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Photosynthesis Research

, Volume 130, Issue 1–3, pp 373–387 | Cite as

Electrical signals as mechanism of photosynthesis regulation in plants

  • Vladimir Sukhov
Review

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.

Keywords

Action potential Electrical signals Photosynthesis Photosynthesis regulation System potential Variation potential 

Notes

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).

References

  1. Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69PubMedCrossRefGoogle Scholar
  2. 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 137:263–273PubMedPubMedCentralCrossRefGoogle Scholar
  3. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550PubMedCrossRefGoogle Scholar
  4. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19PubMedCrossRefGoogle Scholar
  5. 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 107:19260–19265PubMedPubMedCentralCrossRefGoogle Scholar
  6. Beilby MJ (1982) C1 channels in Chara. Philos Trans R Soc London B 299:435–445CrossRefGoogle Scholar
  7. Beilby MJ (1984) Calcium and plant action potentials. Plant Cell Environ 7:415–421CrossRefGoogle Scholar
  8. Beilby MJ (2007) Action potential in charophytes. Int Rev Cytol 257:43–82PubMedCrossRefGoogle Scholar
  9. 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 21:3965–3983CrossRefGoogle Scholar
  10. 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 78:3536–3540PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bukhov NG (2004) Dynamic light regulation of photosynthesis (a review). Russ J Plant Physiol 51:742–753CrossRefGoogle Scholar
  12. 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 59:81–93CrossRefGoogle Scholar
  13. Bulychev AA, Komarova AV (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells. Biochemistry (Moscow) 79: 273–281Google Scholar
  14. 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 4:232–239CrossRefGoogle Scholar
  15. 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 202:11–19PubMedCrossRefGoogle Scholar
  16. 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 60:33–40CrossRefGoogle Scholar
  17. 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 309–320Google Scholar
  18. Degli Agosti R (2014) Touch-induced action potentials in Arabidopsis thaliana. Arch Des Sci 67:125–138Google Scholar
  19. Dziubinska H, Trêbacz K (1989) Zawadzki T The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum. Physiol Plant 75:417–423CrossRefGoogle Scholar
  20. 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 160:1203–1210PubMedCrossRefGoogle Scholar
  21. Evron Y, Johnson EA, McCarty RE (2000) Regulation of proton flow and ATP synthesis in chloroplasts. J Bioenerg Biomembr 32:501–506PubMedCrossRefGoogle Scholar
  22. Farmer EE, Ryan CA (1990) Interplant communication—airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716PubMedPubMedCentralCrossRefGoogle Scholar
  23. Favre P, Degli Agosti R (2007) Voltage-dependent action potentials in Arabidopsis thaliana. Physiol Plant 131:263–272PubMedGoogle Scholar
  24. Favre P, Greppin H, Degli Agosti R (2011) Accession-dependent action potentials in Arabidopsis. J Plant Physiol 168:653–660PubMedCrossRefGoogle Scholar
  25. Felle HH, Zimmermann MR (2007) Systemic signaling in barley through action potentials. Planta 226:203–214PubMedCrossRefGoogle Scholar
  26. 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 123:39–46CrossRefGoogle Scholar
  27. 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 45:456–459PubMedCrossRefGoogle Scholar
  28. Fischer BB, Hideg É, Krieger-Liszkay A (2013) Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid Redox Signal 18:2145–2162PubMedCrossRefGoogle Scholar
  29. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905PubMedCrossRefGoogle Scholar
  30. Fromm J (1991) Control of phloem unloading by action potentials in Mimosa. Physiol Plant 83:529–533CrossRefGoogle Scholar
  31. Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469CrossRefGoogle Scholar
  32. Fromm J, Eshrich W (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. J Plant Physiol 141:673–680CrossRefGoogle Scholar
  33. Fromm J, Fei H (1998) Electrical signaling and gas exchange in maize plants of drying soil. Plant Sci 132:203–213CrossRefGoogle Scholar
  34. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedCrossRefGoogle Scholar
  35. 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 4:239PubMedPubMedCentralCrossRefGoogle Scholar
  36. 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 61:3697–7308PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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 36:542–552PubMedCrossRefGoogle Scholar
  38. Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Environ Exp Bot 114:15–21CrossRefGoogle Scholar
  39. Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114PubMedCrossRefGoogle Scholar
  40. Gradmann D (2001) Models for oscillations in plants. Aust J Plant Physiol 28:577–590Google Scholar
  41. 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 30:79–84PubMedCrossRefGoogle Scholar
  42. 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 32:319–326PubMedCrossRefGoogle Scholar
  43. 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 36:737–742Google Scholar
  44. 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 112:853–860PubMedPubMedCentralGoogle Scholar
  45. 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 20:136–141CrossRefGoogle Scholar
  46. 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 119:213–218PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 105:179–184CrossRefGoogle Scholar
  48. Hlavácková V, Naus J (2007) Chemical signal as a rapid long-distance information messenger after local wounding of a plant? Plant Signal Behav 2:103–105PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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 225:235–244PubMedCrossRefGoogle Scholar
