Membrane voltage as a dynamic platform for spatiotemporal signaling, physiological, and developmental regulation

Abstract

Membrane voltage arises from the transport of ions through ion-translocating ATPases, ion-coupled transport of solutes, and ion channels, and is an integral part of the bioenergetic “currency” of the membrane. The dynamics of membrane voltage—so-called action, systemic, and variation potentials—have also led to a recognition of their contributions to signal transduction, both within cells and across tissues. Here, we review the origins of our understanding of membrane voltage and its place as a central element in regulating transport and signal transmission. We stress the importance of understanding voltage as a common intermediate that acts both as a driving force for transport—an electrical “substrate”—and as a product of charge flux across the membrane, thereby interconnecting all charge-carrying transport across the membrane. The voltage interconnection is vital to signaling via second messengers that rely on ion flux, including cytosolic free Ca2+, H+, and the synthesis of reactive oxygen species generated by integral membrane, respiratory burst oxidases. These characteristics inform on the ways in which long-distance voltage signals and voltage oscillations give rise to unique gene expression patterns and influence physiological, developmental, and adaptive responses such as systemic acquired resistance to pathogens and to insect herbivory.

Electrical Signaling of Plants under Abiotic Stressors: Transmission of Stimulus-Specific Information

“…An AP in plants is a self-propagating electrical signal that obeys the “all-or-nothing” law, similar to APs in animals. That is, an excitable cell in which the threshold level of depolarization is reached will generate a standard electrical pulse, and its amplitude and duration will not depend on the parameters of the stimulus [ 6 , 253 , 254 ].…”

“…The duration of APs in locomotive plants is only several seconds, at a propagation speed of up to 8–9 cm/s, while in non-locomotive plants the duration reaches tens of seconds at a propagation speed of less than 3 cm/s [ 6 , 8 , 11 , 254 ]. There are also a few works showing a certain variability of AP parameters, depending on the direction of propagation and the organ from which the parameters are recorded [ 28 , 214 ].…”

“…Along with the analysis of the VP parameters themselves, such as the amplitude and duration, it is also important to consider their changes as the reaction propagates. The decrement in the amplitude and speed of a VP propagation is commonly considered a feature that distinguishes it from an AP [ 6 , 9 , 254 ]. Of note, the existence of a decrement is in good agreement with the concept that a VP is not a self-propagating electrical signal, but is a local electrical reaction induced by a hydraulic or chemical signal [ 6 , 9 , 254 ] (Box 1).…”

“…The decrement in the amplitude and speed of a VP propagation is commonly considered a feature that distinguishes it from an AP [ 6 , 9 , 254 ]. Of note, the existence of a decrement is in good agreement with the concept that a VP is not a self-propagating electrical signal, but is a local electrical reaction induced by a hydraulic or chemical signal [ 6 , 9 , 254 ] (Box 1). A comparative analysis of the decrement of VPs induced by different stimuli ( Figure 6 B,D,E) demonstrated the presence of a pronounced ES attenuation after burning and mechanical damage, whereas, under heating, the amplitudes of VPs in fact did not decrease [ 54 , 218 , 226 , 235 ].…”

“…When considering propagation of all types of ES, it is necessary to note the shifts in the concentrations of calcium and protons in cell cytoplasm and apoplasts associated with their generation [ 6 , 8 , 254 ]. It is known that the calcium signature determines the peculiar features of the functional response induced by the distant signal, in particular, gene expression and hormone production [ 8 , 37 , 42 ].…”