Article

ISSN 0006-2979, Biochemistry (Moscow), 2023, Vol. 88, No. 10, pp. 1488-1503 © Pleiades Publishing, Ltd., 2023.

Russian Text © The Author(s), 2023, published in Biokhimiya, 2023, Vol. 88, No. 10, pp. 1800-1817.

1488

REVIEW

Changes in Activity of the Plasma Membrane H

-ATPase

as a Link Between Formation of Electrical Signals

and Induction of Photosynthetic Responses in Higher Plants

Ekaterina M. Sukhova

, Lyubov’ M. Yudina

, and Vladimir S. Sukhov

1,a

Lobachevsky State University of Nizhny Novgorod, 603022 Nizhny Novgorod, Russia

e-mail: vssuh@mail.ru

Received June 22, 2023

Revised September 5, 2023

Accepted September 13, 2023

Abstract— Action of numerous adverse environmental factors on higher plants is spatially-heterogenous; it means that in-

duction of a systemic adaptive response requires generation and transmission of the stress signals. Electrical signals(ESs)

induced by local action of stressors include action potential, variation potential, and system potential and they participate

in formation of fast physiological changes at the level of a whole plant, including photosynthetic responses. Generation

of these ESs is accompanied by the changes in activity of H

-ATPase, which is the main system of electrogenic proton

transport across the plasma membrane. Literature data show that the changes in H

-ATPase activity and related changes in

intra- and extracellular pH play a key role in the ES-induced inactivation of photosynthesis in non-irritated parts of plants.

This inactivation is caused by both suppression of CO

influx into mesophyll cells in leaves, which can be induced by the

apoplast alkalization and, probably, cytoplasm acidification, and direct influence of acidification of stroma and lumen of

chloroplasts on light and, probably, dark photosynthetic reactions. The ES-induced inactivation of photosynthesis results

in the increasing tolerance of photosynthetic machinery to the action of adverse factors and probability of the plant survival.

DOI: 10.1134/S0006297923100061

Keywords: higher plants, electrical signals, action potential, variation potential, system potential, H

-ATPase, intracellu-

larpH, extracellular pH, photosynthesis

Abbreviations: AP, action potential; ES, electric signal;

ROS,reactive oxygen species; SP,system potential; VP,vari-

ation potential.

* To whom correspondence should be addressed.

INTRODUCTION

Plants exist in unstable environment and could be

subjected to the action of adverse factors with many

of them affecting a plant in a spatially-heterogenous

manner (such as excessive illumination, high and low

temperatures, water deficit, biotic damage, and many

others). That is why plants must have a system of

‘long-distance’ stress signals, which appear in the zone

of the local effect and are transmitted into the intact

parts of the plant organism causing adaptive physiolog-

ical changes. Electrical signals (ESs) comprise an im-

portant group of stress signals affecting a wide range of

physiological processes and lead to the increase of toler-

ance of the pant to adverse factors[1-7].

ESs are reversible changes of electrical potential

differences on a plasma membrane that are capable of

propagating within the plant. The main approach of

measuring such electrical signals is the use of non-po-

larizing electrodes [1, 2]. In this case, when the mea-

suring electrodes are placed extracellularly they contact

with different parts of the plant surface, which allows

more effectively to investigate propagation of the signals;

in the case of intracellular placement of electrodes, the

measuring electrode is introduced inside the plant cell,

which allows to investigate parameters of ESs and their

ionic mechanisms in more details.

It is known that ESs could stimulate in higher plants

expression of protective genes (such as pin1, pin2, and

vsp2 participating in protection against insects [8, 9]),

production of stress-related phytohormones (for ex-

ample, abscisic and jasmonic acid [10-12]), activa-

tion of respiration [13-15], increase of ATP content

in leaves [16], as well as stop of assimilate movement

in phloem [17-19], changes in transpiration [20, 21],

ROLE OF H

-ATPase IN ES AND PHOTOSYNTHETIC RESPONSES 1489

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

slowing down growth processes [22], and many other re-

sponses. Role of ESs in the development of such phys-

iological responses is conformed by the association of

their parameters with characteristics of electrical signals

[2,6]. This role has been also demonstrated by revealing

induction of the physiological responses during imita-

tion of ES generation (treatment with inhibitors of pro-

ton transport or protonophores) and by suppression of

the response development during blocking of the signal

transduction by subjecting the stem to local effect of low

temperatures or sodium azide[2, 6, 13, 23]. In particu-

lar, it was shown that expression of the protective genes

occurs only in those Arabidopsis leaves where prolonged

ESs are generated or those subjected to direct effects of

electrical current[9].

Photosynthetic processes should be mentioned as a

separate ‘target’ of ESs, because it is known that elec-

trical signals could cause either short-term (5-10 min) or

long-term (tens of minutes, likely hours) inactivation of

photosynthesis [6, 7, 23]. Such inactivation is manifested

by decrease of photosynthetic assimilation of CO

[10,

11, 16, 20, 24], decrease of quantum yields of the pho-

tosystems I and II [25-27] and of non-cyclic electron

flow [28], and by the increase of non-photochemical

quenching of the chlorophyll fluorescence [14, 27-29] (in

particular of the energy-dependent component [30]), as

well as increase of the cyclic electron flow around the

photosystem I[28].

