Abstract
The sessile lifestyle of plants exposes them to many challenges that must be overcome to ensure their survival. Despite their apparent lack of movement and behaviour, plants are very active organisms that constantly respond to external cues and internal signals, making fine tunings at the metabolic, cellular and tissue levels. To accomplish this, plants largely rely on their relationship between phenotypic plasticity and cognitive abilities, which requires an information (or signalling) system. This information system is composed of many different signals, and among them are the electrical ones. Besides, in plants, there are many electrical activities that are not necessarily considered electrical signals. However, the sum of all electrical activity of a plant, considering all levels of organization, engenders the electrical dimension of their life. This dimension of life that encompasses all the living beings has recently been named “electrome”, in analogy with the other ‘omics’ from system biology approach. In the present review, we will explore this concept to describe the plant electrical activities. Furthermore, some basic aspects that are underlying the plant electrome will be presented, including the principles of biophysics that sustain the electrical activity of the cells. Moreover, some examples of electrical activities and signals that are vital to the plants will be exposed. Then, our most relevant and recent breakthroughs about plant electrome dynamics under different environmental conditions will be presented. Finally, some considerations about the possible involvement of the electrome plasticity and cognition features associated with the adaptive behaviour of plants will be discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abásalo D, Hornero R, Espino P, Poza J, Sánches C, de La Rosa R (2005) Analysis of regularity in the EEG background activity of Alzheimer’s disease patients with approximate entropy. Clin Neurophys 116:1826–1834
Al Khazaaly S, Walker NA, Beilby MJ, Shepherd VA (2009) Membrane potential fluctuations in Chara australis: a characteristic signature of high external sodium. Eur Biophys J 39:167–174
Almeida JG, dos Santos JA, Alberton B, Morellato LPC, Torres RS (2015) Phenological visual rhythms: compact representations for fine-grained plant species identification. Pattern Recogn Lett. https://doi.org/10.1016/j.patrec.2015.11.028
Bak P (1996) How nature works: the science of self-organized criticality. Springer, New York
Bak P, Tang C (1989) Earthquakes as a self-organized critical phenomenon. J Geophys Res 94:635–637
Bak P, Tang C, Wiesenfield K (1987) Self-organized criticality: an explanation of 1/f noise. Physic Rev Lett 59:381–384
Baluška F (ed) (2013) Long-distance systemic signaling and communication in plants. Springer, Berlin
Baluška F, Mancuso S (2009a) Plant neurobiology: from sensory biology, via plant communication, to social plant behavior. Cogn Process 10(Suppl 1):S3–S7. https://doi.org/10.1007/s10339-008-0239-6
Baluška F, Mancuso S (2009b) Deep evolutionary origins of neurobiology: turning the essence of ‘neural’ upside-down. Commun Integr Biol 2(1):60–65
Baluška F, Mancuso S (2013a) Ion channels in plants: from bioelectricity, via signaling, to behavioral actions. Plant Signal Behav 8(1):e23009
Baluška F, Mancuso S (2013b) Root apex transition zone as a oscillatory zone. Front Plant Sci 4(354):1–15
Baluška F, Miller WB (2018) Senomic view of the cell: senome versus genome. Commun Integr Biol 11:1–9. https://doi.org/10.1080/19420889.2018.1489184
Baluška F, Mancuso S, Volkamann D (2006) Communication in plants: neuronal aspects of plant life. Springer, Berlin
Behrens HM, Gradmann D, Sievers A (1985) Membrane-potential responses following gravistimulation in roots of Lepidium sativum L. Planta 163:463–472
