Ion Channels in Electrical Signaling in Higher Plants

Mudrilov, Maxim A.; Ladeynova, Maria M.; Kuznetsova, Darya V.; Vodeneev, Vladimir A.

doi:10.1134/S000629792310005X

Ion Channels in Electrical Signaling in Higher Plants

REVIEW
Published: 26 October 2023

Volume 88, pages 1467–1487, (2023)
Cite this article

Download PDF

Access provided by Autonomous University of Puebla

Biochemistry (Moscow) Aims and scope Submit manuscript

Ion Channels in Electrical Signaling in Higher Plants

Download PDF

Maxim A. Mudrilov¹,
Maria M. Ladeynova¹,
Darya V. Kuznetsova¹ &
…
Vladimir A. Vodeneev¹

336 Accesses
4 Citations
Explore all metrics

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 Ca²⁺, 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 comparison of the data from molecular-genetic and electrophysiological studies. Based on such characteristics of ion channels as selectivity, activation mechanism, and intracellular and tissue localization, those ion channels that meet the requirements 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 Ca²⁺ 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.

Ca²⁺ channels and Ca²⁺ signals involved in abiotic stress responses in plant cells: recent advances

Article 29 November 2017

Electrical Signaling and Its Functions Under Conditions of Abiotic Stress: A Review of Methodological Approaches and Physiological Implications

Principles of Calcium Signal Generation and Transduction in Plant Cells

Article 10 November 2018

Use our pre-submission checklist

Avoid common mistakes on your manuscript.

INTRODUCTION

Plants in nature are subjected to the action of various adverse environmental factors. In order to develop coordinated systemic response to the action of environmental factors long-distance signal transmission is required. Three types of long-distance signals are recognized in plants – chemical, hydraulic, and electrical, which differ both in nature and in the rate of transmission. 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 functional changes in the non-affected parts of the plant. The ES-induced responses include changes in photosynthesis activity and transpiration, enhancement of respiration, changes in ATP content, expression of protective genes, and others [1, 3, 5]. Such changes play an important role in the plant adaptation to the changing environmental 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 Ca²⁺ and H⁺ concentrations 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 systems, primarily ion channels [2, 3, 7]. However, molecular nature of such channels remains poorly understood.

Elucidation of the molecular nature of ion channels participating in generation of ESs in higher plants is challenging. Firstly, it must be mentioned that investigation of the parameters of ESs and mechanisms of their generation was conducted with different plant species. In particular, plants exhibiting locomotion comprise traditional objects in the area of plant electrophysiology. Another model object, for which a significant amount of data on the mechanisms of ES generation was accumulated and involvement of ion channel in these processes was for the first time demonstrated, are giant cells of charophyte 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 object 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 comparison of the electrophysiological and molecular genetics 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 mechanisms 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 generation 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 level 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 significant 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 generation 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]. The latter is not considered in this review due to insufficient knowledge on the mechanisms of its generation. Classification of the signals into different types is based on several characteristics including direction of the potential change (de-/hyperpolarization), duration of electrical reaction, nature of its propagation, as well as typical stressors triggering the signal of a certain type.

Action potential (AP) comprises a transient depolarization 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 locomotion [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 Ca²⁺ and efflux of anions, primarily Cl^–, as well as, likely, with the temporary decrease of the H⁺-ATPase activity. In the process, Ca²⁺ ions play predominantly signaling role inducing anion flow and inactivation of the H⁺-ATPase [1, 12, 13]. At the same time, the defining role of Ca²⁺ in the change of the level of electric potential during formation of depolarization phase was demonstrated for some plant species [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 Ca²⁺ ions [3, 8, 13].

Propagation of AP within the plant (Fig. 1) occurs 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 decrement-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 appearance 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 mechanisms 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 remains unresolved. Conducting bundles in higher plants are generally recognized as a pathway of systemic transmission 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 connections, probably as a fading signal [1, 12, 13].

Various non-damaging stimuli such as changing of temperature, illumination intensity, touching, and others cause generation of AP. The mechanisms of transformation of the energy of stimulus into changes of potential 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, comprises 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 considering 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 repolarization in VP with duration of depolarization phase usually not exceeding several seconds as in the case of AP. 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 0.1-10 mm/s. With the increasing 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⁺-ATPase 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 Ca²⁺, Cl^–, and K⁺ ions that appear, likely, during activation of corresponding 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 Ca²⁺ into the cell, 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 depolarization phase [5, 12, 25, 26]. Formation of repolarization phase occurs due to restoration of the H⁺-ATPase activity, 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 (Ca²⁺, 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 possibility of VP induction by artificially increasing pressure [27] supports the role of hydraulic wave in its induction, which suggests activation of mechanosensitive ion channels [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 conducting bundles, which induces influx of Ca²⁺ into the cell. According to the modern notion, reactive oxygen species (ROS) produced by NADPH-oxidases, probably respiratory burst oxidase homolog D (RBOHD), could function as such signaling molecules [28]. Systemic spread of H₂O₂ has been demonstrated during the action of the typical VP-inducing stimuli – during mechanical damage, heating, and excessive illumination [28-30]. In turn, Ca²⁺ is capable of activating RBOHD causing increase of H₂O₂ production [7, 31], which, consequently, could facilitate self-sustaining propagation of the signal.

The abovementioned information on the mechanisms of generation and propagation of ESs in higher plants was obtained with the use of a complex of electrophysiological methods including analysis of gradients of electrochemical potentials for different ions, recording the shifts of ion concentrations during excitation, varying 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 Ca²⁺ ions due to low Ca²⁺ concentrations in cytosol and high concentrations in apoplast 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 significant outward-directed gradient [6]. For K⁺ concentration, 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 parameters of ESs. Using this approach participation of Ca²⁺, Cl^–, and K⁺ in generation of AP in higher plants was revealed [8, 13]. This approach was also used to establish the source of the Ca²⁺ ion concentration increases in cytosol, which is extracellular depot, because chelating of Ca²⁺ in the extracellular space results in practically complete suppression of AP, but not in the complete suppression of VP [14, 25, 26].

Due to the long duration, generation of even a single ES in plants, unlike in animals, causes noticeable changes of ion concentrations. Relative changes are pronounced more in those compartments, where ion concentration at rest is low – Ca²⁺ 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 photometry and radioactive indicators [8], as well as ion-sensitive chemical or genetically encoded fluorescent sensors [40]. The results indicate influx of Ca²⁺ 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 confirm that the flows of the indicated ions are passive moving 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 argument 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 mediated the revealed ion fluxes forming ES were investigated with the help of blockers. In particular, participation of Ca²⁺-channels in generation of ES was demonstrated by suppression of ES by the blocker of all types of Ca²⁺-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 Ca²⁺ efflux from intracellular sources showed participation of corresponding Ca²⁺-channels in generation of AP [15, 42, 43]. Gd³⁺, inhibitor of mechanosensitive Ca²⁺-channels suppressed propagation of VP into unstressed tissues, but not suppressed generation of VP in the zone of stimulation [24]. The blockers of anion channels, such as etacrynic acid, NPPB (5-nitro-2-(3-phenylpropylamino)-benzoic acid), and A-9-C (anthracene-9-carboxylic acid) decrease amplitude and rate of depolarization 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 depolarization [15, 41, 43]. The latter indicates that the efflux 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 Ca²⁺-channels, while generation of VP is associated with activation of ligand-dependent and Ca²⁺-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 generation 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 – vacuole [33]. Electroexcitation of tonoplast and the role of vacuole as a source of Ca²⁺ 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 Ca²⁺ from the vacuole was demonstrate in the Arabidopsis 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 depolarization and repolarization phases of ESs. Based on the analysis of the data of electrophysiological studies, selection of the channels potentially involved in generation of ES should be based on the following criteria: (i) selectivity, the channels mediating Ca²⁺, K⁺, and Cl^– transport are the most interesting; (ii) activation mechanism, 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 electrophysiological 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 performed mainly for some groups of ion channels such a K⁺-channels [46, 47]. At the same time, the genes encoding Ca²⁺-channels, in particular plasmalemma Ca²⁺-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).

