Oscillations of chlorophyll fluorescence after plasma membrane excitation in Chara originate from nonuniform composition of signaling metabolites in the streaming cytoplasm.

Excitable cells of higher plants and characean algae respond to stressful stimuli by generating action potentials (AP) whose regulatory influence on chlorophyll (Chl) fluorescence and photosynthesis extends over tens of minutes. Unlike plant leaves where the efficiency of photosystem II reaction (YII) undergoes a separate reversible depression after an individual AP, characean algae exhibit long-lasting oscillations of YII after firing AP, provided that Chl fluorescence is measured on microscopic cell regions. Internodal cells of charophytes feature an extremely fast cytoplasmic streaming that stops immediately during the spike and recovers within ~10 min after AP. In this study a possibility was examined that multiple oscillations of YII and Chl fluorescence parameters (F ′, F m ′) result from the combined influence of metabolic rearrangements in chloroplasts and the cyclosis cessation–recovery cycle induced by the Ca2+ influx during AP. It is shown that the AP-induced F m ′ and YII oscillations disappear when the fluidic communications between the analyzed area (AOI) and surrounding cell regions are restricted or eliminated. The microfluidic signaling was manipulated in two ways: by narrowing the illuminated cell area and by arresting the cytoplasmic streaming with cytochalasin D (CD). The inhibition of F m ′ and YII oscillations was not caused by the loss of cell excitability, since CD-treated cells retained the capacity of AP generation. The mechanism of AP-induced oscillations of YII and Chl fluorescence seems to involve the lateral microfluidic transport of signaling substances in combination with the distribution pattern of these substances that was enhanced during the period of streaming cessation. • Chl fluorescence F m ′ at small Chara areas starts oscillating after cell excitation. • Cell excitation in presence of methyl viologen induces steady quenching of F m ′. • Narrowing illuminated cell area to Ø ~1 mm removes the majority of oscillations. • Oscillations vanish after elimination of cytoplasmic streaming by cytochalasin D. • Oscillations emerge from cytoplasmic flow of unevenly distributed metabolites. [ABSTRACT FROM AUTHOR]