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Electrical signals as mechanism of photosynthesis regulation in plants

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Abstract

This review summarizes current works concerning the effects of electrical signals (ESs) on photosynthesis, the mechanisms of the effects, and its physiological role in plants. Local irritations of plants induce various photosynthetic responses in intact leaves, including fast and long-term inactivation of photosynthesis, and its activation. Irritation-induced ESs, including action potential, variation potential, and system potential, probably causes the photosynthetic responses in intact leaves. Probable mechanisms of induction of fast inactivation of photosynthesis are associated with Ca2+- and (or) H+-influxes during ESs generation; long-term inactivation of photosynthesis might be caused by Ca2+- and (or) H+-influxes, production of abscisic and jasmonic acids, and inactivation of phloem H+-sucrose symporters. It is probable that subsequent development of inactivation of photosynthesis is mainly associated with decreased CO2 influx and inactivation of the photosynthetic dark reactions, which induces decreased photochemical quantum yields of photosystems I and II and increased non-photochemical quenching of photosystem II fluorescence and cyclic electron flow around photosystem I. However, other pathways of the ESs influence on the photosynthetic light reactions are also possible. One of them might be associated with ES-connected acidification of chloroplast stroma inducing ferredoxin-NADP+ reductase accumulation at the thylakoids in Tic62 and TROL complexes. Mechanisms of ES-induced activation of photosynthesis require further investigation. The probable ultimate effect of ES-induced photosynthetic responses in plant life is the increased photosynthetic machinery resistance to stressors, including high and low temperatures, and enhanced whole-plant resistance to environmental factors at least during 1 h after irritation.

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References

  • Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137:263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  CAS  PubMed  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19

    Article  CAS  PubMed  Google Scholar 

  • Alte F, Stengel A, Benz JP, Petersen E, Soll J, Groll M, Bölter B (2010) Ferredoxin: NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc Natl Acad Sci USA 107:19260–19265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beilby MJ (1982) C1− channels in Chara. Philos Trans R Soc London B 299:435–445

    Article  CAS  Google Scholar 

  • Beilby MJ (1984) Calcium and plant action potentials. Plant Cell Environ 7:415–421

    Article  CAS  Google Scholar 

  • Beilby MJ (2007) Action potential in charophytes. Int Rev Cytol 257:43–82

    Article  CAS  PubMed  Google Scholar 

  • Benz JP, Stengel A, Lintala M, Lee YH, Weber A, Philippar K, Gügel IL, Kaieda S, Ikegami T, Mulo P, Soll J, Bölter B (2010) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21:3965–3983

    Article  CAS  Google Scholar 

  • Bishop PD, Makus DJ, Pearce G, Ryan CA (1981) Proteinase inhibitor inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls. Proc Natl Acad Sci USA 78:3536–3540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukhov NG (2004) Dynamic light regulation of photosynthesis (a review). Russ J Plant Physiol 51:742–753

    Article  CAS  Google Scholar 

  • Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: Leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93

    Article  CAS  Google Scholar 

  • Bulychev AA, Komarova AV (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells. Biochemistry (Moscow) 79: 273–281

  • Bulychev AA, Krupenina NA (2010) Inactivation of plasmalemma conductance in alkaline zones of chara corallina after generation of action potential. Biochem (Moscow) Suppl Ser A 4:232–239

    Article  Google Scholar 

  • Bulychev AA, Kamzolkina NA, Luengviriya J, Rubin AB, Müller SC (2004) Effect of a single excitation stimulus on photosynthetic activity and light-dependent pH banding in Chara cells. J Membr Biol 202:11–19

    Article  CAS  PubMed  Google Scholar 

  • Bulychev AA, Alova AV, Rubin AB (2013) Fluorescence transients in chloroplasts of Chara corallina cells during transmission of photoinduced signal with the streaming cytoplasm. Russ J Plant Physiol 60:33–40

    Article  CAS  Google Scholar 

  • Davies E, Stankovic B (2006) Electrical signals, the cytoskeleton, and gene expression: a hypothesis on the coherence of the cellular responses to environmental insult. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Neuronal aspects of plant life. Springer, New York, pp 309–320

