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Changes in Activity of the Plasma Membrane H+-ATPase as a Link Between Formation of Electrical Signals and Induction of Photosynthetic Responses in Higher Plants

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Abstract

Action of numerous adverse environmental factors on higher plants is spatially-heterogenous; it means that induction of a systemic adaptive response requires generation and transmission of the stress signals. Electrical signals (ESs) induced by local action of stressors include action potential, variation potential, and system potential and they participate in formation of fast physiological changes at the level of a whole plant, including photosynthetic responses. Generation of these ESs is accompanied by the changes in activity of H+-ATPase, which is the main system of electrogenic proton transport across the plasma membrane. Literature data show that the changes in H+-ATPase activity and related changes in intra- and extracellular pH play a key role in the ES-induced inactivation of photosynthesis in non-irritated parts of plants. This inactivation is caused by both suppression of CO2 influx into mesophyll cells in leaves, which can be induced by the apoplast alkalization and, probably, cytoplasm acidification, and direct influence of acidification of stroma and lumen of chloroplasts on light and, probably, dark photosynthetic reactions. The ES-induced inactivation of photosynthesis results in the increasing tolerance of photosynthetic machinery to the action of adverse factors and probability of the plant survival.

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Abbreviations

AP:

action potential

ES:

electric signal

ROS:

reactive oxygen species

SP:

system potential

VP:

variation potential

References

  1. Fromm, J., and Lautner, S. (2007) Electrical signals and their physiological significance in plants, Plant Cell Environ., 30, 249-257, https://doi.org/10.1111/j.1365-3040.2006.01614.x.

    Article  CAS  PubMed  Google Scholar 

  2. Gallé, A., Lautner, S., Flexas, J., and Fromm, J. (2015) Environmental stimuli and physiological responses: the current view on electrical signaling, Environ. Exp. Bot., 114, 15-21, https://doi.org/10.1016/j.envexpbot.2014.06.013.

    Article  Google Scholar 

  3. Choi, W. G., Hilleary, R., Swanson, S. J., Kim, S. H., and Gilroy, S. (2016) Rapid, long-distance electrical and calcium signaling in plants, Annu. Rev. Plant Biol., 67, 287-307, https://doi.org/10.1146/annurev-arplant-043015-112130.

    Article  CAS  PubMed  Google Scholar 

  4. Hedrich, R., Salvador-Recatalà, V., and Dreyer, I. (2016) Electrical wiring and long-distance plant communication, Trends Plant Sci., 21, 376-387, https://doi.org/10.1016/j.tplants.2016.01.016.

    Article  CAS  PubMed  Google Scholar 

  5. Szechyńska-Hebda, M., Lewandowska, M., and Karpiński, S. (2017) Electrical signaling, photosynthesis and systemic acquired acclimation, Front. Physiol., 8, 684, https://doi.org/10.3389/fphys.2017.00684.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sukhov, V., Sukhova, E., and Vodeneev, V. (2019) Long-distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants, Progr. Biophys. Mol. Biol., 146, 63-84, https://doi.org/10.1016/j.pbiomolbio.2018.11.009.

    Article  CAS  Google Scholar 

  7. Sukhova, E., and Sukhov, V. (2021) Electrical signals, plant tolerance to actions of stressors, and programmed cell death: is interaction possible? Plants, 10, 1704, https://doi.org/10.3390/plants10081704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wildon, D. C., Thain, J. F., Minchin, P. E. H., Gubb, I. R., Reilly, A. J., Skipper, Y. D., Doherty, H. M., O’Donnell, P. J., and Bowles, D. (1992) Electrical signalling and systemic proteinase inhibitor Induction in the wounded plant, Nature, 360, 62-65, https://doi.org/10.1038/360062a0.

    Article  CAS  Google Scholar 

  9. Mousavi, S. A., Chauvin, A., Pascaud, F., Kellenberger, S., and Farmer, E. E. (2013) Glutamate receptor-like genes mediate leaf-to-leaf wound signalling, Nature, 500, 422-426, https://doi.org/10.1038/nature12478.

    Article  CAS  PubMed  Google Scholar 

  10. Hlavácková, V., Krchnák, P., Naus, J., Novák, O., Spundová, M., and Strnad, M. (2006) Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning, Planta, 225, 235-244, https://doi.org/10.1007/s00425-006-0325-x.

