction of function-
al response to the propagating ES is based on the chang-
es of ion concentration in the cells and tissues caused
by propagation of ES [5, 6]. In future it would facili-
tate resolving such important issues such as possibility
of information transmission with participation of ES in
plants [3] and interaction of electrical signaling system
with other types of signalling systems such hormonal,
calcium, and ROS [1, 2, 4, 7].
Contributions. V.A.V. concept and supervision of
the study; M.A.M., M.M.L., D.V.K., and V.A.V. search
for materials; M.A.M. and M.M.L. writing text of the
paper; M.M.L. and D.V.K. preparation of figures;
M.A.M., M.M.L., and V.A.V. editing text of the paper.
Funding. This work was financially supported by the
Russian Science Foundation, grant 22-14-00388.
Ethics declarations. The authors declare no conflicts
of interests in financial or any other spheres. This article
does not contain any studies with human participants or
animals performed by any of the authors.
REFERENCES
1. Huber, A. E., and Bauerle, T. L. (2016) Long-distance
plant signaling pathways in response to multiple stress-
ors: the gap in knowledge, J. Exp. Bot., 67, 2063-2079,
doi:10.1093/jxb/erw099.
2. Johns, S., Hagihara, T., Toyota, M., and Gilroy, S. (2021) The
fast and the furious: rapid long-range signaling in plants,
Plant Physiol., 185, 694-706, doi:10.1093/plphys/kiaa098.
3. Mudrilov, M., Ladeynova, M., Grinberg, M., Balalaeva, I.,
and Vodeneev, V. (2021) Electrical signaling of plants
under abiotic stressors: transmission of stimulus-specif-
ic information, Int.J. Mol. Sci., 22, 10715, doi:10.3390/
ijms221910715.
MUDRILOV et al.1482
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
4. Ladeynova, M., Kuznetsova, D., Mudrilov, M., and
Vodeneev, V. (2023) Integration of electrical signals and
phytohormones in the control of systemic response, Int.J.
Mol. Sci., 24, 847, doi:10.3390/ijms24010847.
5. Sukhov, V., Sukhova, E., and Vodeneev, V. (2019)
Long-distance electrical signals as a link between the local
action of stressors and the systemic physiological respons-
es in higher plants, Prog. Biophys. Mol. Biol., 146, 63-84,
doi:10.1016/j.pbiomolbio.2018.11.009.
6. Klejchova, M., Silva-Alvim, F. A. L., Blatt, M. R., and
Alvim, J.C. (2021) Membrane voltage as a dynamic plat-
form for spatiotemporal signaling, physiological, and de-
velopmental regulation, Plant Physiol., 185, 1523-1541,
doi:10.1093/plphys/kiab032.
7. Farmer, E. E., Gao, Y., Lenzoni, G., Wolfender, J., and
Wu, Q. (2020) Wound- and mechanostimulated electri-
cal signals control hormone responses, New Phytol., 227,
1037-1050, doi:10.1111/nph.16646.
8. Opritov, V. A., Pyatygin, S. S., and Retivin, V. G., Bioelec-
trogenesis in higher plants, Moscow: Nauka, 1991.
9. Bulychev, A. A., and Komarova, A. V. (2014) Long-dis-
tance signal transmission and regulation of photosynthe-
sis in characean cells, Biochemistry (Moscow), 79, 273-281,
doi:10.1134/S0006297914030134.
10. Kisnieriene, V., Trębacz, K., Pupkis, V., Koselski, M., and
Lapeikaite, I. (2022) Evolution of long-distance signalling
upon plant terrestrialization: comparison of action po-
tentials in Characean algae and liverworts, Ann. Bot., 130,
457-475, doi:10.1093/aob/mcac098.
11. Lunevsky, V. Z., Zherelova, O. M., Vostrikov, I. Y., and
Berestovsky, G. N. (1983) Excitation of Characeae cell
membranes as a result of activation of calcium and chlo-
ride channels, J. Membr. Biol., 72, 43-58, doi: 10.1007/
BF01870313.
12. Vodeneev, V. A., Katicheva, L. A., and Sukhov, V. S.
(2016) Electric signals in higher plants: mechanisms of
generation and propagation, Biophysics, 61, 505-512,
doi:10.1134/S0006350916030209.
13. Fromm, J., and Lautner, S. (2007) Electrical signals
and their physiological significance in plants: electri-
cal signals in plants, Plant Cell Environ., 30, 249-257,
doi:10.1111/j.1365-3040.2006.01614.x.
14. Hodick, D., and Sievers, A. (1988) The action potential of
Dionaea muscipula Ellis, Planta, 174, 8-18, doi:10.1007/
BF00394867.
15. Krol, E., Dziubinska, H., Stolarz, M., and Trebacz, K.
(2006) Effects of ion channel inhibitors on cold- and
electrically-induced action potentials in Dionaea mus-
cipula, Biol. Plant., 50, 411-416, doi: 10.1007/s10535-
006-0058-5.
16. Stahlberg, R., Cleland, R. E., and Van Volkenburgh,E.
(2006) Slow wave potentials – a propagating electri-
cal signal unique to higher plants, in Communication in
Plants (Baluška, F., Mancuso, S., and Volkmann, D., eds)
Springer Berlin Heidelberg, Berlin, Heidelberg, pp.291-
308, doi:10.1007/978-3-540-28516-8_20.
17. Li, Q., Wang, C., and Mou, Z. (2020) Perception of
damaged self in plants,
Plant Physiol., 182, 1545-1565,
doi:10.1104/pp.19.01242.
18. Vodeneev, V., Mudrilov, M., Akinchits, E., Balalaeva, I.,
and Sukhov, V. (2018) Parameters of electrical signals and
photosynthetic responses induced by them in pea seed-
lings depend on the nature of stimulus, Funct. Plant Biol.,
45, 160, doi:10.1071/FP16342.
19. Mudrilov, M., Ladeynova, M., Berezina, E., Grinberg, M.,
Brilkina, A., Sukhov, V., and Vodeneev, V. (2021) Mecha-
nisms of specific systemic response in wheat plants under
different locally acting heat stimuli, J.Plant Physiol., 258-
259, 153377, doi:10.1016/j.jplph.2021.153377.
20. Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellen-
berger,S., and Farmer, E.E. (2013) Glutamate receptor-like
genes mediate leaf-to-leaf wound signalling, Nature,
500, 422-426, doi:10.1038/nature12478.
21. Salvador-Recatalà, V., Tjallingii, W. F., and Farmer, E.E.
(2014) Real-time, invivo intracellular recordings of cater-
pillar-induced depolarization waves in sieve elements using
aphid electrodes, New Phytol., 203, 674-684, doi:10.1111/
nph.12807.
22. Julien, J. L., Desbiez, M. O., De Jaegher, G., and Fra-
chisse, J.M. (1991) Characteristics of the wave of depo-
larization induced by wounding in Bidens PilosaL., J.Exp.
Bot., 42, 131-137, doi:10.1093/jxb/42.1.131.
23. Shao, Q., Gao, Q., Lhamo, D., Zhang, H., and Luan,S.
(2020) Two glutamate- and pH-regulated Ca
2+
chan-
nels are required for systemic wound signaling in Arabi-
dopsis, Sci. Signal., 13, eaba1453, doi: 10.1126/scisignal.
aba1453.
24. Zimmermann, M. R., and Felle, H. H. (2009) Dissec-
tion of heat-induced systemic signals: superiority of ion
fluxes to voltage changes in substomatal cavities, Planta,
229, 539-547, doi:10.1007/s00425-008-0850-x.
25. Katicheva, L., Sukhov, V., Akinchits, E., and Vodeneev,V.
(2014) Ionic nature of burn-induced variation poten-
tial in wheat leaves, Plant Cell Physiol., 55, 1511-1519,
doi:10.1093/pcp/pcu082.
26. Vodeneev, V., Akinchits, E., and Sukhov, V. (2015) Varia-
tion potential in higher plants: Mechanisms of generation
and propagation, Plant Signal. Behav., 10, e1057365, doi:1
0.1080/15592324.2015.1057365.
27. Stahlberg, R., and Cosgrove, D. J. (1997) The propaga-
tion of slow wave potentials in pea epicotyls, Plant Physiol.,
113, 209-217, doi:10.1104/pp.113.1.209.
28. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres,
M.A., Shulaev, V., Dangl, J.L., and Mittler, R. (2009)
The plant NADPH oxidase RBOHD mediates rapid sys-
temic signaling in response to diverse stimuli, Sci. Signal.,
2, ra45, doi:10.1126/scisignal.2000448.
29. Devireddy, A. R., Zandalinas, S. I., Gómez-Cadenas, A.,
Blumwald, E., and Mittler, R. (2018) Coordinating the
overall stomatal response of plants: rapid leaf-to-leaf com-
munication during light stress, Sci. Signal., 11, eaam9514,
doi:10.1126/scisignal.aam9514.
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1483
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
30. Volkov, R. A., Panchuk, I. I., Mullineaux, P.M., and Schöf-
fl, F. (2006) Heat stress-induced H
2
O
2
is required for ef-
fective expression of heat shock genes in Arabidopsis, Plant
Mol. Biol., 61, 733-746, doi:10.1007/s11103-006-0045-4.
31. Kawarazaki, T., Kimura, S., Iizuka, A., Hanamata, S.,
Nibori, H., Michikawa, M., Imai, A., Abe, M., Kaya,H.,
and Kuchitsu, K. (2013) A low temperature-inducible
protein AtSRC2 enhances the ROS-producing activity of
NADPH oxidase AtRbohF, Biochim. Biophys. Acta, 1833,
2775-2780, doi:10.1016/j.bbamcr.2013.06.024.
32. Hedrich, R. (2012) Ion channels in plants, Physiol. Rev.,
92, 1777-1811, doi:10.1152/physrev.00038.2011.
33. Costa, A., Navazio, L., and Szabo, I. (2018) The contribu-
tion of organelles to plant intracellular calcium signalling,
J.Exp. Bot., 69, 4175-4193, doi:10.1093/jxb/ery185.
34. Kollist, H., Jossier, M., Laanemets, K., and Thom-
ine, S. (2011) Anion channels in plant cells: plant an-
ion channels, FEBS J., 278, 4277-4292, doi: 10.1111/
j.1742-4658.2011.08370.x.
35. Véry, A.-A., and Sentenac, H. (2002) Cation channels in
the Arabidopsis plasma membrane, Trends Plant Sci.Sci.,
7, 168-175, doi:10.1016/S1360-1385(02)02262-8.
36. Fromm, J., and Spanswick, R. (1993) Characteristics of
action potentials in willow (Salix viminalisL.), J.Exp. Bot.,
44, 1119-1125, doi:10.1093/jxb/44.7.1119.
37. Iosip, A. L., Böhm, J., Scherzer, S., Al-Rasheid, K.A.S.,
Dreyer, I., Schultz, J., Becker, D., Kreuzer, I., and
Hedrich, R. (2020) The Venus flytrap trigger hair-specif-
ic potassium channel KDM1 can reestablish the K
+
gra-
dient required for hapto-electric signaling, PLoS Biol.,
18, e3000964, doi:10.1371/journal.pbio.3000964.
38. Vodeneev, V. A., Akinchits, E. K., Orlova, L. A., and Suk-
hov, V.S. (2011) The role of Ca
2+
, H
+
, and Cl
−
ions in gener-
ation of variation potential in pumpkin plants, Russ.J. Plant
Physiol., 58, 974-981, doi:10.1134/S1021443711050256.
39. Shabala, S., Cuin, T. A., Shabala, L., and Newman, I.
(2012) Quantifying kinetics of net ion fluxes from plant
tissues by non-invasive microelectrode measuring MIFE
technique, in Plant Salt Tolerance (Shabala, S., and Cuin,
T. A., eds) Humana Press, Totowa, NJ, pp. 119-134,
doi:10.1007/978-1-61779-986-0_7.