The presumed result of the ES-induced physiolog-

ical changes is increase of the plant organism tolerance

to adverse environmental factors [6, 7, 23, 31]. In par-

ticular, it was shown that propagation of ESs decreases

damage of cell membranes and photosynthetic apparatus

under excessive illumination [32, 33], decreases negative

effects of heat [33-39] and cold[34] on photosynthetic

processes, as well as increases resistance at the level of

whole plant to low [40] and high[36] temperatures.

Hence, ESs play an important role in the system-

ic adaptation of higher plants to unstable environmental

conditions [6, 7, 31]. Photosynthetic responses, develop-

ment of which important for formation of the ES-induced

increase of resistance of plants to adverse conditions,

provide significant contribution to this adaptation[23].

That is why the main goal of this review is analysis of

the pathways involved in formation of such responses for

different types of electrical signals, which are based on

their ionic mechanisms.

TYPES OF ELECTRICAL SIGNALS IN PLANTS

AND ROLE OF THE PLASMA MEMBRANE

-ATPase IN THEIR FORMATION

Action potential (AP), variation potential (VP), and

system potential (SP) are the main types of ESs in high-

er plants [5-7].

AP is a relatively short impulse reaction (tens of

seconds) appearing during local action of damaging

stressors (such as cooling by several degrees) that in-

volves two phases (depolarization and repolarization)[1,

6, 7](Fig.1). In higher plants this signal is character-

ized by the existence of potential generation threshold,

all-or-none type of signal initiation, prolonged refrac-

tory period (hours), and ability for active transmission

along the sieve elements and/or symplast parenchymal

cells of the plant vascular bundles via local electrical

currents in plasmodesmata.

It must be mentioned that the mechanisms of AP

generation are similar in higher plants and in Charo-

phyte algae, therefore ionic mechanism of AP and as-

sociation of its generation with the changes in activity

of proton transport were first demonstrated for Charo-

phyte algae [41-44] and later confirmed in higher plants.

Thefactor initiating generation of AP is depolarization

of the membrane potential to the threshold level result-

ing in activation of the voltage-gated Ca

-channels in

plasma membrane and influx of calcium ions into the

cell [1, 45-47]. Significant increase of Ca

concen-

tration in cytoplasm [47] results in activation of anion

channels and efflux of Cl

–

ions from the cell [45], as well

as in temporary inactivation of the plasma membrane

-ATPase [46]; these both processes lead to formation

of the depolarization phase of AP. Depolarization results

in activation of the outwardly-rectifying K

-channels

that mediate efflux of potassium ions from cytoplasm

into extracellular space [47]. Significant depolarization

also leads to the closing of Ca

-channels, decrease of

calcium ion concentration in cytoplasm, and, as a result,

decrease in activity of anion channels and re-activation

of H

-ATPase [47]. These processes result in formation

of the repolarization phase and return of the membrane

potential to the initial level.

Variation potential (VP) appears under the action

of damaging stressors (including burn, extreme heat,

mechanical damage); it has long duration (up to tens of

minutes and more) and complex shape[6, 23, 48] includ-

ing two components: prolonged depolarization wave and

AP-like spikes, which are not always observed (Fig. 2).

The AP-like spikes are typical action potentials induced

by the positive shift of membrane potential in the course

of formation of the long-term depolarization wave,

which have the same ionic mechanisms as AP [48];

at the same time, the long-term wave is the main com-

ponent of VP. One of the important features of VP (pre-

dominantly of the long-term depolarization wave) is

decrease of its transmission rate[49, 50] and/or its am-

plitude [16, 29, 50] with the increase of the distance

from the zone of damage.

VP comprises a local electrical response to trans-

mission of a signal with non-electrical nature[48], which

could be either hydraulic or chemical. The hydraulic

hypothesis [22, 48, 51, 52] suggests that during local

SUKHOVA et al.1490

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

Fig. 1. Action potential in higher plants and schematic representation of the mechanisms of its generation and transmission along the vascular

bundles in plants.

damages in the zone of the stressor action a region of

increased pressure is formed that induces transmission

of a fading hydraulic wave in the plant, which, in turn,

causes activation of the mechanosensitive Ca

-channels

followed by the development of VP [44]. Experimen-

tal [51] and theoretical [53] studies show that the de-

crease of amplitude of the hydraulic wave results in the

increase of the lag-phase before the changes of electrical

potential, and, thus, causes reduction of the apparent

rate of VP transmission with the increase of the distance

from the zone of the stressor action. Low amplitude of

the hydraulic wave does not cause formation of VP.

