Slow wave potentials - A propagating electrical signal unique to higher plants

Abstract

Plants have at least three kinds of propagating electrical signals. In addition to a sustained wound potential (WP) that stops a few millimeters from dying cells, these signals are action potentials (APs) and slow wave potentials (SWPs). All three signals consist of a transient change in the membrane potential of plant cells (depolarization and subsequent repolarization), but only SWPs and APs make use of the vascular bundles to achieve a potentially systemic spread through the entire plant. The principal difference used to differentiate SWPs from APs is that SWPs show longer, delayed repolarizations. Unfortunately, SWP repolarizations also show a large range of variation that makes a distinction difficult. SWPs and APs do differ more clearly, however, in the causal factors stimulating their appearance, the ionic mechanisms of their depolarization and repolarization phases as well as the mechanisms and pathways of propagation. The depolarizations of a SWP arise with an increase in turgor pressure cells experience in the wake of a hydraulic pressure wave that spreads through the xylem conduits after rain, embolism, bending, local wounds, organ excision and local burning. The generation of APs occurs under different environmental and internal influences (e.g. touch, light changes, cold treatment, cell expansion) that - mediated through varying generator potentials - trigger a voltage-dependent depolarization spike in an all-or-nothing manner. While APs and WPs can be triggered in excised organs, SWPs depend on the pressure difference between the atmosphere and an intact plant interior. High humidity and prolonged darkness will also suppress SWP signaling. The ionic mechanism of the SWP is thought to involve a transient shutdown of a P-type H+-ATPase in the plasma membrane and differs from the mechanism underlying APs. Another defining characteristic of SWPs is the hydraulic mode of propagation that enables them - but not APs - to pass through killed or poisoned areas. Unlike APs they can easily communicate between leaf and stem. SWPs can move in both directions of the plant axis, while their amplitudes show a decrement of about 2.5% cm-1 and move with speeds that can be slower than APs in darkness and faster in bright light. The SWPs move with a rapid pressure increase that establishes an axial pressure gradient in the xylem. This gradient translates distance (perhaps via changing kinetics in the rise of turgor pressure) into increasing lag phases for the pressure-induced depolarizations in the epidermis cells. Haberlandt (1890), after studying propagating responses in Mimosa pudica, suggested the existence of hydraulically propagated electric potentials at a time when only APs were conceivable. It took a century to realize that such signals do exist and that they coincide with the characteristics of SWPs rather than those of APs. Moreover, we begin to understand that SWPs are not only ubiquitous among higher plants but represent a unique, defining characteristic without parallels in lower plants or animals.