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

Martina Klejchova,Jonas Chaves Alvim,Fernanda A L Silva-Alvim,Michael R Blatt

doi:10.1093/plphys/kiab032

Martina Klejchova, Jonas Chaves Alvim + Show 2 more

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https://doi.org/10.1093/plphys/kiab032

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Journal: Plant physiology	Publication Date: Feb 3, 2021
Citations: 25	License type: CC BY 4.0

Affiliation: University of Glasgow

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.

Highlights

Voltage is, at once, one of the simplest of membrane variables to quantify and one of the most challenging to comprehend
In terrestrial plants, membrane voltage transients may propagate along vascular traces, both through the parenchymal cells lining the xylem and through the phloem. Propagation of such voltage transients is associated with glutamate receptor-like channels that may contribute to plasma membrane Ca2 + flux and [Ca2 + ]i elevations
The mechanistic connection to membrane voltage was made by Grabov and Blatt (1998), who reported cyclic [Ca2 + ]i increases in guard cells, recorded with the Ca2 + -sensitive dye Fura2, when the plasma membrane hyperpolarized and quantified this dependence under voltage clamp. Their studies led to the identification of the dominant, voltage-activated Ca2 + channel in the guard cell plasma membrane that is activated by the water-stress hormone abscisic acid (ABA) (Hamilton et al, 2000, 2001) and by redox stress (Pei et al, 2000), and to its role in triggering endomembrane Ca2 + release (Grabov and Blatt, 1999; Garcia-Mata et al, 2003)

Summary

Introduction

At once, one of the simplest of membrane variables to quantify and one of the most challenging to comprehend. Propagation of such voltage transients is associated with glutamate receptor-like channels that may contribute to plasma membrane Ca2 + flux and [Ca2 + ]i elevations.

Results

Conclusion