Photosynthesis Research

, Volume 136, Issue 2, pp 215–228 | Cite as

Influence of the variation potential on photosynthetic flows of light energy and electrons in pea

  • Ekaterina Sukhova
  • Maxim Mudrilov
  • Vladimir Vodeneev
  • Vladimir Sukhov
Original Article
  • 156 Downloads

Abstract

Local damage (mainly burning, heating, and mechanical wounding) induces propagation of electrical signals, namely, variation potentials, which are important signals during the life of plants that regulate different physiological processes, including photosynthesis. It is known that the variation potential decreases the rate of CO2 assimilation by the Calvin–Benson cycle; however, its influence on light reactions has been poorly investigated. The aim of our work was to investigate the influence of the variation potential on the light energy flow that is absorbed, trapped and dissipated per active reaction centre in photosystem II and on the flow of electrons through the chloroplast electron transport chain. We analysed chlorophyll fluorescence in pea leaves using JIP-test and PAM-fluorometry; we also investigated delayed fluorescence. The electrical signals were registered using extracellular electrodes. We showed that the burning-induced variation potential stimulated a nonphotochemical loss of energy in photosystem II under dark conditions. It was also shown that the variation potential gradually increased the flow of light energy absorbed, trapped and dissipated by photosystem II. These changes were likely caused by an increase in the fraction of absorbed light distributed to photosystem II. In addition, the variation potential induced a transient increase in electron flow through the photosynthetic electron transport chain. Some probable mechanisms for the influence of the variation potential on the light reactions of photosynthesis (including the potential role of intracellular pH decrease) are discussed in the work.

Keywords

Electron flow Light energy dissipation Light energy flow pH changes Regulation of photosynthesis Variation potential 

Notes

Acknowledgements

The detailed investigation of photosynthetic flows of light energy and electrons was supported by the Russian Science Foundation (Project No. 17-76-20032). The investigation of the dependence of photosynthetic changes on variation potential propagation was supported by the Ministry of Education and Science of the Russian Federation (contract no. 6.3199.2017/PCh).

Supplementary material

11120_2017_460_MOESM1_ESM.pdf (188 kb)
Supplementary material 1 (PDF 188 KB)