40. Hilleary, R., Choi, W.-G., Kim, S.-H., Lim, S. D., and
Gilroy, S. (2018) Sense and sensibility: the use of fluo-
rescent protein-based genetically encoded biosensors in
plants, Curr. Opin. Plant Biol., 46, 32-38, doi: 10.1016/
j.pbi.2018.07.004.
41. Lewis, B. D., Karlin-Neumann, C., and Spalding, E.P.
(1997) Ca
2+
-activated anion channels and membrane de-
polarizations induced by blue light and cold in arabidop-
sis seedlings, Plant Physiol., 114, 1327-1334, doi:10.1104/
pp.114.4.1327.
42. Krol, E., Dziubinska, H., and Trebacz, K. (2004) Low-
temperature-induced transmembrane potential chang-
es in mesophyll cells of Arabidopsis thaliana, Helian-
thus annuus and Vicia faba, Physiol. Plant, 120, 265-270,
doi:10.1111/j.0031-9317.2004.0244.x.
43. Vodeneev, V. A., Opritov, V. A., and Pyatygin, S. S.
(2006) Reversible changes of extracellular pH during
action potential generation in a higher plant Cucurbita
pepo, Russ. J. Plant Physiol., 53, 481-487, doi: 10.1134/
S102144370604008X.
44. Dindas, J., Dreyer, I., Huang, S., Hedrich, R., and Roelf-
sema, M.R.G. (2021) A voltage-dependent Ca
2+
homeo-
stat operates in the plant vacuolar membrane, New Phytol.,
230, 1449-1460, doi:10.1111/nph.17272.
45. Demidchik, V., Shabala, S., Isayenkov, S., Cuin, T. A.,
and Pottosin, I. (2018) Calcium transport across plant
membranes: mechanisms and functions, New Phytol., 220,
49-69, doi:10.1111/nph.15266.
46. Dreyer, I., and Uozumi, N. (2011) Potassium channels in
plant cells: potassium channels in plants, FEBSJ., 278,
4293-4303, doi:10.1111/j.1742-4658.2011.08371.x.
47. Sharma, T., Dreyer, I., and Riedelsberger, J. (2013) The
role of K
+
channels in uptake and redistribution of potas-
sium in the model plant Arabidopsis thaliana, Front. Plant
Sci., 4, 224, doi:10.3389/fpls.2013.00224.
48. Naz, R., Khan, A., Alghamdi, B. S., Ashraf, G. M., Al-
ghanmi, M., Ahmad, A., Bashir, S.S., and Haq, Q.M.R.
(2022) An insight into animal glutamate receptors homolog
of Arabidopsis thaliana and their potential applications–
a review, Plants, 11, 2580, doi:10.3390/plants11192580.
49. Zheng, Y., Luo, L., Wei, J., Chen, Q., Yang, Y., Hu, X.,
and Kong, X. (2018) The glutamate receptors AtGLR1.2
and AtGLR1.3 increase cold tolerance by regulating jas-
monate signaling in Arabidopsis thaliana, Biochem. Bio-
phys. Res. Commun., 506, 895-900, doi: 10.1016/j.bbrc.
2018.10.153.
50. Michard, E., Lima, P. T., Borges, F., Silva, A. C., Portes,
M.T., Carvalho, J.E., Gilliham, M., Liu, L.-H., Ober-
meyer, G., and Feijó, J.A. (2011) Glutamate receptor-like
genes form Ca
2+
channels in pollen tubes and are regulated
by pistil D-serine, Science, 332, 434-437, doi:10.1126/sci-
ence.1201101.
51. Yu, B., Liu, N., Tang, S., Qin, T., and Huang, J. (2022)
Roles of glutamate receptor-like channels (GLRs) in plant
growth and response to environmental stimuli, Plants,
11, 3450, doi:10.3390/plants11243450.
52. Tapken, D., Anschütz, U., Liu, L.-H., Huelsken, T., See-
bohm, G., Becker, D., and Hollmann, M. (2013) A plant
homolog of animal glutamate receptors is an ion channel
gated by multiple hydrophobic amino acids, Sci. Signal., 6,
ra47, doi:10.1126/scisignal.2003762.
53. Nguyen, C. T., Kurenda, A., Stolz, S., Chételat, A., and
Farmer, E. E. (2018) Identification of cell populations
necessary for leaf-to-leaf electrical signaling in a wound-
ed plant, Proc. Natl. Acad. Sci. USA, 115, 10178-10183,
doi:10.1073/pnas.1807049115.
54. Meyerhoff, O., Müller, K., Roelfsema, M. R. G., Latz,A.,
Lacombe, B., Hedrich, R., Dietrich, P., and Becker, D.
(2005) AtGLR3.4, a glutamate receptor channel-like
gene is sensitive to touch and cold, Planta, 222, 418-427,
doi:10.1007/s00425-005-1551-3.
MUDRILOV et al.1484
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
55. Ghosh, S., Bheri, M., and Pandey, G. K. (2021) Delin-
eating calcium signaling machinery in plants: tapping the
potential through functional genomics, Curr. Genomics,
22, 404-439, doi:10.2174/1389202922666211130143328.
56. Salvador-Recatalà, V. (2016) New roles for the glutamate
receptor-like 3.3, 3.5, and 3.6 genes as on/off switches of
wound-induced systemic electrical signals, Plant Signal.
Behav., 11, e1161879, doi:10.1080/15592324.2016.1161879.
57. Toyota, M., Spencer, D., Sawai-Toyota, S., Jiaqi, W.,
Zhang, T., Koo, A.J., Howe, G.A., and Gilroy, S. (2018)
Glutamate triggers long-distance, calcium-based plant
defense signaling, Science, 361, 1112-1115, doi: 10.1126/
science.aat7744.
58. Jha, S. K., Sharma, M., and Pandey, G. K. (2016) Role
of cyclic nucleotide gated channels in stress management
in plants, Curr. Genomics, 17, 315-329, doi: 10.2174/
1389202917666160331202125.