Alternative hypothesis suggests that the release of

a specific chemical compound (‘wound substance’) oc-

curs in the damaged zone, diffusion of which causes ac-

tivation of the ligand-dependent Ca

-channels and de-

velopment of VP [48]; low intensity of such signal does

not induce formation of the variation potential. H

often assumed as such wound substance [54-56]; how-

ever, participation of other compounds (such as systemin

[57] or glutamate [58]) cannot be ruled out. The key

problem of the chemical hypothesis is the low speed of

molecular diffusion of the wound substance[48]. There

are several approaches allowing to overcome this limita-

tion. Firstly, according to the Malone hypothesis [59],

which has been theoretically tested in a number of math-

ematical models [60, 61], local increase of pressure in

the zone of damage could result in emergence of addi-

tional flows of water along the xylem, which could bring

the wound substance to undamaged part of the plant.

Secondly, the possibility of accelerated spread of the

chemical agent within a plant, which likely is associated

with the enhancement of convective (turbulent) diffu-

sion in a fluid flow in the xylem, has been previously

shown in our studies[49, 62]. It must be mentioned that

despite the relatively low rates of fluid flow in the xy-

lem vessels, turbulent flows could potentially appear as

a result of periodic constriction of their diameter[62].

And, thirdly, according to the hypothesis suggested by

Mittleret al. [54] and developed further in the later stud-

ies [55, 56, 63], secondary generation of H

(based on

activation of Ca

-channels, increase of Ca

concentra-

tion that causes activation of NADPH oxidases RbohD

in the plasma membrane, which, in turn, produce reac-

tive oxygen species (ROS)) could occur during propa-

gation of the chemical signal; this secondary generation

could accelerate transmission of the chemical signal in

the plant. Both experimental data [63] demonstrating

propagation of the ROS wave (increase of their concen-

tration) and suppression of this wave under the action

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-ATPase IN ES AND PHOTOSYNTHETIC RESPONSES 1491

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

Fig. 2. Variation potential in higher plants and schematic presentation of the suggested mechanisms of its generation and transmission along the

vascular bundles in plants. Scheme of formation of long-term depolarization wave associated with high or medium increase of Ca

concentration

in cytoplasm is shown. Mechanisms of AP-like spikes are similar to AP mechanisms (see Fig.1) and are not shown in this figure.

of inhibitor of RbohD oxidases and the results of math-

ematical modeling support this hypothesis.

It is generally accepted that propagation of chem-

ical signal or of hydraulic wave results in the long-term

activation of the ligand-dependent or mechanosensitive

-channel in the plasma membrane, and, respective-

ly, influx of calcium ions into the cell [48]. Moderate (or

large) and long-term increase of Ca

concentration in

cytoplasm (500-600nM and above [49]) causes inacti-

vation of the H

-ATPase[64] and formation of the long-

term depolarization wave. In the background of this

wave, the membrane potential could reach the threshold

level and activate the voltage-gated Ca

-channels, thus

forming AP-like spikes, mechanism of which is similar

to the AP mechanism [48,49].

System potential (SP), which comprises a propa-

gating wave of hyperpolarization (Fig. 3), is the least

investigated type of electrical signals in plants [6]. It is

known that SP could appear in response to the action of

a wide spectrum of stressors including inorganic salts,

moderate and high heat, burn, mechanical damage, and

attacks of insects [9, 65-71]. In the process, the shape

and duration of SP could vary significantly depending

on the type of stressor, plant species, and distance from

the zone of damage [9, 65-71]. It must be mentioned

that SP could be closely associated with VP, because

(i) a number of stressors cause generation of VP close to

the damage zone, while SP appears at a larger distance

from it [9, 67, 69-71]; (ii) local burn causes VP in the

plants watered regularly, but could cause development of

SP under severe water deficit [69]; (iii) stressors could

cause VP during first exposure, and the repeated expo-

sure causes SP [66]; (iv) depending on location of the

zone of stressor action in the plant the same stressor

could cause either VP or SP [65].

It is generally considered that activation of the

-ATPase in plasma membrane is the main mecha-

nism of SP generation [66], which has been confirmed

by suppression of the signal during prior inhibition of this

transporter (sodium orthovanadate) and by induction

SUKHOVA et al.1492

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

Fig. 3. System potential in higher plants and schematic presentation of potential mechanism of its generation and propagation along the vascular

bundles in plants. Possible effects of a moderate increase of Ca

concentration in cytoplasm on H

-ATPase (activation) and on inwardly-rectify-

ing K

-channels of plasma membrane (inactivation) are shown by dashed lines.

of SP during local exposure to the H

-ATPase induc-

er (fusicoccin); however, nature of the signal causing

such activation is still undetermined. We have suggested

previously [69-71] that transmission of SP is associated

with propagation of the small-amplitude hydraulic sig-

nal, which activates mechanosensitive Ca

-channels in

the plasma membrane and causes moderate increase of

calcium ion concentration in cytoplasm. There are data

available [72,73] demonstrating that moderate increase

of Ca

concentration could cause activation of the

plasma membrane H

-ATPase, which, in turn, results

in hyperpolarization. On the other hand, a number of

studies show that the moderate increase of Ca

concen-

tration in cytoplasm (200-400 nM) causes inactivation

of the inwardly-rectifying K

-channel in the plasma

membrane [74,75], which mediates influx of potassium

ions from the extracellular space into the cell cytoplasm.