    Article  CAS  PubMed  Google Scholar 

  11. Hlavinka, J., Nožková-Hlaváčková, V., Floková, K., Novák, O., and Nauš, J. (2012) Jasmonic acid accumulation and systemic pho-to-synthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pre-treated by ABA, Plant Physiol. Biochem., 54, 89-96, https://doi.org/10.1016/j.plaphy.2012.02.014.

    Article  CAS  PubMed  Google Scholar 

  12. Farmer, E. E., Gao, Y. Q., Lenzoni, G., Wolfender, J. L., and Wu, Q. (2020) Wound- and mechanostimulated electrical signals control hormone responses, New Phytol., 227, 1037-1050, https://doi.org/10.1111/nph.16646.

    Article  CAS  PubMed  Google Scholar 

  13. Filek, M., and 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, https://doi.org/10.1016/S0168-9452(96)04567-0.

    Article  CAS  Google Scholar 

  14. Pavlovič, A., Slováková, L., Pandolfi, C., and 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, https://doi.org/10.1093/jxb/erq404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Lautner, S., Stummer, M., Matyssek, R., Fromm, J., and Grams, T. E. E. (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, https://doi.org/10.1111/pce.12150.

    Article  CAS  PubMed  Google Scholar 

  16. Surova, L., Sherstneva, O., Vodeneev, V., Katicheva, L., Semina, M., and Sukhov, V. (2016) Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves, J. Plant Physiol., 202, 57-64, https://doi.org/10.1016/j.jplph.2016.05.024.

    Article  CAS  PubMed  Google Scholar 

  17. Furch, A. C., van Bel, A. J., Fricker, M. D., Felle, H. H., Fuchs, M., and Hafke, J. B. (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba, Plant Cell, 21, 2118-2132, https://doi.org/10.1105/tpc.108.063107.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Furch, A. C., Zimmermann, M. R., Will, T., Hafke, J. B., and van Bel, A. J. (2010) Remote-controlled flow by biphasic occlusion in Cucurbita maxima, J. Exp. Bot., 61, 3697-3708, https://doi.org/10.1093/jxb/erq181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Van Bel, A. J., Furch, A. C., Will, T., Buxa, S. V., Musetti, R., and Hafke, J. B. (2014) Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway, J. Exp. Bot., 65, 1761-1787, https://doi.org/10.1093/jxb/ert425.

    Article  CAS  PubMed  Google Scholar 

  20. Kaiser, H., and Grams, T. E. (2006) Rapid hydropassive opening and subsequent active stomatal closure follow heat-induced electrical signals in Mimosa pudica, J. Exp. Bot., 57, 2087-2092, https://doi.org/10.1093/jxb/erj165.

    Article  CAS  PubMed  Google Scholar 

  21. Yudina, L. M., Sherstneva, O. N., Mysyagin, S. A., Vodeneev, V. A., and Sukhov, V. S. (2019) Impact of local damage on transpiration of pea leaves at various air humidity, Russ. J. Plant Physiol., 66, 87-94, https://doi.org/10.1134/S1021443719010163.

    Article  CAS  Google Scholar 

  22. Stahlberg, R., and Cosgrove, D. J. (1996) Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L., Planta, 200, 416-425, https://doi.org/10.1007/BF00231397.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Gallé, A., Lautner, S., Flexas, J., Ribas-Carbo, M., Hanson, D., Roesgen, J., and 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, https://doi.org/10.1111/j.1365-3040.2012.02594.x.

    Article  CAS  PubMed  Google Scholar 

  25. Grams, T. E., Lautner, S., Felle, H. H., Matyssek, R., and 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, https://doi.org/10.1111/j.1365-3040.2008.01922.x.

    Article  CAS  PubMed  Google Scholar 

  26. Sukhov, V., Orlova, L., Mysyagin, S., Sinitsina, J., and Vodeneev, V. (2012) Analysis of the photosynthetic response induced by variation potential in geranium, Planta, 235, 703-712, https://doi.org/10.1007/s00425-011-1529-2.

    Article  CAS  PubMed  Google Scholar 

  27. Sukhov, V., Sherstneva, O., Surova, L., Katicheva, L., and Vodeneev, V. (2014) Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea, Plant Cell Environ., 37, 2532-2541, https://doi.org/10.1111/pce.12321.

