High-resolution non-contact measurement of the electrical activity of plants in situ using optical recording

The limitations of conventional extracellular recording and intracellular recording make high-resolution multisite recording of plant bioelectrical activity in situ challenging. By combining a cooled charge-coupled device camera with a voltage-sensitive dye, we recorded the action potentials in the stem of Helianthus annuus and variation potentials at multiple sites simultaneously with high spatial resolution. The method of signal processing using coherence analysis was used to determine the synchronization of the selected signals. Our results provide direct visualization of the phloem, which is the distribution region of the electrical activities in the stem and leaf of H. annuus, and verify that the phloem is the main action potential transmission route in the stems of higher plants. Finally, the method of optical recording offers a unique opportunity to map the dynamic bioelectrical activity and provides an insight into the mechanisms of long-distance electrical signal transmission in higher plants.

[1]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[2]  Alastair M. Glass,et al.  High−sensitivity optical recording in KTN by two−photon absorption , 1975 .

[3]  F. Baret,et al.  PROSPECT: A model of leaf optical properties spectra , 1990 .

[4]  E. Davies,et al.  Characteristics of action potentials in Helianthus annuus , 1991 .

[5]  Eric Davies,et al.  Characteristics of action potentials generated spontaneously in Helianthus annuus , 1995 .

[6]  M. Emri,et al.  Flow cytometric determination of absolute membrane potential of cells. , 1995, Journal of photochemistry and photobiology. B, Biology.

[7]  I. T. Young,et al.  Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy. , 1995, Biophysical journal.

[8]  Jose-Angel Conchello,et al.  Fluorescence photobleaching correction for expectation-maximization algorithm , 1995, Electronic Imaging.

[9]  K. Oparka,et al.  Sieve Elements and Companion Cells—Traffic Control Centers of the Phloem , 1999, Plant Cell.

[10]  Tadeusz Zawadzki,et al.  Transmission route for action potentials and variation potentials in Helianthus annuus L. , 2001 .

[11]  K. Muraki,et al.  Usefulness and limitation of DiBAC4(3), a voltage-sensitive fluorescent dye, for the measurement of membrane potentials regulated by recombinant large conductance Ca2+-activated K+ channels in HEK293 cells. , 2001, Japanese journal of pharmacology.

[12]  Vladimir G. Fast,et al.  Recording Action Potentials Using Voltage-Sensitive Dyes , 2005 .

[13]  P. Cheng Interaction of Light with Botanical Specimens , 2006 .

[14]  E. Van Volkenburgh,et al.  Shade-Induced Action Potentials in Helianthus annuus L. Originate Primarily from the Epicotyl , 2006, Plant signaling & behavior.

[15]  Hubert H. Felle,et al.  Systemic signalling in barley through action potentials , 2007, Planta.

[16]  Enrique Valentín Paravani,et al.  Photobleaching correction in fluorescence microscopy images , 2007 .

[17]  A. Schulz,et al.  Journal of Experimental Botany Advance Access published July 19, 2007 Journal of Experimental Botany, Page 1 of 12 , 2022 .

[18]  J. Fromm,et al.  Electrical signals and their physiological significance in plants. , 2007, Plant, cell & environment.

[19]  Jürgen Kurths,et al.  Phase Synchronization and Coherence Analysis: Sensitivity and specificity , 2007, Int. J. Bifurc. Chaos.

[20]  R. Hedrich,et al.  The use of voltage-sensitive dyes to monitor signal-induced changes in membrane potential-ABA triggered membrane depolarization in guard cells. , 2008, The Plant journal : for cell and molecular biology.

[21]  Frank W. Ohl,et al.  Normalization of Voltage-Sensitive Dye Signal with Functional Activity Measures , 2008, PloS one.

[22]  Ha-il Jung,et al.  Isolation of protoplasts from tissues of 14-day-old seedlings of Arabidopsis thaliana. , 2009, Journal of visualized experiments : JoVE.

[23]  F. Arecchi,et al.  Spatiotemporal dynamics of the electrical network activity in the root apex , 2009, Proceedings of the National Academy of Sciences.

[24]  Xiaojun Qiao,et al.  Research progress on electrical signals in higher plants , 2009 .

[25]  Guixue Bu,et al.  Uniform action potential repolarization within the sarcolemma of in situ ventricular cardiomyocytes. , 2009, Biophysical journal.

[26]  F. Maathuis,et al.  Vacuolar ion channels: Roles in plant nutrition and signalling , 2010, FEBS letters.

[27]  Walther Akemann,et al.  Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins , 2010, Nature Methods.

[28]  R. Lemoine,et al.  The phloem pathway: new issues and old debates. , 2010, Comptes rendus biologies.

[29]  M. Stolarz,et al.  Glutamate induces series of action potentials and a decrease in circumnutation rate in Helianthus annuus. , 2010, Physiologia plantarum.

[30]  Katsushige Sato,et al.  Functional development of the vagal and glossopharyngeal nerve-related nuclei in the embryonic rat brainstem: optical mapping with a voltage-sensitive dye , 2011, Neuroscience.