Considering that the inwardly-rectifying K

-channels

and H

-ATPase of plasma membrane are the main sys-

tems of electrogenic ion transport under rest condition

[47, 76, 77] (in accordance with the previously conduct-

ed theoretical analysis of the developed mathematical

model of electrogenesis in the cell of higher plants [47]),

decrease of permeability of K

-channels should result in

hyperpolarization. In the process, development of hy-

perpolarization would be due to decrease of the contri-

bution of electrical conductance of the inwardly-rectify-

ing K

-channels to the total conductance of the plasma

membrane. The latter could be confirmed by the chang-

es of membrane potential(E

) described in a simplified

manner by the equation(1):

+ g

1 + g

, (1)

where E

– electromotive force (EMF) of H

-ATPase

(around –450 mV) and E

 – Nernst potential for

potassium ions (around –100 mV; based on [49, 76,

77]) under conditions of reduction of conductance

of K

-channels (g

) with respect to conductance of

-ATPase (g

). The presented equation based on the

parallel electrical circuit of the inwardly-rectifying

-channels and H

-ATPase provides stationary solu-

tion for the membrane potential.

Hypothesis on inactivation of the inwardly-rec-

tifying K

-channels is in good agreement with the

suppression of generation of SP by the action of the

ROLE OF H

-ATPase IN ES AND PHOTOSYNTHETIC RESPONSES 1493

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

specific blocker of the K

-channels, tetraethyl ammo-

nium [65]. The main advantage of the suggested hy-

pothesis is its ability to explain association between VP

and SP, because the decrease of amplitude of the hy-

draulic wave (with the decrease of the stimulus strength

during drought development or with the increase of the

distance from the zone of stimulation [51, 53, 68-71])

should decrease influx of Ca

into the cell, which could

result in the change of the type of ES: long-term wave of

depolarization (in the case of large or moderate increase

of calcium ion concentration in cytoplasm) is replaced

with the hyperpolarization wave (in the case of slight

increase of Ca

concentration). However, it should be

mentioned that the suggested mechanism is potential-

ly compatible with the chemical hypothesis of the sig-

nal transmission; in this case induction of the calcium

ion influx could occur through the ligand-dependent

-channels[48].

Hence, common feature of AP, VP, and SP gen-

eration involves changes in activity of the H

-ATPase

in plasma membrane, which is in good agreement with

the key role of the P-type ATPases in maintenance of a

number of physiological processes in plants and in re-

sponses to the action of environmental factors [78, 79],

including changes in activity of H

-ATPase under the

action of abiotic and biotic stressors. The key mech-

anism of the changes of H

-ATPase activity is phos-

phorylation of amino acid residues of the R-domain

at the C-end of the enzyme [78, 79]: phosphorylation

of Thr947 facilitates attachment of the 14-3-3 proteins

to the C-end and causes activation of the enzyme; and,

on the contrary, phosphorylation of a number of other

amino acid residues disrupts binding of the 14-3-3 pro-

teins and results in inactivation of H

-ATPase. It must

be mentioned that the Ca

-dependent inactivation of

-ATPase, which could be prevented by the treat-

ment with the H-7protein kinase inhibitor [46] is like-

ly associated with phosphorylation of one of the amino

acid residues (Ser944, Thr942, Tyr946) and disruption

of binding of the 14-3-3 proteins to the C-end of the

enzyme [79].

It is likely that the direct contributions of the

-ATPase to formation of electrical signals vary. Inpar-

ticular, in the case of AP, elimination of the H

-ATPase

inactivation affects only slightly the shape and ampli-

tude of the signal, but completely suppresses the accom-

panying alkalization of apoplast [46, 47]. On the other

hand, inactivation of H

-ATPase is the main mecha-

nism of VP generation [48], because decrease of activ-

ity of this transporter results in significant suppression

of the long-term depolarization wave, which is the basis

of variation potential [49,64,80].

More complicated pattern is observed in the case

of SP. The main hypothesis [66, 67, 69-71] describing

mechanisms of SP suggests increase of the absolute ac-

tivity of H

-ATPase; however, this suggestion contra-

dicts the data on alkalization of apoplast during devel-

opment of the system potential [66]. Similar alkalization

observed during inactivation of H

-ATPase in the course

of generation of AP [46, 47] and VP [25, 27] more like-

ly indicates decrease of activity of this transporter.

The suggestion on increase of the relative activity of

-ATPase due to Ca

-dependent decrease of the ac-

tivity of inwardly-rectifying K

-channels[74, 75] is more

in line with such data, because development of hyper-

polarization should decrease active transport of protons

from the cell and results in alkalization of apoplast due

to increase of the proton electrochemical gradient di-

rected against such transport.