    Article  CAS  PubMed  Google Scholar 

  28. Sukhov, V., Surova, L., Sherstneva, O., Katicheva, L., and Vodeneev, V. (2015) Variation potential influence on photosynthetic cyclic electron flow in pea, Front. Plant Sci., 5, 766, https://doi.org/10.3389/fpls.2014.00766.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Sukhova, E., Mudrilov, M., Vodeneev, V., and Sukhov, V. (2018) Influence of the variation potential on photosynthetic flows of light energy and electrons in pea, Photosynth. Res., 136, 215-228, https://doi.org/10.1007/s11120-017-0460-1.

    Article  CAS  PubMed  Google Scholar 

  30. Sukhov, V., Sukhova, E., Gromova, E., Surova, L., Nerush, V., and Vodeneev, V. (2019) The electrical signal-induced systemic photosynthetic response is accompanied by changes in the photochemical reflectance index in pea, Func. Plant Biol., 46, 328-338, https://doi.org/10.1071/FP18224.

    Article  CAS  Google Scholar 

  31. Sukhova, E., and Sukhov, V. (2023) Electrical signals in systemic adaptive response of higher plants: Integration through separation, Bioelectricity, 5, 126-131, https://doi.org/10.1089/bioe.2022.0042.

    Article  Google Scholar 

  32. Szechyńska-Hebda, M., Kruk, J., Górecka, M., Karpińska, B., and Karpiński, S. (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis, Plant Cell, 22, 2201-2218, https://doi.org/10.1105/tpc.109.069302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zandalinas, S. I., Fichman, Y., Devireddy, A. R., Sengupta, S., Azad, R. K., and Mittler, R. (2020) Systemic signaling during abiotic stress combination in plants, Proc. Natl. Acad. Sci. USA, 117, 13810-13820, https://doi.org/10.1073/pnas.2005077117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Retivin, V. G., Opritov, V. A., Lobov, S. A., Tarakanov, S. A., and Khudyakov, V. A. (1999) 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, 790-798.

    Google Scholar 

  35. Sukhov, V., Surova, L., Sherstneva, O., and Vodeneev, V. (2014) Influence of variation potential on resistance of the photosynthetic machinery to heating in pea, Physiol. Plant., 152, 773-783, https://doi.org/10.1111/ppl.12208.

    Article  CAS  PubMed  Google Scholar 

  36. Sukhov, V., Surova, L., Sherstneva, O., Bushueva, A., and Vodeneev, V. (2015) Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea, Funct. Plant. Biol., 42, 727-736, https://doi.org/10.1071/FP15052.

    Article  PubMed  Google Scholar 

  37. Surova, L., Sherstneva, O., Vodeneev, V., and Sukhov, V. (2016) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways, Plant. Sign. Behav., 11, e1145334, https://doi.org/10.1080/15592324.2016.1145334.

    Article  CAS  Google Scholar 

  38. Sukhov, V., Gaspirovich, V., Mysyagin, S., and Vodeneev, V. (2017) High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea, Front. Physiol., 8, 763, https://doi.org/10.3389/fphys.2017.00763.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Grinberg, M. A., Gudkov, S. V., Balalaeva, I. V., Gromova, E., Sinitsyna, Y., Sukhov, V., and Vodeneev, V. (2021) Effect of chronic β-radiation on long-distance electrical signals in wheat and their role in adaptation to heat stress, Environ. Exp. Bot., 184, 104378, https://doi.org/10.1016/j.envexpbot.2021.104378.

    Article  CAS  Google Scholar 

  40. Retivin, V. G., Opritov, V. A., and Fedulina, S. B. (1997) Pre-adaptation of the stem tissues of Cucurbita pepo to the damaging action of low temperatures induced by action potential [in Russian], Fiziol. Rast., 44, 499-510.

    Google Scholar 

  41. Williamson, R. E., and Ashley, C. C. (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara, Nature, 296, 647-650, https://doi.org/10.1038/296647a0.

    Article  CAS  PubMed  Google Scholar 

  42. Lunevsky, V. Z., Zherelova, O. M., Vostrikov, I. Y., and Berestovsky, G. N. (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels, J. Membrain Biol., 72, 43-58, https://doi.org/10.1007/BF01870313.