Berque A (2017) Qu’est-ce que la mésologie, Blog Mésologiques. Accessed 14 Oct 2018
Bialasek M, Górecka M, Mittler R et al (2017) Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis. Plant Cell Physiol 58:207–215. https://doi.org/10.1093/pcp/pcw232
Bose JC (1926) The nervous mechanism of plants. Longman, Green & Co, New York
Bray D (1995) Protein molecules as computational elements in living cells. Nature 376:307–312
Brenner RP (1985) The electroencephalogram in altered states of consciousness. Neurol Clin 3:615–631
Brenner ED, Stahlberg R, Mancuso S, Vivanco JM, Baluška F, van Volkenburgh E (2007) Plant neurobiology: an integrated view of plant signaling. Trend Plant Sci 11(8):413–419
Buchanan BB, Gruissem W, Jones RL (2015) Biochemistry and molecular biology of plants, 2nd edn. Wiley-Blackwell, Hoboken, NJ
Burbach C, Markus K, Zhang Y, Schlicht M, Baluška F (2012) Photophobic behavior of maize roots. Plant Signal Behav 7:874–878
Burdon-Sanderson J (1873) Note on the electrical phenomena which accompany stimulation of the leaf of Dionea muscipula. Proc R Soc 21:495–496
Burioka N, Miyata M, Cornelissen G, Halberg F, Takeshima T, Kaplan DT, Suyama H, Endo M, Maegaki Y, Nomura T, Tomita Y, Nakashima K, Shimuzu E (2005) Approximate entropy in the electroencephalogram during wake and sleep. Clin EEG Neurosc 36:21–24
Cabral EF, Pecora PC, Arce AIC, Tech ARB, Costa EJX (2011) The oscillatory bioelectrical signal from plants explained by a simulated electrical model and tested using Lempel-Ziv complexity. Comput & Electron in Agric 76:1–5
Calvo P (2016) The philosophy of plant neurobiology: a manifesto. Synthese 193:1323–1343. https://doi.org/10.1007/s11229-016-1040-1
Calvo P, Sahi VP, Trewavas A (2017) Are plants sentient? Plant, Cell Environ 40:2858–2869
Canales J, Henriquez-Valencia C, Brauchi S (2018) The integration of electrical signals originating in the root of vascular plants. Front Plant Sci 8:2173. https://doi.org/10.3389/fpls.2017.02173
Catania KC (2016) Leaping eels electrify threats, supporting Humboldt’s account of a battle with horses. Proc Natl Acad Sci USA 113:6979–6984. https://doi.org/10.1073/pnas.1604009113
Chen Y, Zhao DJ, Wang ZY, Wang ZY, Tang G, Huang L (2016) Plant electrical signal classification based on waveform similarity. Algorithms. https://doi.org/10.3390/a9040070
Choi W-G, Hilleary R, Swanson SJ, Kim S-H, Gilroy S (2016) Rapid, long-distance electrical and calcium signaling in plants. Annu Rev Plan Biol 67(1):287–307. https://doi.org/10.1146/annurev-arplant-043015-112130
Choi WG, Miller G, Wallace I et al (2017) Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J 90:698–707. https://doi.org/10.1111/tpj.13492
Clarke D, Whitney H, Sutton G, Robert D (2013) Detection and learning of floral electric fields by bumblebees. Science 340:66–69
Collings DA, White RG, Overall RL (1992) Ionic current changes associated with the gravity-induced bending response in roots of Zea mays L. Plant Phys 100:1417–1426
Cuddington KM, Yodzis P (1999) Black noise and population persistence. Proc R Soc Lond B 266:969–973. https://doi.org/10.1098/rspb.1999.0731
Davies E (1993) Intercellular and intracellular signals and their transduction via the plasma membrane—cytoskeleton interface. Semin Cell Biol 4:139–147
de Arcangelis L, Herrmann HJ (2010) Learning as phenomenon occurring in a critical state. Proc Nat Acad Sci USA 107:3977–3981. https://doi.org/10.1073/pnas.0912289107
de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82
de Loof A (1986) The electrical dimension of cells: the cell as a miniature electrophoresis chamber. lnt Rev Cytol 88:251–352
de Loof A (2016) The cell’s self-generated “electrome”: the biophysical essence of the immaterial dimension of life? Commun Integr Biol 1:e1197446
