Solitary waves in soybean induced by localized thermal stress

Action potentials in higher plants are believed to be the information carriers in intercellular and intracellular communication in the presence of an environmental stressor. Plant electrophysiologists have recorded long distance electrical signaling in higher plants during the last two hundred years. Reproducing the duration, speed of propagation, and the shape of the action potential is challenging. Early measurements revealed that the speed of action potential propagation in plants is extremely slow – from 0.1 mm/s to 20 cm/s, although many faster plant responses to stress have been recorded as well. We hypothesized that this discrepancy is most likely due to the artifacts of aliasing from slow registration systems. In this study, we employ real time measurements using modern data acquisition techniques to detect ultra fast action potentials in green plants induced by localized heat stress. Thermal shock or heat stress is the most common environmental stress. Based on more sophisticated measuring techniques, we show that plants transmit solitary waves and that the speed of action potential propagation in green plants is similar to the speed of action potentials in mammalians, varying from a few meters per second up to 105 m/s. Possible pathways for electrical signal propagation in vascular plants are discussed.

[1]  A. Hetherington,et al.  The effects of manipulating phospholipase C on guard cell ABA-signalling. , 2003, Journal of experimental botany.

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

[3]  J. Passioura.  The effect of root geometry on the yield of wheat growing on stored water , 1972 .

[4]  K. Raschke,et al.  A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing , 1992, FEBS letters.

[5]  Byeong Wook Jeon,et al.  Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. , 2007, The Plant journal : for cell and molecular biology.

[6]  Patrick Favre,et al.  Repetitive action potentials induced in Arabidopsis thaliana leaves by wounding and potassium chloride application , 2001 .

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

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

[9]  I. Hwang,et al.  Phosphatidylinositol 3- and 4-Phosphate Are Required for Normal Stomatal Movements Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004143. , 2002, The Plant Cell Online.

[10]  W. Boss,et al.  Phosphoinositide kinases and the synthesis of polyphosphoinositides in higher plant cells. , 1999, International review of cytology.

[11]  Byeong Wook Jeon,et al.  Phosphatidylinositol 3- and 4-phosphate modulate actin filament reorganization in guard cells of day flower. , 2008, Plant, cell & environment.

[12]  A. Volkov,et al.  Electrochemistry of soybean: effects of uncouplers, pollutants, and pesticides , 2001 .

[13]  I. Hwang,et al.  A Role for Phosphatidylinositol 3-Phosphate in Abscisic Acid-Induced Reactive Oxygen Species Generation in Guard Cells1 , 2003, Plant Physiology.

[14]  N. Leonhardt,et al.  ATP Binding Cassette Modulators Control Abscisic Acid–Regulated Slow Anion Channels in Guard Cells , 1999, Plant Cell.

[15]  J. C. Bose.  Transmission of Stimuli in Plants , 1925, Nature.

[16]  W. Gruissem,et al.  Molecular characterization of At5PTase1, an inositol phosphatase capable of terminating inositol trisphosphate signaling. , 2001, Plant physiology.

[17]  J. K. Roberts,et al.  Acquisition of Thermotolerance in Soybean Seedlings : Synthesis and Accumulation of Heat Shock Proteins and their Cellular Localization. , 1984, Plant physiology.

[18]  A. Volkov,et al.  Electrical signaling in Aloe vera induced by localized thermal stress. , 2007, Bioelectrochemistry.

[19]  J. Schroeder,et al.  Anion-Channel Blockers Inhibit S-Type Anion Channels and Abscisic Acid Responses in Guard Cells , 1995, Plant physiology.

[20]  S. H. Vines.  Lectures on the physiology of plants , 1886 .

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

[22]  Todd E. Woerner,et al.  Coupling Diurnal Cytosolic Ca2+ Oscillations to the CAS-IP3 Pathway in Arabidopsis , 2007, Science.

[23]  ' M.MALONE,et al.  Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat , 2005 .

[24]  S. Assmann,et al.  Abscisic Acid-Induced Phosphoinositide Turnover in Guard Cell Protoplasts of Vicia faba , 1996, Plant physiology.

[25]  B. Mueller‐Roeber,et al.  Inositol Phospholipid Metabolism in Arabidopsis. Characterized and Putative Isoforms of Inositol Phospholipid Kinase and Phosphoinositide-Specific Phospholipase C1 , 2002, Plant Physiology.