    Article  Google Scholar 

  43. Bulychev, A. A., Kamzolkina, N. A., Luengviriya, J., Rubin, A. B., and Müller, S. C. (2004) Effect of a single excitation stimulus on photosynthetic activity and light-dependent pH banding in Chara cells, J. Membr. Biol., 202, 11-19, https://doi.org/10.1007/s00232-004-0716-5.

    Article  CAS  PubMed  Google Scholar 

  44. Bulychev, A. A., and Krupenina, N. A. (2009) Transient removal of alkaline zones after excitation of Chara cells is associated with inactivation of high conductance in the plasmalemma, Plant. Signal. Behav., 4, 727-734, https://doi.org/10.4161/psb.4.8.9306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Felle, H. H., and Zimmermann, M. R. (2007) Systemic signalling in barley through action potentials, Planta, 226, 203-214, https://doi.org/10.1007/s00425-006-0458-y.

    Article  CAS  PubMed  Google Scholar 

  46. Vodeneev, V. A., Opritov, V. A., and Pyatygin, S. S. (2006) Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo, Russ. J. Plant Physiol., 53, 481-487, https://doi.org/10.1134/S102144370604008X.

    Article  CAS  Google Scholar 

  47. Sukhov, V., and Vodeneev, V. (2009) A mathematical model of action potential in cells of vascular plants, J. Membr. Biol., 232, 59-67, https://doi.org/10.1007/s00232-009-9218-9.

    Article  CAS  PubMed  Google Scholar 

  48. Vodeneev, V., Akinchits, E., and Sukhov, V. (2015) Variation potential in higher plants: mechanisms of generation and propagation, Plant Sign. Behav., 10, e1057365, https://doi.org/10.1080/15592324.2015.1057365.

    Article  CAS  Google Scholar 

  49. Sukhov, V., Akinchits, E., Katicheva, L., and Vodeneev, V. (2013) Simulation of variation potential in higher plant cells, J. Membr. Biol., 246, 287-296, https://doi.org/10.1007/s00232-013-9529-8.

    Article  CAS  PubMed  Google Scholar 

  50. Ladeynova, M., Mudrilov, M., Berezina, E., Kior, D., Grinberg, M., Brilkina, A., Sukhov, V., and Vodeneev, V. (2020) Spatial and temporal dynamics of electrical and photosynthetic activity and the content of phytohormones induced by local stimulation of pea plants, Plants, 9, 1364, https://doi.org/10.3390/plants9101364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Stahlberg, R., and Cosgrove, D. J. (1997) The propagation of slow wave potentials in pea epicotyls, Plant Physiol., 113, 209-217, https://doi.org/10.1104/pp.113.1.209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Mancuso, S. (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera, Aust. J. Plant Physiol., 26, 55-61, https://doi.org/10.1071/PP98098.

    Article  Google Scholar 

  53. Sukhova, E., Akinchits, E., Gudkov, S. V., Pishchalnikov, R. Y., Vodeneev, V., and Sukhov, V. A. (2021) Theoretical analysis of relations between pressure changes along xylem vessels and propagation of variation potential in higher plants, Plants, 10, 372, https://doi.org/10.3390/plants10020372.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., Dangl, J. L., and Mittler, R. (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli, Sci. Signal., 2, ra45, https://doi.org/10.1126/scisignal.2000448.

    Article  PubMed  Google Scholar 

  55. Suzuki, N., and Mittler, R. (2012) Reactive oxygen species-dependent wound responses in animals and plants, Free Radic. Biol. Med., 53, 2269-2276, https://doi.org/10.1016/j.freeradbiomed.2012.10.538.

    Article  CAS  PubMed  Google Scholar 

  56. Choi, W. G., Miller, G., Wallace, I., Harper, J., Mittler, R., and Gilroy, S. (2017) Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals, Plant J., 90, 698-707, https://doi.org/10.1111/tpj.13492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Peña-Cortés, H., Fisahn, J., and 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, https://doi.org/10.1073/pnas.92.10.4106.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Toyota, M., Spencer, D., Sawai-Toyota, S., Jiaqi, W., Zhang, T., Koo, A. J., Howe, G. A., and Gilroy, S. (2018) Glutamate triggers long-distance, calcium-based plant defense signaling, Science, 361, 1112-1115, https://doi.org/10.1126/science.aat7744.

