Channelrhodopsin-mediated optogenetics highlights a central role of depolarization-dependent plant proton pumps

In plants, environmental stressors trigger plasma membrane depolarizations. Being electrically interconnected via plasmodesmata, proper functional dissection of electrical signaling by electrophysiology is basically impossible. The green alga Chlamydomonas reinhardtii evolved blue light-excited chan...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2020-08, Vol.117 (34), p.20920-20925
Hauptverfasser: Reyer, Antonella, Häßler, Melanie, Scherzer, Sönke, Huang, Shouguang, Pedersen, Jesper Torbøl, Al-Rascheid, Khaled A. S., Bamberg, Ernst, Palmgren, Michael, Dreyer, Ingo, Nagel, Georg, Hedrich, Rainer, Becker, Dirk
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container_issue 34
container_start_page 20920
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 117
creator Reyer, Antonella
Häßler, Melanie
Scherzer, Sönke
Huang, Shouguang
Pedersen, Jesper Torbøl
Al-Rascheid, Khaled A. S.
Bamberg, Ernst
Palmgren, Michael
Dreyer, Ingo
Nagel, Georg
Hedrich, Rainer
Becker, Dirk
description In plants, environmental stressors trigger plasma membrane depolarizations. Being electrically interconnected via plasmodesmata, proper functional dissection of electrical signaling by electrophysiology is basically impossible. The green alga Chlamydomonas reinhardtii evolved blue light-excited channelrhodopsins (ChR1, 2) to navigate. When expressed in excitable nerve and muscle cells, ChRs can be used to control the membrane potential via illumination. In Arabidopsis plants, we used the algal ChR2-light switches as tools to stimulate plasmodesmata-interconnected photosynthetic cell networks by blue light and monitor the subsequent plasma membrane electrical responses. Blue-dependent stimulations of ChR2 expressing mesophyll cells, resting around −160 to −180 mV, reproducibly depolarized the membrane potential by 95 mV on average. Following excitation, mesophyll cells recovered their prestimulus potential not without transiently passing a hyperpolarization state. By combining optogenetics with voltage-sensing microelectrodes, we demonstrate that plant plasma membrane AHA-type H⁺-ATPase governs the gross repolarization process. AHA2 protein biochemistry and functional expression analysis in Xenopus oocytes indicates that the capacity of this H⁺ pump to recharge the membrane potential is rooted in its voltageand pH-dependent functional anatomy. Thus, ChR2 optogenetics appears well suited to noninvasively expose plant cells to signal specific depolarization signatures. From the responses we learn about the molecular processes, plants employ to channel stress-associated membrane excitations into physiological responses.
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subjects Adenosine triphosphatase
Algae
Aquatic plants
Biological Sciences
Depolarization
Electric potential
Electrophysiology
Environmental stress
Excitation
Functional anatomy
Gametocytes
Genetics
H+-transporting ATPase
Hydrogen
Hyperpolarization
Information processing
Membrane potential
Membranes
Mesophyll
Microelectrodes
Muscles
Oocytes
Optics
pH effects
Photosynthesis
Physiological responses
Plant cells
Plasmodesmata
Switches
Voltage
title Channelrhodopsin-mediated optogenetics highlights a central role of depolarization-dependent plant proton pumps
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