  50. 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 54:89–96PubMedCrossRefGoogle Scholar
  51. 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 6:420PubMedPubMedCentralGoogle Scholar
  52. 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 235:819–828PubMedCrossRefGoogle Scholar
  53. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389PubMedCrossRefGoogle Scholar
  54. 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 403–416CrossRefGoogle Scholar
  55. 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 42:131–137CrossRefGoogle Scholar
  56. Katicheva L, Sukhov V, Akinchits E, Vodeneev V (2014) Ionic nature of burn-induced variation potential in wheat leaves. Plant Cell Physiol 55:1511–1519PubMedCrossRefGoogle Scholar
  57. 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:e993231PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kim K, Portis AR Jr (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 571:124–128PubMedCrossRefGoogle Scholar
  59. 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 PubMedGoogle Scholar
  60. Koziolek C, Grams TEE, Schreiber U, Matyssek R, Fromm J (2004) Transient knockout of photosynthesis mediated by electrical signals. New Phytol 161:715–722CrossRefGoogle Scholar
  61. Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163CrossRefGoogle Scholar
  62. Kreimer G, Melkonian M, Latzko E (1985) An electrogenic uniport mediates light-dependent Ca2+ influx into intact spinach chloroplasts. FEBS Lett 180:253–258CrossRefGoogle Scholar
  63. 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 50:411–416CrossRefGoogle Scholar
  64. 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 1–26Google Scholar
  65. 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 1767:781–788PubMedCrossRefGoogle Scholar
  66. 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 7:681–688PubMedCrossRefGoogle Scholar
  67. 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 11:707–726PubMedPubMedCentralCrossRefGoogle Scholar
  68. Lang RD, Volkov AG (2008) Solitary waves in soybean induced by localized thermal stress. Plant Signal Behav 3:224–228PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138:2200–2209PubMedPubMedCentralCrossRefGoogle Scholar
  70. 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 37:254–260PubMedCrossRefGoogle Scholar
  71. Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9PubMedCrossRefGoogle Scholar
  72. 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 169:226–233PubMedCrossRefGoogle Scholar
  73. 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:e23033PubMedPubMedCentralCrossRefGoogle Scholar
  74. Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96CrossRefGoogle Scholar
  75. Malone M (1994) Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. New Phytol 128:49–56CrossRefGoogle Scholar
  76. Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Aust J Plant Physiol 26:55–61CrossRefGoogle Scholar
  77. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  78. 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 46:629–637PubMedCrossRefGoogle Scholar
  79. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signaling. Nature 500:422–426PubMedCrossRefGoogle Scholar
  80. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 429:579–582PubMedCrossRefGoogle Scholar
  82. Murata N (2009) The discovery of state transitions in photosynthesis 40 years ago. Photosynth Res 99:155–160PubMedCrossRefGoogle Scholar
  83. Muto S, Izawa S, Miyachi S (1982) Light-induced Ca2+ uptake by intact chloroplasts. FEBS Lett 139:250–254CrossRefGoogle Scholar
  84. 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 587:3372–3381PubMedCrossRefGoogle Scholar
  85. 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 274:1914–1917PubMedCrossRefGoogle Scholar
  86. Opritov VA, Pyatygin SS, Retivin VG (1991) Biolectrogenesis in higher plants. Nauka, MoskowGoogle Scholar
  87. 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 52:801–808CrossRefGoogle Scholar
  88. Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans (I. Oxygen evolution and chlorophyll fluorescence). Plant Physiol 112:1245–1251PubMedPubMedCentralGoogle Scholar
  89. Pavlovič A, Mancuso S (2011) Electrical signaling and photosynthesis. Can they co-exist together? Plant Sign Behav 6:840–842CrossRefGoogle Scholar
  90. 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 62:1991–2000PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898PubMedCrossRefGoogle Scholar
  92. 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 92:4106–4113PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 95:1229–1236PubMedPubMedCentralCrossRefGoogle Scholar
  94. Pfannschmidt T, Allen JF, Oelmüller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112:1–9CrossRefGoogle Scholar
  95. Pikulenko MM, Bulychev AA (2005) Light-triggered action potentials and changes in quantum efficiency of photosystem ii in Anthoceros cells. Russ J Plant Physiol 52:584–590CrossRefGoogle Scholar
  96. Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55:285–291CrossRefGoogle Scholar
  97. 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 44:432–442Google Scholar
  98. 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 46:689–696Google Scholar
  99. 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, 124–131Google Scholar
  100. Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362PubMedPubMedCentralCrossRefGoogle Scholar
  101. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051PubMedCrossRefGoogle Scholar
  102. 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 136:10–15PubMedCrossRefGoogle Scholar
  103. Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52:712–722PubMedCrossRefGoogle Scholar
  104. 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 31:1575–1591PubMedCrossRefGoogle Scholar
  105. 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) 80:776–784CrossRefGoogle Scholar
  106. 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 10:60–67CrossRefGoogle Scholar