Ca²⁺-, 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	Ca²⁺	PM	leaf, root, pollen	cold	Ser, ~~Glu~~	[45, 48-51]
GLR1.3		PM	leaf, stem, root	cold		[48, 49]
GLR1.4	Na⁺, K⁺, NH₄⁺, 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	Ca²⁺	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	Ca²⁺ > Na⁺ = K⁺		leaf, root, CT	BS, MD, Grv	Glu, Ala, Asn, Gln, Cys, Gly, Ser, GSH	[23, 48, 51]
GLR3.4	Ca²⁺ > 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	Ca²⁺ > Na⁺ = K⁺	PM	leaf, stem, root, CT	BS, MD	Glu	[23, 48,51, 57]
GLR3.7	Ca²⁺	PM	leaf, stem, root	NaCl		[48]
CNGC1	Ca²⁺, K⁺, Pb⁺, Na⁺, Zn²⁺, Mn²⁺, Cd²⁺		root, ~~leaf~~	HM		[58]
CNGC2	Ca²⁺, 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	Ca²⁺, Na⁺, K⁺			BS		[58]
CNGC5	Mg²⁺, Ca²⁺, Na⁺	PM	leaf, root, GC		Hyp, cGMP	[61]
CNGC6	Mg²⁺, Ca²⁺, 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	Ca²⁺, K⁺	PM		BS	cAMP, ~~cGMP~~	[65]
CNGC14	Ca²⁺	PM	root	Grv	auxins, ~~ATP~~	[66, 67]
CNGC15	Ca²⁺	PM, nucleus			NO₃^–	[67, 68]
CNGC16	Ca²⁺		pollen	heating	cGMP	[69]
CNGC17		PM			cGMP	[70]
CNGC18	Ca²⁺	PM	pollen		cAMP, cGMP	[58]
CNGC19	Ca²⁺	T, PM, EM	leaf, root, CT	BS, MD	Hyp, cAMP, DAMP	[55, 58, 71]
CNGC20		T, EM	root, GC, flower, mesophyll	NaCl		[58]
ANN1	Ca²⁺ = K⁺ > Na⁺	PM, T, EM, Cyt	root, epidermis	NaCl, MD, cold, heat, ↓Ψ_w	OH˙, H₂O₂, MT	[72-77]
ANN2	Ca²⁺	PM, Cyt	leaf, root, flower, hypocotyl, pods	↓Ψ_w, heating	~~CRY2~~	[72,74]
ANN3	Ca²⁺	PM, Cyt	root, hypocotyl, cotyledons	↓Ψ_w, heating	~~CRY2~~	[74]
ANN4	Ca²⁺, K⁺	PM, EM	leaf, root, flower, stem	↓Ψ_w, NaCl, cold		[73, 76]
ANN5	Ca²⁺?	PM, nucleus, Cyt	flower, pods, pollen, ~~root~~		[Ca²⁺]_cyt	[78, 79]
ANN8		PM, ~~nucleus~~		↓Ψ_w, NaCl		[80]
TPC1	Ca²⁺ ≈ K⁺ ≈ Na⁺	T	leaf, CT, root, flower, epidermis, mesophyll	BS, NaCl	Dep, [Ca²⁺]_cyt, [Ca²⁺]_vac, ~~↓pH~~	[32, 45, 55, 81]
MCA1	Ca²⁺	PM, T, EM	leaf, CT, stem, root, flower, pods, ~~epidermis~~	cold, ↓Ψ_w, Grv	MT	[82, 83]
MCA2	Ca²⁺	PM, T, EM	leaf, CT, stem, root, flower, pods	cold, Grv		[82, 83]
OSCA1.1	K⁺ > Ba²⁺ ≈ Ca²⁺ > Na⁺ = Mg²⁺ = Cs⁺	PM	leaf, root, flower, GC	↓Ψ_w	MT	[84]
OSCA1.3	Ca²⁺	PM	GC	BS	DAMP	[85]
OSCA1.7	Ca²⁺?			BS	DAMP	[85]
Piezo1	Ca²⁺?	T	leaf, hypocotyl, root, CT	BS, touch	MT	[86, 87]
DEK1	Ca²⁺	PM	epidermis		MT	[88]
MSL1	Cl^– ≈ K⁺	EM, PM		heating, HM, ↓Ψ_w, ~~NaCl~~	MT	[55, 89]
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^– > Ca²⁺	PM, EM		↓Ψ_w	MT	[90, 92]
MSL10	Cl^– > Ca²⁺ ≈ Na⁺	PM, EM	CT	↓Ψ_w	MT	[90, 92-96]
SLAC1	Cl^–, NO₃^–		GC, hypocotyl	BS, ↓Ψ_w, dark	ABA, Ca²⁺	[32, 97, 98]
SLAH1	Cl^–, NO₃^–		root			[32, 97, 98]
SLAH2	NO₃^–		root			[32, 34, 97, 98]
SLAH3	NO₃^–		root, leaf, GC		Dep, pH, ABA, NO₃^–	[32, 34, 97-99]
ALMT6	malate, fumarate > citrate, Cl^–, NO₃^–	T	leaf, GC, flower, ~~root~~		Ca²⁺, pH, malate	[100, 101]
ALMT12/QUAC1	malate and sulfate		GC		Dep, malate	[32, 98]
TMEM16A		EM			Ca²⁺	[32, 102]
DTX33 DTX35		T	root, leaf, GC, flower, stem		pH	[103]
VCCN1	Cl^– > NO₃^–	EM	leaf, flower	light	Dep, Ca²⁺	[104]
GORK1	K⁺, NH₄⁺		root, GC, leaf	BS, NaCl, ROS	Dep, H₂O₂, ~~↓pH~~, ~~Hyp~~	[47, 105, 106]
SKOR	K⁺ > Na⁺		root, CT, ~~stem~~, ~~leaf~~		Dep, H₂O₂, [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, Ca²⁺, cAMP, ~~↓pH~~	[47, 105, 109, 111]
TPK1	K⁺ > NH₄⁺ ≫ Na⁺	T	GC, root, mesophyll, CT, pollen	NaCl	[Ca²⁺]_cyt, ABA, CO₂, ~~↓pH~~, ~~↑pH~~	[47, 112]
TPK4	K⁺ > NH₄⁺ ≫ Na⁺	PM	root, pollen		MT, ~~↓pH~~_cyt, ~~↓ΨW~~, [Ca²⁺]_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, plasma 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.

