Electrical Signals in Systemic Adaptive Response of Higher Plants: Integration Through Separation

Introduction

Terrestrial plants can be affected by action of changeable environmental conditions, including local action of numerous stressors. Induction of systemic adaptive responses on this action requires propagation of stress signals, including long-distance electrical signals (ESs),^1–3 which cause fast and long-term changes in physiological processes in plants.^4–6 These ESs are transient changes in the electrical potential across the plasma membrane induced by the local action of stressors; these changes can propagate into intact parts of plants.^6,7

ESs include action potential, variation potential, and system potential. ⁶ Action potential is a short-term depolarization spike (Fig. 1) induced by moderate local irritations and based on transient activation of Ca²⁺, anion, and K⁺ channels; ⁴ however, transient inactivation of H⁺-ATPase in the plasma membrane can also participate in generation of this signal. ⁸ Variation potential is a long-term depolarization signal with irregular shape; it is induced by local damages and is mainly based on the transient inactivation of H⁺-ATPase ⁹ caused by activation of Ca²⁺ channels in the plasma membrane and calcium ion influx. ¹⁰ System potential is a long-term hyperpolarization signal based on transient activation of H⁺-ATPase; ¹¹ its mechanisms require future investigations.

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FIG. 1.

Schematic figures of action potential, system potential, and variation potentials with different shapes. Arrow marks time of the local irritation. Variation potential includes a long-term depolarization and can additionally include action potential-like spike(s).

It should be noted that influence of system potential on physiological processes is weakly investigated. ⁶ As a result, we only analyze the depolarization ESs (action potential and variation potential) in this study; their influence on plant physiological processes can be considered as similar. ⁶

Influence of ESs on Physiological Processes and Plant Tolerance to Stressors

ESs strongly influence physiological processes inducing increase of expression of genes participating in plant defense against phytopathogens and insects,^6,12 stimulation of production of stress phytohormones (mainly, abscisic and jasmonic acids), ¹³ changes in photosynthetic processes (mainly, fast and long-term photosynthetic inactivation),^14,15 activation of respiration, ¹⁶ increase of adenosine triphosphate (ATP) content in leaves, ¹⁶ suppression of phloem mass flow, ¹⁷ changes in transpiration (short-term activation or inactivation and following long-term inactivation), ⁶ and others.

Mechanisms of influence of ESs on the most of physiological processes in plants require future investigations; however, ways of influence of action potential and variation potential on photosynthesis are relatively investigated now.^6,14,18 The ESs-related transient inactivation of H⁺-ATPase^8,9 increases pH in the apoplast ¹⁹ and decreases pH in the cytoplasm, ¹⁹ stroma, and lumen of chloroplasts; ²⁰ these pH changes suppress carbon dioxide (CO₂) flux into the cytoplasm and stroma, inactivate photosynthetic dark reactions, decrease activity of the electron-transport chain in chloroplasts, and, thereby, form the fast inactivation of photosynthesis. ¹⁴ It is interesting that similar mechanism is probable to cause ESs-induced activation of respiration. ²¹ The long-term photosynthetic inactivation is probable to be caused by stimulation of production of abscisic and jasmonic acids^22,23 because these phytohormones close stomata, decrease the mesophyll CO₂ conductance, and suppress photosynthetic dark reactions.^6,18

Earlier, we hypothesized^6,14 that increasing plant tolerance to action of stressors is caused by ESs-induced physiological changes, including the photosynthetic inactivation that modifies tolerance of a photosynthetic machinery to increased temperatures. ¹⁴ Other ESs-induced responses can also participate in increasing the plant tolerance to stressors; for example, stimulation of the defense gene expression^24,25 protects plant against biotic damages, and activation of respiration and increase of the ATP content contribute reparation after action of stressors. ¹⁴ Moreover, our previous review ¹⁷ shows that ESs is probable to stimulate a programmed cell death that can be also important for plant survival under action of stressors.

Thus, ESs can be considered as a mechanism of induction of the systemic adaptive response under the local action of stressors; that is, ESs participate in a plant integration under adverse conditions. However, some ESs-induced physiological changes can stimulate separation between cells, between parts of plants, and between plant and environment. We suppose that this separation plays positive role for the plant survival; this hypothesis is discussed in the further analysis.

