Variation potential in higher plants: Mechanisms of generation and propagation

Long-distance intercellular electrical signals, including variation potential (VP) in higher plants, are a potential mechanism of coordinate functional responses in different plant cells under action of stressors. VP, which is caused by damaging factors (e.g., heating, crushing), is transient depolarization with an irregular shape. It can include a long-term depolarization and fast impulse depolarization (‘AP-like’ spikes). Mechanisms of VP generation and propagation are still under investigation. It is probable that VP is a local electrical response induced by propagation of hydraulic wave and (or) chemical agent. Both hypotheses are based on numerous experimental results but they predict VP velocities which are not in a good accordance with speed of variation potential propagation. Thus combination of hydraulic and chemical signals is the probable mechanism of VP propagation. VP generation is traditionally connected with transient H+-ATPase inactivation, but AP-like spikes are also connected with passive ions fluxes. Ca2+ influx is a probable mechanism which triggers H+-ATPase inactivation and ions channels activation at VP.

[1]  M. Roelfsema,et al.  Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding , 2008, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[2]  J. Hancock,et al.  Hydrogen peroxide signalling. , 2002, Current opinion in plant biology.

[3]  V. Sukhov,et al.  Analysis of the photosynthetic response induced by variation potential in geranium , 2011, Planta.

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

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

[6]  D. Los,et al.  Signaling role of reactive oxygen species in plants under stress , 2012, Russian Journal of Plant Physiology.

[7]  O. Lamotte,et al.  Cross-talk between ROS and calcium in regulation of nuclear activities. , 2010, Molecular plant.

[8]  H. Felle,et al.  Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities , 2009, Planta.

[9]  V. G. Retivin,et al.  Generation of action potential induces preadaptation of Cucurbita pepo L. stem tissues to freezing injury , 1997 .

[10]  V. Sukhov,et al.  The role of Ca2+, H+, and Cl− ions in generation of variation potential in pumpkin plants , 2011, Russian Journal of Plant Physiology.

[11]  G. Pearce,et al.  A Polypeptide from Tomato Leaves Induces Wound-Inducible Proteinase Inhibitor Proteins , 1991, Science.

[12]  Zatsepina Gn,et al.  Electrical nature of the spread of the variable potential of Tradescantia , 1980 .

[13]  V. Sukhov,et al.  Ionic nature of burn-induced variation potential in wheat leaves. , 2014, Plant & cell physiology.

[14]  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.

[15]  V. Sukhov,et al.  Simulation of action potential propagation in plants. , 2011, Journal of theoretical biology.

[16]  M. De Roo,et al.  Electrophysiological characterization of tomato hypocotyl putative action potentials induced by cotyledon heating. , 2002, Physiologia plantarum.

[17]  D. Cosgrove,et al.  Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. , 1996, Planta.

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

[19]  Jörg Durner,et al.  Salicylic acid and disease resistance in plants , 1997 .

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

[21]  F. Sánchez,et al.  Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter , 2014, Front. Plant Sci..

[22]  M. Malone Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings , 1992, Planta.

[23]  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 .

[24]  M. Malone,et al.  An hydraulic interpretation of rapid, long-distance wound signalling in the tomato , 1994, Planta.

[25]  B. Pickard,et al.  Electrical characteristics of cells from leaves of Lycopersicon , 1977 .

[26]  Michitaka Notaguchi,et al.  Dynamics of long-distance signaling via plant vascular tissues , 2015, Front. Plant Sci..

[27]  Hubert H. Felle,et al.  System Potentials, a Novel Electrical Long-Distance Apoplastic Signal in Plants, Induced by Wounding1 , 2009, Plant Physiology.

[28]  V. Sukhov,et al.  A Mathematical Model of Action Potential in Cells of Vascular Plants , 2009, Journal of Membrane Biology.

[29]  Silke Lautner,et al.  Environmental stimuli and physiological responses: The current view on electrical signalling , 2015 .

[30]  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.

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

[32]  G. Pearce,et al.  Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Malone,et al.  Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. , 1994, The New phytologist.

[34]  A. Bulychev,et al.  Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. , 2007, Biochimica et biophysica acta.

[35]  E. Davies,et al.  Characterization of the Variation Potential in Sunflower , 1997, Plant physiology.

