Ether anesthetics prevents touch-induced trigger hair calcium-electrical signals excite the Venus flytrap

Abstract

Plants do not have neurons but operate transmembrane ion channels and can get electrical excited by physical and chemical clues. Among them the Venus flytrap is characterized by its peculiar hapto-electric signaling. When insects collide with trigger hairs emerging the trap inner surface, the mechanical stimulus within the mechanosensory organ is translated into a calcium signal and an action potential (AP). Here we asked how the Ca2+ wave and AP is initiated in the trigger hair and how it is feed into systemic trap calcium-electrical networks. When Dionaea muscipula trigger hairs matures and develop hapto-electric excitability the mechanosensitive anion channel DmMSL10/FLYC1 and voltage dependent SKOR type Shaker K+ channel are expressed in the sheering stress sensitive podium. The podium of the trigger hair is interface to the flytrap’s prey capture and processing networks. In the excitable state touch stimulation of the trigger hair evokes a rise in the podium Ca2+ first and before the calcium signal together with an action potential travel all over the trap surface. In search for podium ion channels and pumps mediating touch induced Ca2+ transients, we, in mature trigger hairs firing fast Ca2+ signals and APs, found OSCA1.7 and GLR3.6 type Ca2+ channels and ACA2/10 Ca2+ pumps specifically expressed in the podium. Like trigger hair stimulation, glutamate application to the trap directly evoked a propagating Ca2+ and electrical event. Given that anesthetics affect K+ channels and glutamate receptors in the animal system we exposed flytraps to an ether atmosphere. As result propagation of touch and glutamate induced Ca2+ and AP long-distance signaling got suppressed, while the trap completely recovered excitability when ether was replaced by fresh air. In line with ether targeting a calcium channel addressing a Ca2+ activated anion channel the AP amplitude declined before the electrical signal ceased completely. Ether in the mechanosensory organ did neither prevent the touch induction of a calcium signal nor this post stimulus decay. This finding indicates that ether prevents the touch activated, glr3.6 expressing base of the trigger hair to excite the capture organ.

Diethyl ether anesthesia induces transient cytosolic [Ca2+] increase, heat shock proteins, and heat stress tolerance of photosystem II in Arabidopsis

“…Significantly upregulated GO-MF categories of “calcium ion binding” and “calmodulin binding” are in accordance with the role of Ca 2+ in signaling during anesthesia ( Figure 2F ). This finding is partially interesting in the view of recent studies showing that diethyl ether blocked wound-induced glutamate-dependent Ca 2+ transient and systemic response mediated by GLR channels in A. thaliana ( Jakšová et al, 2021 ) and D. muscipula ( Scherzer et al, 2022 ). Different kinetics of these [Ca 2+ ] cyt responses suggest participation of two different Ca 2+ channels.…”

“…Recent studies showed that the anesthetic diethyl ether strongly suppresses the sensing of different stimuli in plants (e.g., light, touch, or wounding, Milne and Beamish, 1999 ; De Luccia, 2012 ; Yokawa et al, 2018 ; Pavlovič et al, 2020 ; Böhm and Scherzer, 2021 ; Jakšová et al, 2021 ; Scherzer et al, 2022 ). Here we show it concomitantly triggers also a strong cellular response.…”

“…In previous studies, it was shown that plants exposed to diethyl ether anesthesia were neither able to sense mechanical stimuli, wounding, or light and lack also expressive motoric responses. For example, touch-induced leaf movement in sensitive plant Mimosa pudica , trap closing reactions in carnivorous plant Dionaea muscipula , trap bending movement in carnivorous sundew Drosera capensis and autonomous circumnutations movements of tendrils of pea ( Pisum sativum ) were completely stopped ( Milne and Beamish, 1999 ; De Luccia, 2012 ; Yokawa et al, 2018 ; Pavlovič et al, 2020 ; Böhm and Scherzer, 2021 ; Scherzer et al, 2022 ). We found that disappearance of some of these plant reactions were caused by inhibition of electrical signal generation and propagation, a target of anesthetics is remarkably similar to animal organisms.…”

“…Also in the case of Arabidopsis thaliana plants, in which motoric responses are not easily observable, etherized individuals lost ability of systemic electrical and Ca 2+ signals propagation from damaged to neighboring leaves after heat wounding ( Jakšová et al, 2021 ). Since electrical and Ca 2+ signal propagation is dependent on ligand-gated glutamate receptor like channels (GLRs, Mousavi et al, 2013 ; Toyota et al, 2018 ), and diethyl ether attenuated also glutamate-induced Ca 2+ signal ( Jakšová et al, 2021 ; Scherzer et al, 2022 ), GLR channels have been suspected as the possible targets of anesthesia in plants, like in animals. In the absence of electrical signals in etherized plants, the downstream sequence of events in systemic leaves were blocked, including accumulation of phytohormones of the jasmonates (JA) group and expression of JA-responsive genes, indicating the inhibition of sensing as well as responsive behavior in plants ( Pavlovič et al, 2020 ; Jakšová et al, 2021 ).…”

Mechanotransduction in the spotlight of mechano-sensitive channels

“…Figure 2: Phylogenetic distribution, membrane localization and functions of MSL, OSCA, MCA and Piezo channels. MSLs: Redox homeostasis and Membrane potential dissipation[101], Osmoprotection[102] [54],[103], Pollen rehydration[59], Root mechanosensitivity[31], Modulation of the susceptibility to Pseudomonas[58] [104], Long distance wound-induced electrical and Ca 2+ signaling[63],Cell swelling[60], Amplification of oscillatory signals[34], Prey recognition[65] [64]; OSCAs: Adaptation to osmotic stress[91], Candidate to drought stress tolerance[90], Candidate to abiotic stress tolerance[92], Immunity based stomatal closure [89], Osmotic signaling in guard cells and root cells[85]; MCAs: Gravity sensing[72], Osmotic signaling[74], Plant architecture[75],[76],[105], Penetration of the root[73] [71]; Piezos: Root apex mechanosensing[83]and root Ca 2+ signaling[83],[84], Immune response to virus[82], Regulation of vacuole shape[78] …”