59. Wang, L., Ning, Y., Sun, J., Wilkins, K. A., Matthus, E.,
McNelly, R.E., Dark, A., Rubio, L., Moeder, W., Yosh-
ioka, K., Véry, A., Stacey, G., Leblanc-Fournier, N., Le-
gué,V., Moulia, B., and Davies, J.M. (2022) Arabidopsis
thaliana cyclic nucleotide-gated channel2 mediates extra-
cellular ATP signal transduction in root epidermis, New
Phytol., 234, 412-421, doi:10.1111/nph.17987.
60. Gobert, A., Park, G., Amtmann, A., Sanders, D., and
Maathuis, F.J.M. (2006) Arabidopsis thaliana cyclic nu-
cleotide gated channel 3 forms a non-selective ion trans-
porter involved in germination and cation transport,
J.Exp. Bot., 57, 791-800, doi:10.1093/jxb/erj064.
61. Wang, Y.-F., Munemasa, S., Nishimura, N., Ren, H.-M.,
Robert, N., Han, M., Puzõrjova, I., Kollist, H., Lee, S.,
Mori, I., and Schroeder, J.I. (2013) Identification of cy-
clic GMP-activated nonselective Ca
2+
-permeable cat-
ion channels and associated CNGC5 and CNGC6 genes
in Arabidopsis guard cells, Plant Physiol., 163, 578-590,
doi:10.1104/pp.113.225045.
62. Gao, F., Han, X., Wu, J., Zheng, S., Shang, Z., Sun, D.,
Zhou, R., and Li, B. (2012) A heat-activated calcium-per-
meable channel– Arabidopsis cyclic nucleotide-gated ion
channel 6– is involved in heat shock responses: CNGC6
is a heat-activated calcium channel, Plant J., 70, 1056-
1069, doi:10.1111/j.1365-313X.2012.04969.x.
63. Tunc-Ozdemir, M., Rato, C., Brown, E., Rogers, S.,
Mooneyham, A., Frietsch, S., Myers, C. T., Poulsen,
L.R., Malhó, R., and Harper, J.F. (2013) Cyclic nucle-
otide gated channels 7 and 8 Are essential for male re-
productive fertility, PLoS One, 8, e55277, doi: 10.1371/
journal.pone.0055277.
64. Christopher, D. A., Borsics, T., Yuen, C. Y., Ullmer, W.,
Andème-Ondzighi, C., Andres, M.A., Kang, B.-H., and
Staehelin, L.A. (2007) The cyclic nucleotide gated cation
channel AtCNGC10 traffics from the ER via Golgi vesi-
cles to the plasma membrane of Arabidopsis root and leaf
cells, BMC Plant Biol., 7, 48, doi:10.1186/1471-2229-7-48.
65. Yoshioka, K., Moeder, W., Kang, H.-G., Kachroo,
P., Masmoudi, K., Berkowitz, G., and Klessig, D. F.
(2006) The chimeric Arabidopsis cyclic nucleotide-gat-
ed ion channel11/12 activates multiple pathogen resis-
tance responses, Plant Cell, 18, 747-763, doi: 10.1105/
tpc.105.038786.
66. Shih, H.-W., DePew, C. L., Miller, N. D., and Mon-
shausen, G.B. (2015) The cyclic nucleotide-gated chan-
nel CNGC14 regulates root gravitropism in Arabidop-
sis thaliana, Curr. Biol., 25, 3119-3125, doi: 10.1016/
j.cub.2015.10.025.
67. DeFalco, T. A., Moeder, W., and Yoshioka, K. (2016)
Opening the gates: insights into cyclic nucleotide-gated
channel-mediated signaling, Trends Plant Sci., 21, 903-
906, doi:10.1016/j.tplants.2016.08.011.
68. Tipper, E., Leitão, N., Dangeville, P., Lawson, D. M.,
and Charpentier, M. (2023) A novel mutant allele of
AtCNGC15 reveals a dual function of nuclear calcium re-
lease in the root meristem, J.Exp. Bot., 74, 2572-2584,
doi:10.1093/jxb/erad041.
69. Tunc-Ozdemir, M., Tang, C., Ishka, M. R., Brown, E.,
Groves, N. R., Myers, C. T., Rato, C., Poulsen, L.R.,
McDowell, S., Miller, G., Mittler, R., and Harper, J.F.
(2013) A cyclic nucleotide-gated channel (CNGC16) in
pollen is critical for stress tolerance in pollen reproductive
development, Plant Physiol., 161, 1010-1020, doi:10.1104/
pp.112.206888.
70. Ladwig, F., Dahlke, R. I., Stührwohldt, N., Hartmann,J.,
Harter, K., and Sauter, M. (2015) Phytosulfokine regulates
growth in Arabidopsis through a response module at the
plasma membrane that includes cyclic nucleotide-gat-
ed channel17, H
+
-ATPase, and BAK1, Plant Cell, 27,
1718-1729, doi:10.1105/tpc.15.00306.
71. Meena, M. K., Prajapati, R., Krishna, D., Divakaran, K.,
Pandey, Y., Reichelt, M., Mathew, M. K., Boland, W.,
Mithöfer, A., and Vadassery, J. (2019) The Ca
2+
channel
CNGC19 regulates Arabidopsis defense against spodop-
tera herbivory, Plant Cell, 31, 1539-1562, doi: 10.1105/
tpc.19.00057.
72. Wang, X., Ma, X., Wang, H., Li, B., Clark, G., Guo, Y.,
Roux, S., Sun, D., and Tang, W. (2015) Proteomic study
of microsomal proteins reveals a key role for Arabidopsis
annexin1 in mediating heat stress-induced increase in in-
tracellular calcium levels, Mol. Cell. Proteomics, 14, 686-
694, doi:10.1074/mcp.M114.042697.
73. Liu, Q., Ding, Y., Shi, Y., Ma, L., Wang, Y., Song, C.,
Wilkins, K.A., Davies, J.M., Knight, H., Knight, M.R.,
Gong, Z., Guo, Y., and Yang, S. (2021) The calcium
transporter ANNEXIN1 mediates cold-induced calcium
signaling and freezing tolerance in plants, EMBOJ., 40,
e104559, doi:10.15252/embj.2020104559.