[36]  T. Sibaoka Application of leaf extract causes repetitive action potentials inBiophytum sensitivum , 1997, Journal of Plant Research.

[37]  Vladimir Sukhov,et al.  Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. , 2014, Physiologia plantarum.

[38]  H. Leyser,et al.  Ethylene as a Signal Mediating the Wound Response of Tomato Plants , 1996, Science.

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

[40]  Janusz Koscielniak,et al.  Variation and action potentials evoked by thermal stimuli accompany enhancement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. , 2003, Journal of plant physiology.

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

[42]  J. Bonnemain,et al.  Propagation in Vicia faba Stem of a Potential Variation Induced by Wounding , 1985 .

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

[44]  V. Sukhov,et al.  The mechanism of propagation of variation potentials in wheat leaves. , 2012, Journal of plant physiology.

[45]  D. Gradmann,et al.  Impact of Apoplast Volume on Ionic Relations in Plant Cells , 2001, The Journal of Membrane Biology.

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

[47]  Veselin Dimitrov Petrov,et al.  Hydrogen peroxide—a central hub for information flow in plant cells , 2012, AoB PLANTS.

[48]  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.

[49]  V. Sukhov,et al.  Variation potential influence on photosynthetic cyclic electron flow in pea , 2015, Front. Plant Sci..

[50]  M. Beilby Action potential in charophytes. , 2007, International review of cytology.

[51]  S. Bruckenstein Physicochemical hydrodynamics , 1977, Nature.

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

[53]  A. Meyer,et al.  Wound-Induced Changes of Membrane Voltage, Endogenous Currents, and Ion Fluxes in Primary Roots of Maize , 1997, Plant physiology.

[54]  J. Patrick,et al.  (Questions)n on phloem biology. 2. Mass flow, molecular hopping, distribution patterns and macromolecular signalling. , 2011, Plant science : an international journal of experimental plant biology.

[55]  J. Frachisse,et al.  Involvement of the proton pump and proton conductance change in the wave of depolarization induced by wounding in Bidens pilosa , 1992 .

[56]  Stefano Mancuso,et al.  Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera , 1999 .

[57]  J. Davies,et al.  Is ATP a Signaling Agent in Plants?1 , 2003, Plant Physiology.

[58]  A. Jagendorf,et al.  Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Gabriel Roblin,et al.  Analysis of the Variation Potential Induced by Wounding in Plants , 1985 .

[60]  J. D. Rhodes,et al.  Evidence for Physically Distinct Systemic Signalling Pathways in the Wounded Tomato Plant , 1999 .

[61]  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 .

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

[63]  E. Van Volkenburgh,et al.  Long-distance signaling within Coleus × hybridus leaves; mediated by changes in intra-leaf CO2? , 2001, Planta.

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

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

[66]  M. Malone,et al.  Rapid, Long-distance Signal Transmission in Higher Plants , 1996 .

[67]  D. Cosgrove,et al.  Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings , 1992, Planta.

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

[69]  Eric Davies,et al.  Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato , 1997, Planta.

[70]  J. D. Rhodes,et al.  Signals and Signalling Pathways in Plant Wound Responses , 2006 .

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

[72]  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.

[73]  J. Sánchez-Serrano,et al.  Wound signalling in plants. , 2001, Journal of experimental botany.

[74]  Lyubov Katicheva,et al.  Simulation of Variation Potential in Higher Plant Cells , 2013, The Journal of Membrane Biology.

[75]  V. Vodeneev,et al.  Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo , 2006, Russian Journal of Plant Physiology.

[76]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[77]  A. Roth Water transport in xylem conduits with ring thickenings , 1996 .

[78]  J. Nauš,et al.  Chemical Signal as a Rapid Long-Distance Information Messenger After Local Wounding of a Plant? , 2007, Plant signaling & behavior.

[79]  D. Gradmann Models for oscillations in plants , 2001 .

[80]  Jean-Marie Frachisse,et al.  Characteristics of the Wave of Depolarization Induced by Wounding in Bidens pilosa L. , 1991 .

[81]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

[82]  M. Harrison Cross-Talk Between Phytohormone Signaling Pathways Under Both Optimal and Stressful Environmental Conditions , 2012 .

[83]  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.

[84]  E. Davies,et al.  Electrical Signals in Plants: Facts and Hypotheses , 2006 .

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