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 Ca²⁺-selective filters. Instead, plants have Ca²⁺-permeable cation channels 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 publications, and we follow the suite in this review. Based on their electrophysiological characteristics Ca²⁺-channels are classified into three groups: depolarization-activated Ca²⁺ channels (DACC), hyperpolarization-activated Ca²⁺ channels (HACC), and voltage-independent Ca²⁺ channels (VICC); sometimes mechanosensitive Ca²⁺ 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. Ca²⁺-channels are also classified according to kinetics of their activation: fast channels (responding 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 Ca²⁺-channels have been identified so far: ionotropic glutamate-like receptors (GLR), cyclic nucleotide-gated channels CNGC), annexins (ANN), two-pore channels (TPCs), Mid1-complementing activity channels (MCA), hyperosmolality-induced [Ca²⁺]_i increase 1 channel (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 predominantly 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 individual 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). Number 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 mechanical damages [48, 51, 55, 116]. It is well known that this set of stimuli also induces both changes of membrane potential and intracellular Ca²⁺ concentration [3], which, 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 hyperpolarization has been established, which allows considering 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 membrane and tonoplast. Many CNGC are tissue-specific and are mainly present in conducting tissues, epidermis, 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]. Localization 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 generation of ES in higher plants.

Annexins represent a group of cytoplasmic proteins capable of binding to phospholipids of plasmalemma, 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, salinization, temperature change. ROS could play a role of annexin 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 advantage for Ca²⁺ [55, 116]. It is known that TPC1 is activated by depolarization and cytosolic Ca²⁺ [45, 55]. TPC1 participates in the protective response to various stressors such as salinization, flooding, attacks of pests, etc., is associated with stomatal closure, hormonal regulation, 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 tonoplast, and mechanism of activation, TPC1 could be considered as a promising participant in ES generation.

Consideration of mechanosensitive Ca²⁺-channels should begin with the MCA family [45, 55], which are localized on plasmalemma and expressed at especially high level in conducting tissues [55, 82, 90]. MCA are activated by the changes in membrane tension caused by osmotic stress, mechanical actions, cold, and other stimuli [82, 90, 116-118]. Permeability for Ca²⁺ and localization in conducting bundles allows considering this family of channels as the most probable participants in generation of ES among the mechanosensitive Ca²⁺-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-associated molecular patterns (DAMP), and indirectly participate 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 conductance [45, 55]. RMA is located predominantly on plasmalemma of epidermal cells and, most likely, is responsible 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, where it mostly detected on tonoplast. Its main functions are associated with mechanosensitivity of the roots in the solid substrate and antiviral immunity [86, 87, 119]. Limited amount of information on the channels 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 representatives from a number of Ca²⁺-channels families potentially could participate in generation of ES in plants. Based on such criteria as localization, mechanism of activation, 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 including nitrates, sulfates, and some organic anions. One important feature is the fact that under normal conditions intracellular concentration of anions are higher than extracellular, hence, concentration gradient is directed outward. Based on electrophysiological characteristics 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 predominantly transport chlorides, nitrates, and sulfates, while the S-type channels are voltage-independent with activation/deactivation times around 10 s, exhibit high permeability 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 anion channels in guard cells; later another types of anion channels have been discovered such as separately recognized aluminum-sensitive channels, mechanosensitive anion channels, and endomembrane anion channels [32, 34].

Mechanosensitive-like channels (MSL) exhibit, predominantly, anion permeability in higher plants, despite the traditional for many reviews attribution of MSL to Ca²⁺-channels [45, 55]. Representatives of this family are localized mainly on plasmalemma and ER membrane (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 expressed in conducting tissues along with roots [45, 90, 94, 96]. MSLs are activated by changes in membrane tensions including during osmotic stress, and are characterized 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 conducting cells, it is also capable of activating production of ROS with participation of NADPH-oxidase, operation of which, as mentioned above, could provide contribution 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 family: 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 stimuli, and some of them cause changes in electrical activity such as attack of pathogens, increase of CO₂ concentration, drought, darkness, etc., likely via the Ca²⁺-dependent pathway. SLAH3, in addition to Ca²⁺-dependent 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 assigned to the group of potential participants in ES generation, 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 channel 1 (QUAC1) has been given to this channel due to the absence 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 depolarization, exhibits activation/deactivation times characteristic for R-type of channels, and transports malate and sulfate. Another member of the family, ALMT6, which is localized on tonoplast, exhibits predominantly malate and fumarate permeability, but also transports chloride, it is activated by Ca²⁺ and acidic pH in vacuole [100, 101]. Other well investigated at present representatives 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 information 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 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, function as a Ca²⁺-activated anion channel [32, 102]. There is also information on the voltage-dependent Cl^– channel 1 (VCCN1) in thylakoids, which is activated by depolarization and light, but not by Ca²⁺, and participates in regulation of photosynthesis [104].

Hence, from the point of view of potential participation 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 classification of K⁺-channels is based on the mechanism of activation 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 localized on plasmalemma, while the voltage-independent, with some exception, are endomembrane K⁺-channels [46, 47]. The voltage-dependent K⁺-channels are sub-divided into the channels mediating potassium efflux (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 Shaker-type K⁺-channel family belong to the voltage-dependent 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 participation of Ca²⁺-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 outside of roots (table), hence, the possibility of its participation 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 pollen plasmalemma [46, 47]. Activation by Ca²⁺ and acidification of cytosol (pH 6.7 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 extracellular Ca²⁺ [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 available 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 overexpression. 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 comparison 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 signaling, however, such approach is applicable only to the ligand-activated channels [23, 123]. The abovementioned methods also have drawbacks. One of such drawbacks 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 double- and more mutants also could not provide as unambiguous answer whether the change of ES parameters is associated with the fact that certain heteromeric channels are not formed, or some of the homomeric channels 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 compensated by overexpression of another gene that perform the same or similar role, also could complicate interpretation 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 mutants does not provide an unambiguous answer, but at present there is no other approach for analysis of electrophysiological and molecular genetics data at the level of whole organism.

The most investigated participants of ES generation in plants are Ca²⁺-channels, primarily from the GLR family (Fig. 2) [51]. Complete suppression of VP propagation outside of the region of the leaf subjected to mechanical damage [20, 21, 53, 56, 122], attack of chewing insects [20], excessive light [122], and laser-initiate damage [53] was observed in the glr3.3glr3.6 double mutant of Arabidopsis. In the process, amplitude of electrical 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 comparison with the wild type plant [23]. In the case of single 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 depolarization, in the glr3.6 mutant only the latter is suppressed [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, because 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 important to note that during comparison of the glr mutant with the wild type coordinated changes were observed during simultaneous recording of the dynamics of Ca²⁺ concentration and dynamics of electric potential: in the mutant forms with GLR deficit both Ca²⁺-wave and VP were suppressed [23, 53, 122]. This indicates direct association between the changes of Ca²⁺ 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 Ca²⁺ 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 Ca²⁺ or generation of ES [23, 57]. These data together with consideration of the temporal-spatial dynamics of Ca²⁺ 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 transmission 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 amplitude [128].

Predominant expression of GLR3.3 and GLR3.6 in conducting bundles provides additional support to the suggestion that these channels participate in the systemic propagation of ESs. In particular, pronounced expression 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 primary 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 reaction nor local reaction were suppressed completely [53]. It has been suggested that GLR3.1 participates in propagation of ES outside the limits of conducting bundles due to disruption of the ES-associated radial propagation of the Ca²⁺ 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 provides 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, homolog 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 Ca²⁺-channel with functions similar to the functions of GLR3.3 and GLR3.6 of Arabidopsis could be highlighted among the GLRs: systemic 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 amino 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 participation in formation of ES was determined using molecular 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 mechanical 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 mutant 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 bundles including both phloem and xylem. The MSL10 channel demonstrates anion conductance, but not calcium conductance [93, 132]. Nevertheless, functioning of MSL10, most likely, activates influx of Ca²⁺ into the cell during mechanical damage through GLR3.3 and GLR3.6. It was demonstrated also that the initial depolarization phase occurs before the start of the changes in Ca²⁺ concentration [93], which raises the question regarding the accepted mechanism of VP generation.

