Transient depletion of transported metabolites in the streaming cytoplasm of Chara upon shading the long-distance transmission pathway

• Published in: Biochimica et biophysica acta. Bioenergetics Vol. 1861; no. 10; p. 148257
• Main Author: Bulychev, Alexander A.
• Format: Journal Article
• Language: English
• Published: Elsevier B.V 01.10.2020
• Subjects: adenosine triphosphate; algae; carbon dioxide; Chara; chlorophyll; Chlorophyll fluorescence induction curves; Chloroplast envelope; chloroplasts; Cytoplasmic streaming; lighting; Long-distance communications; Metabolite translocators; metabolites; NADP (coenzyme); photosystem II; reducing agents; shade; transporters; LL; Chloroplast envelope; PQ; Metabolite translocators; BGL; Chlorophyll fluorescence induction curves; AOI; Cytoplasmic streaming; PS I and PSII; Long-distance communications
• ISSN: 0005-2728; 1879-2650; 1879-2650
• DOI: 10.1016/j.bbabio.2020.148257

Export of reducing power from chloroplasts to cytoplasm serves to balance the NADPH/ATP ratio that is optimal for CO2 assimilation. Rapid cytoplasmic streaming in characean algae conveys the exported metabolites downstream towards the shaded plastids where envelope transporters may operate for the import of reducing power in accordance with the direction of concentration gradients. Import of reducing equivalents by chloroplasts in the analyzed area transiently enhances the pulse-modulated chlorophyll fluorescence F′ controlled by the redox state of photosystem II acceptor QA. When the microfluidic pathway was transferred to darkness while the analyzed cell area remained in dim background light, the amplitude of cyclosis-mediated F′ changes dropped sharply and then recovered within 5–10 min. The suppression of long-distance signaling indicates temporal depletion of transmitted metabolites in the streaming cytoplasm. The return to overall background illumination induced an exceptionally large F′ response to the first local light pulse admitted to a remote cell region. This indicates the appearance of excess reductants in the streaming cytoplasm at a certain stage of photosynthetic induction. The results suggest highly dynamic exchange of metabolites between stationary chloroplasts lining the microfluidic pathway and the streaming cytoplasm upon light–dark and dark–light transitions. Evidence is obtained that slow stages of chlorophyll fluorescence induction in algae with rapid cytoplasmic streaming directly depend on cyclosis-mediated long-distance delivery of metabolites produced far beyond the analyzed cell area. [Display omitted] •Characean algae use cytoplasmic streaming for faraway export of reducing power.•Metabolites exported under light are consumed by chloroplasts in shaded cell parts.•Changes in irradiance transiently deplete or replenish the metabolites in the stream.•Fluid-carried metabolites are subject to similar losses in darkness and steady light.•Cytoplasmic flow is involved in slow induction of Chl fluorescence under dim light.