Changes in activity of H+-ATPase of plasma membrane as a link between forming electrical signals and induction of photosynthetic responses in higher plants

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

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 propagation stress signals. Electrical signals (ESs) induced by local action of stressors include action potential, variation potential, and system potential and participate in forming fast physiological changes at the level of the whole plant, including photosynthetic responses. Generation of these ESs is accompanied by 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 ESs-induced photosynthetic inactivation in non-irritated parts of plants. This inactivation is caused by both suppression of CO2 flux 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 photosynthetic light and, probably, dark reactions. Result of the ESs-induced photosynthetic inactivation is increasing tolerance of photosynthetic machinery to action of adverse factors and probability of survive of plants.

About the authors

E. M Sukhova

N. I. Lobachevsky State University of Nizhny Novgorod

603022 Nizhny Novgorod, Russia

L. M Yudina

N. I. Lobachevsky State University of Nizhny Novgorod

603022 Nizhny Novgorod, Russia

V. S Sukhov

N. I. Lobachevsky State University of Nizhny Novgorod

Email: vssuh@mail.ru
603022 Nizhny Novgorod, Russia

References

  1. Fromm, J., and Lautner, S. (2007) Electrical signals and their physiological significance in plants, Plant Cell Environ., 30, 249-257, doi: 10.1111/j.1365-3040.2006.01614.x.
  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, doi: 10.1016/j.envexpbot.2014.06.013.
  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, doi: 10.1146/annurev-arplant-043015-112130.
  4. Hedrich, R., Salvador-Recatalà, V., and Dreyer, I. (2016) Electrical wiring and long-distance plant communication, Trends Plant Sci., 21, 376-387, doi: 10.1016/j.tplants.2016.01.016.
  5. Szechyńska-Hebda, M., Lewandowska, M., and Karpiński, S. (2017) Electrical signaling, photosynthesis and systemic acquired acclimation, Front. Physiol., 8, 684, doi: 10.3389/fphys.2017.00684.
  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, doi: 10.1016/j.pbiomolbio.2018.11.009.
  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, doi: 10.3390/plants10081704.
  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, doi: 10.1038/360062a0.
  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, doi: 10.1038/nature12478.
  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, doi: 10.1007/s00425-006-0325-x.
  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, doi: 10.1016/j.plaphy.2012.02.014.
  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, doi: 10.1111/nph.16646.
  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, doi: 10.1016/S0168-9452(96)04567-0.
  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, doi: 10.1093/jxb/erq404.
  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, doi: 10.1111/pce.12150.
  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, doi: 10.1016/j.jplph.2016.05.024.
  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, doi: 10.1105/tpc.108.063107.
  18. Furch, A. C., Zimmermann, M. R., Will, T., Hafke, J. B., and van Bel, A. J. (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima, J. Exp. Bot., 61, 3697-3708, doi: 10.1093/jxb/erq181.
  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, doi: 10.1093/jxb/ert425.
  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, doi: 10.1093/jxb/erj165.
  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, doi: 10.1134/S1021443719010163.
  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, doi: 10.1007/BF00231397.
  23. Sukhov, V. (2016) Electrical signals as mechanism of photosynthesis regulation in plants, Photosynth. Res., 130, 373-387, doi: 10.1007/s11120-016-0270-x.
  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, doi: 10.1111/j.1365-3040.2012.02594.x.
  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, doi: 10.1111/j.1365-3040.2008.01922.x.
  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, doi: 10.1007/s00425-011-1529-2.
  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, doi: 10.1111/pce.12321.
  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, doi: 10.3389/fpls.2014.00766.
  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, doi: 10.1007/s11120-017-0460-1.
  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, doi: 10.1071/FP18224.
  31. Sukhova, E., and Sukhov, V. (2023) Electrical signals in systemic adaptive response of higher plants: Integration through separation, Bioelectricity, 5, 126-131, doi: 10.1089/bioe.2022.0042.