And, finally, a channel has been identified ensuring 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 higher in comparison with the wild type, while repolarization was significantly slower (Fig. 2). The following mathematical modeling confirmed participation of this channel in generation of AP. It was also shown that GORK1 is activated already at the phase of depolarization decreasing its rate and amplitude under normal conditions [105]. It was also demonstrated in this study that another K⁺-channel, AKT2, could affect generation of AP, but not directly through regulation of the plasmalemma excitability [105].

Participation of two K⁺-channels, DmSKOR belonging to the same group as the previously considered GORK1and KDM1, homolog of the KAT1 of Arabidopsis, was demonstrated in the recent studies on Venus flytrap [37, 129]. Suppression of the DmSKOR expression by coronatine, which suppresses expression of the genes associated with excitability in Venus flytrap, resulted 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 comparison 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 generation 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 Ca²⁺-signals, because there is close similarity between the dynamics of Ca²⁺ concentration and dynamics of the changes of electric potential during excitation [53, 129]. In particular, decrease of amplitude and of the rate of Ca²⁺ 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, overexpression of TPC1 results in systemic increase of Ca²⁺, which is not observed in the wild type [121]. Nevertheless, the authors suggested only auxiliary role of TPC1 in initiating response to salinization and mechanical damage involving enhancement of the Ca²⁺ concentration shift initiated by other channels [133, 134]. The demonstrated role of TPC1 in formation of Ca²⁺-wave induced by different stimuli together with the presumed 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 generation of ES. Contribution to formation of Ca²⁺-signal was also demonstrated for the channel from a different family, CNGC19, localized on the plasmalemma of phloem cells: participation of the channel in the increase of Ca²⁺ concentration in response to the attack of chewing insect was revealed, moreover, activation of CNGC19 could be mediated by either Pep1 (Protein elicitor peptide 1, one of the DAMP released during the cell damage) or directly by cAMP, content of which also increases during the damage [71].

In addition to the results of investigating propagating Ca²⁺-signal, data on the changes of Ca²⁺ concentration in the zone of stimulus action exemplified, in particular, 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 Arabidopsis) [135] mutants demonstrated decrease of the amplitude of Ca²⁺ 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 Ca²⁺-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 Ca²⁺ concentration was not completely 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 compensatory expression of other genes, or existence of different participants in the processes of changing Ca²⁺ levels in different plant species [73, 118, 135]. Suppression of the Ca²⁺ wave in cytosol induced by another well investigated stimulus, heating, was shown in the CNGC2, CNGC6, OsCNGC14, OsCNGC16, ANN1, and ANN2 mutant plants; furthermore, the heating-induced increase of Ca²⁺ level in the wild type plants is similar to the VP in shape and duration [62, 72, 135, 136]. The abovementioned information implies that the discussed channels could provide contribution to generation of electrical response in the zone of the corresponding stimulus action.

In general, it could be stated with confidence that the following Ca²⁺-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 Ca²⁺-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 possibility of their potential involvement in generation of ES.

CONCLUSIONS

In conclusion of our analysis of molecular mechanisms of electrical signaling in higher plants, it must be mentioned that further detailed investigations are necessary. Most significant results could be expected if the efforts are concentrated on the following issues: (i) identification of molecular nature of the voltage-dependent Ca²⁺-channels of plasmalemma responsible for initiation of AP appearing in plants when the threshold level of depolarization is reached [8]; (ii) search for the genes encoding ion channels in different species of plants including 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, genetically encoded fluorescent sensors.

Identification and characterization of ion channels participating in generation of ES could provide significant 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 functional response to the propagating ES is based on the changes of ion concentration in the cells and tissues caused by propagation of ES [5, 6]. In future it would facilitate 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].

Abbreviations

AP:: action potential
ES:: electrical signal
SP:: system potential
VP:: variation potential