74. Liu, T., Du, L., Li, Q., Kang, J., Guo, Q., and Wang,S.
(2021) AtCRY2 negatively regulates the functions of
AtANN2 and AtANN3 in drought tolerance by affecting
their subcellular localization and transmembrane Ca
2+
flow,
Front. Plant Sci., 12, 754567, doi:10.3389/fpls.2021.754567.
75. Davies, J. (2014) Annexin-mediated calcium signalling in
plants, Plants, 3, 128-140, doi:10.3390/plants3010128.
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1485
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
76. Huh, S. M., Noh, E. K., Kim, H. G., Jeon, B.W., Bae,K.,
Hu, H.-C., Kwak, J.M., and Park, O.K. (2010) Arabi-
dopsis annexins AnnAt1 and AnnAt4 interact with each
other and regulate drought and salt stress responses, Plant
Cell Physiol., 51, 1499-1514, doi:10.1093/pcp/pcq111.
77. Laohavisit, A., Shang, Z., Rubio, L., Cuin, T. A., Véry,
A.-A., Wang, A., Mortimer, J. C., Macpherson, N., Cox-
on, K. M., Battey, N. H., Brownlee, C., Park, O. K., Sen-
tenac, H., Shabala, S., Webb, A. A. R., and Davies, J. M.
(2012) Arabidopsis Annexin1 mediates the radical-activat-
ed plasma membrane Ca
2+
- and K
+
-permeable conduc-
tance in root cells, Plant Cell, 24, 1522-1533, doi:10.1105/
tpc.112.097881.
78. Lichocka, M., Rymaszewski, W., Morgiewicz, K., Barymow-
Filoniuk, I., Chlebowski, A., Sobczak, M., Samuel, M.A.,
Schmelzer, E., Krzymowska, M., and Hennig, J. (2018)
Nucleus- and plastid-targeted annexin5 promotes repro-
ductive development in Arabidopsis and is essential for
pollen and embryo formation, BMC Plant Biol., 18, 183,
doi:10.1186/s12870-018-1405-3.
79. Zhu, J., Wu, X., Yuan, S., Qian, D., Nan, Q., An, L., and
Xiang, Y. (2014) Annexin5 plays a vital role in Arabidop-
sis pollen development via Ca
2+
-dependent membrane
trafficking, PLoS One, 9, e102407, doi: 10.1371/journal.
pone.0102407.
80. Yadav, D., Ahmed, I., Shukla, P., Boyidi, P., and Kir-
ti,P. (2016) Overexpression of Arabidopsis AnnAt8 alle-
viates abiotic stress in transgenic Arabidopsis and tobacco,
Plants, 5, 18, doi:10.3390/plants5020018.
81. Evans, M. J., Choi, W.-G., Gilroy, S., and Morris, R.J.
(2016) A ROS-assisted calcium wave dependent on the
AtRBOHD NADPH oxidase and TPC1 cation channel
propagates the systemic response to salt stress, Plant Physi-
ol., 171, 1771-1784, doi:10.1104/pp.16.00215.
82. Yamanaka, T., Nakagawa, Y., Mori, K., Nakano, M.,
Imamura, T., Kataoka, H., Terashima, A., Iida, K., Ko-
jima, I., Katagiri, T., Shinozaki, K., and Iida, H. (2010)
MCA1 and MCA2 that mediate Ca
2+
uptake have distinct
and overlapping roles in Arabidopsis, Plant Physiol., 152,
1284-1296, doi:10.1104/pp.109.147371.
83. Hattori, T., Otomi, Y., Nakajima, Y., Soga, K., Waka-
bayashi, K., Iida, H., and Hoson, T. (2020) MCA1 and
MCA2 are involved in the response to hypergravity in
Arabidopsis hypocotyls, Plants, 9, 590, doi: 10.3390/
plants9050590.
84. Yuan, F., Yang, H., Xue, Y., Kong, D., Ye, R., Li, C.,
Zhang, J., Theprungsirikul, L., Shrift, T., Krichilsky, B.,
Johnson, D.M., Swift, G.B., He, Y., Siedow, J.N., and
Pei, Z.-M. (2014) OSCA1 mediates osmotic-stress-evoked
Ca
2+
increases vital for osmosensing in Arabidopsis,
Nature, 514, 367-371, doi:10.1038/nature13593.
85. Thor, K., Jiang, S., Michard, E., George, J., Scherzer, S.,
Huang, S., Dindas, J., Derbyshire, P., Leitão, N., DeFal-
co, T. A., Köster, P., Hunter, K., Kimura, S., Gronnier, J.,
Stransfeld, L., Kadota, Y., Bücherl, C. A., Charpenti-
er, M., Wrzaczek, M., MacLean, D., Oldroyd, G. E. D.,
Menke, F. L. H., Roelfsema, M. R. G., Hedrich, R., Fei-
jó, J., and Zipfel, C. (2020) The calcium-permeable chan-
nel OSCA1.3 regulates plant stomatal immunity, Nature,
585, 569-573, doi:10.1038/s41586-020-2702-1.
86. Fang, X., Liu, B., Shao, Q., Huang, X., Li, J., Luan, S.,
and He, K. (2021) AtPiezo plays an important role in
root cap mechanotransduction, Int.J. Mol. Sci., 22, 467,
doi:10.3390/ijms22010467.
87. Radin, I., Richardson, R. A., Coomey, J. H., Weiner,
E.R., Bascom, C.S., Li, T., Bezanilla, M., and Haswell,
E. S. (2021) Plant PIEZO homologs modulate vacuole
morphology during tip growth, Science, 373, 586-590,
doi:10.1126/science.abe6310.
88. Tran, D., Galletti, R., Neumann, E. D., Dubois, A., Sharif-
Naeini, R., Geitmann, A., Frachisse, J.-M., Hamant,O.,
and Ingram, G.C. (2017) A mechanosensitive Ca
2+
channel
activity is dependent on the developmental regulator DEK1,
Nat. Commun., 8, 1009, doi:10.1038/s41467-017-00878-w.