In conclusion to this section, it must mention spe-

cifically that the changes of pH that accompany the

changes of activity of the plasma membrane H

-ATPase

during development of ES are to a large degree associ-

ated with the existence of the oppositely directed proton

flows. In accordance with the mathematical model of

electrogenesis in the cells of higher plants previously de-

veloped in our work [47, 77], such flows may be due to

activities of H

-antiporters and 2H

/Cl

–

-symporters,

and leakage of protons through the plasma membrane.

In particular, such flows could facilitate rapid transport

of protons inside the cell during decrease of compen-

sating efflux of H

under conditions of H

-ATPase in-

activation. Potentially the abovementioned oppositely

directed proton flows could be regulated by certain fac-

tors. However, such regulation is not required for real-

istic description of electrical responses in plants during

modeling [47, 76, 77], that is why the hypothesis on reg-

ulation of the inward H

flows is, most likely, excessive

in the case of the cells of higher plants.

In general, participation of the changes of H

ATPase activity in generation of all main types of ESs

allows suggesting that such changes could play a certain

physiological role; in particular, the idea of involvement

of such changes in regulation of photosynthetic process-

es by electrical signals in higher plants attracts attention

of researchers [23].

CHANGES OF PLASMA MEMBRANE H

-ATPase

ACTIVITY AS A MECHANISM UNDERLYING

EFFECTS OF ELECTRICAL SIGNALS

ON PHOTOSYNTHESIS

As was mentioned above, there are several argu-

ments showing similarities in the decrease of absolute

activity of the plasma membrane H

-ATPase during

generation of all three types of ESs; first of all, this is

illustrated by the fact of alkalization of apoplast ob-

served during generation of AP [46, 47], VP[25, 27], and

SP[66]. If such decrease indeed causes the ES-induced

inactivation of photosynthesis, it can be expected that

this inactivation would be observed during propagation of

SUKHOVA et al.1494

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

all three types of ES. According to the literature data,

AP [14, 81, 82], VP [16, 24-30, 83], and SP [66, 71]

could cause similar changes in the intensity of photo-

synthetic processes including decrease of intensity of

assimilation, decrease of the quantum yield of the

photosystem II, and increase of non-photochemical

quenching of the chlorophyll fluorescence.

The ES-induced responses of photosynthesis in-

clude short-term (5-10 min) and long-term (tens of

minutes, and, probably hours) inactivation [6, 7, 23].

In some cases, only long-term inactivation could be ob-

served in plants (see, for example, papers published by

Hlaváckováet al. [10], Herdeet al. [84], andSherstne-

vaet al. [85]). It was shown in a number of studies [14,

26, 35] that the decrease of CO

concentration in the

medium results in inactivation of the light-dependent

reactions of photosynthesis similar to the one caused

by ES and reduces the amplitude of photosynthetic

responses induced by electrical signals; however, no

complete suppression of the short-term and long-term

changes of the parameters of the light-dependent reac-

tions has been observed. It has been suggested based on

this information[6, 23] that the short-term, and, proba-

bly, long-term inactivation of photosynthesis are associ-

ated with two different types of mechanisms:

(i) With the decrease of intensity of the dark reac-

tions of photosynthesis resulting in the decrease of the

ADP/ATP and NADP

/NADPH ratios in the chloro-

plast stroma and, respectively, in suppression of the pro-

cesses of the light-dependent reactions due to increase

of the electrochemical gradient on the thylakoid mem-

brane (results of reduction of H

-ATP-synthase activi-

ty due to substrate deficit) and disruption of the elec-

tron leakage from the electron-transport chain [14, 26].

Decrease of the leaf mesophyll conductance to CO

[24]

and, probably, closing of stomata [21] are the suggested

mechanisms of suppression of the dark reactions of pho-

tosynthesis.

(ii) With the suppression of the light reactions of

photosynthesis that is not caused by the inhibition of

Calvin cycle, which, potentially, also could have differ-

ent mechanisms (in particular, increase of non-photo-

chemical quenching [27, 29] and decrease of activity of

the ferredoxin-NADP

-reductase[26]).

There are several hypotheses explaining mecha-

nisms of photosynthesis inactivation[23]. Among them

suppression of activity of the Calvin cycle enzymes due

to influx of Ca

in the cytoplasm and further to chloro-

plast stroma [81] and inactivating effects of ROS (likely

) [83] should be mentioned. In the case of long-

term inactivation of photosynthesis involvement of the

stress hormones (abscisic and jasmonic acids [10, 11,

50]), which trigger stomata closing and suppression

of photosynthesis, has also been considered. At the

same time, reversible inactivation of plasma membrane

- ATPase seems to be the most plausible mechanism

of the development of the ES-induced photosynthet-

ic responses in plants [6, 23]. It must be mentioned,

first of all, that such inactivation could be the conse-

quence of all the mentioned mechanisms. In partic-

ular, it is known that the increase of calcium ion con-

centration could result in suppression of the plasma

membrane H

-ATPase [86], spread of H

is consid-

ered to be associated with activation of Ca

-channels,

influx of calcium ions, and inactivation of H

-ATPase

[6, 54-56]. The effect of abscisic acid on photosynthe-

sis also could be mediated by the decrease of activity

of H

-ATPase[87,88].