References

Huber, A. E., and Bauerle, T. L. (2016) Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge, J. Exp. Bot., 67, 2063-2079, https://doi.org/10.1093/jxb/erw099.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1093/plphys/kiaa098.
Article CAS PubMed PubMed Central Google Scholar
Mudrilov, M., Ladeynova, M., Grinberg, M., Balalaeva, I., and Vodeneev, V. (2021) Electrical signaling of plants under abiotic stressors: transmission of stimulus-specific information, Int. J. Mol. Sci., 22, 10715, https://doi.org/10.3390/ijms221910715.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.3390/ijms24010847.
Article CAS PubMed PubMed Central Google Scholar
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 responses in higher plants, Prog. Biophys. Mol. Biol., 146, 63-84, https://doi.org/10.1016/j.pbiomolbio.2018.11.009.
Article CAS PubMed Google Scholar
Klejchova, M., Silva-Alvim, F. A. L., Blatt, M. R., and Alvim, J. C. (2021) Membrane voltage as a dynamic platform for spatiotemporal signaling, physiological, and developmental regulation, Plant Physiol., 185, 1523-1541, https://doi.org/10.1093/plphys/kiab032.
Article CAS PubMed PubMed Central Google Scholar
Farmer, E. E., Gao, Y., Lenzoni, G., Wolfender, J., and Wu, Q. (2020) Wound- and mechanostimulated electrical signals control hormone responses, New Phytol., 227, 1037-1050, https://doi.org/10.1111/nph.16646.
Article CAS PubMed Google Scholar
Opritov, V. A., Pyatygin, S. S., and Retivin, V. G., Bioelectrogenesis in higher plants, Moscow: Nauka, 1991.
Bulychev, A. A., and Komarova, A. V. (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells, Biochemistry (Moscow), 79, 273-281, https://doi.org/10.1134/S0006297914030134.
Article CAS PubMed Google Scholar
Kisnieriene, V., Trębacz, K., Pupkis, V., Koselski, M., and Lapeikaite, I. (2022) Evolution of long-distance signalling upon plant terrestrialization: comparison of action potentials in Characean algae and liverworts, Ann. Bot., 130, 457-475, https://doi.org/10.1093/aob/mcac098.
Article CAS PubMed PubMed Central Google Scholar
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 chloride channels, J. Membr. Biol., 72, 43-58, https://doi.org/10.1007/BF01870313.
Article Google Scholar
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, https://doi.org/10.1134/S0006350916030209.
Article CAS Google Scholar
Fromm, J., and Lautner, S. (2007) Electrical signals and their physiological significance in plants: electrical signals in plants, Plant Cell Environ., 30, 249-257, https://doi.org/10.1111/j.1365-3040.2006.01614.x.
Article CAS PubMed Google Scholar
Hodick, D., and Sievers, A. (1988) The action potential of Dionaea muscipula Ellis, Planta, 174, 8-18, https://doi.org/10.1007/BF00394867.
Article CAS PubMed Google Scholar
Krol, E., Dziubinska, H., Stolarz, M., and Trebacz, K. (2006) Effects of ion channel inhibitors on cold- and electrically-induced action potentials in Dionaea muscipula, Biol. Plant., 50, 411-416, https://doi.org/10.1007/s10535-006-0058-5.
Article CAS Google Scholar
Stahlberg, R., Cleland, R. E., and Van Volkenburgh, E. (2006) Slow wave potentials – a propagating electrical 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, https://doi.org/10.1007/978-3-540-28516-8_20.
Li, Q., Wang, C., and Mou, Z. (2020) Perception of damaged self in plants, Plant Physiol., 182, 1545-1565, https://doi.org/10.1104/pp.19.01242.
Article CAS PubMed PubMed Central Google Scholar
Vodeneev, V., Mudrilov, M., Akinchits, E., Balalaeva, I., and Sukhov, V. (2018) Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus, Funct. Plant Biol., 45, 160, https://doi.org/10.1071/FP16342.
Article CAS PubMed Google Scholar
Mudrilov, M., Ladeynova, M., Berezina, E., Grinberg, M., Brilkina, A., Sukhov, V., and Vodeneev, V. (2021) Mechanisms of specific systemic response in wheat plants under different locally acting heat stimuli, J. Plant Physiol., 258-259, 153377, https://doi.org/10.1016/j.jplph.2021.153377.
Article CAS PubMed Google Scholar
Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S., and Farmer, E. E. (2013) Glutamate receptor-like genes mediate leaf-to-leaf wound signalling, Nature, 500, 422-426, https://doi.org/10.1038/nature12478.
Article CAS PubMed Google Scholar
Salvador-Recatalà, V., Tjallingii, W. F., and Farmer, E. E. (2014) Real-time, in vivo intracellular recordings of caterpillar-induced depolarization waves in sieve elements using aphid electrodes, New Phytol., 203, 674-684, https://doi.org/10.1111/nph.12807.
Article CAS PubMed Google Scholar
Julien, J. L., Desbiez, M. O., De Jaegher, G., and Frachisse, J. M. (1991) Characteristics of the wave of depolarization induced by wounding in Bidens Pilosa L., J. Exp. Bot., 42, 131-137, https://doi.org/10.1093/jxb/42.1.131.
Article Google Scholar
Shao, Q., Gao, Q., Lhamo, D., Zhang, H., and Luan, S. (2020) Two glutamate- and pH-regulated Ca²⁺ channels are required for systemic wound signaling in Arabidopsis, Sci. Signal., 13, eaba1453, https://doi.org/10.1126/scisignal.aba1453.
Article CAS PubMed Google Scholar
Zimmermann, M. R., and Felle, H. H. (2009) Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities, Planta, 229, 539-547, https://doi.org/10.1007/s00425-008-0850-x.
Article CAS PubMed Google Scholar
Katicheva, L., Sukhov, V., Akinchits, E., and Vodeneev, V. (2014) Ionic nature of burn-induced variation potential in wheat leaves, Plant Cell Physiol., 55, 1511-1519, https://doi.org/10.1093/pcp/pcu082.
Article CAS PubMed Google Scholar
Vodeneev, V., Akinchits, E., and Sukhov, V. (2015) Variation potential in higher plants: Mechanisms of generation and propagation, Plant Signal. Behav., 10, e1057365, https://doi.org/10.1080/15592324.2015.1057365.
Article CAS PubMed PubMed Central Google Scholar
Stahlberg, R., and Cosgrove, D. J. (1997) The propagation of slow wave potentials in pea epicotyls, Plant Physiol., 113, 209-217, https://doi.org/10.1104/pp.113.1.209.
Article CAS PubMed PubMed Central Google Scholar
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 systemic signaling in response to diverse stimuli, Sci. Signal., 2, ra45, https://doi.org/10.1126/scisignal.2000448.
Article PubMed Google Scholar
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 communication during light stress, Sci. Signal., 11, eaam9514, https://doi.org/10.1126/scisignal.aam9514.
Article CAS PubMed Google Scholar
Volkov, R. A., Panchuk, I. I., Mullineaux, P. M., and Schöffl, F. (2006) Heat stress-induced H₂O₂ is required for effective expression of heat shock genes in Arabidopsis, Plant Mol. Biol., 61, 733-746, https://doi.org/10.1007/s11103-006-0045-4.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1016/j.bbamcr.2013.06.024.
Article CAS PubMed Google Scholar
Hedrich, R. (2012) Ion channels in plants, Physiol. Rev., 92, 1777-1811, https://doi.org/10.1152/physrev.00038.2011.
Article CAS PubMed Google Scholar
Costa, A., Navazio, L., and Szabo, I. (2018) The contribution of organelles to plant intracellular calcium signalling, J. Exp. Bot., 69, 4175-4193, https://doi.org/10.1093/jxb/ery185.
Article CAS Google Scholar
Kollist, H., Jossier, M., Laanemets, K., and Thomine, S. (2011) Anion channels in plant cells: plant anion channels, FEBS J., 278, 4277-4292, https://doi.org/10.1111/j.1742-4658.2011.08370.x.
Article CAS PubMed Google Scholar
Véry, A.-A., and Sentenac, H. (2002) Cation channels in the Arabidopsis plasma membrane, Trends Plant Sci.Sci., 7, 168-175, https://doi.org/10.1016/S1360-1385(02)02262-8.
Article Google Scholar
Fromm, J., and Spanswick, R. (1993) Characteristics of action potentials in willow (Salix viminalis L.), J. Exp. Bot., 44, 1119-1125, https://doi.org/10.1093/jxb/44.7.1119.
Article Google Scholar
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-specific potassium channel KDM1 can reestablish the K⁺ gradient required for hapto-electric signaling, PLoS Biol., 18, e3000964, https://doi.org/10.1371/journal.pbio.3000964.
Article CAS PubMed PubMed Central Google Scholar
Vodeneev, V. A., Akinchits, E. K., Orlova, L. A., and Sukhov, V. S. (2011) The role of Ca²⁺, H⁺, and Cl⁻ ions in generation of variation potential in pumpkin plants, Russ. J. Plant Physiol., 58, 974-981, https://doi.org/10.1134/S1021443711050256.
Article CAS Google Scholar
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, https://doi.org/10.1007/978-1-61779-986-0_7.
Hilleary, R., Choi, W.-G., Kim, S.-H., Lim, S. D., and Gilroy, S. (2018) Sense and sensibility: the use of fluorescent protein-based genetically encoded biosensors in plants, Curr. Opin. Plant Biol., 46, 32-38, https://doi.org/10.1016/j.pbi.2018.07.004.
Article CAS PubMed Google Scholar
Lewis, B. D., Karlin-Neumann, C., and Spalding, E. P. (1997) Ca²⁺-activated anion channels and membrane depolarizations induced by blue light and cold in arabidopsis seedlings, Plant Physiol., 114, 1327-1334, https://doi.org/10.1104/pp.114.4.1327.
Article CAS PubMed PubMed Central Google Scholar
Krol, E., Dziubinska, H., and Trebacz, K. (2004) Low-temperature-induced transmembrane potential changes in mesophyll cells of Arabidopsis thaliana, Helianthus annuus and Vicia faba, Physiol. Plant, 120, 265-270, https://doi.org/10.1111/j.0031-9317.2004.0244.x.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1134/S102144370604008X.
Article CAS Google Scholar
Dindas, J., Dreyer, I., Huang, S., Hedrich, R., and Roelfsema, M. R. G. (2021) A voltage-dependent Ca²⁺ homeostat operates in the plant vacuolar membrane, New Phytol., 230, 1449-1460, https://doi.org/10.1111/nph.17272.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1111/nph.15266.
Article CAS PubMed Google Scholar
Dreyer, I., and Uozumi, N. (2011) Potassium channels in plant cells: potassium channels in plants, FEBS J., 278, 4293-4303, https://doi.org/10.1111/j.1742-4658.2011.08371.x.
Article CAS PubMed Google Scholar
Sharma, T., Dreyer, I., and Riedelsberger, J. (2013) The role of K⁺ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana, Front. Plant Sci., 4, 224, https://doi.org/10.3389/fpls.2013.00224.