89. Lee, C. P., Maksaev, G., Jensen, G. S., Murcha, M.W.,
Wilson, M.E., Fricker, M., Hell, R., Haswell, E.S., Mil-
lar, A.H., and Sweetlove, L.J. (2016) MSL1 is a mech-
anosensitive ion channel that dissipates mitochondrial
membrane potential and maintains redox homeostasis in
mitochondria during abiotic stress, PlantJ., 88, 809-825,
doi:10.1111/tpj.13301.
90. Hamilton, E. S., Schlegel, A. M., and Haswell, E. S.
(2015) United in diversity: mechanosensitive ion channels
in plants, Annu. Rev. Plant Biol., 66, 113-137, doi:10.1146/
annurev-arplant-043014-114700.
91. Hamilton, E. S., Jensen, G. S., Maksaev, G., Katims, A.,
Sherp, A.M., and Haswell, E.S. (2015) Mechanosensi-
tive channel MSL8 regulates osmotic forces during pol-
len hydration and germination, Science, 350, 438-441,
doi:10.1126/science.aac6014.
92. Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meye-
rowitz, E.M., and Frachisse, J.-M. (2008) Two MscS ho-
mologs provide mechanosensitive channel activities in the
Arabidopsis root, Curr. Biol., 18, 730-734, doi: 10.1016/
j.cub.2008.04.039.
93. Moe-Lange, J., Gappel, N. M., Machado, M., Wudick,
M. M., Sies, C. S. A., Schott-Verdugo, S. N., Bonus,
M., Mishra, S., Hartwig, T., Bezrutczyk, M., Basu, D.,
Farmer, E. E., Gohlke, H., Malkovskiy, A., Haswell, E.
S., Lercher, M. J., Ehrhardt, D. W., Frommer, W. B., and
Kleist, T. J. (2021) Interdependence of a mechanosen-
sitive anion channel and glutamate receptors in distal
wound signaling, Sci. Adv., 7, eabg4298, doi: 10.1126/
sciadv.abg4298.
94. Tran, D., Girault, T., Guichard, M., Thomine, S., Leblanc-
Fournier, N., Moulia, B., De Langre, E., Allain, J.-M.,
and Frachisse, J.-M. (2021) Cellular transduction of me-
chanical oscillations in plants by the plasma-membrane
mechanosensitive channel MSL10, Proc. Natl. Acad. Sci.
USA, 118, e1919402118, doi:10.1073/pnas.1919402118.
95. Guerringue, Y., Thomine, S., and Frachisse, J.-M. (2018)
Sensing and transducing forces in plants with MSL10 and
MUDRILOV et al.1486
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
DEK1 mechanosensors, FEBS Lett., 592, 1968-1979,
doi:10.1002/1873-3468.13102.
96. Basu, D., and Haswell, E. S. (2020) The mechanosensitive
ion channel MSL10 potentiates responses to cell swelling
in Arabidopsis seedlings, Curr. Biol., 30, 2716-2728.e6,
doi:10.1016/j.cub.2020.05.015.
97. Hedrich, R., and Geiger, D. (2017) Biology of SLAC1-
type anion channels – from nutrient uptake to stomatal
closure, New Phytol., 216, 46-61, doi:10.1111/nph.14685.
98. Barbier-Brygoo, H., De Angeli, A., Filleur, S., Frachisse,
J.-M., Gambale, F., Thomine, S., and Wege, S. (2011)
Anion channels/transporters in plants: from molecular
bases to regulatory networks, Annu. Rev. Plant Biol., 62,
25-51, doi:10.1146/annurev-arplant-042110-103741.
99. Lehmann, J., Jørgensen, M. E., Fratz, S., Müller, H. M.,
Kusch, J., Scherzer, S., Navarro-Retamal, C., Mayer, D.,
Böhm, J., Konrad, K. R., Terpitz, U., Dreyer, I., Mueller,
T.D., Sauer, M., Hedrich, R., Geiger, D., and Maierhofer, T.
(2021) Acidosis-induced activation of anion channel SLAH3
in the flooding-related stress response of Arabidopsis, Curr.
Biol., 31, 3575-3585.e9, doi:10.1016/j.cub.2021.06.018.
100. Ye, W., Koya, S., Hayashi, Y., Jiang, H., Oishi, T.,
Kato,K., Fukatsu, K., and Kinoshita, T. (2021) Identifi-
cation of genes preferentially expressed in stomatal guard
cells of Arabidopsis thaliana and involvement of the alu-
minum-activated malate transporter 6 vacuolar malate
channel in stomatal opening, Front. Plant Sci., 12, 744991,
doi:10.3389/fpls.2021.744991.
101. Meyer, S., Scholz-Starke, J., De Angeli, A., Kover-
mann,P., Burla, B., Gambale, F., and Martinoia, E. (2011)
Malate transport by the vacuolar AtALMT6 channel in
guard cells is subject to multiple regulation: AtALMT6
mediates malate transport in guard cells, Plant J., 67,
247-257, doi:10.1111/j.1365-313X.2011.04587.x.
102. Boccaccio, A., Picco, C., Di Zanni, E., and Scholz-
Starke, J. (2022) Phospholipid scrambling by a TMEM16
homolog of Arabidopsis thaliana, FEBS J., 289, 2578-
2592, doi:10.1111/febs.16279.
103. Zhang, H., Zhao, F.-G., Tang, R.-J., Yu, Y., Song, J.,
Wang, Y., Li, L., and Luan, S. (2017) Two tonoplast
MATE proteins function as turgor-regulating chloride
channels in Arabidopsis, Proc. Natl. Acad. Sci. USA, 114,
E2036-E2045, doi:10.1073/pnas.1616203114.
104. Herdean, A., Teardo, E., Nilsson, A. K., Pfeil, B.E., Jo-
hansson, O.N., Ünnep, R., Nagy, G., Zsiros, O., Dana, S.,
Solymosi, K., Garab, G., Szabó, I., Spetea, C., and Lun-
din, B. (2016) A voltage-dependent chloride channel fine-
tunes photosynthesis in plants, Nat. Commun., 7, 11654,
doi:10.1038/ncomms11654.