Debono MW (2008) Transdisciplinarity: a new approach to metadynamics and consciousness. In: Nicolescu B (ed) Transdisciplinarity: theory & practice. Hampton Press Creskill, New Jersey
Debono MW (2013a) Dynamic proto-neural networks in plants: a new approach of spontaneous extracellular potential variations. Plant Signal Behav 8:e24207
Debono M (2013b) Perceptive levels in plants: a transdisciplinary challenge in living organism’s plasticity. Transdiscipl J Eng Sci 4:21–39
Debono MW, Bouteau F (1992) Spontaneous and evoked surface potentials in Kalanchoe tissues. Life Sci Adv Plant Physiol 11:107–117
Edwards AM, Phillips RA, Watkins NW, Freeman MP, Murphy EJ, Afanasyev V, Buldyrev SV, da Luz MGE, Raposo EP, Stanley HE (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449:1044–1049
Evans MJ, Choi WG, Gilroy S, Morris RJA (2016) ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress. Plant Phys 171(3):1535–1539. https://doi.org/10.1104/pp.16.00938
Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463:485–492. https://doi.org/10.1038/nature08908
Frohlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67:129–143
Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469
Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell Environ 30:249–257
Gagliano M, Vyazovskiy VV, Borbély AA, Grimonprez M, Depczynski M (2016) Learning by association in plants. Sci Rep 6:38427. https://doi.org/10.1038/srep38427
Gallé A, Lautner S, Flexas J et al (2013) Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signaling are predominantly governed by modifications of mesophyll conductance for CO2. Plant, Cell Environ 36:542–552. https://doi.org/10.1111/j.1365-3040.2012.02594.x
Gallé A, Lautner S, Flexas J et al (2015) Environmental stimuli and physiological responses: the current view on electrical signaling. Environ Exp Bot 114:15–21. https://doi.org/10.1016/j.envexpbot.2014.06.013
Gao J, Hu J, Tung W-W, Cao Y, Sarshar N, Roychowdhury VP (2006) Assessment of long-range correlation in time series: how to avoid pitfalls. Phys Rev E 73:016117
Gardiner J (2012) Insights into plant consciousness from neuroscience, physics and mathematics: a role for quasicrystals? Plant Signal Behav 7:1049–1055. https://doi.org/10.4161/psb.21325
Gardiner J (2013) Fractals and the irreducibility of consciousness in plants and animals. Plant Signal Behav 8(8):e25296
Genoud T, Métraux J-P (1999) Crosstalks in plant cell signaling: structure and function of the genetic network. Trends Plant Sci 4:503–507
Gensler W, Yan TL (1988) Investigation of the causative reactant of the apoplast electropotentials of plants. J Electrochem Soc Electrochem Sci Technol 135:2991–2995
Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630. https://doi.org/10.1016/j.tplants.2014.06.013
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpínski S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615
Grams T, Koziolek C, Lautner S et al (2007) Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. Plant, Cell Environ 30:79–84. https://doi.org/10.1111/j.1365-3040.2006.01607.x
Hausdorf JM, Peng C-K (1996) Multiscaled randomness: a possible source of 1/f noise in biology. Phys Rev E 54(2):2154–2157. https://doi.org/10.1103/PhysRevE.54.2
Hedrich R (2012) Ion channels in plants. Physiol Rev 92:1777–1811. https://doi.org/10.1152/physrev.00038.2011
Hedrich R, Salvador-Recatalà V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trend Plant Sci 21(5):376–387
Herd O, Peña-Cortés H, Fuss H et al (1999) Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants. Physiol Plant 105:179–184. https://doi.org/10.1034/j.1399-3054.1999.105126.x
Higinbotham N (1973) Electro potentials of plant cells. Ann Rev Plan Phys 24:25–46