Article PubMed PubMed Central Google Scholar
Naz, R., Khan, A., Alghamdi, B. S., Ashraf, G. M., Alghanmi, 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, https://doi.org/10.3390/plants11192580.
Article CAS PubMed PubMed Central Google Scholar
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 jasmonate signaling in Arabidopsis thaliana, Biochem. Biophys. Res. Commun., 506, 895-900, https://doi.org/10.1016/j.bbrc.2018.10.153.
Article CAS PubMed Google Scholar
Michard, E., Lima, P. T., Borges, F., Silva, A. C., Portes, M. T., Carvalho, J. E., Gilliham, M., Liu, L.-H., Obermeyer, G., and Feijó, J. A. (2011) Glutamate receptor-like genes form Ca²⁺ channels in pollen tubes and are regulated by pistil D-serine, Science, 332, 434-437, https://doi.org/10.1126/science.1201101.
Article CAS PubMed Google Scholar
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, https://doi.org/10.3390/plants11243450.
Article CAS PubMed PubMed Central Google Scholar
Tapken, D., Anschütz, U., Liu, L.-H., Huelsken, T., Seebohm, 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, https://doi.org/10.1126/scisignal.2003762.
Article CAS PubMed Google Scholar
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 wounded plant, Proc. Natl. Acad. Sci. USA, 115, 10178-10183, https://doi.org/10.1073/pnas.1807049115.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1007/s00425-005-1551-3.
Article CAS PubMed Google Scholar
Ghosh, S., Bheri, M., and Pandey, G. K. (2021) Delineating calcium signaling machinery in plants: tapping the potential through functional genomics, Curr. Genomics, 22, 404-439, https://doi.org/10.2174/1389202922666211130143328.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1080/15592324.2016.1161879.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1126/science.aat7744.
Article CAS PubMed Google Scholar
K. Jha, S., Sharma, M., and K. Pandey, G. (2016) Role of cyclic nucleotide gated channels in stress management in plants, Curr. Genomics, 17, 315-329, https://doi.org/10.2174/1389202917666160331202125.
Article CAS PubMed PubMed Central Google Scholar
Wang, L., Ning, Y., Sun, J., Wilkins, K. A., Matthus, E., McNelly, R. E., Dark, A., Rubio, L., Moeder, W., Yoshioka, K., Véry, A., Stacey, G., Leblanc-Fournier, N., Legué, V., Moulia, B., and Davies, J. M. (2022) Arabidopsis thaliana cyclic nucleotide-gated channel2 mediates extracellular ATP signal transduction in root epidermis, New Phytol., 234, 412-421, https://doi.org/10.1111/nph.17987.
Article CAS PubMed PubMed Central Google Scholar
Gobert, A., Park, G., Amtmann, A., Sanders, D., and Maathuis, F. J. M. (2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport, J. Exp. Bot., 57, 791-800, https://doi.org/10.1093/jxb/erj064.
Article CAS PubMed Google Scholar
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 cyclic GMP-activated nonselective Ca²⁺-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells, Plant Physiol., 163, 578-590, https://doi.org/10.1104/pp.113.225045.
Article CAS PubMed PubMed Central Google Scholar
Gao, F., Han, X., Wu, J., Zheng, S., Shang, Z., Sun, D., Zhou, R., and Li, B. (2012) A heat-activated calcium-permeable 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, https://doi.org/10.1111/j.1365-313X.2012.04969.x.
Article CAS PubMed Google Scholar
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 nucleotide gated channels 7 and 8 Are essential for male reproductive fertility, PLoS One, 8, e55277, https://doi.org/10.1371/journal.pone.0055277.
Article CAS PubMed PubMed Central Google Scholar
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 vesicles to the plasma membrane of Arabidopsis root and leaf cells, BMC Plant Biol., 7, 48, https://doi.org/10.1186/1471-2229-7-48.
Article CAS PubMed PubMed Central Google Scholar
Yoshioka, K., Moeder, W., Kang, H.-G., Kachroo, P., Masmoudi, K., Berkowitz, G., and Klessig, D. F. (2006) The chimeric Arabidopsis cyclic nucleotide-gated ion channel11/12 activates multiple pathogen resistance responses, Plant Cell, 18, 747-763, https://doi.org/10.1105/tpc.105.038786.
Article CAS PubMed PubMed Central Google Scholar
Shih, H.-W., DePew, C. L., Miller, N. D., and Monshausen, G. B. (2015) The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana, Curr. Biol., 25, 3119-3125, https://doi.org/10.1016/j.cub.2015.10.025.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1016/j.tplants.2016.08.011.
Article CAS PubMed Google Scholar
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 release in the root meristem, J. Exp. Bot., 74, 2572-2584, https://doi.org/10.1093/jxb/erad041.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1104/pp.112.206888.
Article CAS PubMed Google Scholar
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-gated channel17, H⁺-ATPase, and BAK1, Plant Cell, 27, 1718-1729, https://doi.org/10.1105/tpc.15.00306.
Article CAS PubMed PubMed Central Google Scholar
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 Ca²⁺ channel CNGC19 regulates Arabidopsis defense against spodoptera herbivory, Plant Cell, 31, 1539-1562, https://doi.org/10.1105/tpc.19.00057.
Article CAS PubMed PubMed Central Google Scholar
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 annexin 1 in mediating heat stress-induced increase in intracellular calcium levels, Mol. Cell. Proteomics, 14, 686-694, https://doi.org/10.1074/mcp.M114.042697.
Article CAS PubMed PubMed Central Google Scholar
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, EMBO J., 40, e104559, https://doi.org/10.15252/embj.2020104559.
Article CAS PubMed Google Scholar
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 Ca²⁺ flow, Front. Plant Sci., 12, 754567, https://doi.org/10.3389/fpls.2021.754567.
Article PubMed PubMed Central Google Scholar
Davies, J. (2014) Annexin-mediated calcium signalling in plants, Plants, 3, 128-140, https://doi.org/10.3390/plants3010128.
Article CAS PubMed PubMed Central Google Scholar
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) Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt stress responses, Plant Cell Physiol., 51, 1499-1514, https://doi.org/10.1093/pcp/pcq111.
Article CAS PubMed Google Scholar
Laohavisit, A., Shang, Z., Rubio, L., Cuin, T. A., Véry, A.-A., Wang, A., Mortimer, J. C., Macpherson, N., Coxon, K. M., Battey, N. H., Brownlee, C., Park, O. K., Sentenac, H., Shabala, S., Webb, A. A. R., and Davies, J. M. (2012) Arabidopsis Annexin1 mediates the radical-activated plasma membrane Ca²⁺- and K⁺-permeable conductance in root cells, Plant Cell, 24, 1522-1533, https://doi.org/10.1105/tpc.112.097881.
Article CAS PubMed PubMed Central Google Scholar
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 annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation, BMC Plant Biol., 18, 183, https://doi.org/10.1186/s12870-018-1405-3.
Article CAS PubMed PubMed Central Google Scholar
Zhu, J., Wu, X., Yuan, S., Qian, D., Nan, Q., An, L., and Xiang, Y. (2014) Annexin5 plays a vital role in Arabidopsis pollen development via Ca²⁺-dependent membrane trafficking, PLoS One, 9, e102407, https://doi.org/10.1371/journal.pone.0102407.
Article CAS PubMed PubMed Central Google Scholar
Yadav, D., Ahmed, I., Shukla, P., Boyidi, P., and Kirti, P. (2016) Overexpression of Arabidopsis AnnAt8 alleviates abiotic stress in transgenic Arabidopsis and tobacco, Plants, 5, 18, https://doi.org/10.3390/plants5020018.
Article CAS PubMed PubMed Central Google Scholar
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 Physiol., 171, 1771-1784, https://doi.org/10.1104/pp.16.00215.
Article CAS PubMed PubMed Central Google Scholar
Yamanaka, T., Nakagawa, Y., Mori, K., Nakano, M., Imamura, T., Kataoka, H., Terashima, A., Iida, K., Kojima, I., Katagiri, T., Shinozaki, K., and Iida, H. (2010) MCA1 and MCA2 that mediate Ca²⁺ uptake have distinct and overlapping roles in Arabidopsis, Plant Physiol., 152, 1284-1296, https://doi.org/10.1104/pp.109.147371.
Article CAS PubMed PubMed Central Google Scholar
Hattori, T., Otomi, Y., Nakajima, Y., Soga, K., Wakabayashi, K., Iida, H., and Hoson, T. (2020) MCA1 and MCA2 are involved in the response to hypergravity in Arabidopsis hypocotyls, Plants, 9, 590, https://doi.org/10.3390/plants9050590.
Article CAS PubMed PubMed Central Google Scholar
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 Ca²⁺ increases vital for osmosensing in Arabidopsis, Nature, 514, 367-371, https://doi.org/10.1038/nature13593.
Article CAS PubMed Google Scholar
Thor, K., Jiang, S., Michard, E., George, J., Scherzer, S., Huang, S., Dindas, J., Derbyshire, P., Leitão, N., DeFalco, T. A., Köster, P., Hunter, K., Kimura, S., Gronnier, J., Stransfeld, L., Kadota, Y., Bücherl, C. A., Charpentier, M., Wrzaczek, M., MacLean, D., Oldroyd, G. E. D., Menke, F. L. H., Roelfsema, M. R. G., Hedrich, R., Feijó, J., and Zipfel, C. (2020) The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity, Nature, 585, 569-573, https://doi.org/10.1038/s41586-020-2702-1.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.3390/ijms22010467.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1126/science.abe6310.
Article CAS PubMed Google Scholar
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 Ca²⁺ channel activity is dependent on the developmental regulator DEK1, Nat. Commun., 8, 1009, https://doi.org/10.1038/s41467-017-00878-w.
Article CAS PubMed PubMed Central Google Scholar
Lee, C. P., Maksaev, G., Jensen, G. S., Murcha, M. W., Wilson, M. E., Fricker, M., Hell, R., Haswell, E. S., Millar, A. H., and Sweetlove, L. J. (2016) MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress, Plant J., 88, 809-825, https://doi.org/10.1111/tpj.13301.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1146/annurev-arplant-043014-114700.
Article CAS PubMed Google Scholar
Hamilton, E. S., Jensen, G. S., Maksaev, G., Katims, A., Sherp, A. M., and Haswell, E. S. (2015) Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination, Science, 350, 438-441, https://doi.org/10.1126/science.aac6014.
Article CAS PubMed PubMed Central Google Scholar
Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E. M., and Frachisse, J.-M. (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root, Curr. Biol., 18, 730-734, https://doi.org/10.1016/j.cub.2008.04.039.
Article CAS PubMed Google Scholar
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 mechanosensitive anion channel and glutamate receptors in distal wound signaling, Sci. Adv., 7, eabg4298, https://doi.org/10.1126/sciadv.abg4298.
Article CAS PubMed PubMed Central Google Scholar
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 mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10, Proc. Natl. Acad. Sci. USA, 118, e1919402118, https://doi.org/10.1073/pnas.1919402118.
Article CAS PubMed Google Scholar
Guerringue, Y., Thomine, S., and Frachisse, J.-M. (2018) Sensing and transducing forces in plants with MSL10 and DEK1 mechanosensors, FEBS Lett., 592, 1968-1979, https://doi.org/10.1002/1873-3468.13102.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1016/j.cub.2020.05.015.
Article CAS PubMed Google Scholar
Hedrich, R., and Geiger, D. (2017) Biology of SLAC1-type anion channels – from nutrient uptake to stomatal closure, New Phytol., 216, 46-61, https://doi.org/10.1111/nph.14685.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1146/annurev-arplant-042110-103741.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1016/j.cub.2021.06.018.
Article CAS PubMed Google Scholar
Ye, W., Koya, S., Hayashi, Y., Jiang, H., Oishi, T., Kato, K., Fukatsu, K., and Kinoshita, T. (2021) Identification of genes preferentially expressed in stomatal guard cells of Arabidopsis thaliana and involvement of the aluminum-activated malate transporter 6 vacuolar malate channel in stomatal opening, Front. Plant Sci., 12, 744991, https://doi.org/10.3389/fpls.2021.744991.
Article PubMed PubMed Central Google Scholar
Meyer, S., Scholz-Starke, J., De Angeli, A., Kovermann, 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, https://doi.org/10.1111/j.1365-313X.2011.04587.x.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1111/febs.16279.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1073/pnas.1616203114.
Article CAS PubMed PubMed Central Google Scholar
Herdean, A., Teardo, E., Nilsson, A. K., Pfeil, B. E., Johansson, O. N., Ünnep, R., Nagy, G., Zsiros, O., Dana, S., Solymosi, K., Garab, G., Szabó, I., Spetea, C., and Lundin, B. (2016) A voltage-dependent chloride channel fine-tunes photosynthesis in plants, Nat. Commun., 7, 11654, https://doi.org/10.1038/ncomms11654.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.3390/ijms19040926.
Article CAS PubMed PubMed Central Google Scholar
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 hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death, J. Cell Sci., 123, 1468-1479, https://doi.org/10.1242/jcs.064352.
Article CAS PubMed Google Scholar
Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J.-B., and Sentenac, H. (1998) Identification and disruption of a plant shaker-like outward channel involved in K⁺ release into the xylem sap, Cell, 94, 647-655, https://doi.org/10.1016/S0092-8674(00)81606-2.
Article CAS PubMed Google Scholar
Lebaudy, A., Pascaud, F., Véry, A.-A., Alcon, C., Dreyer, I., Thibaud, J.-B., and Lacombe, B. (2010) Preferential KAT1-KAT2 heteromerization determines inward K⁺ current properties in Arabidopsis guard cells, J. Biol. Chem., 285, 6265-6274, https://doi.org/10.1074/jbc.M109.068445.
Article CAS PubMed Google Scholar
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, Plant J., 67, 570-582, https://doi.org/10.1111/j.1365-313X.2011.04617.x.
Article CAS PubMed Google Scholar
Kwak, J. M., Murata, Y., Baizabal-Aguirre, V. M., Merrill, 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, https://doi.org/10.1104/pp.010428.
Article CAS PubMed PubMed Central Google Scholar
Michard, E., Dreyer, I., Lacombe, B., Sentenac, H., and Thibaud, J.-B. (2005) Inward rectification of the AKT2 channel abolished by voltage-dependent phosphorylation: regulation of AKT2 by phosphorylation, Plant J., 44, 783-797, https://doi.org/10.1111/j.1365-313X.2005.02566.x.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1073/pnas.0702595104.
Article CAS PubMed PubMed Central Google Scholar
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., Czempinski, K., and Hedrich, R. (2004) AtTPK4, an Arabidopsis tandem-pore K⁺ channel, poised to control the pollen membrane voltage in a pH- and Ca²⁺-dependent manner, Proc. Natl. Acad. Sci. USA, 101, 15621-15626, https://doi.org/10.1073/pnas.0401502101.
Article CAS PubMed PubMed Central Google Scholar
Rocchetti, A., Sharma, T., Wulfetange, C., Scholz-Starke, J., Grippa, A., Carpaneto, A., Dreyer, I., Vitale, A., Czempinski, K., and Pedrazzini, E. (2012) The putative K⁺ channel subunit AtKCO3 forms stable dimers in Arabidopsis, Front. Plant Sci., 3, 251, https://doi.org/10.3389/fpls.2012.00251.
Article PubMed PubMed Central Google Scholar
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 complex-regulated pollen hydration on the stigma: SPIK functions in pollen hydration on stigma, J. Integr. Plant Biol., 59, 604-611, https://doi.org/10.1111/jipb.12563.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1111/j.1742-4658.2011.08369.x.
Article CAS PubMed Google Scholar
Basu, D., and Haswell, E. S. (2017) Plant mechanosensitive ion channels: an ocean of possibilities, Curr. Opin. Plant Biol., 40, 43-48, https://doi.org/10.1016/j.pbi.2017.07.002.
Article CAS PubMed PubMed Central Google Scholar
Mori, K., Renhu, N., Naito, M., Nakamura, A., Shiba, H., Yamamoto, T., Suzaki, T., Iida, H., and Miura, K. (2018) Ca²⁺-permeable mechanosensitive channels MCA1 and MCA2 mediate cold-induced cytosolic Ca²⁺ increase and cold tolerance in Arabidopsis, Sci. Rep., 8, 550, https://doi.org/10.1038/s41598-017-17483-y.
Article CAS PubMed PubMed Central Google Scholar
Zhang, Z., Tong, X., Liu, S.-Y., Chai, L.-X., Zhu, F.-F., Zhang, X.-P., Zou, J.-Z., and Wang, X.-B. (2019) Genetic analysis of a Piezo-like protein suppressing systemic movement of plant viruses in Arabidopsis thaliana, Sci. Rep., 9, 3187, https://doi.org/10.1038/s41598-019-39436-3.
Article CAS PubMed PubMed Central Google Scholar
Véry, A.-A., and Sentenac, H. (2003) Molecular mechanisms and regulation of K⁺ transport in higher plants, Annu. Rev. Plant Biol., 54, 575-603, https://doi.org/10.1146/annurev.arplant.54.031902.134831.
Article PubMed Google Scholar
Vincent, T. R., Avramova, M., Canham, J., Higgins, P., Bilkey, N., Mugford, S. T., Pitino, M., Toyota, M., Gilroy, 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 calcium elevations in Arabidopsis during aphid feeding, Plant Cell, 29, 1460-1479, https://doi.org/10.1105/tpc.17.00136.
Article CAS PubMed PubMed Central Google Scholar
Fichman, Y., and Mittler, R. (2021) Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants, Plant J., 107, 7-20, https://doi.org/10.1111/tpj.15360.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1111/nph.17859.
Article CAS PubMed Google Scholar
Kong, D., Hu, H.-C., Okuma, E., Lee, Y., Lee, H. S., Munemasa, S., Cho, D., Ju, C., Pedoeim, L., Rodriguez, B., Wang, J., Im, W., Murata, Y., Pei, Z.-M., and Kwak, J. M. (2016) L-Met activates Arabidopsis GLR Ca²⁺ channels upstream of ROS production and regulates stomatal movement, Cell Rep., 17, 2553-2561, https://doi.org/10.1016/j.celrep.2016.11.015.
Article CAS PubMed Google Scholar
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, https://doi.org/10.1105/tpc.114.128082.
Article CAS PubMed PubMed Central Google Scholar
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, https://doi.org/10.1093/jxb/erac399.
Article CAS PubMed PubMed Central Google Scholar
Bellandi, A., Papp, D., Breakspear, A., Joyce, J., Johnston, M. G., de Keijzer, J., Raven, E. C., Ohtsu, M., Vincent, 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, https://doi.org/10.1126/sciadv.abo6693.
Article CAS PubMed PubMed Central Google Scholar
Hu, C., Duan, S., Zhou, J., and Yu, J. (2021) Characteristics of herbivory/wound-elicited electrical signal transduction in tomato, Front. Agr. Sci. Eng., 8, 292-301, https://doi.org/10.15302/J-FASE-2021395.
Article Google Scholar
Scherzer, S., Böhm, J., Huang, S., Iosip, A. L., Kreuzer, I., Becker, D., Heckmann, M., Al-Rasheid, K. A. S., Dreyer, I., and Hedrich, R. (2022) A unique inventory of ion transporters poises the Venus flytrap to fast-propagating action potentials and calcium waves, Curr. Biol., 32, 4255-4263.e5, https://doi.org/10.1016/j.cub.2022.08.051.
Article CAS PubMed Google Scholar
Hedrich, R., and Kreuzer, I. (2023) Demystifying the Venus flytrap action potential, New Phytol., 239, 2108-2112, https://doi.org/10.1111/nph.19113.
Article CAS PubMed Google Scholar
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, https://doi.org/10.3390/agronomy10101539.
Article CAS Google Scholar
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, https://doi.org/10.1073/pnas.1213931109.
Article PubMed PubMed Central Google Scholar
Choi, W.-G., Toyota, M., Kim, S.-H., Hilleary, R., and Gilroy, S. (2014) Salt stress-induced Ca²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants, Proc. Natl. Acad. Sci. USA, 111, 6497-6502, https://doi.org/10.1073/pnas.1319955111.
Article CAS PubMed PubMed Central Google Scholar
Kiep, V., Vadassery, J., Lattke, J., Maaß, J., Boland, W., Peiter, E., and Mithöfer, A. (2015) Systemic cytosolic Ca²⁺ elevation is activated upon wounding and herbivory in Arabidopsis, New Phytol., 207, 996-1004, https://doi.org/10.1111/nph.13493.
Article CAS PubMed Google Scholar
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 Channels 14 and 16 promote tolerance to heat and chilling in rice, Plant Physiol., 183, 1794-1808, https://doi.org/10.1104/pp.20.00591.
Article CAS PubMed PubMed Central Google Scholar
Finka, A., Cuendet, A. F. H., Maathuis, F. J. M., Saidi, Y., and Goloubinoff, P. (2012) Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance, Plant Cell, 24, 3333-3348, https://doi.org/10.1105/tpc.112.095844.
Article CAS PubMed PubMed Central Google Scholar

