Communication and Information Theory of Single Action Potential Signals in Plants

Many plants, such as Mimosa pudica (the “sensitive plant”), employ electrochemical signals known as action potentials (APs) for rapid intercellular communication. In this paper, we consider a reaction–diffusion model of individual AP signals to analyze APs from a communication- and information-theoretic perspective. We use concepts from molecular communication to explain the underlying process of information transfer in a plant for a single AP pulse that is shared with one or more receiver cells. We also use the chemical Langevin equation to accommodate the deterministic as well as stochastic component of the system. Finally, we present an information-theoretic analysis of single action potentials, obtaining achievable information rates for these signals. We show that, in general, the presence of an AP signal can increase the mutual information and information propagation speed among neighboring cells with receivers in different settings.

[1]  Ian F. Akyildiz,et al.  Nanonetworks: A new communication paradigm , 2008, Comput. Networks.

[2]  V. Sukhov,et al.  Influence of the variation potential on photosynthetic flows of light energy and electrons in pea , 2018, Photosynthesis Research.

[3]  R. Morris,et al.  Chemical agents transported by xylem mass flow propagate variation potentials , 2017, The Plant journal : for cell and molecular biology.

[4]  Filipe Tostevin,et al.  Mutual information in time-varying biochemical systems. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[5]  Chun Tung Chou,et al.  Extended Master Equation Models for Molecular Communication Networks , 2012, IEEE Transactions on NanoBioscience.

[6]  Raviraj S. Adve,et al.  Characterizing Information Propagation in Plants , 2018, 2018 IEEE Global Communications Conference (GLOBECOM).

[7]  M. Beilby Current-voltage characteristics of the proton pump atChara plasmalemma: I. pH dependence , 1984, The Journal of Membrane Biology.

[8]  D. Gradmann,et al.  Electrocoupling of Ion Transporters in Plants: Interaction with Internal Ion Concentrations , 1998, The Journal of Membrane Biology.

[9]  M. Beilby,et al.  Re-modeling Chara action potential: I. from Thiel model of Ca 2+ transient to action potential form , 2016 .

[10]  Nobuhiro Suzuki,et al.  ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants1[OPEN] , 2016, Plant Physiology.

[11]  Chun Tung Chou,et al.  Impact of Receiver Molecular Circuits on the Performance of Reaction Shift Keying , 2015, NANOCOM.

[12]  Chun Tung Chou,et al.  Generalized Solution for the Demodulation of Reaction Shift Keying Signals in Molecular Communication Networks , 2016, IEEE Transactions on Communications.

[13]  Chun Tung Chou,et al.  Impact of Receiver Reaction Mechanisms on the Performance of Molecular Communication Networks , 2013, IEEE Transactions on Nanotechnology.

[14]  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 and Environment.

[15]  Chun Tung Chou,et al.  Demodulation of reaction shift keying signals in molecular communication network with protein kinase receiver circuit , 2016, 2016 IEEE Wireless Communications and Networking Conference.

[16]  V. Sukhov,et al.  Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. , 2015, Functional plant biology : FPB.

[17]  Andrew W. Eckford,et al.  A Comprehensive Survey of Recent Advancements in Molecular Communication , 2014, IEEE Communications Surveys & Tutorials.

[18]  Vladimir Sukhov,et al.  Mathematical Models of Electrical Activity in Plants , 2017, The Journal of Membrane Biology.

[19]  Hamdan Awan,et al.  Reducing the Effect of Reaction Rate Constants on the Performance of Molecular Communication Networks , 2016, NANOCOM.

[20]  Satoshi Hiyama,et al.  Molecular communication: Harnessing biochemical materials to engineer biomimetic communication systems , 2010, Nano Commun. Networks.

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

[22]  D. Gradmann,et al.  Action potentials inAcetabularia: Measurement and simulation of voltage-gated fluxes , 1991, The Journal of Membrane Biology.

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

[24]  Desmond J. Higham,et al.  Modeling and Simulating Chemical Reactions , 2008, SIAM Rev..

[25]  John G. Proakis,et al.  Probability, random variables and stochastic processes , 1985, IEEE Trans. Acoust. Speech Signal Process..

[26]  Chun Tung Chou,et al.  Improving the Capacity of Molecular Communication Using Enzymatic Reaction Cycles , 2017, IEEE Transactions on NanoBioscience.

[27]  V. Sukhov,et al.  Mathematical model of action potential in higher plants with account for the involvement of vacuole in the electrical signal generation , 2017, Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology.

[28]  Chun Tung Chou Noise properties of linear molecular communication networks , 2013, Nano Commun. Networks.

[29]  Nariman Farsad,et al.  A simple mathematical model for information rate of active transport molecular communication , 2011, 2011 IEEE Conference on Computer Communications Workshops (INFOCOM WKSHPS).

[30]  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.

[31]  Chun Tung Chou,et al.  Using spatial partitioning to reduce receiver signal variance in diffusion-based molecular communication , 2018, NANOCOM.

[32]  V. Sukhov,et al.  Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus. , 2018, Functional plant biology : FPB.

[33]  V. Sukhov,et al.  Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves. , 2016, Journal of plant physiology.

[34]  R. Gallager Information Theory and Reliable Communication , 1968 .

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

[36]  V. Sukhov,et al.  Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings , 2015, Biochemistry (Moscow).

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

[38]  Stanisław Karpiński,et al.  Electrical Signaling, Photosynthesis and Systemic Acquired Acclimation , 2017, Front. Physiol..

[39]  R. Stephenson A and V , 1962, The British journal of ophthalmology.

[40]  Massimiliano Pierobon A Molecular Communication System Model Based on Biological Circuits , 2014, NANOCOM' 14.

[41]  Kevin Barraclough,et al.  I and i , 2001, BMJ : British Medical Journal.

[42]  P. R. ten Wolde,et al.  Exact results for noise power spectra in linear biochemical reaction networks. , 2005, The Journal of chemical physics.

[43]  Massimiliano Pierobon,et al.  A physical end-to-end model for molecular communication in nanonetworks , 2010, IEEE Journal on Selected Areas in Communications.

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

[45]  Aarnout Brombacher,et al.  Probability... , 2009, Qual. Reliab. Eng. Int..

[46]  J. C. Bose An Automatic Method for the Investigation of Velocity of Transmission of Excitation in Mimosa , 1914 .

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

[48]  Chun Tung Chou,et al.  Molecular communication networks with general molecular circuit receivers , 2013, NANOCOM' 14.

[49]  Vladimir Sukhov,et al.  High-Temperature Tolerance of Photosynthesis Can Be Linked to Local Electrical Responses in Leaves of Pea , 2017, Front. Physiol..

[50]  S. Mennerick,et al.  Review Action Potential Initiation and Propagation: Upstream Influences on Neurotransmission , 2022 .

[51]  V. Sukhov Electrical signals as mechanism of photosynthesis regulation in plants , 2016, Photosynthesis Research.

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

[53]  A. Vasilakos,et al.  Molecular Communication Among Biological Nanomachines: A Layered Architecture and Research Issues , 2014, IEEE Transactions on NanoBioscience.