Electrical signals of the plasma membrane and their effect on chlorophyll fluorescence in chara chloroplasts in vivo

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Abstract

Action potentials of plant cells are involved in regulation of many cell processes, such as photosynthesis and cytoplasmic streaming. Excitable cells of characean algae submerged in media with elevated K+ content are able to generate hyperpolarizing electrical responses. This active response of plasma membrane arises upon the passage of inward electric current comparable in extent to natural currents circulating in illuminated Chara internodes. It remains currently unknown whether the hyperpolarizing electrical signals in Chara affect the photosynthetic activity. Here we show that the negative shift of cell membrane potential, which causes the K+ influx into the cytoplasm, is accompanied by a delayed decrease in the effective chlorophyll fluorescence yield (F′) and maximal yield (Fm′) under low background light (12.5 µmol m-2 s-1). The transient changes in F′ and Fm′ were evident under illumination only, which indicates their close relation to photosynthetic energy conversion in chloroplasts. The passage of inward current caused an increase in pH at the cell surface (pHo), which reflects a high H+/OH- conductance of the plasmalemma and points to the decrease in cytoplasmic pH due to H+ entry into the cell. The shifts in pHo arising in response to the first hyperpolarizing pulse disappeared upon repeated stimulations, thus indicating the long-term inactivation of plasmalemmal H+/OH- conductance. Despite the suppression of plasmalemmal H+ fluxes, the hyperpolarizing responses and the analyzed chlorophyll fluorescence changes did not disappear. The results indicate the participation of K+ flows between the outer medium, cytoplasm, and stroma in chloroplast functional changes that are reflected by the dynamics of F′ and Fm′.