The results of our earlier studies [88, 89] demon-

strate that the moderate increase or decrease of the

initial activity of H

-ATPase in the plants treated with

activators (fusicoccin) or inhibitors (sodium orthovana-

date) of this ion transporter results, respectively, in the

increase or decrease of the photosynthetic response de-

veloping during the further induction of VP. These re-

sults confirm participation of H

-ATPase in formation

of the ES-induced changes in photosynthesis, because

while the value of relative change of its activity remains

constant, the absolute value of such change increases in

the case of prior activation of H

-ATPase or decreases

in the case of its prior inactivation, which would result

in the increase or decrease of the ES-induced photosyn-

thetic response, respectively.

Changes of intracellular and extracellular pH that

accompany inactivation of the H

-ATPase are consid-

ered as a possible mechanism of development of the

ES-induced photosynthetic responses [2, 6, 23]. Sev-

eral arguments exist supporting this hypothesis. Firstly,

it was shown in a considerable number of studies that

generation of different types of ES in plants is accompa-

nied with the increase of pH in apoplast, and decrease

of pH in cytoplasm [25, 27, 45, 46, 66, 85]. Moreover,

it was revealed by indirect methods that acidification

of the chloroplast stroma and lumen accompany gen-

eration of VP [90]. Furthermore, it was shown in some

studies [91, 92] that there is a strong association between

the changes of pH and parameters of photosynthesis,

which supports their role in induction of photosynthet-

ic responses. Secondly, it was shown that the artificial

induction of pH changes by exposure of leaves parts to

protonophores [27] or by inhibiting H

-ATPase activity

in protoplasts with sodium orthovanadate[89] results in

induction of photosynthetic responses, which are similar

to the ones observed during propagation of ES (decrease

of quantum yield of photosystem II and increase of

non-photochemical quenching). Thirdly, acidification

of the chloroplast incubation medium that mimics de-

crease of pH in cytoplasm during ES development also

induces photosynthetic responses similar to the respons-

es caused by electrical signals [25, 27, 85]; amplitude

of such responses linearly correlate with the degree of

pH changes[27, 85]. Similar effect was revealed during

ROLE OF H

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BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

perfusion of the cells of Charophyte algae with acidified

solutions [93].

It was shown in our previous studies [91, 92] that

the increase of extracellular pH accompanying VP is as-

sociated primarily with the decrease of photosynthetic

assimilation of CO

, while the decrease of intracellular

pH is associated with the increase of non-photochem-

ical fluorescence quenching. Based on these facts it

could be suggested [6, 23] that the ES-induced alkali-

zation of apoplast mainly affects supply of CO

to the

cells, while acidification of the cytoplasm, stroma, and

lumen of chloroplasts could directly affect reactions of

the light-dependent stage of photosynthesis. This sug-

gestion is in good agreement with the ES-induced de-

crease of conductance of the leaf mesophyll to CO

[24]

and with the observed changes of the light-dependent

reactions of photosynthesis induced by electrical signals,

which are not associated with inactivation of the dark

reactions[26,27,29].

The pH-dependent decrease of the CO

/HCO

–

ra-

tio could be suggested as a simple mechanism of the

effect of alkalization of apoplast on the supply of CO

into photosynthesizing cells [23], because the charged

form penetrates biological membrane much less than

the neutral one [94]. This suggestion was pre-confirmed

by the analysis of the simplified mathematical model

describing effects of inactivation of H

-ATPase on the

fraction of the neutral form of CO

[95]; however, fur-

ther investigation of the more detailed photosynthetic

model of a leaf did not confirm significant contribution

of this mechanism to the decrease of activity of photo-

synthesis during alkalization of apoplast (at least for the

stationary CO

flow described for an uniform apoplast

and used parameters of the model)[96,97].

The alternative hypothesis describing the ES-in-

duced effect of pH changes on the leaf mesophyll con-

ductance to CO

was suggested by Gallé et al. [24].

Inaccordance with this theory such changes affect con-

ductance of aquaporins, which play an important role in

supplying carbon dioxide to the cells of higher plants [98]

and could be controlled by pH [99-101]. Such hypoth-

esis is in good agreement with the results of modeling

[97] demonstrating dependence of the stationary inten-

sity of photosynthesis on the conductance of plasma

membrane to CO

; however, the literature data [99-101]

show that the conductance of aquaporins decreases with

acidification of cytoplasm, but not with alkalization of

apoplast. Despite the fact that both processes accom-

pany generation of ES [25, 27], our data indicate [91,

92] very weak association of the cytoplasm acidification

with the decrease of intensity of the dark reactions of

photosynthesis; in other words, there is certain contra-

diction between the hypothesis on participation of aqua-

porins in the development of ES-induced photosyn-

thetic responses and experimental peculiarities of these

responses.