References

  1. Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B 104:1–8PubMedCrossRefGoogle Scholar
  2. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32PubMedCrossRefGoogle Scholar
  3. Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36:4149–4154PubMedCrossRefGoogle Scholar
  4. Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443–1453PubMedPubMedCentralCrossRefGoogle Scholar
  5. Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371PubMedCrossRefGoogle Scholar
  6. Avenson TJ, Kanazawa A, Cruz JA, Takizawa K, Ettinger WE, Kramer DM (2005) Integrating the proton circuit into photosynthesis: progress and challenges. Plant Cell Environ 28:97–109CrossRefGoogle Scholar
  7. Beilby MJ (2007) Action potential in Charophytes. Int Rev Cytol 257:43–82PubMedCrossRefGoogle Scholar
  8. Beilby MJ, Walker NA (1981) Chloride transport in Chara. J Exp Bot 32:43–54CrossRefGoogle Scholar
  9. Beilby MJ, Shepherd VA, Absolonova M (2017) The role of H+/OH channels in saline pathology of Chara australis: brief history. Botany Let. doi: 10.1080/23818107.2017.1356745 Google Scholar
  10. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1113–1121Google Scholar
  11. Białasek M, Górecka M, Mittler R, Karpiński S (2017) Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis. Plant Cell Physiol. doi: 10.1093/pcp/pcw232 PubMedPubMedCentralGoogle Scholar
  12. Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci 2:85PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bulychev AA, Komarova AV (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells. BioChemistry 79:273–281PubMedGoogle Scholar
  14. Charles SA, Halliwell B (1980) Action of calcium ions on spinach (Spinacia oleracea) chloroplast fructose bisphosphatase and other enzymes of the Calvin cycle. Biochem J 188:775–779PubMedPubMedCentralCrossRefGoogle Scholar
  15. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228CrossRefGoogle Scholar
  16. Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 49:377–386PubMedCrossRefGoogle Scholar
  17. Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill S (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Funct Plant Biol 31:913–920CrossRefGoogle Scholar
  18. Dziubinska H, Filek M, Koscielniak J, Trebacz K (2003) Variation and action potentials evoked by thermal stimuli accompany enhacement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. J Plant Physiol 160:1203–1210PubMedCrossRefGoogle Scholar
  19. Eremin A, Bulychev A, Hauser MJ (2013) Cyclosis-mediated transfer of H2O2 elicited by localized illumination of Chara cells and its relevance to the formation of pH bands. Protoplasma 250:1339–1349PubMedCrossRefGoogle Scholar
  20. Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1385PubMedPubMedCentralCrossRefGoogle Scholar
  21. Finazzi G, Petroutsos D, Tomizioli M, Flori S, Sautron E, Villanova V, Rolland N, Seigneurin-Berny D (2015) Ions channels/transporters and chloroplast regulation. Cell Calcium 58:86–97PubMedCrossRefGoogle Scholar
  22. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedCrossRefGoogle Scholar
  23. 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
  24. Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signaling. Environ Exp Bot 114:15–21CrossRefGoogle Scholar
  25. García-Plazaola JI, Esteban R, Fernández-Marín B, Kranner I, Porcar-Castell (2012) A thermal energy dissipation and xanthophyll cycles beyond the Arabidopsis model. Photosynth Res 113:89–103PubMedCrossRefGoogle Scholar
  26. 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 Physiol 171:1606–1615PubMedPubMedCentralCrossRefGoogle Scholar
  27. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101:217–232PubMedCrossRefGoogle Scholar
  28. Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893CrossRefGoogle Scholar
  29. Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32PubMedCrossRefGoogle Scholar
  30. 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
  31. Hlaváčková V, Nauš J (2007) Chemical signal as a rapid long-distance information messenger after local wounding of a plant? Plant Signal Behav 2:103–105PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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
  33. 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 pretreated by ABA. Plant Physiol Biochem 54:89–96PubMedCrossRefGoogle Scholar
  34. Höhner R, Aboukila A, Kunz H-H, Venema K (2016) Proton gradients and proton-dependent transport processes in the chloroplast. Front Plant Sci 7:218PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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
  36. Hung S-H, Yu C-W, Lin CH (2005) Hydrogen peroxide functions as a stress signal in plants. Bot Bull Acad Sin 46:1–10Google Scholar
  37. Ivanov AG, Allakhverdiev SI, Huner NPA, Murata N (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 1817:1374–1379PubMedCrossRefGoogle Scholar