  107. Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30PubMedCrossRefGoogle Scholar
  108. Sibaoka T (1991) Rapid plant movements triggered by action potentials. Bot Mag Tokyo 104:73–95CrossRefGoogle Scholar
  109. 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 101:10211–10216PubMedPubMedCentralCrossRefGoogle Scholar
  110. Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64PubMedCrossRefGoogle Scholar
  111. 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 291–308Google Scholar
  112. Stanković B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279PubMedCrossRefGoogle Scholar
  113. Sukhov V, Vodeneev V (2009) A mathematical model of action potential in cells of vascular plants. J Membr Biol 232:59–67PubMedCrossRefGoogle Scholar
  114. Sukhov VS, Pyatygin SS, Opritov VA, Krauz VO (2008a) Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: theoretical analysis. Biophysics 53:308–312CrossRefGoogle Scholar
  115. Sukhov VS, Pyatygin SS, Opritov VA, Krauz VO (2008b) Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: experimental analysis. Biophysics 53:226–228CrossRefGoogle Scholar
  116. Sukhov V, Nerush V, Orlova L, Vodeneev V (2011) Simulation of action potential propagation in plants. J Theor Biol 291:47–55PubMedCrossRefGoogle Scholar
  117. Sukhov V, Orlova L, Mysyagin S, Sinitsina J, Vodeneev V (2012) Analysis of the photosynthetic response induced by variation potential in geranium. Planta 235:703–712PubMedCrossRefGoogle Scholar
  118. Sukhov V, Akinchits E, Katicheva L, Vodeneev V (2013a) Simulation of variation potential in higher plant cells. J Membr Biol 246:287–296PubMedCrossRefGoogle Scholar
  119. 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 7:163–169CrossRefGoogle Scholar
  120. 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 58:361–365CrossRefGoogle Scholar
  121. 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 37:2532–2541PubMedCrossRefGoogle Scholar
  122. 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 152:773–783PubMedCrossRefGoogle Scholar
  123. 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 42:727–736CrossRefGoogle Scholar
  124. Sukhov V, Surova L, Sherstneva O, Katicheva L, Vodeneev V (2015b) Variation potential influence on photosynthetic cyclic electron flow in pea. Front Plant Sci 5:766PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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:e1145334CrossRefGoogle Scholar
  126. Suzuki N, Mittler R (2012) Reactive oxygen species-dependent wound responses in animals and plants. Free Radic Biol Med 53:2269–2276PubMedCrossRefGoogle Scholar
  127. Tikhonov AN (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534PubMedCrossRefGoogle Scholar
  128. Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183PubMedCrossRefGoogle Scholar
  129. Tikkanen M, Aro EM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17PubMedCrossRefGoogle Scholar
  130. Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215PubMedCrossRefGoogle Scholar
  131. Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764PubMedCrossRefGoogle Scholar
  132. Trebacz K, Sievers A (1998) Action potentials evoked by light in traps of Dionaea muscipula Ellis. Plant Cell Physiol 39:369–372CrossRefGoogle Scholar
  133. 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 277–290Google Scholar
  134. 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 163:515–523CrossRefGoogle Scholar
  135. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737PubMedCrossRefGoogle Scholar
  136. 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 20:648–657PubMedPubMedCentralCrossRefGoogle Scholar
  137. 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 53:481–487CrossRefGoogle Scholar
  138. 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 58:974–981CrossRefGoogle Scholar
  139. 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 169:949–954PubMedCrossRefGoogle Scholar
  140. Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signal Behav 10:e1057365PubMedPubMedCentralCrossRefGoogle Scholar
  141. Volkov AG, Adesina T, Markin VS, Jovanov E (2008a) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702PubMedPubMedCentralCrossRefGoogle Scholar
  142. 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 175:642–649CrossRefGoogle Scholar
  143. 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 170:242–250PubMedCrossRefGoogle Scholar
  144. Wacke M, Thiel G, Hütt MT (2003) Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. J Membr Biol 191:179–192PubMedCrossRefGoogle Scholar
  145. 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 396:276–292PubMedCrossRefGoogle Scholar
  146. Wolosiuk RA, Ballicora MA, Hagelin K (1993) The reductive pentose phosphate cycle for photosynthetic CO2 assimilation: enzyme modulation. FASEB J 7:622–637PubMedGoogle Scholar
  147. Wu W, Berkowitz GA (1992) Stromal pH and photosynthesis are affected by electroneutral K+ and H+ exchange through chloroplast envelope ion channels. Plant Physiol 98:666–672PubMedPubMedCentralCrossRefGoogle Scholar
  148. 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 68:966–976PubMedCrossRefGoogle Scholar
  149. Zhang R, Sharkey TD (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100:29–43PubMedCrossRefGoogle Scholar
  150. 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 4:5435PubMedPubMedCentralGoogle Scholar
  151. 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 5:13425PubMedPubMedCentralCrossRefGoogle Scholar
  152. Zimmermann MR, Felle HH (2009) Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities. Planta 229:539–547PubMedCrossRefGoogle Scholar
  153. 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 149:1593–1600PubMedPubMedCentralCrossRefGoogle Scholar
  154. 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 117:529–546PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of BiophysicsN. I. Lobachevsky State University of Nizhny NovgorodNizhny NovgorodRussia

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