Environmental stimuli and physiological responses: The current view on electrical signalling

Abstract Electrical signals have been studied in numerous species so far. It appears that two main types of such signals occur in plants, rapid action potentials (APs) and slower variation potentials (VPs). While APs are generally evoked by non-invasive stimuli and follow the all-or-nothing principle as in neurons, VPs are mostly triggered by wounding and do not follow the all-or-nothing law. They are correlated to the stimulus strength and last longer than APs. The transmission of both, APs and VPs, occurs via the phloem over long distances and via plasmodesmata over short distances from cell to cell. Regarding physiological functions of electrical signals, numerous examples exist. They regulate rapid leaf movements in order to catch insects and for instance, affect nutrient uptake, gene expression and phloem transport. Recently, it was shown that apart from hydraulic signals, electric signals also play a significant role in root-to-shoot communication of drought-stressed plants. Re-irrigation of plants after soil drying initiates rapid hydraulic as well as electric signalling which affects the gas exchange of leaves. In addition, evidence was found for a link between electrical signals and photosynthesis as well as respiration. Wound-induced VPs cause a transient suppression in photosynthetic activity and an increase in respiratory CO2 release. The results led us to conclude that different stimulation types trigger characteristic electrical signals each with specific influence on physiological processes.

[1]  M. Filek,et al.  The effect of wounding the roots by high temperature on the respiration rate of the shoot and propagation of electric signal in horse bean seedlings (Vicia faba L. minor) , 1997 .

[2]  J. Fromm,et al.  Electrical signaling and gas exchange in maize plants of drying soil , 1998 .

[3]  A. L. Houwink,et al.  The conduction of excitation in Mimosa pudica , 1935 .

[4]  Alexander G. Volkov,et al.  Plants as Environmental Biosensors , 2006, Plant signaling & behavior.

[5]  I. Newman,et al.  Proton and calcium flux oscillations in the elongation region correlate with root nutation. , 1997, Physiologia plantarum.

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

[7]  A. Furch,et al.  Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima , 2010, Journal of experimental botany.

[8]  P. Minchin,et al.  Electrical signalling and systemic proteinase inhibitor induction in the wounded plant , 1992, Nature.

[9]  M. Malone,et al.  The transpiration stream - Hydraulic signals , 1993 .

[10]  C. Slayman,et al.  Ion channels in Arabidopsis plasma membrane : transport characteristics and involvement in light-induced voltage changes. , 1992, Plant physiology.

[11]  Barbara G. Pickard,et al.  Mediation of rapid electrical, metabolic, transpirational, and photosynthetic changes by factors released from wounds. II. Mediation of the variation potential by Ricca's factor , 1976 .

[12]  E. Grill,et al.  Hydraulic signals in long-distance signaling. , 2013, Current opinion in plant biology.

[13]  A. Volkov,et al.  Electrical memory in Venus flytrap. , 2009, Bioelectrochemistry.

[14]  P. Simons,et al.  The action plant : movement and nervous behaviour in plants , 1992 .

[15]  U. Zimmermann,et al.  Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique , 1998 .

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

[17]  Stefano Mancuso,et al.  On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis) , 2011, Journal of experimental botany.

[18]  J. Fisahn,et al.  Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants , 1999 .

[19]  Jörg Fromm,et al.  Characteristics of Action Potentials in Willow (Salix viminalis L.) , 1993 .

[20]  G. Hörmann Studien über die Protoplasmaströmung bei den Characeen , 1898 .

[21]  D. B. Fisher,et al.  Measurement of the sieve tube membrane potential. , 1981, Plant physiology.

[22]  R. Hedrich Ion channels in plants. , 2012, Physiological reviews.

[23]  R. Matyssek,et al.  Involvement of respiratory processes in the transient knockout of net CO2 uptake in Mimosa pudica upon heat stimulation. , 2014, Plant, cell & environment.

[24]  U. Schurr,et al.  Composition of xylem sap of plants experiencing root water stress - a descriptive study. , 1990 .

[25]  R. M. Spanswick,et al.  Propagation of the neuroid action potential of the carnivorous plantDrosera , 1976, Journal of comparative physiology.

[26]  L. Mahadevan,et al.  How the Venus flytrap snaps , 2005, Nature.

[27]  M. Fricker,et al.  Sieve Element Ca2+ Channels as Relay Stations between Remote Stimuli and Sieve Tube Occlusion in Vicia faba[W] , 2009, The Plant Cell Online.

[28]  A. M. Sinyukhin,et al.  Action Potentials in the Reproductive System of Plants , 1967, Nature.

[29]  R. Matyssek,et al.  Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. , 2009, Plant, cell & environment.

[30]  T. Cuin,et al.  Electrical Signalling and Cytokinins Mediate Effects of Light and Root Cutting on Ion Uptake in Intact Plants , 2022 .

[31]  W. J. Davies,et al.  ABA-based chemical signalling: the co-ordination of responses to stress in plants. , 2002, Plant, cell & environment.