    Google Scholar 

  • Degli Agosti R (2014) Touch-induced action potentials in Arabidopsis thaliana. Arch Des Sci 67:125–138

    CAS  Google Scholar 

  • Dziubinska H, Trêbacz K (1989) Zawadzki T The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum. Physiol Plant 75:417–423

    Article  Google Scholar 

  • Dziubinska H, Filek M, Koscielniak J, Trebacz K (2003) Variation and action potentials evoked by thermal stimuli accompany enhancement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. J Plant Physiol 160:1203–1210

    Article  CAS  PubMed  Google Scholar 

  • Evron Y, Johnson EA, McCarty RE (2000) Regulation of proton flow and ATP synthesis in chloroplasts. J Bioenerg Biomembr 32:501–506

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication—airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Favre P, Degli Agosti R (2007) Voltage-dependent action potentials in Arabidopsis thaliana. Physiol Plant 131:263–272

    CAS  PubMed  Google Scholar 

  • Favre P, Greppin H, Degli Agosti R (2011) Accession-dependent action potentials in Arabidopsis. J Plant Physiol 168:653–660

    Article  CAS  PubMed  Google Scholar 

  • Felle HH, Zimmermann MR (2007) Systemic signaling in barley through action potentials. Planta 226:203–214

    Article  CAS  PubMed  Google Scholar 

  • Filek M, Kościelniak J (1997) 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). Plant Sci 123:39–46

    Article  CAS  Google Scholar 

  • Fisahn J, Herde O, Willmitzer L, Peña-Cortés H (2004) 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. Plant Cell Physiol 45:456–459

    Article  CAS  PubMed  Google Scholar 

  • Fischer BB, Hideg É, Krieger-Liszkay A (2013) Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid Redox Signal 18:2145–2162

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

  • Fromm J (1991) Control of phloem unloading by action potentials in Mimosa. Physiol Plant 83:529–533

    Article  Google Scholar 

  • Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469

    Article  Google Scholar 

  • Fromm J, Eshrich W (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. J Plant Physiol 141:673–680

    Article  CAS  Google Scholar 

  • Fromm J, Fei H (1998) Electrical signaling and gas exchange in maize plants of drying soil. Plant Sci 132:203–213

    Article  CAS  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    Article  CAS  PubMed  Google Scholar 

  • Fromm J, Hajirezaei MR, Becker VK, Lautner S (2013) Electrical signaling along the phloem and its physiological responses in the maize leaf. Front Plant Sci 4:239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Furch AC, Zimmermann MR, Will T, Hafke JB, van Bel AJ (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–7308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallé A, Lautner S, Flexas J, Ribas-Carbo M, Hanson D, Roesgen J, Fromm J (2013) Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO2. Plant Cell Environ 36:542–552

    Article  PubMed  CAS  Google Scholar 

  • Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Environ Exp Bot 114:15–21

    Article  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114

    Article  CAS  PubMed  Google Scholar 

  • Gradmann D (2001) Models for oscillations in plants. Aust J Plant Physiol 28:577–590

    CAS  Google Scholar 

  • Grams TEE, Koziolek C, Lautner S, Matyssek R, Fromm J (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

    Article  PubMed  Google Scholar 

  • Grams TEE, 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 Environ 32:319–326

    Article  CAS  PubMed  Google Scholar 

  • Herde O, Fuss H, Peña-Cortés H, Fisahn J (1995) Proteinase inhibitor II gene expression induced by electrical stimulation and control of photosynthetic activity in tomato plants. Plant Cell Physiol 36:737–742

    CAS  Google Scholar 

  • Herde O, Atzorn R, Fisahn J, Wasternack C, Willmitzer L, Pena-Cortes H (1996) Localized wounding by heat initiates the accumulation of proteinase inhibitor ii in abscisic acid-deficient plants by triggering jasmonic acid biosynthesis. Plant Physiol 112:853–860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Herde O, Peña-Cortés H, Willmitzer L, Fisahn J (1997) Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wiid-type and ABA-deficient tomato plants. Plant Cell Environ 20:136–141