[26]  N. Chua,et al.  Arabidopsis PLC1 Is Required for Secondary Responses to Abscisic Acid Signals , 2001, Plant Cell.

[27]  Emil Jovanov,et al.  Closing of Venus Flytrap by Electrical Stimulation of Motor Cells , 2007, Plant signaling & behavior.

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

[29]  G. Gillaspy,et al.  An Arabidopsis Inositol 5-Phosphatase Gain-of-Function Alters Abscisic Acid Signaling1 , 2003, Plant Physiology.

[30]  P. Minorsky,et al.  Temperature sensing by plants: a review and hypothesis , 1989 .

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

[32]  Imara Y. Perera,et al.  Inositol signaling and plant growth , 2000, Trends in plant science.

[33]  Alexander G. Volkov,et al.  Electrophysiology and Phototropism , 2006 .

[34]  M. O’Connell,et al.  Expression of the Heat Shock Response in a Tomato Interspecific Hybrid Is Not Intermediate between the Two Parental Responses. , 1990, Plant physiology.

[35]  N. Chua,et al.  Rac Homologues and Compartmentalized Phosphatidylinositol 4, 5-Bisphosphate Act in a Common Pathway to Regulate Polar Pollen Tube Growth , 1999, The Journal of cell biology.

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

[37]  M. Blatt,et al.  Reversible inactivation of K+ channels of Vcia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate , 1990, Nature.

[38]  J. Burke,et al.  The heat-shock response in higher plants: a biochemical model , 1988 .

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

[40]  A. Vian,et al.  Two Different Wound Signals Evoke Very Rapid, Systemic CMBP Transcript Accumulation in Tomato , 2006, Plant signaling & behavior.

[41]  J. Lee,et al.  Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. , 2004, The New phytologist.

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

[43]  B. Mueller‐Roeber,et al.  Phospholipase C is required for the control of stomatal aperture by ABA. , 2003, The Plant journal : for cell and molecular biology.

[44]  J. Schroeder,et al.  Identification of High-Affinity Slow Anion Channel Blockers and Evidence for Stomatal Regulation by Slow Anion Channels in Guard Cells. , 1993, The Plant cell.

[45]  R. Hedrich,et al.  Blue light inhibits guard cell plasma membrane anion channels in a phototropin-dependent manner. , 2007, The Plant journal : for cell and molecular biology.

[46]  T. Shimmen.  Electrophysiology in Mechanosensing and Wounding Response , 2006 .

[47]  Courtney L. Brown,et al.  Electrochemistry of Plant Life , 2006 .

[48]  A. Hetherington,et al.  Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Julius Sachs,et al.  Lectures on the Physiology of Plants , 2007 .

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

[51]  A. Goldsworthy.  THE EVOLUTION OF PLANT ACTION POTENTIALS , 1983 .

[52]  Imara Y. Perera,et al.  Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in Nicotiana tabacum[W][OA] , 2007, The Plant Cell Online.

[53]  Volko.  Green plants : electrochemical interfaces , 2000 .

[54]  G. Gillaspy,et al.  Molecular Characterization of an Arabidopsis Gene Encoding a Phospholipid-Specific Inositol Polyphosphate 5-Phosphatase1[w] , 2004, Plant Physiology.

[55]  J. Burdon Sanderson,et al.  On the Electromotive Properties of the Leaf of Dionaea in the Excited and Unexcited States. Second Paper , 1888 .

[56]  E. Bois-Reymond.  Untersuchungen über thierische Elektricität , 1848 .

[57]  T. Gadella,et al.  Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. , 2007, The Plant journal : for cell and molecular biology.

[58]  Two types of anion channel currents in guard cells with distinct voltage regulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Eric Davies,et al.  Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses , 1987 .

[60]  Y. Lee,et al.  Actin Filaments of Guard Cells Are Reorganized in Response to Light and Abscisic Acid , 1997, Plant physiology.

[61]  A. Trewavas,et al.  Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure , 1990, Nature.

[62]  K. Shinozaki,et al.  A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[63]  A. Volkov,et al.  Plant bioelectrochemistry: effects of CCCP on electrical signaling in soybean. , 2002, Bioelectrochemistry.

[64]  J. D. Rhodes,et al.  The pathway for systemic electrical signal conduction in the wounded tomato plant , 1996, Planta.

[65]  V. V. Roshchina,et al.  Neurotransmitters in Plant Life , 2001 .