[32]  Ernst Steudle,et al.  A hydraulic signal in root-to-shoot signalling of water shortage. , 2007, The Plant journal : for cell and molecular biology.

[33]  E. Volkenburgh,et al.  Light-induced membrane potential changes of epidermal and mesophyll cells in growing leaves of Pisum sativum , 1995, Planta.

[34]  E. Davies,et al.  New functions for electrical signals in plants. , 2004, The New phytologist.

[35]  K. Ramaiah,et al.  Wounding Inhibits Protein Synthesis yet Stimulates Polysome Formation in Aged, Excised Pea Epicotyls , 1986 .

[36]  Guozeng Zhang,et al.  Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca signalling, is required for abscisic acid responses in Arabidopsis thaliana. , 2009, The Plant journal : for cell and molecular biology.

[37]  J. Fisahn,et al.  Localized Wounding by Heat Initiates the Accumulation of Proteinase Inhibitor II in Abscisic Acid-Deficient Plants by Triggering Jasmonic Acid Biosynthesis , 1996, Plant physiology.

[38]  T. Sibaoka,et al.  Physiology of Rapid Movements in Higher Plants , 1969 .

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

[40]  J. Flexas,et al.  Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO(2). , 2013, Plant, cell & environment.

[41]  Ondřej Novák,et al.  Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning , 2006, Planta.

[42]  D. Gradmann,et al.  Voltage dependent potassium fluxes and the significance of action potentials in Acetabularia. , 1976, Biochimica et biophysica acta.

[43]  C Kung,et al.  Pressure-sensitive ion channel in Escherichia coli. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

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

[45]  Simon Gilroy,et al.  Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants , 2014, Proceedings of the National Academy of Sciences.

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

[47]  Takashi Shiina,et al.  Action Potential in Luffa cylindlica and its Effects on Elongation Growth , 1986 .

[48]  H. Dziubińska,et al.  The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum , 1989 .

[49]  G. Thiel,et al.  Cl− and K+ channel currents during the action potential in Chara. simultaneous recording of membrane voltage and patch currents , 1994, The Journal of Membrane Biology.

[50]  S. Shabala,et al.  Oscillations in H+ and Ca2+ Ion Fluxes around the Elongation Region of Corn Roots and Effects of External pH , 1997, Plant physiology.

[51]  Barbara G. Pickard,et al.  Mediation of rapid electrical, metabolic, transpirational, and photosynthetic changes by factors released from wounds. I. Variation potentials and putative action potentials in intact plants , 1976 .

[52]  J. Fisahn,et al.  Proteinase Inhibitor II Gene Expression Induced by Electrical Stimulation and Control of Photosynthetic Activity in Tomato Plants , 1995 .

[53]  M. Tazawa,et al.  Participation of Ca2+ in cessation of cytoplasmic streaming induced by membrane excitation inCharaceae internodal cells , 1979, Protoplasma.

[54]  Emil Jovanov,et al.  Kinetics and Mechanism of Dionaea muscipula Trap Closing1[C][OA] , 2007, Plant Physiology.

[55]  Jörg Fromm,et al.  Action potentials in maize sieve tubes change phloem translocation , 1994 .

[56]  Hydraulic Signals , 2017 .

[57]  Bratislav Stankovic,et al.  Action potentials and variation potentials in sunflower: An analysis of their relationships and distinguishing characteristics , 1998 .

[58]  D. Hodick,et al.  On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis) , 1989, Planta.

[59]  K. Shinozaki,et al.  Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots , 2007, Proceedings of the National Academy of Sciences.

[60]  K. Okihara,et al.  A Ca2+- and Voltage-Dependent Cl− -Sensitive Anion Channel in the Chara Plasmalemma: A Patch-Clamp Study , 1991 .

[61]  Rainer Matyssek,et al.  Transient knockout of photosynthesis mediated by electrical signals. , 2004, The New phytologist.

[62]  R. Hedrich,et al.  Light-induced modification of plant plasma membrane ion transport. , 2010, Plant biology.

[63]  E. Van Volkenburgh,et al.  Light-regulated leaf expansion in two Populus species: dependence on developmentally controlled ion transport. , 2002, Journal of experimental botany.

[64]  Shabala,et al.  Light-induced changes in hydrogen, calcium, potassium, and chloride ion fluxes and concentrations from the mesophyll and epidermal tissues of bean leaves. Understanding the ionic basis of light-induced bioelectrogenesis , 1999, Plant physiology.

[65]  B. Stanković,et al.  Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato , 1996, FEBS letters.

[66]  E. Król,et al.  Electrical Signals in Long-Distance Communication in Plants , 2006 .

[67]  J. Feijó,et al.  The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm. , 2009, The International journal of developmental biology.

[68]  V. Vodeneev,et al.  Signaling role of action potential in higher plants , 2008, Russian Journal of Plant Physiology.

[69]  M. Fricker,et al.  Forisome dispersion in Vicia faba is triggered by Ca2+ hotspots created by concerted action of diverse Ca2+ channels in sieve element , 2009, Plant signaling & behavior.