Download references

Funding

This work was financially supported by the Russian Science Foundation, grant 22-14-00388.

Author information

Authors and Affiliations

Department of Biophysics, Lobachevsky National Research State University of Nizhny Novgorod, 603950, Nizhny Novgorod, Russia
Maxim A. Mudrilov, Maria M. Ladeynova, Darya V. Kuznetsova & Vladimir A. Vodeneev

Authors

Maxim A. Mudrilov
View author publications
You can also search for this author in PubMed Google Scholar
Maria M. Ladeynova
View author publications
You can also search for this author in PubMed Google Scholar
Darya V. Kuznetsova
View author publications
You can also search for this author in PubMed Google Scholar
Vladimir A. Vodeneev
View author publications
You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Vladimir A. Vodeneev.

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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mudrilov, M.A., Ladeynova, M.M., Kuznetsova, D.V. et al. Ion Channels in Electrical Signaling in Higher Plants. Biochemistry Moscow 88, 1467–1487 (2023). https://doi.org/10.1134/S000629792310005X

Download citation

Received: 21 June 2023
Revised: 16 September 2023
Accepted: 18 September 2023
Published: 26 October 2023
Issue Date: October 2023
DOI: https://doi.org/10.1134/S000629792310005X

Keywords

Use our pre-submission checklist

Avoid common mistakes on your manuscript.