    Article  CAS  PubMed  Google Scholar 

  59. Malone, M. (1994) Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L., New Phytol., 128, 49-56, https://doi.org/10.1111/j.1469-8137.1994.tb03985.x.

    Article  CAS  PubMed  Google Scholar 

  60. Evans, M. J., and Morris, R. J. (2017) Chemical agents transported by xylem mass flow propagate variation potentials, Plant J., 91, 1029-1037, https://doi.org/10.1111/tpj.13624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Blyth, M. G., and Morris, R. J. (2019) Shear-enhanced dispersion of a wound substance as a candidate mechanism for variation potential transmission, Front. Plant Sci., 10, 1393, https://doi.org/10.3389/fpls.2019.01393.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Vodeneev, V., Orlova, A., Morozova, E., Orlova, L., Akinchits, E., Orlova, O., and Sukhov, V. (2012) The mechanism of propagation of variation potentials in wheat leaves, J. Plant Physiol., 169, 949-954, https://doi.org/10.1016/j.jplph.2012.02.013.

    Article  CAS  PubMed  Google Scholar 

  63. Evans, M. J., Choi, W. G., Gilroy, S., and Morris, R. J. (2016) A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress, Plant Physiol., 171, 1771-1784, https://doi.org/10.1104/pp.16.00215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Julien, J. L., Desbiez, M. O., de Jaeger, G., Frachisse, J. M. (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L., J. Exp. Bot., 42, 131-137, https://doi.org/10.1093/jxb/42.1.131.

    Article  Google Scholar 

  65. Lautner, S., Grams, T. E. E., Matyssek, R., Fromm, J. (2005) Characteristics of electrical signals in poplar and responses in photosynthesis, Plant Physiol., 138, 2200-2209, https://doi.org/10.1104/pp.105.064196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zimmermann, M. R., Maischak, H., Mithöfer, A., Boland, W., and Felle, H. H. (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding, Plant Physiol., 149, 1593-1600, https://doi.org/10.1104/pp.108.133884.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zimmermann, M. R., Mithöfer, A., Will, T., Felle, H. H., and Furch, A. C. (2016) Herbivore-triggered electrophysiological reactions: candidates for systemic signals in higher plants and the challenge of their identification, Plant Physiol., 170, 2407-2419, https://doi.org/10.1104/pp.15.01736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Vuralhan-Eckert, J., Lautner, S., and Fromm, J. (2018) Effect of simultaneously induced environmental stimuli on electrical signalling and gas exchange in maize plants, J. Plant Physiol., 223, 32-36, https://doi.org/10.1016/j.jplph.2018.02.003.

    Article  CAS  PubMed  Google Scholar 

  69. Yudina, L., Gromova, E., Grinberg, M., Popova, A., Sukhova, E., and Sukhov, V. (2022) Influence of burning-induced electrical signals on photosynthesis in pea can be modified by soil water shortage, Plants, 11, 534, https://doi.org/10.3390/plants11040534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Yudina, L., Sukhova, E., Popova, A., Zolin, Yu., Abasheva, K., Grebneva, K., and Sukhov, V. (2023) Local action of moderate heating and illumination induces propagation of hyperpolarization electrical signals in wheat plants, Front. Sustain. Food Syst., 6, 1062449, https://doi.org/10.3389/fsufs.2022.1062449.

    Article  Google Scholar 

  71. Yudina, L., Sukhova, E., Popova, A., Zolin, Y., Abasheva, K., Grebneva, K., and Sukhov, V. (2023) Hyperpolarization electrical signals induced by local action of moderate heating influence photosynthetic light reactions in wheat plants, Front. Plant Sci., 14, 1153731, https://doi.org/10.3389/fpls.2023.1153731.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Lew, R. R. (1989) Calcium activates an electrogenic proton pump in neurospora plasma membrane, Plant Physiol., 91, 213-216, https://doi.org/10.1104/pp.91.1.213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Grinberg, M., Mudrilov, M., Kozlova, E., Sukhov, V., Sarafanov, F., Evtushenko, A., Ilin, N., Vodeneev, V., Price, C., and Mareev, E. (2022) Effect of extremely low-frequency magnetic fields on light-induced electric reactions in wheat, Plant Signal. Behav., 17, e2021664, https://doi.org/10.1080/15592324.2021.2021664.