    Article  CAS  Google Scholar 

  • Herde O, Pena Cortes H, Wasternack C, Willmitzer L, Fisahn J (1999a) Electric signaling and pin2 gene expression on different abiotic stimuli depend on a distinct threshold level of endogenous abscisic acid in several abscisic acid-deficient tomato mutants. Plant Physiol 119:213–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herde O, Peña-Cortés H, Fuss H, Willmitzer L, Fisahn J (1999b) Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants. Physiol Plant 105:179–184

    Article  CAS  Google Scholar 

  • Hlavácková V, Naus J (2007) Chemical signal as a rapid long-distance information messenger after local wounding of a plant? Plant Signal Behav 2:103–105

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hlavinka J, Nožková-Hlaváčková V, Floková K, Novák O, Nauš J (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

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LS (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Huang W, Yang SJ, Zhang SB, Zhang JL, Cao KF (2012) Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta 235:819–828

    Article  CAS  PubMed  Google Scholar 

  • Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389

    Article  CAS  PubMed  Google Scholar 

  • Johnson CH, Shingles R, Ettinger WF (2006) Regulation and role of calcium fluxes in the chloroplast. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 403–416

    Chapter  Google Scholar 

  • Julien JL, Desbiez MO, de Jaeger G, Frachisse JM (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L. J Exp Bot 42:131–137

    Article  Google Scholar 

  • Katicheva L, Sukhov V, Akinchits E, Vodeneev V (2014) Ionic nature of burn-induced variation potential in wheat leaves. Plant Cell Physiol 55:1511–1519

    Article  CAS  PubMed  Google Scholar 

  • Katicheva L, Sukhov V, Bushueva A, Vodeneev V (2015) Evaluation of the open time of calcium channels at variation potential generation in wheat leaf cells. Plant Signal Behav 10:e993231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim K, Portis AR Jr (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 571:124–128

    Article  CAS  PubMed  Google Scholar 

  • Kisnieriene V, Lapeikaite I, Sevriukova O, Ruksenas O (2016) The effects of Ni2+ on electrical signaling of Nitellopsis obtusa cells. J Plant Res. doi:10.1007/s10265-016-0794-3

    PubMed  Google Scholar 

  • Koziolek C, Grams TEE, Schreiber U, Matyssek R, Fromm J (2004) Transient knockout of photosynthesis mediated by electrical signals. New Phytol 161:715–722

    Article  CAS  Google Scholar 

  • Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163

    Article  CAS  Google Scholar 

  • Kreimer G, Melkonian M, Latzko E (1985) An electrogenic uniport mediates light-dependent Ca2+ influx into intact spinach chloroplasts. FEBS Lett 180:253–258

    Article  CAS  Google Scholar 

  • Krol E, Dziubinska H, Stolarz M, Trebacz K (2006) Effects of ion channel inhibitors on cold- and electrically-induced action potentials in Dionaea muscipula. Biol Plant 50:411–416

    Article  CAS  Google Scholar 

  • Król E, Dziubiñska H, Trêbacz K (2010) What do plants need action potentials for? In: DuBois ML (ed) Action potential: biophysical and cellular context, initiation, phases and propagation. Nova Science Publishers, New York, pp 1–26

    Google Scholar 

  • Krupenina NA, Bulychev AA (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

    Article  CAS  PubMed  Google Scholar 

  • Krupenina NA, Bulychev AA, Roelfsema MRG, Schreiber U (2008) Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding. Photochem Photobiol Sci 7:681–688

    Article  CAS  PubMed  Google Scholar 

  • Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers transport and sugar sensing. Plant Cell 11:707–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang RD, Volkov AG (2008) Solitary waves in soybean induced by localized thermal stress. Plant Signal Behav 3:224–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138:2200–2209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lautner S, Stummer M, Matyssek R, Fromm J, Grams TEE (2014) Involvement of respiratory processes in the transient knockout of net CO2 uptake in Mimosa pudica upon heat stimulation. Plant Cell Environ 37:254–260