ESs-Induced Separation Between Plant Cells

It is known that interactions between cells can be based on their direct connections through plasmodesmata, which are membrane-lined structures forming low-resistance pathway between neighboring plant cells (“symplastic way”), or on the common apoplastic volume (“apoplastic way”).^6,26

There are several arguments supporting influence of ESs on plasmodesmata. (i) Propagation of action potential, which is based on electrical connections between cells through plsmodesmata, ⁷ has a long-term refractory period (hours). ⁶ It can be explained by closing plasmodesmata after the action potential propagation. (ii) “Action potential-like” spikes, which can be component of variation potential (Fig. 1),^7,14 do not induce propagating action potentials. It can be also explained by closing plasmodesmata under generation of a long-term depolarization (another component of variation potential). (iii) It is known that increasing the cytoplasmic concentration of Ca²⁺ closes plasmodesmata ²⁷ and that Ca²⁺ influx is the first stage of generation of action potential and variation potential.^6,7,18 These last points show potential mechanism of the ESs-induced closure of plasmodesmata.

Our theoretical investigation ⁷ shows that weak electrical connections between cells decrease threshold of the ESs generation under the local irritations and restrict the action potential propagation from neighboring cells. The threshold decrease should stimulate generation of local electrical responses in cells under the direct action of stressors that can increase tolerance of these cells ²⁸ (e.g., through stimulation of K⁺ efflux ⁶ ).

Alternatively, this stimulation can contribute to induction of the programmed cell death in some sensitive cells; ¹⁸ it can be another mechanism of the whole plant tolerance to stressors. In contrast, the suppression of the propagation of secondary action potentials should eliminate induction of additional physiological responses (after induction of the initial physiological response caused by the first ES), which can be dangerous for plants. ⁶ Finally, it can be speculated that the closure of plasmodesmata can decrease transmission of infections, reactive oxygen species, disturbances in Ca²⁺ and H⁺ concentrations, and other potentially dangerous factors between cells.

Suppression of the apoplastic way of interaction between cells can be based on decreasing transport processes across the plasma membrane. The transient inactivation of H⁺-ATPase, which is an energy source of the most of transporters in the plasma membrane, ²⁹ accompanies generation of the action potential ⁸ and variation potential. ⁹ This inactivation decreases activity of transporters in the plasma membrane ⁶ and can be mechanism of the apoplastic way suppression. At least, a positive effect of this suppression on the cell tolerance to stressors can be based on decreasing ATP consumption and increasing its content in cells that facilitates adaptive changes and stimulates reparation of damaged cell structures.^6,14,30

Another mechanism of the ESs-induced suppression of the apoplastic way is based on the decreasing rate of photosynthetic dark reactions ³¹ (through decreasing the mesophyll CO₂ conductance ³² ) and stimulation of respiration.^33,34 Both processes increase ATP content ¹⁶ (this increase can be up to 50% under the photosynthetic inactivation and up to 20% under the respiration activation; the initial ATP content in leaf is 66–77 nmol/g fresh weight) and should decrease sucrose concentration in leaf cells because the inactivation of photosynthetic dark reactions suppresses its production, and the respiration activation stimulates its consumption.

Sucrose is known to be transported from mesophyll cells to the apoplast through specific sucrose transporters (SWEETs) and to be transported from the apoplast into phloem sieve elements through H⁺-sucrose symporter.^14,35 It means that decreasing sucrose efflux suppresses interaction between cells based on the apoplastic sucrose concentration and contributes to storage of energy (ATP) in separate cells ¹⁶ that should positively influence their tolerance to action of stressors.^6,14

Thus, the ESs-induced separation between cells based on the symplastic way suppression can stimulate individual cell adaptive responses on action of stressors, eliminate dangerous secondary propagation of ESs, and, probably, decrease transmission of damaging factors between cells. In contrast, the ESs-induced separation based on the apoplastic way suppression can increase ATP content in individual cells and, thereby, should contribute increasing their tolerance to stressors.