105. Cuin, T., Dreyer, I., and Michard, E. (2018) The role of
potassium channels in Arabidopsis thaliana long distance
electrical signalling: AKT2 modulates tissue excitability
while GORK shapes action potentials, Int. J. Mol. Sci.,
19, 926, doi:10.3390/ijms19040926.
106. Demidchik, V., Cuin, T. A., Svistunenko, D., Smith, S.J.,
Miller, A.J., Shabala, S., Sokolik, A., and Yurin, V. (2010)
Arabidopsis root K
+
-efflux conductance activated by hy-
droxyl radicals: single-channel properties, genetic basis
and involvement in stress-induced cell death, J.Cell Sci.,
123, 1468-1479, doi:10.1242/jcs.064352.
107. Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D.,
Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thi-
baud, J.-B., and Sentenac, H. (1998) Identification and
disruption of a plant shaker-like outward channel in-
volved in K
+
release into the xylem sap, Cell, 94, 647-655,
doi:10.1016/S0092-8674(00)81606-2.
108. Lebaudy, A., Pascaud, F., Véry, A.-A., Alcon, C., Drey-
er,I., Thibaud, J.-B., and Lacombe, B. (2010) Preferential
KAT1-KAT2 heteromerization determines inward K
+
cur-
rent properties in Arabidopsis guard cells, J.Biol. Chem.,
285, 6265-6274, doi:10.1074/jbc.M109.068445.
109. Jeanguenin, L., Alcon, C., Duby, G., Boeglin, M.,
Chérel, I., Gaillard, I., Zimmermann, S., Sentenac, H.,
and Véry, A.-A. (2011) AtKC1 is a general modulator of
Arabidopsis inward Shaker channel activity: Modulatory
subunit of inward K
+
channel activity, PlantJ., 67, 570-
582, doi:10.1111/j.1365-313X.2011.04617.x.
110. Kwak, J. M., Murata, Y., Baizabal-Aguirre, V. M., Mer-
rill,J., Wang, M., Kemper, A., Hawke, S. D., Tallman,G.,
and Schroeder, J.I. (2001) Dominant negative guard cell
K
+
channel mutants reduce inward-rectifying K
+
currents
and light-induced stomatal opening in Arabidopsis, Plant
Physiol., 127, 473-485, doi:10.1104/pp.010428.
111. Michard, E., Dreyer, I., Lacombe, B., Sentenac, H., and
Thibaud, J.-B. (2005) Inward rectification of the AKT2
channel abolished by voltage-dependent phosphoryla-
tion: regulation of AKT2 by phosphorylation, PlantJ., 44,
783-797, doi:10.1111/j.1365-313X.2005.02566.x.
112. Gobert, A., Isayenkov, S., Voelker, C., Czempinski, K.,
and Maathuis, F. J. M. (2007) The two-pore channel
TPK1 gene encodes the vacuolar K
+
conductance and
plays a role in K
+
homeostasis, Proc. Natl. Acad. Sci. USA,
104, 10726-10731, doi:10.1073/pnas.0702595104.
113. Becker, D., Geiger, D., Dunkel, M., Roller, A., Bertl, A.,
Latz, A., Carpaneto, A., Dietrich, P., Roelfsema, M. R.G.,
Voelker, C., Schmidt, D., Mueller-Roeber, B., Czem-
pinski, K., and Hedrich, R. (2004) AtTPK4, an Arabi-
dopsis tandem-pore K
+
channel, poised to control the
pollen membrane voltage in a pH- and Ca
2+
-dependent
manner, Proc. Natl. Acad. Sci. USA, 101, 15621-15626,
doi:10.1073/pnas.0401502101.
114. Rocchetti, A., Sharma, T., Wulfetange, C., Scholz-Starke, J.,
Grippa, A., Carpaneto, A., Dreyer, I., Vitale, A., Czemp-
inski, K., and Pedrazzini, E. (2012) The putative K
+
chan-
nel subunit AtKCO3 forms stable dimers in Arabidopsis,
Front. Plant Sci., 3, 251, doi:10.3389/fpls.2012.00251.
115. Li, D.-D., Guan, H., Li, F., Liu, C.-Z., Dong, Y.-X.,
Zhang, X.-S., and Gao, X.-Q. (2017) Arabidopsis shaker
pollen inward K
+
channel SPIK functions in SnRK1 com-
plex-regulated pollen hydration on the stigma: SPIK func-
tions in pollen hydration on stigma, J.Integr. Plant Biol.,
59, 604-611, doi:10.1111/jipb.12563.
ION CHANNELS IN ELECTRICAL SIGNALING IN HIGHER PLANTS 1487
BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023
116. Jammes, F., Hu, H.-C., Villiers, F., Bouten, R., and
Kwak, J.M. (2011) Calcium-permeable channels in plant
cells: plant calcium channels, FEBS J., 278, 4262-4276,
doi:10.1111/j.1742-4658.2011.08369.x.
117. Basu, D., and Haswell, E. S. (2017) Plant mechanosen-
sitive ion channels: an ocean of possibilities, Curr. Opin.
Plant Biol., 40, 43-48, doi:10.1016/j.pbi.2017.07.002.
118. Mori, K., Renhu, N., Naito, M., Nakamura, A., Shiba, H.,
Yamamoto, T., Suzaki, T., Iida, H., and Miura, K. (2018)
Ca
2+
-permeable mechanosensitive channels MCA1 and
MCA2 mediate cold-induced cytosolic Ca
2+
increase
and cold tolerance in Arabidopsis, Sci. Rep., 8, 550,
doi:10.1038/s41598-017-17483-y.
119. Zhang, Z., Tong, X., Liu, S.-Y., Chai, L.-X., Zhu, F.-F.,
Zhang, X.-P., Zou, J.-Z., and Wang, X.-B. (2019) Ge-
netic analysis of a Piezo-like protein suppressing system-
ic movement of plant viruses in Arabidopsis thaliana, Sci.
