Electrical Signals at the Plasma Membrane and Their Influence on Chlorophyll Fluorescence of Chara Chloroplasts in vivo

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Alexander A. Bulychev^1,a*, Stepan Yu. Shapiguzov¹, and Anna V. Alova¹

¹Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russia

^* To whom correspondence should be addressed.

Received May 31, 2023; Revised June 30, 2023; Accepted July 2, 2023

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Action potentials of plant cells are engaged in the regulation of many cell processes, including photosynthesis and cytoplasmic streaming. Excitable cells of characean algae submerged in a medium with an elevated K⁺ content are capable of generating hyperpolarizing electrical responses. These active responses of plasma membrane originate upon the passage of inward electric current comparable in strength to natural currents circulating in illuminated Chara internodes. So far, it remained unknown whether the hyperpolarizing electrical signals in Chara affect the photosynthetic activity. Here, we showed that the negative shift of cell membrane potential, which drives K⁺ influx into the cytoplasm, is accompanied by a delayed decrease in the actual yield of chlorophyll fluorescence F′ and the maximal fluorescence yield F_m′ under low background light (12.5 µmol m^–2 s^–1). The transient changes in F′ and F_m′ were evident only under illumination, which suggests their close relation to the photosynthetic energy conversion in chloroplasts. Passing the inward current caused an increase in pH at the cell surface (pH_o), which reflected high H⁺/OH^– conductance of the plasmalemma and indicated a decrease in cytoplasmic pH due to the H⁺ entry into the cell. The shifts in pH_o arising in response to the first hyperpolarizing pulse disappeared upon repeated stimulation, thus indicating the long-term inactivation of plasmalemmal H⁺/OH^– conductance. Suppression of plasmalemmal H⁺ fluxes did not abolish the hyperpolarizing responses and the analyzed changes in chlorophyll fluorescence. These results suggest that K⁺ fluxes between the extracellular medium, cytoplasm, and stroma are involved in the functional changes of chloroplasts reflected by transients of F′ and F_m′.

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KEY WORDS: Chara, electrical signaling, hyperpolarization, plasmalemmal K⁺ conductance, chlorophyll fluorescence changes, H⁺/OH^– transport, plasmalemma–chloroplast interactions

DOI: 10.1134/S0006297923100048

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