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

Abstract

In response to both biotic and abiotic stresses, vascular plants transmit long-distance Ca2+and electrical signals from localized stress sites to distant tissues through their vasculature. Various models have been proposed for the mechanisms underlying the long-distance signaling, primarily centered around the presence of vascular bundles. We here demonstrate that the non-vascular liverwortMarchantia polymorphapossesses a mechanism for propagating Ca2+waves and electrical signals in response to wounding. The propagation velocity of these signals was approximately 1-2 mm/s, equivalent to that observed in vascular plants. Both Ca2+waves and electrical signals were inhibited by La3+as well as tetraethylammonium chloride, suggesting crucial importance of both Ca2+channel(s) and K+channel(s) in wound-induced membrane depolarization as well as the subsequent long-distance signal propagation. Simultaneous recordings of Ca2+and electrical signals indicated a tight coupling between the dynamics of these two signaling modalities. Furthermore, molecular genetic studies revealed that a GLUTAMATE RECEPTOR-LIKE (GLR) channel plays a central role in the propagation of both Ca2+waves and electrical signals. Conversely, none of the three two-pore channels (TPCs) were implicated in either signal propagation. These findings shed light on the evolutionary conservation of rapid long-distance Ca2+wave and electrical signal propagation involving GLRs in land plants, even in the absence of vascular tissue.