Rep., 9, 3187, doi:10.1038/s41598-019-39436-3.
120. Véry, A.-A., and Sentenac, H. (2003) Molecular mech-
anisms and regulation of K
+
transport in higher plants,
Annu. Rev. Plant Biol., 54, 575-603, doi:10.1146/annurev.
arplant.54.031902.134831.
121. Vincent, T. R., Avramova, M., Canham, J., Higgins, P.,
Bilkey, N., Mugford, S.T., Pitino, M., Toyota, M., Gil-
roy, S., Miller, A.J., Hogenhout, S.A., and Sanders, D.
(2017) Interplay of plasma membrane and vacuolar ion
channels, together with BAK1, elicits rapid cytosolic cal-
cium elevations in Arabidopsis during aphid feeding, Plant
Cell, 29, 1460-1479, doi:10.1105/tpc.17.00136.
122. Fichman, Y., and Mittler, R. (2021) Integration of elec-
tric, calcium, reactive oxygen species and hydraulic signals
during rapid systemic signaling in plants, Plant J., 107,
7-20, doi:10.1111/tpj.15360.
123. Yu, B., Wu, Q., Li, X., Zeng, R., Min, Q., and Huang, J.
(2022) Glutamate receptor-like gene OsGLR3.4 is required
for plant growth and systemic wound signaling in rice
(Oryza sativa), New Phytol., 233, 1238-1256, doi:10.1111/
nph.17859.
124. Kong, D., Hu, H.-C., Okuma, E., Lee, Y., Lee, H. S.,
Munemasa, S., Cho, D., Ju, C., Pedoeim, L., Rodri-
guez,B., Wang, J., Im, W., Murata, Y., Pei, Z.-M., and
Kwak, J.M. (2016) L-Met activates Arabidopsis GLR Ca
2+
channels upstream of ROS production and regulates sto-
matal movement, Cell Rep., 17, 2553-2561, doi:10.1016/
j.celrep.2016.11.015.
125. Veley, K. M., Maksaev, G., Frick, E. M., January, E.,
Kloepper, S. C., and Haswell, E. S. (2014) Arabidopsis
MSL10 has a regulated cell death signaling activity that is
separable from its mechanosensitive ion channel activity,
Plant Cell, 26, 3115-3131, doi:10.1105/tpc.114.128082.
126. Xue, N., Zhan, C., Song, J., Li, Y., Zhang, J., Qi, J.,
and Wu, J. (2022) The glutamate receptor-like 3.3 and
3.6 mediate systemic resistance to insect herbivores in
Arabidopsis, J. Exp. Bot., 73, 7611-7627, doi: 10.1093/
jxb/erac399.
127. Bellandi, A., Papp, D., Breakspear, A., Joyce, J., John-
ston, M. G., de Keijzer, J., Raven, E.C., Ohtsu, M., Vin-
cent, T.R., Miller, A.J., Sanders, D., Hogenhout, S.A.,
Morris, R.J., and Faulkner, C. (2022) Diffusion and bulk
flow of amino acids mediate calcium waves in plants, Sci.
Adv., 8, eabo6693, doi:10.1126/sciadv.abo6693.
128. Hu, C., Duan, S., Zhou, J., and Yu, J. (2021) Charac-
teristics of herbivory/wound-elicited electrical signal
transduction in tomato, Front. Agr. Sci. Eng., 8, 292-301,
doi:10.15302/J-FASE-2021395.
129. Scherzer, S., Böhm, J., Huang, S., Iosip, A. L., Kreuzer,I.,
Becker, D., Heckmann, M., Al-Rasheid, K. A. S., Drey-
er, I., and Hedrich, R. (2022) A unique inventory of ion
transporters poises the Venus flytrap to fast-propagat-
ing action potentials and calcium waves, Curr. Biol., 32,
4255-4263.e5, doi:10.1016/j.cub.2022.08.051.
130. Hedrich, R., and Kreuzer, I. (2023) Demystifying the
Venus flytrap action potential, New Phytol., 239, 2108-
2112, doi:10.1111/nph.19113.
131. Zeng, H., Zhao, B., Wu, H., Zhu, Y., and Chen, H. (2020)
Comprehensive in silico characterization and expression
profiling of nine gene families associated with calcium
transport in soybean, Agronomy, 10, 1539, doi:10.3390/
agronomy10101539.
132. Maksaev, G., and Haswell, E. S. (2012) MscS-Like10 is
a stretch-activated ion channel from Arabidopsis thaliana
with a preference for anions, Proc. Natl. Acad. Sci. USA,
109, 19015-19020, doi:10.1073/pnas.1213931109.
133. Choi, W.-G., Toyota, M., Kim, S.-H., Hilleary, R., and
Gilroy, S. (2014) Salt stress-induced Ca
2+
waves are asso-
ciated with rapid, long-distance root-to-shoot signaling
in plants, Proc. Natl. Acad. Sci. USA, 111, 6497-6502,
doi:10.1073/pnas.1319955111.
134. Kiep, V., Vadassery, J., Lattke, J., Maaß, J., Boland, W.,
Peiter, E., and Mithöfer, A. (2015) Systemic cytosolic
Ca
2+
elevation is activated upon wounding and herbivory
in Arabidopsis, New Phytol., 207, 996-1004, doi:10.1111 /
nph.13493.
135. Cui, Y., Lu, S., Li, Z., Cheng, J., Hu, P., Zhu, T.,
Wang,X., Jin, M., Wang, X., Li, L., Huang, S., Zou, B.,
and Hua, J. (2020) Cyclic nucleotide-gated ion Chan-
nels 14 and 16 promote tolerance to heat and chilling
in rice, Plant Physiol., 183, 1794-1808, doi: 10.1104/
pp.20.00591.
136. Finka, A., Cuendet, A. F. H., Maathuis, F.J.M., Saidi,Y.,
and Goloubinoff, P. (2012) Plasma membrane cyclic nu-
cleotide gated calcium channels control land plant ther-
mal sensing and acquired thermotolerance, Plant Cell,
24, 3333-3348, doi:10.1105/tpc.112.095844.