    Article  CAS  PubMed  Google Scholar 

  • Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9

    Article  CAS  PubMed  Google Scholar 

  • Lovelli S, Scopa A, Perniola M, Di Tommaso T, Sofo A (2012) Abscisic acid root and leaf concentration in relation to biomass partitioning in salinized tomato plants. J Plant Physiol 169:226–233

    Article  CAS  PubMed  Google Scholar 

  • Luo HB, Ma L, Xi HF, Duan W, Li SH, Loescher W, Wang JF, Wang LJ (2011) Photosynthetic responses to heat treatments at different temperatures and following recovery in grapevine (Vitis amurensis L.) leaves. PLoS One 6:e23033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Malone M (1994) Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. New Phytol 128:49–56

    Article  Google Scholar 

  • Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Aust J Plant Physiol 26:55–61

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves–relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637

    Article  CAS  PubMed  Google Scholar 

  • Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signaling. Nature 500:422–426

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  CAS  PubMed  Google Scholar 

  • Murata N (2009) The discovery of state transitions in photosynthesis 40 years ago. Photosynth Res 99:155–160

    Article  CAS  PubMed  Google Scholar 

  • Muto S, Izawa S, Miyachi S (1982) Light-induced Ca2+ uptake by intact chloroplasts. FEBS Lett 139:250–254

    Article  CAS  Google Scholar 

  • Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, Aro EM, Nam HG, Lee CH (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett 587:3372–3381

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917

    Article  PubMed  Google Scholar 

  • Opritov VA, Pyatygin SS, Retivin VG (1991) Biolectrogenesis in higher plants. Nauka, Moskow

    Google Scholar 

  • Opritov VA, Lobov SA, Pyatygin SS, Mysyagin SA (2004) Analysis of possible involvement of local bioelectric responses in chilling perception by higher plants exemplified by Cucurbita pepo. Russ J Plant Physiol 52:801–808

    Article  CAS  Google Scholar 

  • Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans (I. Oxygen evolution and chlorophyll fluorescence). Plant Physiol 112:1245–1251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pavlovič A, Mancuso S (2011) Electrical signaling and photosynthesis. Can they co-exist together? Plant Sign Behav 6:840–842

    Article  CAS  Google Scholar 

  • Pavlovič A, Slováková L, Pandolfi C, Mancuso S (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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898

    Article  CAS  PubMed  Google Scholar 

  • Peña-Cortés H, Fisahn J, Willmitzer L (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci USA 92:4106–4113

    Article  PubMed  PubMed Central  Google Scholar 

  • Peters JS, Berkowitz GA (1991) Studies on the system regulating proton movement across the chloroplast envelope. Effects of ATPase inhibitors, Mg2+, and an amine anesthetic on stromal pH and photosynthesis. Plant Physiol 95:1229–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfannschmidt T, Allen JF, Oelmüller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112:1–9

    Article  CAS  Google Scholar 

  • Pikulenko MM, Bulychev AA (2005) Light-triggered action potentials and changes in quantum efficiency of photosystem ii in Anthoceros cells. Russ J Plant Physiol 52:584–590

    Article  CAS  Google Scholar 

  • Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55:285–291

    Article  CAS  Google Scholar 

  • Retivin VG, Opritov VA, Fedulina SB (1997) Generation of action potential induces preadaptation of Cucurbita pepo L. stem tissues to freezing injury. Russ J Plant Physiol 44:432–442

    CAS  Google Scholar 

  • Retivin VG, Opritov VA, Lobov SA, Tarakanov SA, Khudyakov VA (1999a) Changes in the resistance of photosynthesizing cotyledon cells of pumpkin seedlings to cooling and heating, as induced by the stimulation of the root system with KCl solution. Russ J Plant Physiol 46:689–696

    CAS  Google Scholar 

  • Retivin VG, Opritov VA, Abramova NN, Lobov SA, Fedulina SB (1999b) ATP level in the phloem exudate of higher plant shoot after propagation of electric responses to the burning or cooling. Vestn Nizhegorod Univ im NI Lobachevskogo, Ser Biol, 124–131

  • Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051

    Article  CAS  PubMed  Google Scholar 

  • Sevriukova O, Kanapeckaite A, Lapeikaite I, Kisnieriene V, Ladygiene R, Sakalauskas V (2014) Charophyte electrogenesis as a biomarker for assessing the risk from low-dose ionizing radiation to a single plant cell. J Environ Radioact 136:10–15

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52:712–722

    Article  CAS  PubMed  Google Scholar 

  • Shepherd VA, Beilby MJ, Al Khazaaly SA, Shimmen T (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant Cell Environ 31:1575–1591

    Article  CAS  PubMed  Google Scholar 

  • Sherstneva ON, Vodeneev VA, Katicheva LA, Surova LM, Sukhov VS (2015) Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings. Biochemistry (Moscow) 80:776–784

    Article  CAS  Google Scholar 

  • Sherstneva ON, Surova LM, Vodeneev VA, Plotnikova YI, Bushueva AV, Sukhov VS (2016) The role of the intra- and extracellular protons in the photosynthetic response induced by the variation potential in pea seedlings. Biochem (Moscow) Suppl Ser A 10:60–67

    Article  Google Scholar 

  • Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30

    Article  CAS  PubMed  Google Scholar 

  • Sibaoka T (1991) Rapid plant movements triggered by action potentials. Bot Mag Tokyo 104:73–95

    Article  Google Scholar 

  • Song C-P, Guo Y, Qiu Q, Lambert G, Galbraith DW, Jagendorf A, Zhu J-K (2004) A probable Na+ (K+) H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10211–10216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Stanković B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279

    Article  PubMed  Google Scholar 

  • Sukhov V, Vodeneev V (2009) A mathematical model of action potential in cells of vascular plants. J Membr Biol 232:59–67

    Article  CAS  PubMed  Google Scholar 

  • Sukhov VS, Pyatygin SS, Opritov VA, Krauz VO (2008a) Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: theoretical analysis. Biophysics 53:308–312

    Article  Google Scholar 

  • Sukhov VS, Pyatygin SS, Opritov VA, Krauz VO (2008b) Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: experimental analysis. Biophysics 53:226–228

    Article  Google Scholar 

  • Sukhov V, Nerush V, Orlova L, Vodeneev V (2011) Simulation of action potential propagation in plants. J Theor Biol 291:47–55

    Article  PubMed  Google Scholar 

  • Sukhov V, Orlova L, Mysyagin S, Sinitsina J, Vodeneev V (2012) Analysis of the photosynthetic response induced by variation potential in geranium. Planta 235:703–712

    Article  CAS  PubMed  Google Scholar 

  • Sukhov V, Akinchits E, Katicheva L, Vodeneev V (2013a) Simulation of variation potential in higher plant cells. J Membr Biol 246:287–296

    Article  CAS  PubMed  Google Scholar 

  • Sukhov VS, Kalinin VA, Surova LM, Sherstneva ON, Vodeneev VA (2013b) Mathematical simulation of H+-sucrose symporter of plasma membrane in higher plants. Biochem (Moscow) Suppl Ser A 7:163–169

    Article  Google Scholar 

  • Sukhov VS, Surova LM, Sherstneva ON, Rumyantsev EA, Vodeneev VA (2013c) Influence of a variation potential on photosynthesis in pumpkin seedlings (Cucurbita pepo L.). Biophysics 58:361–365

    Article  CAS  Google Scholar 

  • Sukhov V, Sherstneva O, Surova L, Katicheva L, Vodeneev V (2014a) Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant Cell Environ 37:2532–2541

    Article  CAS  PubMed  Google Scholar 

  • Sukhov V, Surova L, Sherstneva O, Vodeneev V (2014b) Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. Physiol Plant 152:773–783

    Article  CAS  PubMed  Google Scholar 

  • Sukhov V, Surova L, Sherstneva O, Bushueva A, Vodeneev V (2015a) Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Funct Plant Biol 42:727–736

    Article  Google Scholar 

  • Sukhov V, Surova L, Sherstneva O, Katicheva L, Vodeneev V (2015b) Variation potential influence on photosynthetic cyclic electron flow in pea. Front Plant Sci 5:766

