Role of Membrane H⁺ Transport and Plasmalemma Excitability in Pattern Formation, Long-Distance Transport and Photosynthesis of Characean Algae

Illuminated giant cells of Characeae produce alternating areas with H⁺-pump activity and zones of high H⁺/OH^– conductance, where H⁺ fluxes between the medium and the cytoplasm are oppositely directed. In areas where proton equivalents enter the cell, the pH on cell surface (pH_o) increases to pH 10, while the cytoplasmic pH (pH_c) decreases. Deficiency of the permeant substrate of photosynthesis (CO₂) and the acidic pH_c shift under external alkaline zones promote the redirection of electron transport in chloroplasts from CO₂-dependent assimilatory pathway to O₂ reduction. This bypass route of electron transport elevates the thylakoid membrane ΔpH and enhances nonphotochemical quenching (NPQ) of chlorophyll excitations, which determines strict coordination between nonuniform distributions of pH_o and photosynthetic activity in resting cells. When the action potential (AP) is generated, the longitudinal pH profile is temporarily smoothed out, while the heterogeneous distribution of NPQ and PSII photochemical activity (YII) becomes drastically sharpened. The damping of the pH_o profile is due to the suppression of the H⁺-pump and passive H⁺/OH^– conductance under the influence of an almost 100-fold increase in the cytoplasmic Ca²⁺ level ([Ca²⁺]_c) during AP. The increase in [Ca²⁺]_c stimulates photoreduction of O₂ in chloroplasts underlying external alkaline zones and, at the same time, arrests the cytoplasmic streaming, which lead to the accumulation of excess amounts of H₂O₂ in the cytoplasm in areas of intense production of this metabolite and has a weak effect on areas of CO₂ assimilation. These changes enhance the nonuniform distribution of cell photosynthesis and account for long-term oscillations of chlorophyll fluorescence \(F_{{\text{m}}}^{{{'}}}\) and the quantum efficiency of linear electron flow on microscopic cell areas after the AP generation.