Hence, the problem of specific mechanisms of

the effect of pH changes on the supply of CO

to me-

sophyll cells remains unsolved. Potentially the revealed

contradictions could be explained by uneven spatial dis-

tribution of carbonic anhydrases, which accelerate sig-

nificantly mutual conversion between CO

and HCO

–

because such heterogeneity could provide local pH-de-

pendent changes of the ratio between the neutral and

charged forms of carbon dioxide, which would affect its

penetration through the plasma membrane without sig-

nificant changes of the average concentration of these

forms in apoplast (in the suggested photosynthetic model

of a leaf [96, 97] such possibility was not considered).

Some studies demonstrating that carbonic anhydrases

and aquaporins function together in the plasma mem-

brane[102] and that carbonic anhydrases affect meso-

phyll conductance to CO

[103] provide support to this

hypothesis.

It must be mentioned that the ES-induced closing

of stomata, which could be involved in the long-term

inactivation of photosynthetic processes [21], is also

associated with the suppression of H

-ATPase activi-

ty, because the level of response could be modified by

changing initial activity of this transporter[36]. At the

same, the direct mechanism of the stomata closing is,

most likely, not inactivation of H

-ATPase, but rather

changes of activity of ion channels facilitated by this in-

activation, which results in the efflux of ions from the

guard cells. In particular, significant efflux of chloride

ions was demonstrated in a number of studies, which

accompanied generation of electrical signals of different

types [6,7,48,66].

Direct effect of the cytoplasm acidification on the

parameters of the light stage of photosynthesis is like-

ly due to the flow of protons from cytoplasm to stroma

and chloroplast lumen [23]. The decrease of pH in stro-

ma and lumen during development of VP was indirectly

confirmed in our previous study based on the measure-

ments of both the electrochromic shift of the leaf ab-

sorption and light scattering at 535 nm [90], which indi-

cate proton transport through chloroplast envelopes and

thylakoid membranes.

According to the studies by Alte et al. [104] and

Benz et al. [105], decrease of the chloroplast stroma

pH could cause increase of affinity of the ferredoxin-

NADP

-reductase to the specific binding sites (Tic62

and TROL), which results in the increase of the distance

between the enzyme and photosystem I, thus decreas-

ing electron flow at the acceptor part of this photo-

system. This mechanism is in agreement with the VP-

induced increase of losses at the acceptor side of the

photosystem I [26], which practically is independent

on the intensity of the dark reactions of photosynthe-

sis. It is likely that this mechanism could also facili-

tate the ES-induced activation of the cyclic electron

flow around the photosystem I [28], because decrease

SUKHOVA et al.1496

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

Fig. 4. Schematic presentation of possible pathways involving inactivation of the plasma membrane H

-ATPase in regulation of photosynthesis

by electrical signals. The variant suggesting participation of the inwardly-rectifying K

-channels in hyperpolarization is presented for SP.

ROLE OF H

-ATPase IN ES AND PHOTOSYNTHETIC RESPONSES 1497

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

of the non-cyclic flow, which competes for the substrate

(reduced ferredoxin) should result in the increase of

other flows using the same substrate [106].

The ES-induced acidification of the chloroplast lu-

men would firstly induce increase of the energy-depen-

dent component of the non-photochemical fluorescence

quenching, because electrical signals could cause signif-

icant increase of this component [30], for which close

association with the lumen pH was demonstrated [107-

109]. Direct decrease of the electron flow through the

photosynthetic electron-transport chain also could be the

result of acidification of the chloroplast lumen, because

one of the limiting steps of this process is oxidation of

plastoquinones in the cytochrome b

f complex [110, 111];

it is generally recognized that this step is highly sensi-

tive to the lumen pH and slows down with the increase

of proton concentration. Potentially, the component of

non-photochemical fluorescence quenching occurring

due to the shift of the main pigment–protein light-har-

vesting complex (state transition) could be another ‘tar-

get’ of the pH decrease in the chloroplast lumen [112],

as it has been shown [29] that in the absence of illumi-

nation and, correspondingly, change of the activity of the

dark reactions of photosynthesis, ES could cause chang-

es in the distribution of the absorbed light between the

photosystemsI andII.

Hence, the decrease of the absolute value of the

plasma membrane H

-ATPase activity, which accompa-

nies generation of AP, VP, and, likely, SP, results in the

increase of extracellular and decrease of intracellular pH

and, consequently, causes inactivation of photosynthesis

via several interrelated mechanisms(Fig.4).

One of the presumed results of the ES-induced

changes of photosynthesis in the intact parts of the plant

is increase of tolerance of the photosynthetic apparatus

to the action of stressors on these parts [6, 7, 23, 31].

This tolerance increase would be very significant for the

plant in the case if the local exposure to the stressor that

induces electrical signals, is a precursor of the action of

adverse factors on the other parts of the plant organ-

ism[6, 7]. The mechanisms of ES-induced increase of

the photosynthetic apparatus tolerance could be classi-

fied into several groups [6,7,23,31].