[70]  J. Fromm,et al.  Characteristics and Functions of Phloem-Transmitted Electrical Signals in Higher Plants , 2006 .

[71]  M. Hajirezaei,et al.  The Biochemical Response of Electrical Signaling in the Reproductive System of Hibiscus Plants , 1995, Plant physiology.

[72]  Simon Gilroy,et al.  Ca2+ Regulates Reactive Oxygen Species Production and pH during Mechanosensing in Arabidopsis Roots[C][W] , 2009, The Plant Cell Online.

[73]  R. M. Spanswick,et al.  Plasmodesmata in Nitella translucens: structure and electrical resistance. , 1967, Journal of cell science.

[74]  J. Fromm,et al.  Control of phloem unloading by action potentials in Mimosa , 1991 .

[75]  A. W. Spanjers Bioelectric potential changes in the style of Lilium longiflorum Thunb. after self- and cross-pollination of the stigma , 1981, Planta.

[76]  J. Adler,et al.  Change in membrane potential during bacterial chemotaxis. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[77]  E. Van Volkenburgh,et al.  The effect of light on membrane potential, apoplastic pH and cell expansion in leaves of Pisum sativum L. var. Argenteum. , 1999, Planta.

[78]  J. Feijó,et al.  Gametophyte interaction and sexual reproduction: how plants make a zygote. , 2005, The International journal of developmental biology.

[79]  A. Trewavas,et al.  Calcium signalling in Arabidopsis thaliana responding to drought and salinity. , 1997, The Plant journal : for cell and molecular biology.

[80]  羽山 富雄 Participation of Ca[2+] in cessation of cytoplasmic streaming induced by membrane excitation in Characeae internodal cells , 1979 .

[81]  Rainer Matyssek,et al.  Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis1 , 2005, Plant Physiology.

[82]  D. Cosgrove,et al.  The Propagation of Slow Wave Potentials in Pea Epicotyls , 1997, Plant physiology.

[83]  P. M. Neumann,et al.  Hydraulic Signals from the Roots and Rapid Cell-Wall Hardening in Growing Maize (Zea mays L.) Leaves Are Primary Responses to Polyethylene Glycol-Induced Water Deficits , 1994, Plant physiology.

[84]  V. Z. Lunevsky,et al.  Excitation ofCharaceae cell membranes as a result of activation of calcium and chloride channels , 1983, The Journal of Membrane Biology.

[85]  K. Vandepoele,et al.  ROS signaling: the new wave? , 2011, Trends in plant science.

[86]  Jörg Fromm,et al.  Transport processes in stimulated and non-stimulated leaves of Mimosa pudica , 1988, Trees.

[87]  Caleb M. Rounds,et al.  Calcium entry into pollen tubes. , 2012, Trends in plant science.

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

[89]  J. Fisahn,et al.  Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. , 2004, Plant & cell physiology.

[90]  Bih Scott,et al.  Bioelectric Fields of Bean Roots and their Relation to Salt Accumulation , 1962 .

[91]  B. Pickard,et al.  Properties of action potentials in Drosera tentacles , 1972, Planta.

[92]  Barbara G. Pickard,et al.  Action potentials in higher plants , 1973, The Botanical Review.

[93]  Rainer Stahlberg,et al.  Slow Wave Potentials — a Propagating Electrical Signal Unique to Higher Plants , 2006 .

[94]  Rainer Matyssek,et al.  Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. , 2007, Plant, cell & environment.

[95]  E. Davies,et al.  Electrical Signals, the Cytoskeleton, and Gene Expression: a Hypothesis on the Coherence of the Cellular Responses to Environmental Insult , 2006 .

[96]  B. Pickard,et al.  Receptor potentials and action potentials in Drosera tentacles , 1972, Planta.

[97]  Bruce Schaffer,et al.  Root to leaf electrical signaling in avocado in response to light and soil water content. , 2008, Journal of plant physiology.

[98]  N. Holbrook,et al.  Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. , 2002, Journal of experimental botany.

[99]  Vladislav S. Markin,et al.  Inhibition of the Dionaea muscipula Ellis trap closure by ion and water channels blockers and uncouplers , 2008 .

[100]  T. Sibaoka,et al.  Action Potential in the Trap-lobes of Aldrovanda vesiculosa , 1981 .

[101]  Nobuhiro Suzuki,et al.  Reactive oxygen species-dependent wound responses in animals and plants. , 2012, Free radical biology & medicine.

[102]  J. Feijó The mathematics of sexual attraction , 2010, Journal of biology.

[103]  E. Ober,et al.  Electrophysiological responses of maize roots to low water potentials: relationship to growth and ABA accumulation. , 2003, Journal of experimental botany.

[104]  Vladislav S. Markin,et al.  Biologically Closed Electrical Circuits in Venus Flytrap[OA] , 2009, Plant Physiology.

[105]  W. Ruhland Encyclopedia of plant physiology. , 1958 .