  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, doi: 10.1105/tpc.109.069302.
  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, doi: 10.1073/pnas.2005077117.
  34. Ретивин В. Г., Опритов В. А., Лобов С. А., Тараканов С. А, Худяков В. А (1999). Модификация устойчивости фотосинтезирующих клеток к охлаждению и прогреву после раздражения корней раствором КСl, Физиология растений, 46, 790-798.
  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, doi: 10.1111/ppl.12208.
  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, doi: 10.1071/FP15052.
  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, doi: 10.1080/15592324.2016.1145334.
  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, doi: 10.3389/fphys.2017.00763.
  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, doi: 10.1016/j.envexpbot.2021.104378.
  40. Ретивин В. Г., Опритов В. А., Федулина С. Б. (1997) Предадаптация тканей стебля CUCURBITA PEPO к повреждающему действию низких температур, индуцированная потенциалами действия, Физиология растений, 44, 499-510.
  41. Williamson, R. E., and Ashley, C. C. (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara, Nature, 296, 647-650, doi: 10.1038/296647a0.
  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, doi: 10.1007/BF01870313.
  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, doi: 10.1007/s00232-004-0716-5.
  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, doi: 10.4161/psb.4.8.9306.
  45. Felle, H. H., and Zimmermann, M. R. (2007) Systemic signalling in barley through action potentials, Planta, 226, 203-214, doi: 10.1007/s00425-006-0458-y.
  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, doi: 10.1134/S102144370604008X.
  47. Sukhov, V., and Vodeneev, V. (2009) A mathematical model of action potential in cells of vascular plants, J. Membr. Biol., 232, 59-67, doi: 10.1007/s00232-009-9218-9.
  48. Vodeneev, V., Akinchits, E., and Sukhov, V. (2015) Variation potential in higher plants: mechanisms of generation and propagation, Plant Sign. Behav., 10, e1057365, doi: 10.1080/15592324.2015.1057365.
  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, doi: 10.1007/s00232-013-9529-8.
  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, doi: 10.3390/plants9101364.
  51. Stahlberg, R., and Cosgrove, D. J. (1997) The propagation of slow wave potentials in pea epicotyls, Plant Physiol., 113, 209-217, doi: 10.1104/pp.113.1.209.
  52. Mancuso, S. (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera, Aust. J. Plant Physiol., 26, 55-61, doi: 10.1071/PP98098.
  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, doi: 10.3390/plants10020372.
  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, doi: 10.1126/scisignal.2000448.
  55. Suzuki, N., and Mittler, R. (2012) Reactive oxygen species-dependent wound responses in animals and plants, Free Radic. Biol. Med., 53, 2269-2276, doi: 10.1016/j.freeradbiomed.2012.10.538.
  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, doi: 10.1111/tpj.13492.
  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, doi: 10.1073/pnas.92.10.4106.
  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, doi: 10.1126/science.aat7744.
  59. Malone, M. (1994) Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L., New Phytol., 128, 49-56, doi: 10.1111/j.1469-8137.1994.tb03985.x.
  60. Evans, M. J., and Morris, R. J. (2017) Chemical agents transported by xylem mass flow propagate variation potentials, Plant J., 91, 1029-1037, doi: 10.1111/tpj.13624.
  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, doi: 10.3389/fpls.2019.01393.
  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, doi: 10.1016/j.jplph.2012.02.013.
  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, doi: 10.1104/pp.16.00215.
  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, doi: 10.1093/jxb/42.1.131.
  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, doi: 10.1104/pp.105.064196.
  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, doi: 10.1104/pp.108.133884.
  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, doi: 10.1104/pp.15.01736.
  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, doi: 10.1016/j.jplph.2018.02.003.
  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, doi: 10.3390/plants11040534.
  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, doi: 10.3389/fsufs.2022.1062449.
  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, doi: 10.3389/fpls.2023.1153731.
  72. Lew, R. R. (1989) Calcium activates an electrogenic proton pump in neurospora plasma membrane, Plant Physiol., 91, 213-216, doi: 10.1104/pp.91.1.213.
  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, doi: 10.1080/15592324.2021.2021664.