(i) Positive effect of ESs on tolerance of the pho-

tosystem II in the case of moderate intensity of the

stressors (exemplified with the higher and lower tem-

peratures)[34, 39] could be associated with the increase

of energy-dependent component of the non-photo-

chemical fluorescence quenching [30] and activation of

the cyclic electron flow [28], which represent effective

mechanisms of protection of the photosynthetic appara-

tus under the action of a wide spectrum of stresses [107-

100,113,114].

(ii) In the case of exposure to high temperature, ef-

fect of ESs on the stability of the photosynthetic appara-

tus has a more complicated nature[35, 36]: the decrease

of damage in the photosystem I is accompanied by the

enhanced damage of the photosystem II; these process-

es are interrelated [37]. This result could be explained by

the hypothesis[115, 116] suggesting that, under condi-

tions of extreme intensity of the stressor action, damage

of the photosystem II that is capable of relatively rapid

repair, could lead to preservation of the photosystem I

due to the stoppage of electron influx from water, de-

crease of the excessive reduction of the electron trans-

port chain, and, as a result, decrease of ROS generation.

It is worth mentioning that preservation of the photo-

system I is also important for the following repair of the

photosynthetic apparatus [23], because in this case func-

tioning of the cyclic electron flow and ATP synthesis is

preserved.

(iii) Considering that the increase of ATP content

in leaves is an important result of the ES-induced pho-

tosynthetic responses [16], it can be suggested that this

increase comprises the mechanism of acceleration of the

photosynthetic apparatus repair after the damaging ac-

tion of stressors. Positive effect of ATP on the resistance

of the photosynthetic apparatus in plants [117] and the

data on ES-induced acceleration of the photosystem II

repair [34] support this hypothesis.

Result of the ES-induced increase of stability of the

photosynthetic apparatus is general increase of the plant

resistance, which is manifested in the lesser suppression

of growth [36] and electrical activity [40] under condi-

tions of systemic exposure to stressors.

CONCLUSIONS

The presented review demonstrates that formation of

all types of electrical signals in higher plants is associat-

ed with the changes in activity of the plasma membrane

-ATPase; furthermore, inactivation of H

- ATPase

plays an important role in generation of action potentials

and variation potentials. In the case of system potential,

the problem of particular changes of the H

-ATPase ac-

tivity is more complicated: on the one hand, one cannot

rule out increase of the absolute activity of the trans-

porter, which could be due to the two-phase dependence

of the activity on Ca

concentration in cytoplasm (ac-

tivation with small increase of concentration and inac-

tivation with moderate and high increase). On another

hand, a number of arguments (alkalization of apoplast

during generation of system potential, role of potassium

channels in this generation) indicate high probability of

participation of the relative increase of the H

-ATPase

activity in the generation of system potential; this in-

crease is due to the Ca

-dependent inactivation of the

inwardly-rectifying K

-channels in plasma membrane

with slight increase of the calcium ion concentration.

Absolute activity of the H

-ATPase could decrease in

the process due to increase of the electrochemical

SUKHOVA et al.1498

BIOCHEMISTRY (Moscow) Vol. 88 No. 10 2023

proton gradient directed inward the cell during hyper-

polarization. Increase of the electrochemical gradi-

ent could also decrease total efficiency of H

transport

from the cell due to activation of the systems of second-

ary active transport (such as proton-anion symporter

[118]) and enhancement of passive H

flows into cyto-

plasm[119].

It seems likely that the decrease of absolute activity

of the plasma membrane H

-ATPase is the main mecha-

nism of inactivating effect of action potentials, variation

potentials, and, probably, system potential on photo-

synthesis. Inactivation of photosynthesis induced by the

electrical signals is manifested by the decrease of CO

assimilation, quantum yields of photosystems I and II,

and non-cyclic electron flow, and by the increase of

non-photochemical fluorescence quenching and cyclic

electron flow around the photosystem I. In the process,

the induced by electrical signals increase of pH in ap-

oplast facilitates decrease of CO

supply to the cell, in-

activation of the dark reactions of photosynthesis and,

as a result, suppression of the light-dependent reactions

of photosynthesis; in turn, decrease of pH in cytoplasm

and, as a result, in stroma and chloroplast lumen cause

additional suppression of the light-dependent reactions

of photosynthesis.

The result of the photosynthetic responses induced

by electrical signals is, most likely, increase of tolerance

of the photosynthetic apparatus to the action of stress-

ors and enabling its following repair. Such changes, in

turn, provide contribution to the general increase of re-

sistance of the plant to the systemic action of adverse

factors and facilitate the plant survival under changing

environmental conditions.

Contributions. All authors participated in formu-

lating concept of the paper, preparation of materials,

and writing the paper draft. V.S.S. edited final text of

the review.

Funding. This work was funded by the Russian

Science Foundation, grant no.21-74-10088.

Ethics declarations. The authors declare no conflict

of interests in financial or any other sphere. This article

does not contain any studies with human participants

or animals performed by any of the authors.

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