Illuminated giant cells of Characeae comprise alternating areas with H+ pump activity and zones with high conductivity for H+/OH–, which create counter-directed H+ flows between the medium and the cytoplasm. In areas where H+ enters the cell, the pH on the surface (pHo) increases to pH 10, while the cytoplasmic pH (pHc) decreases. The lack of the permeant substrate of photosynthesis (CO2) and the acidic pHc shift in the region of external alkaline zones redirect electron transport in chloroplasts from CO2-dependent (assimilatory) pathway to O2 reduction. This electron transport route is associated with an increase in thylakoid membrane ΔpH and an enhanced nonphotochemical quenching (NPQ) of chlorophyll excitations, which underlies strict coordination between nonuniform distributions of pHo and photosynthetic activity in resting cells. When the action potential (AP) is generated, the longitudinal pH profile is temporarily smoothed out, while the heterogeneity of the distribution of NPQ and PSII photochemical activity (YII) sharply increases. The damping of the pHo profile is due to the suppression of the H+ pump and passive H+ conductance under the influence of an almost 100-fold increase in the cytoplasmic of Ca2+ level ([Ca2+]c) during AP. The increase in [Ca2+]c stimulates photoreduction of O2 in chloroplasts under external alkaline zones and, at the same time, arrests the cytoplasmic streaming, which causes the accumulation of excess amounts of H2O2 in the cytoplasm in areas of intense production of this metabolite, with a weak effect on areas of CO2 assimilation. These changes enhance the nonuniform distribution of cell photosynthesis and account for the long-term oscillations of chlorophyll fluorescence Fm' and the quantum efficiency of linear electron flow in microscopic cell areas after the AP generation.