Hlavinka J, Nozková-Hlavácková V, Floková K et al (2012) Jasmonic acid accumulation and systemic photosynthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pre-treated by ABA. Plant Physiol Biochem 54:89–96. https://doi.org/10.1016/j.plaphy.2012.02.014
Honigmann A, Pralle A (2016) Compartmentalization of the cell membrane. J Mol Biol 428:4739–4748
Huber AE, Bauerle TL (2016) Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge. J Exp Bot 67:2063–2079
Ivanov PC, Ma QDY, Barstsch RP, Hausdorf JM, Amaral LAN, Schulte-Frohlinde V, Stanley HE, Yoneyama M (2009) Levels of complexity in scale invariance neural signals. Phys Rev E 79:041920–1–041920-12
Iwabuchi A, Yano M, Shimizu H (1989) Development of extracellular electric pattern around Lepidium roots: its possible role in root growth and gravitropism. Protoplasma 148:94–100
Jaffe LF (1977) Electrophoresis along cell membranes. Nature 265:600–602
Jaffe LF, Robinson KR, Nuccitelli R (1974) Local cation entry and self-electrophoresis as an intracellular localization mechanism. In: Electrically mediated growth mechanisms in living systems, vol 238. Annals of the New York Academy of Sciences USA, pp 372–389
Jensen HJ (1998) Self-organized criticality: emergent complex behaviour in physical and biological systems. Cambridge Lecture Notes in Physics. Cambridge University Press, Cambridge, UK
Jones JGD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Josberger EE, Hassanzadeh P, Deng Y, Sohn RMJ, Amemiya CT, Rolandi M (2016) Proton conductivity in ampullae of Lorenzini jelly. Sci Adv 2:e1600112. https://doi.org/10.1126/sciadv.1600112
Karlsson L (1972) Nonrandom bioelectrical signals in plant tissue. Plant Physiol 49:982–986
Krapf D (2018) Compartmentalization of the plasma membrane. Curr Opin Cell Biol 53:15–21
Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PLoS ONE 6(4):e18549. https://doi.org/10.1371/journal.pone.0018549
Krupenina N, Bulychev A (2007) Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 1767:781–788. https://doi.org/10.1016/j.bbabio.2007.01.004
Kwaaitaal M, Huisman R, Maintz J et al (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem J 440:335–365
Lapenna V, Macchiato M, Telesca L (1998) 1/f fluctuations and self-similarity in earthquake dynamics: observation evidences in southern Italy. Phys Earth Planet Inter 106:115–127
Lee JY (2015) Plasmodesmata: a signaling hub at the cellular boundary. Curr Opin Plant Biol 27:133–140. https://doi.org/10.1016/j.pbi.2015.06.019
Levin M, Pezzulo G, Finkelstein JM (2017) Voltage gradients for control of growth and form. Annu Rev Biomed Eng 19:353–387
MacRobbie EAC (1962) Ionic relations in Nitella translucens. J Gener Phys 45:861–878
MacRobbie EAC (2006) Control of volume and turgor in stomatal guard cells. J Membr Biol 210:131–142. https://doi.org/10.1007/s00232-005-0851-7
Mancini R (2002) Op amps for everyone. Texas Instrum Des Ref. https://doi.org/10.1016/b978-075067701-1/50019-5
Marder M (2012) Plant intentionality and the phenomenological framework of plant intelligence. Plant Signal Behav 7(11):1–8
Marder M (2013) Plant intelligence and attention. Plant Signal Behav 8(5):e23902. https://doi.org/10.4161/psb.23902
Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluška F, Arecchi FT, Mancuso S (2009) Spatio-temporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci USA 106:4048–4053. https://doi.org/10.1073/pnas.0804640106
Masi E, Ciszak M, Comparini D, Monetti E, Pandolfi C, Azzarello E, Mugnai S, Baluška F, Mancuso S (2015) The electrical network of maize root apex is gravity dependent. Sci Rep 5:7730. https://doi.org/10.1038/srep07730
Matzke AJM, Weiger TM, Matzke M (2010) Ion channels at the nucleus: electrophysiology meets the genome. Mol Plant 3(4):642–652
May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton
Meisel C, Storch A, Hallmeyer-Elgner S, Bullmore E, Gross T (2012) Failure of adaptive self-organized criticality during epileptic seizure attacks. PLoS Comput Biol 8:e1002312
Miller AL, Gow NAR (1989) Correlation between root-generated ionic currents, pH, fusicoccin, indoleacetic acid, and growth of the primary root of Zea mays. Plant Phys 89:1198–1206
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45. https://doi.org/10.1126/scisignal.2000448
Mott KA, Buckley TN (2000) Patchy stomatal conductance emergent collective behaviour. Trends Plant Sci 5:258–262
Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signaling. Nature 500:422–440
Mousavi SAR, Nguyen CT, Farmer EE, Kellenberger S (2014) Measuring surface potential changes on leaves. Nat Protocol 9(8):1997–2004
Neill SJ, Desikan R, Clarke A, Hancock JT (2002a) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16. https://doi.org/10.1104/pp.010707
Neill SJ, Desikan R, Hancock J (2002b) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395. https://doi.org/10.1016/S1369-5266(02)00282-0
Neto E, Allen EA, Aurlien H, Nordby H, Eichele T (2015) EEG spectral features discriminate between Alzheimer’s and vascular dementia. Front Neurol 6(25):1
Nobel PS (1999) Physicochemical & environmental plant physiology, 2nd edn. Academic press, San Diego
Novikova EM, Vodeneev VA, Sukhov VS (2017) Mathematical model of action potential in higher plants with account for the involvement of vacuole in the electrical signal generation. Membr Cell Biol 11(2):151–167
Nuccitelli R, Robinson K, Jaffe L (1986) On electrical currents in development. BioEssays 5:292–294
Olivotto M, Arcangeli A, Carlà M, Wanke E (1996) Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. BioEssays 18:495–504
Pavlovic A, Slováková L, Pandolfi C et al (2011) On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J Exp Bot 62:1991–2000. https://doi.org/10.1093/jxb/erq404
Pereira DN, Papa JP, Saraiva GFR, Souza GM (2018) Automatic classification of plant electrophysiological responses to environmental stimuli using machine learning and interval arithmetic. Comput Electron Agric 145:35–42
Petchey OL, Gonzalez A, Wilson HB (1997) Effects on population persistence: the interaction between environmental noise color, intraspecific competition and space. Proc R Soc Lond 264:1841–1847
Pickard BG (1973) Action potentials in higher plants. Bot Rev 39:172–201
Pincus SM (1991) Approximate entropy as a measure of system complexity. Proc of Nat Acad Sci USA 88:2297–2301
Pincus SM, Goldberger AL (1994) Physiological time-series analysis: what does regularity quantify? Am J Phys 266:1643–1656
Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Phys 99:1271–1274
Rubinov M, Sporms O, Thivierge J-P, Breakspear M (2011) Neurobiologically realistic determinants of self-organized criticality in networks of spiking neurons. PLoS Comput Biol 7:e1002038
Saraiva GRF, Ferreira AS, Souza GM (2017) Osmotic stress decreases complexity underlying the electrophysiological dynamic in soybean. Plant Biol. https://doi.org/10.1111/plb.12576
Schroeder M (1991) Fractals, chaos, power laws: minutes from an infinite paradise. W.H. Freeman, New York
Scott BIH (1967) Electric fields in plants. Annu Rev Plant Phys 18:409–418
Scott P (2008) Physiology and behaviour of plants. Wiley, West Sussex
Segal AW (2016) NADPH oxidases as electrochemical generators to produce ion fluxes and turgor in fungi, plants and humans. Open Biol 6:160028. https://doi.org/10.1098/rsob.160028
Shabala S, White RG, Djordjevic MA, Ruan YL, Mathesius U (2016) Root-to-shoot signaling: integration of diverse molecules, pathways and functions. Funct Plant Biol 43:87–104. https://doi.org/10.1071/FP15252
Shepherd VA (2005) From semi-conductors to the rhythms of sensitive plants: the research of J.C. Bose. Cell Mol Biol 51:607–619
