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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus

Vladimir Vodeneev A B , Maxim Mudrilov A , Elena Akinchits A , Irina Balalaeva A and Vladimir Sukhov A
+ Author Affiliations
- Author Affiliations

A Department of Biophysics, Lobachevsky State University of Nizhni Novgorod, Gagarin Avenue, 23, Nizhni Novgorod, Russia.

B Corresponding author. Email: v.vodeneev@mail.ru

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.

Functional Plant Biology 45(2) 160-170 https://doi.org/10.1071/FP16342
Submitted: 30 September 2016  Accepted: 9 December 2016   Published: 3 March 2017

Abstract

Local damage induces generation and propagation of variation potentials (VPs) that affect physiological processes in plants. The aims of the work presented here were to investigate parameters of VP induced by burning, heating and mechanical injury in pea seedlings, and to undertake a theoretical analysis of the mechanisms underlying the differences in VP parameters and a study of the photosynthetic responses caused by VPs induced by the damaging factors. The velocity of propagation of burn-induced VP decreased with distance from the damaged area whereas the velocities of heating- and injury-induced VPs were constant. The amplitudes of burn- and heating-induced VPs did not depend on distance whereas the amplitude of VP induced by mechanical injury decreased. VP propagation has been simulated on the basis of wound substance spread. The simulation revealed two possible ways of wound substance propagation: turbulent diffusion from the damaged area and secondary active production in intact cells. The photosynthetic response (decrease in the quantum yield of PSII and raising the level of non-photochemical fluorescence quenching (NPQ)) developed in case of VP entering the intact leaf under heating and burn but was not registered after mechanical injury. An increase in NPQ level was biphasic under burn in comparison with a single-phase one under heating, and the NPQ amplitude was slightly higher under burn. We suggest that differences in photosynthetic responses may be determined by the parameters of VPs induced by stimuli of different nature.

Additional keywords: higher plant, information transduction, variation potential.


References

Böhm J, Scherzer S, Krol E, Kreuzer I, Meyer KV, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KAS, Rennenberg H, Shabala S, Neher E, Hedrich R (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26, 286–295.
The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake.Crossref | GoogleScholarGoogle Scholar |

Borst A, Theunissen FE (1999) Information theory and neural coding. Nature Neuroscience 2, 947–957.
Information theory and neural coding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFGlsr4%3D&md5=2555026f522fda792c3b74a95f0c1f37CAS |

Chatterjee SK, Das S, Maharatna K, Masi E, Santopolo L, Mancuso S, Vitaletti A (2015) Exploring strategies for classification of external stimuli using statistical features of the plant electrical response. Journal of the Royal Society Interface 12, 20141225
Exploring strategies for classification of external stimuli using statistical features of the plant electrical response.Crossref | GoogleScholarGoogle Scholar |

Choi WG, Hilleary R, Swanson SJ, Kim SH, Gilroy S (2016) Rapid, long-distance electrical and calcium signaling in plants. Annual Review of Plant Biology 67, 287–307.
Rapid, long-distance electrical and calcium signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XltFGrtrY%3D&md5=c95315b5f55d6c2fd78e1451152c06f2CAS |

Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30, 249–257.
Electrical signals and their physiological significance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlemu74%3D&md5=0f339e0dc380598533a73d13f28df4ebCAS |

Fromm J, Hajirezaei MR, Becker VK, Lautner S (2013) Electrical signaling along the phloem and its physiological responses in the maize leaf. Frontiers in Plant Science 4, 239
Electrical signaling along the phloem and its physiological responses in the maize leaf.Crossref | GoogleScholarGoogle Scholar |

Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Environmental and Experimental Botany 114, 15–21.
Environmental stimuli and physiological responses: the current view on electrical signalling.Crossref | GoogleScholarGoogle Scholar |

Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiology 171, 1606–1615.
ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVGlsbvF&md5=3554a9536f036809202c146d38e53cf4CAS |

Grams TE, Lautner S, Felle HH, Matyssek R, Fromm J (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant, Cell & Environment 32, 319–326.
Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkslKjsrk%3D&md5=fe456415cf21baa5c86d64e05d382aa7CAS |

Gurovich LA, Hermosilla P (2009) Electric signalling in fruit trees in response to water applications and light–darkness conditions. Journal of Plant Physiology 166, 290–300.
Electric signalling in fruit trees in response to water applications and light–darkness conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitV2lurc%3D&md5=1fd473038c77a81cc3546af5d61c7421CAS |