    Article  PubMed  PubMed Central  Google Scholar 

  • Surova L, Sherstneva O, Vodeneev V, Sukhov V (2016) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Sign Behav 11:e1145334

    Article  CAS  Google Scholar 

  • Suzuki N, Mittler R (2012) Reactive oxygen species-dependent wound responses in animals and plants. Free Radic Biol Med 53:2269–2276

    Article  CAS  PubMed  Google Scholar 

  • Tikhonov AN (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534

    Article  CAS  PubMed  Google Scholar 

  • Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Aro EM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215

    Article  CAS  PubMed  Google Scholar 

  • Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764

    Article  CAS  PubMed  Google Scholar 

  • Trebacz K, Sievers A (1998) Action potentials evoked by light in traps of Dionaea muscipula Ellis. Plant Cell Physiol 39:369–372

    Article  CAS  Google Scholar 

  • Trebacz K, Dziubinska H, Krol 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, New York, pp 277–290

    Google Scholar 

  • Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523

    Article  CAS  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vodeneev VA, Opritov VA, Pyatygin SS (2006) Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo. Russ J Plant Physiol 53:481–487

    Article  CAS  Google Scholar 

  • 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. Russ J Plant Physiol 58:974–981

    Article  CAS  Google Scholar 

  • 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. J Plant Physiol 169:949–954

    Article  CAS  PubMed  Google Scholar 

  • Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signal Behav 10:e1057365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Volkov AG, Adesina T, Markin VS, Jovanov E (2008a) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkov AG, Coopwood KJ, Markin VS (2008b) Inhibition of the Dionaea muscipula Ellis trap closure by ion and water channels blockers and uncouplers. Plant Sci 175:642–649

    Article  CAS  Google Scholar 

  • Vredenberg W, Pavlovič A (2013) Chlorophyll a fluorescence induction (Kautsky curve) in a Venus flytrap (Dionaea muscipula) leaf after mechanical trigger hair irritation. J Plant Physiol 170:242–250

    Article  CAS  PubMed  Google Scholar 

  • Wacke M, Thiel G, Hütt MT (2003) Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. J Membr Biol 191:179–192

    Article  CAS  PubMed  Google Scholar 

  • Werdan K, Heldt HW, Milovancev M (1975) The role of pH in the regulation of carbon fixation in the chloroplast stroma. Studies on CO2 fixation in the light and dark. Biochim Biophys Acta 396:276–292

    Article  CAS  PubMed  Google Scholar 

  • Wolosiuk RA, Ballicora MA, Hagelin K (1993) The reductive pentose phosphate cycle for photosynthetic CO2 assimilation: enzyme modulation. FASEB J 7:622–637

    CAS  PubMed  Google Scholar 

  • Wu W, Berkowitz GA (1992) Stromal pH and photosynthesis are affected by electroneutral K+ and H+ exchange through chloroplast envelope ion channels. Plant Physiol 98:666–672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68:966–976

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Sharkey TD (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100:29–43

    Article  CAS  PubMed  Google Scholar 

  • Zhao DJ, Wang ZY, Huang L, Jia YP, Leng JQ (2014) Spatio-temporal mapping of variation potentials in leaves of Helianthus annuus L. seedlings in situ using multi-electrode array. Sci Rep 4:5435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao DJ, Chen Y, Wang ZY, Xue L, Mao TL, Liu YM, Wang ZY, Huang L (2015) High-resolution non-contact measurement of the electrical activity of plants in situ using optical recording. Sci Rep 5:13425

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 149:1593–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Investigations of the average dynamics of the photosynthetic response in the second leaf were supported by the Russian Science Foundation (Project No. 14-26-00098).

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  1. Department of Biophysics, N. I. Lobachevsky State University of Nizhny Novgorod, Gagarin Avenue 23, Nizhny Novgorod, Russia, 603950

    Vladimir Sukhov

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Sukhov, V. Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130, 373–387 (2016). https://doi.org/10.1007/s11120-016-0270-x

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