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 Ca 2+ 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 the repolarization. The molecular identity of ion channels responsible for these fluxes remains unknown. Publication of the Chara braunii and Marchantia polymorpha genomes opened 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 Ca 2+-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 the duration of APs (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 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.

Rapid propagation of Ca2+waves and electrical signals in a liverwortMarchantia polymorpha

“…TEA inhibits depolarization of cell membrane potential in Conocephalum conicum and Physcomitrium ( Physcomitrella) patens (Trebacz et al 1989, Johannes et al 1997). In Conocephalum , the equilibrium potential of K + is higher than the resting membrane potential, opening of the K + channel may induce depolarization of the membrane potential (Trebacz et al 1994, Kisnieriene et al 2022). Furthermore, simultaneous measurement of [Ca 2+ ] cyt and surface potential revealed that these two signals are tightly interconnected (Fig.…”

Nanopore direct RNA sequencing provides additional insight into transcriptome differentiation during transition to the aquatic environment of amphibious liverwort Riccia fluitans L. (Marchantiales)

“…Comparative transcriptomics of amphibious plants grown submerged versus on land reveal differentially expressed genes involved in underwater acclimation like cuticle and stomatal development, cell elongation, and modi ed photosynthesis [8]. Genomics has also uncovered key roles of plant hormones in regulating heterophylly [13]. Moreover, comparative genomics between aquatic and terrestrial species identify genomic signatures enabling adaptation to submerged life, including changes in submergence tolerance, light sensing, and carbon assimilation genes [14].…”

Epitranscriptome insights into Riccia fluitans L. (Marchantiophyta) aquatic transition using nanopore direct RNA sequencing

“…Comparative transcriptomics of amphibious plants grown submerged versus on land reveal differentially expressed genes involved in underwater acclimation like cuticle and stomatal development, cell elongation, and modified photosynthesis [ 8 ]. Genomics has also uncovered key roles of plant hormones in regulating heterophylly [ 13 ]. Moreover, comparative genomics between aquatic and terrestrial species identify genomic signatures enabling adaptation to submerged life, including changes in submergence tolerance, light sensing, and carbon assimilation genes [ 14 ].…”