  38. Jahns P, Latowski D, Strzalka K (2008) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14PubMedCrossRefGoogle Scholar
  39. Kalaji HM, Carpentier R, Allakhverdiev SI, Bosa K (2012) Fluorescence parameters as early indicators of light stress in barley. J Photochem Photobiol B 112:1–6PubMedCrossRefGoogle Scholar
  40. 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
  41. Kim K, Portis AR Jr (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 571:124–128PubMedCrossRefGoogle Scholar
  42. Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14Google Scholar
  43. Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12PubMedCrossRefGoogle Scholar
  44. Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163CrossRefGoogle Scholar
  45. Krausko M, Perutka Z, Šebela M, Šamajová O, Šamaj J, Novák O, Pavlovič A (2017) The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis. New Phytol 213:1818–1835PubMedCrossRefGoogle Scholar
  46. Kreslavski VD, Carpentier R, Klimov VV, Allakhverdiev SI (2009) Transduction mechanisms of photoreceptor signals in plant cells. J Photochem Photobiol C: Photochem Rev 10:63–80CrossRefGoogle Scholar
  47. Kreslavski VD, Fomina IR, Los DA, Carpentier R, Kuznetsov VV, Allakhverdiev SI (2012) Red and near infra-red signaling: hypothesis and perspectives. J Photochem Photobiol C 13:190–203CrossRefGoogle Scholar
  48. Król E, Dziubińska H, Trebacz K (2010) What do plants need action potentials for? In: Action Potential: DuBois ML (ed) Biophysical and cellular context, initiation, phases and propagation. Nova Science Publishers, New York, pp 1–26Google Scholar
  49. 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
  50. 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
  51. 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
  52. León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signaling in plant. J Exp Bot 52:1–9PubMedCrossRefGoogle Scholar
  53. Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Aust J Plant Physiol 26:55–61CrossRefGoogle Scholar
  54. Mathieu Y, Guern J, Kurkdjian A, Manigault P, Manigault J, Zielinska T, Gillet B, Beloeil J-C, Lallemand J-Y (1989) Regulation of vacuolar pH of plant cells. Plant Physiol 89:19–26PubMedPubMedCentralCrossRefGoogle Scholar
  55. Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of photosystem II in wheat leaves (Triticum aestivum). Biochim Biophys Acta 1807:22–29PubMedCrossRefGoogle Scholar
  56. Maxwell K, Johnson GN (2000) Chlorofill fluorescence—a partical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  57. Mehta P, Allakhverdiev SI, Jajoo A (2010) Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth Res 105:249–255PubMedCrossRefGoogle Scholar
  58. Miyake C, Shinzaki Y, Miyata M, Tomizawa K (2004) Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching (NPQ) of Chl fluorescence in intact leaves of tobacco plants. Plant Cell Physiol 45:1426–1433PubMedCrossRefGoogle Scholar
  59. 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
  60. Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94:217–224PubMedCrossRefGoogle Scholar
  61. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedPubMedCentralCrossRefGoogle Scholar
  62. Muñoz R, Quiles MJ (2013) Illumination in hibiscus plants. Int J Mol Sci 14:5432–5444PubMedPubMedCentralCrossRefGoogle Scholar
  63. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421PubMedCrossRefGoogle Scholar
  64. 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
  65. Pavlovič A, Jakšová J, Novák O (2017) Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol. doi: 10.1111/nph.14747 Google Scholar
  66. 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
  67. Pfannschmidt T, Bräutigam K, Wagner R, Dietzel L, Schröter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103:599–607PubMedCrossRefGoogle Scholar
  68. Poonam R, Kaur R, Bali S, Kaur P, Sirhindi G, Thukral AK, Ohri P, Vig AP (2015) Role of various hormones in photosynthetic responses of green plants under environmental stresses. Curr Protein Pept Sci 16:435–449PubMedCrossRefGoogle Scholar
  69. Prásil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery process. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology. Elsevier Science Publishers, Amsterdam, pp 295–348Google Scholar
  70. Quiles MJ, López NI (2004) Photoinhibition of photosystems I and II induced by exposure to high light intensity during oat plant growth. Effects on the chloroplast NADH dehydrogenase complex. Plant Sci 166:815–823CrossRefGoogle Scholar
  71. Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202CrossRefGoogle Scholar
  72. Rochaix J-D, Lemeille S, Shapiguzov A, Samol I, Fucile G, Willig A, Goldschmidt-Clermont M (2012) Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment. Phil Trans R Soc B 367:3466–3474PubMedPubMedCentralCrossRefGoogle Scholar