    Article  CAS  Google Scholar 

  74. Grabov, A., and Blatt, M. R. (1999) A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in guard cells, Plant Physiol., 119, 277-288, https://doi.org/10.1104/pp.119.1.277.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Gao, Y. Q., Wu, W. H., and Wang, Y. (2019) Electrophysiological identification and activity analyses of plasma membrane K+ channels in maize guard cells, Plant Cell Physiol., 60, 765-777, https://doi.org/10.1093/pcp/pcy242.

    Article  CAS  PubMed  Google Scholar 

  76. Sukhova, E., Akinchits, E., and Sukhov, V. (2017) Mathematical models of electrical activity in plants, J. Membr. Biol., 250, 407-423, https://doi.org/10.1007/s00232-017-9969-7.

    Article  CAS  PubMed  Google Scholar 

  77. Sukhova, E., Ratnitsyna, D., and Sukhov, V. (2021) Stochastic spatial heterogeneity in activities of H+-ATP-ases in electrically connected plant cells decreases threshold for cooling-induced electrical responses, Int. J. Mol. Sci., 22, 8254, https://doi.org/10.3390/ijms22158254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Falhof, J., Pedersen, J. T., Fuglsang, A. T., and Palmgren, M. (2016) Plasma membrane H+-ATPase regulation in the center of plant physiology, Mol. Plant., 9, 323-337, https://doi.org/10.1016/j.molp.2015.11.002.

    Article  CAS  PubMed  Google Scholar 

  79. Fuglsang, A. T., and Palmgren, M. (2021) Proton and calcium pumping P-type ATPases and their regulation of plant responses to the environment, Plant Physiol., 187, 1856-1875, https://doi.org/10.1093/plphys/kiab330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Katicheva, L., Sukhov, V., Akinchits, E., and Vodeneev, V. (2014) Ionic nature of burn-induced variation potential in wheat leaves, Plant Cell Physiol., 55, 1511-1519, https://doi.org/10.1093/pcp/pcu082.

    Article  CAS  PubMed  Google Scholar 

  81. Krupenina, N. A., and Bulychev, A. A. (2007) Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 1767, 781-788, https://doi.org/10.1016/j.bbabio.2007.01.004.

    Article  CAS  PubMed  Google Scholar 

  82. Krausko, M., Perutka, Z., Šebela, M., Šamajová, O., Šamaj, J., Novák, O., and 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, 1818-1835, https://doi.org/10.1111/nph.14352.

    Article  CAS  PubMed  Google Scholar 

  83. Białasek, M., Górecka, M., Mittler, R., and 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., 58, 207-215, https://doi.org/10.1093/pcp/pcw232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Herde, O., Peña-Cortés, H., Fuss, H., Willmitzer, L., and Fisahn, J. (1999) Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants, Physiol. Plant., 105, 179-184, https://doi.org/10.1034/j.1399-3054.1999.105126.x.

    Article  CAS  Google Scholar 

  85. Sherstneva, O. N., Vodeneev, V. A., Katicheva, L. A., Surova, L. M., and Sukhov, V. S. (2015) Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings, Biochemistry (Moscow), 80, 776-784, https://doi.org/10.1134/S0006297915060139.

    Article  CAS  PubMed  Google Scholar 

  86. Kinoshita, T., Nishimura, M., and Shimazaki, Ki. (1995) Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of fava bean, Plant Cell, 7, 1333-1342, https://doi.org/10.1105/tpc.7.8.1333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sukhov, V. S., Gaspirovich, V. V., Gromova, E. N., Ladeynova, M. M., Sinitsyna, Yu. V., Berezina, E. V., Akinchits, E. K., and Vodeneev, V. A. (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, 237-247, https://doi.org/10.1134/S1990747817030096.