  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, doi: 10.1104/pp.119.1.277.
  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, doi: 10.1093/pcp/pcy242.
  76. Sukhova, E., Akinchits, E., and Sukhov, V. (2017) Mathematical models of electrical activity in plants, J. Membr. Biol., 250, 407-423, doi: 10.1007/s00232-017-9969-7.
  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, doi: 10.3390/ijms22158254.
  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, doi: 10.1016/j.molp.2015.11.002.
  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, doi: 10.1093/plphys/kiab330.
  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, doi: 10.1093/pcp/pcu082.
  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, doi: 10.1016/j.bbabio.2007.01.004.
  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, doi: 10.1111/nph.14352.
  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, doi: 10.1093/pcp/pcw232.
  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, doi: 10.1034/j.1399-3054.1999.105126.x.
  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, doi: 10.1134/S0006297915060139.
  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, doi: 10.1105/tpc.7.8.1333.
  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, doi: 10.1134/S1990747817030096.
  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, doi: 10.3390/biology9100324.
  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, doi: 10.3390/plants9111585.
  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, doi: 10.3389/fpls.2016.01092.
  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, doi: 10.1134/S1990747815050116.
  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, doi: 10.1134/S1990747816030089.
  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, doi: 10.1134/S1021443712060039.
  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, doi: 10.1104/pp.111.172346.
  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, doi: 10.1134/S1990747818020149.
  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, doi: 10.3390/plants11233285.
  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, doi: 10.3390/plants11243435.
  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, doi: 10.1105/tpc.107.054023.
  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, doi: 10.1111/j.1365-3040.2004.01295.x.
  100. Chaumont, F., and Tyerman, S. D. (2014) Aquaporins: highly regulated channels controlling plant water relations, Plant Physiol., 164, 1600-1618, doi: 10.1104/pp.113.233791.
  101. Kapilan, R., Vaziri, M., and Zwiazek, J. J. (2018) Regulation of aquaporins in plants under stress, Biol. Res., 51, 4, doi: 10.1186/s40659-018-0152-0.
  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, doi: 10.1105/tpc.15.00637.
  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, doi: 10.1111/j.1365-3040.2007.01757.x.
  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, doi: 10.1073/pnas.1009124107.
  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, doi: 10.1105/tpc.109.069815.
  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, doi: 10.1007/s11120-013-9826-1.
  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, doi: 10.1104/pp.125.4.1558.
  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, doi: 10.1016/j.febslet.2014.01.056.
  109. Ruban, A. V. (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage, Plant Physiol., 170, 1903-1916, doi: 10.1104/pp.15.01935.
  110. Tikhonov, A. N. (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts, Photosynth. Res., 116, 511-534, doi: 10.1007/s11120-013-9845-y.
  111. Tikhonov, A. N. (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways, Plant Physiol. Biochem., 81, 163-183, doi: 10.1016/j.plaphy.2013.12.011.
  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, doi: 10.1098/rstb.2012.0064.
  113. Joliot, P., and Joliot, A. (2006) Cyclic electron flow in C3 plants, Biochim. Biophys. Acta, 1757, 362-368, doi: 10.1016/j.bbabio.2006.02.018.
  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, doi: 10.1073/pnas.1110189108.
  115. Tikkanen, M., and Aro, E. M. (2014) Integrative regulatory network of plant thylakoid energy transduction, Trends Plant Sci., 19, 10-17, doi: 10.1016/j.tplants.2013.09.003.
  116. Tikkanen, 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, doi: 10.1016/j.bbabio.2013.10.001
  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, doi: 10.1104/pp.104.054478.
  118. Gradmann, D. (2001) Impact of apoplast volume on ionic relations in plant cells, J. Membr. Biol., 184, 61-69, doi: 10.1007/s00232-001-0074-5.
  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, doi: 10.1071/PP01030.

Copyright (c) 2023 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies