Action potentials induce biomagnetic fields in carnivorous Venus flytrap plants

Geoffrey Z. Iwata,Rainer Hedrich,Jens Voigt,Lykourgos Bougas,Sönke Scherzer,Dmitry Budker,Katharina Rolfs,Anne Fabricant,Anna Jodko-Władzińska

doi:10.1038/s41598-021-81114-w

Abstract

Upon stimulation, plants elicit electrical signals that can travel within a cellular network analogous to the animal nervous system. It is well-known that in the human brain, voltage changes in certain regions result from concerted electrical activity which, in the form of action potentials (APs), travels within nerve-cell arrays. Electro- and magnetophysiological techniques like electroencephalography, magnetoencephalography, and magnetic resonance imaging are used to record this activity and to diagnose disorders. Here we demonstrate that APs in a multicellular plant system produce measurable magnetic fields. Using atomic optically pumped magnetometers, biomagnetism associated with electrical activity in the carnivorous Venus flytrap, Dionaea muscipula, was recorded. Action potentials were induced by heat stimulation and detected both electrically and magnetically. Furthermore, the thermal properties of ion channels underlying the AP were studied. Beyond proof of principle, our findings pave the way to understanding the molecular basis of biomagnetism in living plants. In the future, magnetometry may be used to study long-distance electrical signaling in a variety of plant species, and to develop noninvasive diagnostics of plant stress and disease.

Highlights

In the plant kingdom, electrical signaling pathways are involved in reception and transduction of external stimuli such as light1, temperature2, touch3,4, wounding[5], and chemicals[6]
We conclude that the temperature “switch” of the Dionaea action potentials (APs) is based on a calcium-dependent process
Our experiments indicate that at temperatures of T ≲ 34 °C the cellular Ca2+ level remains below threshold, but at T ≳ 34 °C there is enough chemical energy to open a critical number of anion channels, driving the fast depolarization phase of the AP

Summary

Introduction

Electrical signaling pathways are involved in reception and transduction of external stimuli such as light1, temperature2, touch3,4, wounding[5], and chemicals[6]. In 60 independent experiments using 10 different traps from 10 different plants, we recorded the temperature at which an AP was first induced When these data were plotted as temperature-dependent AP-firing probability (Fig. 2B), the curve could be well-fitted by a single Boltzmann equation characterized by a 50% AP-firing probability at 33.8 °C. Increasing the thermal energy input changed the probability for an AP to be fired, and led to an increased AP amplitude and decreased half-depolarization time (Supplementary Information) These facts indicate that heat-sensitive ion channels trigger and shape the AP: at higher temperatures, thermal energy input causes more closed Ca2+-activated anion channels to open and depolarize the membrane potential. Fast repolarization (mediated by K + channels) and transient hyperpolarization (caused by depolarization activation of outward-directed protein pumps) were

Methods

Findings

Conclusion