    Article  Google Scholar 

  88. Yudina, L., Sukhova, E., Sherstneva, O., Grinberg, M., Ladeynova, M., Vodeneev, V., and Sukhov, V. (2020) Exogenous abscisic acid can influence photosynthetic processes in peas through a decrease in activity of H+-ATP-ase in the plasma membrane, Biology, 9, 324, https://doi.org/10.3390/biology9100324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Yudina, L., Sherstneva, O., Sukhova, E., Grinberg, M., Mysyagin, S., Vodeneev, V., and Sukhov, V. (2020) Inactivation of H+-ATPase participates in the influence of variation potential on photosynthesis and respiration in peas, Plants, 9, 1585, https://doi.org/10.3390/plants9111585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Sukhov, V., Surova, L., Morozova, E., Sherstneva, O., and Vodeneev, V. (2016) Changes in H+-ATP synthase activity, proton electrochemical gradient, and pH in pea chloroplast can be connected with variation potential, Front. Plant Sci., 7, 1092, https://doi.org/10.3389/fpls.2016.01092.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Sherstneva, O. N., Surova, L. M., Vodeneev, V. A., Plotnikova, Yu. I., Bushueva, A. V., and Sukhov, V. S. (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, https://doi.org/10.1134/S1990747815050116.

    Article  Google Scholar 

  92. Sherstneva, O. N., Vodeneev, V. A., Surova, L. M., Novikova, E. M., and Sukhov, V. S. (2016) Application of a mathematical model of variation potential for analysis of its influence on photosynthesis in higher plants, Biochem. Moscow Suppl. Ser. A, 10, 269-277, https://doi.org/10.1134/S1990747816030089.

    Article  Google Scholar 

  93. Bulychev, A. A., Alova, A. V., and Rubin, A. B. (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, https://doi.org/10.1134/S1021443712060039.

    Article  CAS  Google Scholar 

  94. Tholen, D., and Zhu, X.-G. (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion, Plant Physiol., 156, 90-105, https://doi.org/10.1104/pp.111.172346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sukhova, E. M., and Sukhov, V. S. (2018) Dependence of the CO2 uptake in a plant cell on the plasma membrane H+-ATPase activity: theoretical analysis, Biochem. Moscow Suppl. Ser. A, 12, 146-159, https://doi.org/10.1134/S1990747818020149.

    Article  Google Scholar 

  96. Sukhova, E., Ratnitsyna, D., Gromova, E., and Sukhov, V. (2022) Development of two-dimensional model of photosynthesis in plant leaves and analysis of induction of spatial heterogeneity of CO2 assimilation rate under action of excess light and drought, Plants, 11, 3285, https://doi.org/10.3390/plants11233285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Sukhova, E., Ratnitsyna, D., and Sukhov, V. (2022) Simulated analysis of influence of changes in H+-ATPase activity and membrane CO2 conductance on parameters of photosynthetic assimilation in leaves, Plants, 11, 3435, https://doi.org/10.3390/plants11243435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Uehlein. N., Otto, B., Hanson, D. T., Fischer, M., McDowell, N., and Kaldenhoff, R. (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability, Plant Cell, 20, 648-657, https://doi.org/10.1105/tpc.107.054023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Luu, D.-Y., and Maurel, C. (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status, Plant Cell Environ., 28, 85-96, https://doi.org/10.1111/j.1365-3040.2004.01295.x.

    Article  CAS  Google Scholar 

  100. Chaumont, F., and Tyerman, S. D. (2014) Aquaporins: highly regulated channels controlling plant water relations, Plant Physiol., 164, 1600-1618, https://doi.org/10.1104/pp.113.233791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Kapilan, R., Vaziri, M., and Zwiazek, J. J. (2018) Regulation of aquaporins in plants under stress, Biol. Res., 51, 4, https://doi.org/10.1186/s40659-018-0152-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wang, C., Hu, H., Qin, X., Zeise, B., Xu, D., Rappel, W. J., Boron, W. F., and Schroeder, J. I. (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor, Plant Cell, 28, 568-582, https://doi.org/10.1105/tpc.15.00637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Flexas, J., Ribas-Carbó, M., Diaz-Espejo, A., Galmés, J., and Medrano, H. (2008) Mesophyll conductance to CO2: current knowledge and future prospects, Plant Cell Environ., 31, 602-621, https://doi.org/10.1111/j.1365-3040.2007.01757.x.

    Article  CAS  PubMed  Google Scholar 

  104. Alte, F., Stengel, A., Benz, J. P., Petersen, E., Soll, J., Groll, M., and 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, https://doi.org/10.1073/pnas.1009124107.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Benz, J. P., Stengel, A., Lintala, M., Lee, Y. H., Weber, A., Philippar, K., Gügel, I. L., Kaieda, S., Ikegami, T., Mulo, P., Soll, J., and 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, https://doi.org/10.1105/tpc.109.069815.

    Article  CAS  Google Scholar 

  106. Joliot, P., and Alric, J. (2013) Inhibition of CO2 fixation by iodoacetamide stimulates cyclic electron flow and non-photochemical quenching upon far-red illumination, Photosynth. Res., 115, 55-63, https://doi.org/10.1007/s11120-013-9826-1.

    Article  CAS  PubMed  Google Scholar 

  107. Müller, P., Li, X. P., and Niyogi, K. K. (2001) Non-photochemical quenching. A response to excess light energy, Plant Physiol., 125, 1558-1566, https://doi.org/10.1104/pp.125.4.1558.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Jajoo, A., Mekala, N. R., Tongra, T., Tiwari, A., Grieco, M., Tikkanen, M., and Aro, E. M. (2014) Low pH-induced regulation of excitation energy between the two photosystems, FEBS Lett., 588, 970-974, https://doi.org/10.1016/j.febslet.2014.01.056.

    Article  CAS  PubMed  Google Scholar 

  109. Ruban, A. V. (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage, Plant Physiol., 170, 1903-1916, https://doi.org/10.1104/pp.15.01935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Tikhonov, A. N. (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts, Photosynth. Res., 116, 511-534, https://doi.org/10.1007/s11120-013-9845-y.

    Article  CAS  PubMed  Google Scholar 

  111. Tikhonov, A. N. (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways, Plant Physiol. Biochem., 81, 163-183, https://doi.org/10.1016/j.plaphy.2013.12.011.

    Article  CAS  PubMed  Google Scholar 

  112. Rochaix, J.-D., Lemeille, S., Shapiguzov, A., Samol, I., Fucile, G., Willig, A., and Goldschmidt-Clermont, M. (2012) Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment, Philos. Trans. R. Soc. B, 367, 3466-3474, https://doi.org/10.1098/rstb.2012.0064.

    Article  CAS  Google Scholar 

  113. Joliot, P., and Joliot, A. (2006) Cyclic electron flow in C3 plants, Biochim. Biophys. Acta, 1757, 362-368, https://doi.org/10.1016/j.bbabio.2006.02.018.

    Article  CAS  PubMed  Google Scholar 

  114. Joliot, P., and Johnson, G. N. (2011) Regulation of cyclic and linear electron flow in higher plants, Proc. Natl. Acad. Sci. USA, 108, 13317-13322, https://doi.org/10.1073/pnas.1110189108.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Tikkanen, M., and Aro, E. M. (2014) Integrative regulatory network of plant thylakoid energy transduction, Trends Plant Sci., 19, 10-17, https://doi.org/10.1016/j.tplants.2013.09.003.

    Article  CAS  PubMed  Google Scholar 

  116. ikkanen, M., Mekala, N. R., and Aro, E. M. (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage, Biochim. Biophys. Acta, 1837, 210-215, https://doi.org/10.1016/j.bbabio.2013.10.001.

    Article  CAS  Google Scholar 

  117. Allakhverdiev, S. I., Nishiyama, Y., Takahashi, S., Miyairi, S., Suzuki, I., and 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, https://doi.org/10.1104/pp.104.054478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Gradmann, D. (2001) Impact of apoplast volume on ionic relations in plant cells, J. Membr. Biol., 184, 61-69, https://doi.org/10.1007/s00232-001-0074-5.

    Article  CAS  PubMed  Google Scholar 

  119. Tyerman, S. D., Beilby, M., Whittington, J., Juswono, U., Neyman, L., and Shabala, S. (2001) Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protopasts: MIFE meets patch-clamp, Aust. J. Plant Physiol., 28, 591-604, https://doi.org/10.1071/PP01030.

    Article  CAS  Google Scholar 

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This work was funded by the Russian Science Foundation, grant no. 21-74-10088.

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Sukhova, E.M., Yudina, L.M. & Sukhov, V.S. Changes in Activity of the Plasma Membrane H+-ATPase as a Link Between Formation of Electrical Signals and Induction of Photosynthetic Responses in Higher Plants. Biochemistry Moscow 88, 1488–1503 (2023). https://doi.org/10.1134/S0006297923100061

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