Shepherd VA (2012) At the roots of plant neurobiology. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, pp 3–43. https://doi.org/10.1007/978-3-642-29119-7_1
Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity–complexity–diversity in eco-physiology. Prog Bot 76:211–239
Souza GM, Oliveira RF, Cardoso VJM (2004) Temporal dynamics of stomatal conductance of plants under water deficit: can homeostasis be improved by more complex dynamics. Arq de Biol e Tecnol 47:423–431
Souza GM, Pincus SM, Monteiro JAF (2005) The complexity–stability hypothesis in plant gas exchange under water deficit. Braz J Plant Phys 17:363–373
Souza GM, Ferreira AS, Saraiva GFR, Toledo GRA (2017) Plant “electrome” can be pushed toward a self-organized critical state by external cues: evidences from a study with soybean seedlings subject to different environmental conditions. Plant Signal Behav 12(3):e1290040. https://doi.org/10.1080/15592324.2017.1290040
Spanswick RM (1981) Electrogenic ion pumps. Rev Plant Phys 32:67–89
Spanswick RM, Williams EJ (1964) Electrical potentials and Na, K, and Cl concentrations in the vacuole and cytoplasm of Nitella translucens. J Exp Bot 15:193–200
Srinivasan V, Eswara C, Sriraam N (2007) Approximate entropy-based epileptic EEG detection using artificial neural networks. IEEE Trans Inf Technol Biomed 11:288–295
Stahlberg R (2006) Historical overview on plant neurobiology. Plant Signal Behav 1(1):6–8
Stahlberg R, Cleland RE, van Volkenburgh E (2006) Slow wave potentials: a propagating electrical signal unique to higher plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants: neuronal aspects of plant life. Springer, New York, pp 291–308
Stanković B (2006) Electrophysiology of plant gravitropism. In: Volkov AG (ed) Plant electrophysiology: theory and methods, 1st edn. Springer, Berlin
Stavrinidou E, Gabrielsson R, Gomez E, Crispin X, Nilsson O, Simon DT, Berggren M (2015) Electronic plants. Sci Adv 1(10):e1501136
Stoddard PK (1999) Predation enhances complexity in the evolution of electric fish signals. Nature 400:254–256
Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130:373–387. https://doi.org/10.1007/s11120-016-0270-x
Sukhov V, Orlova L, Mysyagin S et al (2012) Analysis of the photosynthetic response induced by variation potential in geranium. Planta 235:703–712. https://doi.org/10.1007/s00425-011-1529-2
Sukhov V, Sherstneva O, Surova L et al (2014) Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant, Cell Environ 37:2532–2541. https://doi.org/10.1111/pce.12321
Sukhov V, Surova L, Sherstneva O et al (2015) Variation potential influence on photosynthetic cyclic electron flow in pea. Front Plant Sci 5:766. https://doi.org/10.3389/fpls.2014.00766
Sukhova E, Akinchits E, Sukhov V (2017) Mathematical models of electrical activity in plants. J Membr Biol 250:407–423
Surova L, Sherstneva O, Vodeneev V et al (2016) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Sign Behav 11:e1145334. https://doi.org/10.1080/15592324.2016.1145334
Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, Shulaev V, Mittler R (2013) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553–3569. https://doi.org/10.1105/tpc.113.114595
Szechyńska-Hebda M, Lewandowska M, Karpiński S (2017) Electrical signaling, photosynthesis and systemic acquired acclimation. Front Physiol 8:684. https://doi.org/10.3389/fphys.2017.00684
Taiz E, Zeiger E, Møller IM, Murphy A (2014) Plant physiology and development, 6th edn. Sinauer Associates, Sunderland
Thellier M, Lüttge U (2012) Plant memory: a tentative model. Plant Biol 15:1–12
Towlson EK, Vertes PE, Ahnert SE, Schafer WR, Bullmore ET (2013) The rich club of the C. elegans neuronal connectome. J Neurosci 33:6380–6387. https://doi.org/10.1523/JNEUROSCI.3784-12.2013