[31]  L. Wegner,et al.  A patch clamp study on the electro-permeabilization of higher plant cells: Supra-physiological voltages induce a high-conductance, K+ selective state of the plasma membrane. , 2011, Biochimica et biophysica acta.

[32]  Ernane José Xavier Costa,et al.  Original papers: The oscillatory bioelectrical signal from plants explained by a simulated electrical model and tested using Lempel-Ziv complexity , 2011 .

[33]  Patricio Oyarce,et al.  Evidence for the transmission of information through electric potentials in injured avocado trees. , 2011, Journal of plant physiology.

[34]  Igor R. Efimov,et al.  Optical Mapping of Action Potentials and Calcium Transients in the Mouse Heart , 2011, Journal of visualized experiments : JoVE.

[35]  H. Greppin,et al.  Accession-dependent action potentials in Arabidopsis. , 2011, Journal of plant physiology.

[36]  H. Oberleithner,et al.  Membrane potential depolarization decreases the stiffness of vascular endothelial cells , 2011, Journal of Cell Science.

[37]  A. Furch,et al.  (Questions)(n) on phloem biology. 1. Electropotential waves, Ca2+ fluxes and cellular cascades along the propagation pathway. , 2011, Plant science : an international journal of experimental plant biology.

[38]  J. Fromm,et al.  Generation, Transmission, and Physiological Effects of Electrical Signals in Plants , 2012 .

[39]  W. Stein,et al.  Simultaneous measurement of membrane potential changes in multiple pattern generating neurons using voltage sensitive dye imaging , 2012, Journal of Neuroscience Methods.

[40]  Jian Sun,et al.  An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. , 2012, Plant, cell & environment.

[41]  N. Yu,et al.  Changes in the power spectrum of electrical signals in maize leaf induced by osmotic stress , 2012 .

[42]  M. Maffei,et al.  Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. , 2012, Plant science : an international journal of experimental plant biology.

[43]  Vincent A. Pieribone,et al.  Single Action Potentials and Subthreshold Electrical Events Imaged in Neurons with a Fluorescent Protein Voltage Probe , 2012, Neuron.

[44]  A. Bel,et al.  Cellular Basis of Electrical Potential Waves along the Phloem and Impact of Coincident Ca2+ Fluxes , 2012 .

[45]  D. Maclaurin,et al.  Optical recording of action potentials in mammalian neurons using a microbial rhodopsin , 2011, Nature Methods.

[46]  C. Capurro,et al.  Cell Volume Regulation in Cultured Human Retinal Müller Cells Is Associated with Changes in Transmembrane Potential , 2013, PloS one.

[47]  Cheng Wang,et al.  Recording extracellular signals in plants: A modeling and experimental study , 2013, Math. Comput. Model..

[48]  A. Volkov,et al.  Morphing structures and signal transduction in Mimosa pudica L. induced by localized thermal stress. , 2013, Journal of plant physiology.

[49]  M. Hajirezaei,et al.  Electrical signaling along the phloem and its physiological responses in the maize leaf , 2013, Front. Plant Sci..

[50]  A. Volkov,et al.  Electrotonic and action potentials in the Venus flytrap. , 2013, Journal of plant physiology.

[51]  Godfrey L. Smith,et al.  Optical and electrical recordings from isolated coronary-perfused ventricular wedge preparations. , 2013, Journal of molecular and cellular cardiology.

[52]  E. Farmer,et al.  GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling , 2013, Nature.

[53]  Pavel M. Balaban,et al.  Biolistic delivery of voltage-sensitive dyes for fast recording of membrane potential changes in individual neurons in rat brain slices , 2013, Journal of Neuroscience Methods.

[54]  Susan Greenfield,et al.  High-resolution spatio-temporal bioactivity of a novel peptide revealed by optical imaging in rat orbitofrontal cortex in vitro: Possible implications for neurodegenerative diseases , 2013, Neuropharmacology.

[55]  An Liu,et al.  Visualization of synchronous propagation of plant electrical signals using an optical recording method , 2013, Math. Comput. Model..

[56]  Lyubov Katicheva,et al.  Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. , 2014, Plant, cell & environment.

[57]  Kurt I Anderson,et al.  Strategies to overcome photobleaching in algorithm-based adaptive optics for nonlinear in-vivo imaging , 2014, Journal of biomedical optics.

[58]  Zhongyi Wang,et al.  Spatio-temporal mapping of variation potentials in leaves of Helianthus annuus L. seedlings in situ using multi-electrode array , 2014, Scientific Reports.

[59]  Andrea Vitaletti,et al.  Forward and inverse modelling approaches for prediction of light stimulus from electrophysiological response in plants , 2014, 1410.5372.

[60]  Torsten Will,et al.  Spread the news: systemic dissemination and local impact of Ca²⁺ signals along the phloem pathway. , 2014, Journal of experimental botany.

[61]  Fast acquisition of action potentials in Arabidopsis thaliana , 2014 .

[62]  Andrea Vitaletti,et al.  Exploring strategies for classification of external stimuli using statistical features of the plant electrical response , 2015, Journal of The Royal Society Interface.

[63]  F. Baluška,et al.  The Electrical Network of Maize Root Apex is Gravity Dependent , 2015, Scientific Reports.