ESs-Induced Separation Between Parts of Plants

The ESs-induced separation between parts of plants can be based on influence of ESs on the phloem transport. It is known that ESs can disrupt the phloem loading in plants; ³⁶ this response is probable to be related to inactivation of H⁺-ATPases, decrease of a proton gradient across the plasma membrane, and suppression of activity of H⁺-sucrose symporter in the sieve elements. ¹⁴ Another way of the ESs influence on the phloem transport is based on an induction of callose deposition, which causes sieve plate occlusion and suppresses the phloem mass flow. ¹⁷ This response is mediated by the Ca²⁺ influx; its characteristics are dependent on type of ES: ¹⁷ from the detachment/swelling of forisomes, which are protein-bodies controlling the phloem transport between sieve elements in Ca²⁺-dependent manner, and dispersion of forisome ends (action potential) to the full forisome dispersion and callose deposition (burning-induced variation potential).

These ESs-induced changes in the phloem transport decrease connections between the individual leaf and other parts of plant, including other leaves. There are several potential ways of influence of this separation between parts of plant on its tolerance to action of stressors. First, the disruption of the sucrose loading into sieve elements should increase sucrose concentration in the apoplast. SWEETs are known to can participate in two-direction sucrose transport; ³⁵ it means that ESs-induced increasing the apoplastic sucrose concentration should increase the cytoplasmic sucrose concentration and, thereby, stimulate respiration and ATP production. As noted earlier, the increased ATP content increases plant tolerance to stressors.^6,14,18,30

Second, the suppression of the phloem mass flow and blocking of sieve elements should additionally increase the apoplastic sucrose concentration; however, this response can also prevent transmission of infections and other potentially dangerous factors between parts of plant through the phloem vessels.^6,18 It is probable that the last effect participates in localization of damage in the restricted zone and, thereby, protects other parts of plant. In addition, the long-distance propagation of action potential^4,5 is known to be related to sieve elements; it means that propagation of the potentially dangerous secondary ESs through plant should be suppressed by blocking the phloem mass flow in these elements.

Third, it can be speculated that blocking sieve elements can be the initial step of death of some part of the plant (e.g., through induction of the programmed cell death, which can be induced by ESs ³⁷ ) to protect other parts of plant under action of stressors.

Thus, the ESs-induced disruption of the phloem transport stimulates the separation between parts of plant. This separation can participate in the adaptive response through the ATP content increase, localization of infections and other dangerous factors, supporting long-term refractory period after the ES propagation, and maybe stimulation of death of some parts of the plant.

ESs-Induced Separation Between Plant and Environment

The ESs-induced separation between plant and environment is mainly related to closing stomata because ESs (especially, variation potential) often decrease the leaf water conductance and aperture of stomata for long-term time intervals;^38,39 duration of the stomata response can be up to 1 h and more.^6,38 The ESs-related transient inactivation of H⁺-ATPase is a probable mechanism of closing stomata because modification in activity of this transporter strongly influences this response.^14,40 There are several ways of the positive influence of this separation on the plant tolerance to stressors:^6,18 the long-term closure of stomata (i) restricts a passage of phytopathogens (or, maybe, other damaging factors) into leaves, (ii) decreases water loss in plants, and (iii) suppresses the CO₂ flux into leaves and, thereby, photosynthetic dark reactions; it is known that this suppression can positively influence the photosynthetic machinery tolerance to stressors. ⁴¹

Thus, ESs stimulate separation between plant and environment (through the long-term closure of stomata) that can also play adaptive role.

Conclusions

ESs, which are induced by local irritations, influence numerous physiological processes in plants and increase their tolerance to stressors providing induction of the systemic adaptive response. However, ESs-caused physiological changes can also induce separations between cells, between parts of plants, and between plant and environment. In this study, we theoretically discuss ways of induction of these separations and their potential role for the plant tolerance to action of stressors. Figure 2 summarizes results of our investigation and shows participation of the separation in the ESs-induced systemic adaptive response in plants.

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FIG. 2.

Scheme of influence of electrical signals on separation between cells, between parts of plants, and between plant and environment, and participation of these separations in the ESs-induced systemic adaptive response in plants (see sections “ESs-Induced Separation Between Plant Cells”, “ESs-Induced Separation Between Parts of Plants”, and “ESs-Induced Separation Between Plant and Environment” for details). ESs are electrical signals in plants.