Evolution of long-distance signalling upon plant terrestrialization: comparison of action potentials in Characean algae and liverworts

Abstract

Background: In this review, we summarize data concerning action potentials (APs) - long-distance electrical signals in Characean algae and liverworts. These lineages are key in understanding the mechanisms of plant terrestrialization. Liverworts are postulated to be pioneer land plants, whereas aquatic charophytes are considered the closest relatives to land plants. The drastic change of the habitat was coupled with the adaptation of signalling systems to the new environment. Scope: APs fulfil the 'all-or-nothing' law, exhibit refractory periods and propagate with a uniform velocity. Their ion mechanism in the algae and liverworts consists of a Ca2+ influx (from external and internal stores) followed by/coincident with a Cl- efflux, which both evoke the membrane potential depolarization, and a K+ efflux leading to repolarization. The molecular identity of ion channels responsible for these fluxes remains unknown. Publication of the Chara braunii and Marchantia polymorpha genomes opened up new possibilities for studying the molecular basis of APs. Here we present the list of genes which can participate in AP electrogenesis. We also point out the differences between these plant species, e.g. the absence of Ca2+-permeable glutamate receptors (GLRs) and Cl-permeable SLAC1 channel homologues in the Chara genome. Both these channels play a vital role in long-distance signalling in liverworts and vascular plants. Among the common properties of APs in liverworts and higher plants is their duration (dozens of seconds) and the speed of propagation (mm s-1), which are much slower than in the algae (seconds, and dozens of mm s-1, respectively). Conclusions: Future studies with combined application of electrophysiological and molecular techniques should unravel the ion channel proteins responsible for AP generation, their regulation and transduction of those signals to physiological responses. This should also help to understand the adaptation of the signalling systems to the land environment and further evolution of APs in vascular plants.