Trebacz K, Dziubinska H, Król E (2006) Electrical signals in long-distance communication in plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Neuronal aspects of plant life. Springer, Berlin, pp 277–290
Trewavas A (2016) Intelligence, cognition, and language of green plants. Front Psychol 7:588. https://doi.org/10.3389/fpsyg.2016.00588
Trewavas A (2017) The foundations of plant intelligence. Interface Focus 7:20160098
Trewavas A, Baluška F (2011) The ubiquity of consciousness. EMBO Rep 12(12):1221–1225
Tseng A-S, Levin M (2013) Cracking the bioelectric code: probing endogenous ionic controls of pattern formation. Commun Integr Biol 6:1–8
Umrath K (1930) Untersuchungen über Plasma und Plasmaströmungen an Characeen. IV. Potentialmessungen an Nitella mucronata mit besonderer Berücksichtigung der Erregungserscheinungen. Protoplasma 9:576–597
van Bel AJE, Furch ACU, Will T, Buxa SV, Musetti R, Hafke JB (2014) Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway. J Exp Bot 65:1761–1787. https://doi.org/10.1093/jxb/ert425
Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB (2011) Structural properties of the Caenorhabditis elegans neuronal network. PLoS Comput Biol 7:e1001066. https://doi.org/10.1371/journal.pcbi.1001066
Vian A, Stankovic B, Davies E (2015) Signalomics: diversity and methods of analysis of systemic signals in plants. In: Plantomics: the omics of plant science. Springer, Berlin, pp 459–490
Vodeneev VA, Katicheva LA, Sukhov VS (2016a) Electrical signals in higher plants: mechanisms of generation and propagation. Biophysics 61(3):505–512
Vodeneev V, Akinchits E, Sukhov V (2016b) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signal Behav 10:e1057365. https://doi.org/10.1080/15592324.2015.1057365
Volkov AG (2006) Plant electrophysiology: theory and methods, 1st edn. Springer, Berlin
Volkov AG, Collins DJ, Mwesigwa J (2000) Plant electrophysiology: pentachlorophenol induces fast action potentials in soybean. Plant Sci 153:185–190
Volkov AG, Carrell H, Markin VS (2009) Biologically closed electrical circuits in venus flytrap. Plant Phys 149:1661–1667
Weisenseel MH, Nuccitelli R, Jaffe L (1975) Large electrical currents traverse growing pollen tubes. J Cell Biol 66:556–567
Weisenseel MH, Dorn A, Jaffe L (1979) Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.). Plant Phys 64:512–518
Wildon DC, Thain JF, Minchn PEH, Gubb IR, Reily AJ, Skipper YD, Doherty HM, O’Donnel PJ, Bowles DJ (1992) Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360:62–65
Wudick MM, Portes MT, Michard E et al (2018) CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. Science 360(80):533–536. https://doi.org/10.1126/science.aar6464
Yan X, Wang Z, Huang L, Wang C, Hou R, Xu Z, Qiao X (2009) Research progress on electrical signals in higher plants. Progr Nat Sci 19:531–541
Yokawa K, Derrien-Maze N, Mancuso S, Baluška F (2014) Binary decisions in maize root behavior: Y-maze system as tool for unconventional computation in plants. Int J Unconv Comput 10:381–390
Zimmermann MR, Maischak H, Mithoefer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Phys 149:1593–1600
Zimmermann M, Mithofer A, Will T et al (2016) Herbivore-Triggered electrophysiological reactions: candidates for systemic signals in higher plants and the challenge of their identification. Plant Physiol 170:2407–2419. https://doi.org/10.1104/pp.15.01736
Acknowledgements
This work was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), Capes (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and Stoller do Brasil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Toledo, G.R.A., Parise, A.G., Simmi, F.Z. et al. Plant electrome: the electrical dimension of plant life. Theor. Exp. Plant Physiol. 31, 21–46 (2019). https://doi.org/10.1007/s40626-019-00145-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-019-00145-x