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

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Abstract

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 Fm under low background light (12.5 µmol m–2 s–1). The transient changes in F′ and Fm 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 (pHo), 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 pHo 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 Fm.

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Abbreviations

AP:

action potential

APW:

artificial pond water

Chl:

chlorophyll

HR:

hyperpolarizing response

NPQ:

non-photochemical quenching

pHo :

pH in water layers adjacent to the cell surface

PET:

photosynthetic electron transport

PS:

photosystem

PSA:

photosynthetic apparatus

YII:

quantum yield of electron transfer

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Funding

This work was supported by the Russian Foundation for Basic Research (RFBR) (project no. 20-54-12015 NNIO_a) and carried out as part of the Scientific Project of the State Order of the Government of the Russian Federation to the Lomonosov Moscow State University (no. 121032500058-7).

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A.A.B. designed the study, conducted experiments, and wrote the draft manuscript; S.Yu.Sh. carried out experiments and processed raw data; A.V.A. discussed the results and supervised the study.

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Correspondence to Alexander A. Bulychev.

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The authors declare no conflict of interest. This article does not contain description of studies with human participants or animals performed by any of the authors.

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Bulychev, A.A., Shapiguzov, S.Y. & Alova, A.V. Electrical Signals at the Plasma Membrane and Their Influence on Chlorophyll Fluorescence of Chara Chloroplasts in vivo. Biochemistry Moscow 88, 1455–1466 (2023). https://doi.org/10.1134/S0006297923100048

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