About the authors

A. A Bulychev

Faculty of Biology, Lomonosov Moscow State University

Email: bulychev@biophys.msu.ru
119234 Moscow, Russia

S. Yu Shapiguzov

Faculty of Biology, Lomonosov Moscow State University

119234 Moscow, Russia

A. V Alova

Faculty of Biology, Lomonosov Moscow State University

119234 Moscow, Russia

References

  1. Drachev, L. A., Mamedov, M. D., and Semenov, A. Yu. (1987) The antimycin-sensitive electrogenesis in Rhodopseudomonas sphaeroides chromatophores, FEBS Lett., 213, 128-132, doi: 10.1016/0014-5793(87)81477-1.
  2. Bulychev, A. A., Dassen, J. H. A., Vredenberg, W. J., Opanasenko, V. K., and Semenova, G. A. (1998) Stimulation of photocurrent in chloroplasts related to light-induced swelling of thylakoid system, Bioelectrochem. Bioenerg., 46, 71-78, doi: 10.1016/S0302-4598(98)00129-9.
  3. Bulychev, A. A., and Vredenberg, W. J. (1999) Light-triggered electrical events in the thylakoid membrane of plant chloroplasts, Physiol. Plant., 105, 577-584, doi: 10.1034/j.1399-3054.1999.105325.x.
  4. Bulychev, A. A., and Kamzolkina, N. A. (2006) Differential effects of plasma membrane electric excitation on H+ fluxes and photosynthesis in characean cells, Bioelectrochemistry, 69, 209-215, doi: 10.1016/j.bioelechem.2006.03.001.
  5. Bulychev, A. A., and Kamzolkina, N. A. (2006) Effect of action potential on photosynthesis and spatially distributed H+ fluxes in cells and chloroplasts of Chara corallina, Russ. J. Plant Physiol., 53, 1-9, doi: 10.1134/S1021443706010018.
  6. Bulychev, A. A., and Alova, A. V. (2022) Microfluidic interactions involved in chloroplast responses to plasma membrane excitation in Chara, Plant Physiol. Biochem., 183, 111-119, doi: 10.1016/j.plaphy.2022.05.005.
  7. Johnson, C. H., Shingles, R., and Ettinger, W. F. (2007) Regulation and role of calcium fluxes in the chloroplast, in Structure and Function of Plastids (Wise, R. R. and Hoober, J. K., eds.) Springer, Dordrecht, pp. 403-416, doi: 10.1007/978-1-4020-4061-0_20.
  8. Hochmal, A. K., Schulze, S., Trompelt, K., and Hippler, M. (2015) Calcium-dependent regulation of photosynthesis, Biochim. Biophys. Acta Bioenerg., 1847, 993-1003, doi: 10.1016/j.bbabio.2015.02.010.
  9. Williamson, R. E., and Ashley, C. C. (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara, Nature, 296, 647-651, doi: 10.1038/296647a0.
  10. Kreimer, G., Melkonian, M., and Latzko, E. (1985) An electrogenic uniport mediates light-dependent Ca2+ influx into intact spinach chloroplasts, FEBS Lett., 180, 253-258, doi: 10.1016/0014-5793(85)81081-4.
  11. Stael, S., Wurzinger, B., Mair, A. N., Mehlmer, N., Vothknecht, U. C., and Teige, M. (2012) Plant organellar calcium signalling: an emerging field, J. Exp. Bot., 63, 1525-1542, doi: 10.1093/jxb/err394.
  12. 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 Bioenerg., 1767, 781-788, doi: 10.1016/j.bbabio.2007.01.004.
  13. Pottosin, I., and Shabala, S. (2016) Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions, Mol. Plant, 9, 356-370, doi: 10.1016/j.molp.2015.10.006.
  14. Szabò, I., and Spetea, C. (2017) Impact of the ion transportome of chloroplasts on the optimization of photosynthesis, J. Exp. Bot., 68, 3115-3128, doi: 10.1093/jxb/erx063.
  15. Höhner, R., Aboukila, A., Kunz, H. H., and Venema, K. (2016) Proton gradients and proton-dependent transport processes in the chloroplast, Front. Plant Sci., 7, 1-7, doi: 10.3389/fpls.2016.00218.
  16. Wu, W., and Berkowitz, G. A. (1992) Stromal pH and photosynthesis are affected by electroneutral K+ and H+ exchange through chloroplast envelope ion channels, Plant Physiol., 98, 666-672, doi: 10.1104/pp.98.2.666.
  17. Kishimoto, U. (1966) Hyperpolarizing response in Nitella internodes, Plant Cell Physiol., 7, 429-439, doi: 10.1093/oxfordjournals.pcp.a079194.
  18. Homblé, F. (1987) A tight-seal whole cell study of the voltage-dependent gating mechanism of K+-channels of protoplasmic droplets of Chara corallina, Plant Physiol., 84, 433-437, doi: 10.1104/pp.84.2.433.
  19. Schmölzer, P. M., Höftberger, M., and Foissner, I. (2011) Plasma membrane domains participate in pH banding of Chara internodal cells, Plant Cell Physiol., 52, 1274-1288, doi: 10.1093/pcp/pcr074.
  20. Goh, C. H., Schreiber, U., and Hedrich, R. (1999) New approach of monitoring changes in chlorophyll a fluorescence of single guard cells and protoplasts in response to physiological stimuli, Plant Cell Environ., 22, 1057-1070, doi: 10.1046/j.1365-3040.1999.00475.x.
  21. Beilby, M. J. (2015) Salt tolerance at single cell level in giant-celled characeae, Front. Plant Sci., 6, 1-16, doi: 10.3389/fpls.2015.00226.
  22. Прищепов Е. Д., Андрианов В. К., Курелла Г. А., Рубин А. Б. (1984) Структурно-функциональные характеристики поверхностной мембраны капель протоплазмы, полученных из клеток харовых водорослей. IV. Исследование электрических свойств мембраны капли методами фиксации тока и потенциала, Физиология растений, 31, 59-72.
  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. Blinks, L. R. (1936) The effects of current flow on bioelectric potential: III. Nitella, J. Gen. Physiol., 20, 229-265, doi: 10.1085/jgp.20.2.229.
  25. Shaw, J. E., and Koleske, A. J. (2021) Functional interactions of ion channels with the actin cytoskeleton: does coupling to dynamic actin regulate NMDA receptors? J. Physiol., 599, 431-441, doi: 10.1113/JP278702.
  26. Hepler, P. K. (2016) The cytoskeleton and its regulation by calcium and protons, Plant Physiol., 170, 3-22, doi: 10.1104/pp.15.01506.
  27. Beilby, M. J., and Bisson, M. A. (2012) PH banding in charophyte algae, in Plant Electrophysiol. (Volkov, A. G., ed) Springer, Berlin-Heidelberg, pp. 247-271, doi: 10.1007/978-3-642-29119-7_11.
  28. Lucas, W. J., and Nuccitelli, R. (1980) HCO3- and OH- transport across the plasmalemma of Chara, Planta, 150, 120-131, doi: 10.1007/BF00582354.
  29. Yudina, L., Sukhova, E., Popova, A., Zolin, Y., 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, 1-20, doi: 10.3389/fsufs.2022.1062449.
  30. Spetea, C., Herdean, A., Allorent, G., Carraretto, L., Finazzi, G., and Szabo, I. (2017) An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis, Physiol. Plant., 161, 16-27, doi: 10.1111/ppl.12568.
  31. Aranda Sicilia, M. N., Sánchez Romero, M. E., Rodríguez Rosales, M. P., and Venema, K. (2021) Plastidial transporters KEA1 and KEA2 at the inner envelope membrane adjust stromal pH in the dark, New Phytol., 229, 2080-2090, doi: 10.1111/nph.17042.
  32. Bulychev, A. A., Alova, A. V., and Bibikova, T. N. (2013) Strong alkalinization of Chara cell surface in the area of cell wall incision as an early event in mechanoperception, Biochim. Biophys. Acta, 1828, 2359-2369, doi: 10.1016/j.bbamem.2013.07.002.
  33. Alova, A., Erofeev, A., Gorelkin, P., Bibikova, T., Korchev, Y., Majouga, A., and Bulychev, A. (2020) Prolonged oxygen depletion in microwounded cells of Chara corallina detected with novel oxygen nanosensors, J. Exp. Bot., 71, 386-398, doi: 10.1093/jxb/erz433.
  34. Hedrich, R. (2012) Ion channels in plants, Physiol. Rev., 92, 1777-1811, doi: 10.1152/physrev.00038.2011.
  35. Shimmen, T. (2007) The sliding theory of cytoplasmic streaming: fifty years of progress, J. Plant Res., 120, 31-43, doi: 10.1007/s10265-006-0061-0.

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