Hlaváčková V, Krchňák P, Nauš J, Novák O, Špundová M, Strnad M (2006) Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225, 235–244.
Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning.Crossref | GoogleScholarGoogle Scholar |

Hlavinka J, Nozková-Hlavácková V, Floková K, Novák O, Nausa J (2012) Jasmonic acid accumulation and systemic photosynthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pretreated by ABA. Plant Physiology and Biochemistry 54, 89–96.
Jasmonic acid accumulation and systemic photosynthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pretreated by ABA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xls1amtLc%3D&md5=7fa5d806376c8cf1e5d52fcd2b90952fCAS |

Huber AE, Bauerle TL (2016) Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge. Journal of Experimental Botany 67, 2063–2079.
Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWhsr3L&md5=e7329150283e5fe26b02e6243c62e652CAS |

Katicheva L, Sukhov V, Akinchits E, Vodeneev V (2014) Ionic nature of burn-induced variation potential in wheat leaves. Plant & Cell Physiology 55, 1511–1519.
Ionic nature of burn-induced variation potential in wheat leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWmtb7N&md5=ed715655998d23c258b4616a849fcdc8CAS |

Krol E, Dziubinska H, Trebacz K (2003) Low-temperature induced transmembrane potential changes in the liverwort Conocephalum conicum. Plant & Cell Physiology 44, 527–533.
Low-temperature induced transmembrane potential changes in the liverwort Conocephalum conicum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1OhsL0%3D&md5=e6be6479590e651a1690c7ec556512b9CAS |

Maffei ME, Mitho A, Arimura GI, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiology 140, 1022–1035.
Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xislygsrc%3D&md5=2980d5e4c21890538e76491a2eac67e6CAS |

Malone M (1994) Wound induced hydraulic signals and stimulus transmission in Mimosa pudica L. New Phytologist 128, 49–56.
Wound induced hydraulic signals and stimulus transmission in Mimosa pudica L.Crossref | GoogleScholarGoogle Scholar |

Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Australian Journal of Plant Physiology 26, 55–61.
Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera.Crossref | GoogleScholarGoogle Scholar |

Masi E, Ciszak M, Colzi I, Adamec L, Mancuso S (2016) Resting electrical network activity in traps of the aquatic carnivorous plants of the genera Aldrovanda and Utricularia. Scientific Reports 6, 24989
Resting electrical network activity in traps of the aquatic carnivorous plants of the genera Aldrovanda and Utricularia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmvFejs7g%3D&md5=b60540c29463c437e0cd9a2a3761e425CAS |

Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. Journal of Photochemistry and Photobiology. B, Biology 137, 116–126.
Photosynthesis: response to high temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntl2gsrk%3D&md5=85580fa070f67ac69e4c3c6a27de3e1aCAS |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=2c0385b5ba5736dd8d82f4ec79d9e277CAS |

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45
The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.Crossref | GoogleScholarGoogle Scholar |

Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends in Plant Science 16, 300–309.
ROS signaling: the new wave?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVyrs7w%3D&md5=0c657a7cae7167e4ba7437c790ad8a08CAS |

Opritov VA, Lobov SA, Pyatygin SS, Mysyagin SA (2005) Analysis of possible involvement of local bioelectric responses in chilling perception by higher plants exemplified by Cucurbita pepo. Russian Journal of Plant Physiology 52, 801–808.
Analysis of possible involvement of local bioelectric responses in chilling perception by higher plants exemplified by Cucurbita pepo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1enu7vM&md5=b9f7d1fc1999ac68dde61e1b7301a6c9CAS |

Oyarce P, Gurovich L (2011) Evidence for the transmission of information through electric potentials in injured avocado trees. Journal of Plant Physiology 168, 103–108.
Evidence for the transmission of information through electric potentials in injured avocado trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2jurvN&md5=d44c92ad13dc0ffa9bf72a3e6c47adc5CAS |

Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russian Journal of Plant Physiology 55, 285–291.
Signaling role of action potential in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1Ojtbw%3D&md5=aeea28a8d2d444b3a18f7540b4bc92ffCAS |

Rhodes JD, Thain JF, Wildon DC (1999) Evidence for physically distinct systemic signalling pathways in the wounded tomato plant. Annals of Botany 84, 109–116.
Evidence for physically distinct systemic signalling pathways in the wounded tomato plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktV2ks7Y%3D&md5=7c9079266b5971077afc9a514541feefCAS |

Stahlberg R, Cosgrove DJ (1996) Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. Planta 200, 416–425.
Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisFylug%3D%3D&md5=e7b4be5a866e33f8b9bb31bfabe5d772CAS |

Stahlberg R, Cleland RE, Volkenburgh EV (2006) Slow wave potentials – a propagating electrical signal unique to higher plants. In ‘Electrical signals in long-distance communication in plants’. (Eds F Baluska, S Mancuso, D Volkmann) pp. 291–308. (Springer-Verlag: Berlin)

Stankovic B, Witters DL, Zawadzki T, Davies E (1998) Action potentials and variation potentials in sunflower: an analysis of their relationships and distinguishing characteristics. Physiologia Plantarum 103, 51–58.
Action potentials and variation potentials in sunflower: an analysis of their relationships and distinguishing characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFeis7Y%3D&md5=4566b5da7232c997e188ba83bcaf027fCAS |

Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynthesis Research 130, 373–387.

Sukhov V, Akinchits E, Katicheva L, Vodeneev V (2013) Simulation of variation potential in higher plants cells. Journal of Membrane Biology 246, 287–296.
Simulation of variation potential in higher plants cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVGrsrc%3D&md5=ffa7c1e18f79d0bd9f6062b7f84c428aCAS |

Sukhov V, Surova L, Sherstneva O, Vodeneev V (2014) Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. Physiologia Plantarum 152, 773–783.
Influence of variation potential on resistance of the photosynthetic machinery to heating in pea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVamtL3J&md5=62d7ae585afe706c307ee0c77a05c802CAS |

Sukhov V, Surova L, Sherstneva O, Bushueva A, Vodeneev V (2015) Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Functional Plant Biology 42, 727–736.
Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea.Crossref | GoogleScholarGoogle Scholar |

Sukhov V, Surova L, Morozova E, Sherstneva O, Vodeneev V (2016) Changes in H+-ATP synthase activity, proton electrochemical gradient, and pH in pea chloroplast can be connected with variation potential. Frontiers in Plant Science 7, 1092
Changes in H+-ATP synthase activity, proton electrochemical gradient, and pH in pea chloroplast can be connected with variation potential.Crossref | GoogleScholarGoogle Scholar |

Tian L, Meng Q, Wang L, Dong J, Wu H (2015) Research on the effect of electrical signals on growth of Sansevieria under light-emitting diode (LED) lighting environment. PLoS One 10, e0131838
Research on the effect of electrical signals on growth of Sansevieria under light-emitting diode (LED) lighting environment.Crossref | GoogleScholarGoogle Scholar |

Trebacz K, Dziubinska H, Krol E (2006) Electrical signals in long-distance communication in plants. In ‘Communication in Plants: Neuronal Aspects of Plant Life’. (Eds F Baluska, S Mancuso, D Volkmann) pp. 277–290. (Springer-Verlag: Berlin)

Vodeneev VA, Akinchits EK, Orlova LA, Sukhov VS (2011) The role of Ca2+, H+, and Cl– ions in generation of variation potential in pumpkin plants. Russian Journal of Plant Physiology 58, 974–981.
The role of Ca2+, H+, and Cl ions in generation of variation potential in pumpkin plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12qsrfM&md5=30e741e597ba589849e83a416a42ab06CAS |

Vodeneev V, Orlova A, Morozova E, Orlova L, Akinchits E, Orlova O, Sukhov V (2012) The mechanism of propagation of variation potentials in wheat leaves. Journal of Plant Physiology 169, 949–954.
The mechanism of propagation of variation potentials in wheat leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFynt7g%3D&md5=2e55f9d627159a124661c33b7479ee87CAS |

Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signaling & Behavior 10, e1057365
Variation potential in higher plants: mechanisms of generation and propagation.Crossref | GoogleScholarGoogle Scholar |

Vodeneev VA, Sherstneva ON, Surova LM, Semina MM, Katicheva LA, Sukhov VS (2016) Age-dependent changes of photosynthetic responses induced by electrical signals in wheat seedlings. Russian Journal of Plant Physiology 63, 861–868.
Age-dependent changes of photosynthetic responses induced by electrical signals in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs12ntrvP&md5=e05126b974d17ecf8be78f499465d641CAS |

Zhao D-J, Wang Z-Y, Huang L, Jia Y-P, Leng J-Q (2014) Spatio-temporal mapping of variation potentials in leaves of Helianthus annuus L. seedlings in situ using multi-electrode array. Scientific Reports 4, 5435

Zimmermann MR, Felle HH (2009) Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities. Planta 229, 539–547.
Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFSmsr4%3D&md5=f3bb5844e06ad8e48aabe5a779bb0484CAS |