  73. Ruban AV, Young AJ, Horton P (1993) Induction of nonphotochemical energy dissipation and absorbance changes in leaves. Evidence for changes in the state of the light-harvesting system of photosystem II in vivo. Plant Physiol 102:741–750PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 80:776–784PubMedGoogle Scholar
  75. Sherstneva ON, Surova LM, Vodeneev VA, Plotnikova YI, Bushueva AV, Sukhov VS (2016a) The role of the intra- and extracellular protons in the photosynthetic response induced by the variation potential in pea seedlings. Biochemistry (Mosc) Suppl Ser A 10:60–67CrossRefGoogle Scholar
  76. Sherstneva ON, Vodeneev VA, Surova LM, Novikova EM, Sukhov VS (2016b) Application of a mathematical model of variation potential for analysis of its influence on photosynthesis in higher plants. Biochem Moscow Suppl Ser A 10:269–277CrossRefGoogle Scholar
  77. Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signalling: an emerging field. J Exp Bot 63:1525–1542PubMedCrossRefGoogle Scholar
  78. 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, Berlin, pp 291–309Google Scholar
  79. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisme, regulation and adaptation. Taylor and Francis, London, pp 445–483Google Scholar
  80. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326PubMedCrossRefGoogle Scholar
  81. Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130:373–387PubMedCrossRefGoogle Scholar
  82. Sukhov V, Vodeneev V (2009) A mathematical model of action potential in cells of vascular plants. J Membrane Biol 232:59–67CrossRefGoogle Scholar
  83. 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
  84. Sukhov V, Akinchits E, Katicheva L, Vodeneev V (2013) Simulation of variation potential in higher plant cells. J Membrane Biol 246:287–296CrossRefGoogle Scholar
  85. Sukhov V, Sherstneva O, Surova L, Katicheva L, Vodeneev V (2014) Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant Cell Environ 37:2532–2541PubMedCrossRefGoogle Scholar
  86. Sukhov V, Surova L, Sherstneva O, Katicheva L, Vodeneev V (2015) Variation potential in fluence on photosynthetic cyclic electron flow in pea. Front Plant Sci 5:766PubMedPubMedCentralCrossRefGoogle Scholar
  87. Sukhov V, Surova L, Morozova E, Sherstneva O, Vodeneev V (2016) Changes in H+-ATP synthase activity, proton gradient, and pH in pea chloroplast can be connected with variation potential. Front Plant Sci 7:1092PubMedPubMedCentralCrossRefGoogle Scholar
  88. Sukhov VS, Gaspirovich VV, Gromova EN, Ladeynova MM, Sinitsyna YV, Berezina EV, Akinchits EK, Vodeneev VA (2017) Decrease of mesophyll conductance to CO2 is a possible mechanism of abscisic acid influence on photosynthesis in seedlings of pea and wheat. Biochem Moscow Suppl Ser A 11:237–247CrossRefGoogle Scholar
  89. Sukhova E, Akinchits E, Sukhov V (2017) Mathematical models of electrical activity in plants. J Membr Biol 250:407–423PubMedCrossRefGoogle Scholar
  90. Surova L, Sherstneva O, Vodeneev V, Katicheva L, Semina M, Sukhov V (2016a) Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves. J Plant Physiol 202:57–64PubMedCrossRefGoogle Scholar
  91. Surova L, Sherstneva O, Vodeneev V, Sukhov V (2016b) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Sign Behav 11, e1145334CrossRefGoogle Scholar
  92. Tikhonov AN (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534PubMedCrossRefGoogle Scholar
  93. Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183PubMedCrossRefGoogle Scholar
  94. Trebacz K, Dziubinska H, Krol E (2006) Electrical signals in longdistance communication in plants. In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants. Neuronal aspects of plant life. Springer, Berlin, pp 277–290Google Scholar
  95. 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 58:974–981Google Scholar
  96. Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Sign Behav 10:e1057365CrossRefGoogle Scholar
  97. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  98. 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
  99. 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
  100. Wolosiuk RA, Ballicora MA, Hagelin K (1993) The reductive pentose phosphate cycle for photosynthetic CO2 assimilation: enzyme modulation. FASEB J 7:622–637PubMedCrossRefGoogle Scholar
  101. Yamburenko MV, Zubo YO, Börner T (2015) Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: repression by guanosine-30-50-bisdiphosphate and activation by sigma factor 5. Plant J 82:1030–1041PubMedCrossRefGoogle Scholar
  102. 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
  103. 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
  104. 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
  105. Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2017

Authors and Affiliations

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

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