Long-range interactions of Chara chloroplasts are sensitive to plasma-membrane H+ flows and comprise separate photo- and dark-operated pathways

• Published in: Protoplasma Vol. 255; no. 6; pp. 1621 - 1634
• Main Authors: Bulychev, Alexander A., Rybina, Anna A.
• Format: Journal Article
• Language: English
• Published: Vienna Springer Vienna 01.11.2018; Springer Nature B.V
• Subjects: Antimycin A; Antimycin A - analogs & derivatives; Antimycin A - pharmacology; Biomedical and Life Sciences; Cell Biology; Cell Membrane - drug effects; Cell Membrane - metabolism; Chara - drug effects; Chara - metabolism; Chlorophyll; Chlorophyll - metabolism; Chloroplasts; Chloroplasts - drug effects; Chloroplasts - metabolism; Cytoplasm; Darkness; Electron transfer; Ferredoxin; Fluorescence; Hydrogen; Hydrogen-Ion Concentration; Illumination; Life Sciences; Light; Light effects; Metabolites; Original Article; Photosystem II; Photosystem II Protein Complex - metabolism; Plant Sciences; Plastids; Protons; Quinones; Signal Transduction - drug effects; Stroma; Zoology; Apoplastic and cytoplasmic pH; Antimycin A; Cytoplasmic streaming; Electron flows in darkened chloroplasts; Long-distance communications; Chara corallina
• ISSN: 0033-183X; 1615-6102
• DOI: 10.1007/s00709-018-1255-8

Local illumination of the characean internode with a 30-s pulse of white light was found to induce the delayed transient increase of modulated chlorophyll fluorescence in shaded cell parts, provided the analyzed region is located downstream in the cytoplasmic flow at millimeter distances from the light spot. The fluorescence response to photostimulation of a remote cell region indicates that the metabolites produced by source chloroplasts in an illuminated region are carried downstream with the cytoplasmic flow, thus ensuring long-distance communications between anchored plastids in giant internodal cells. The properties of individual stages of metabolite signaling are not yet well known. We show here that the export of assimilates and/or reducing equivalents from the source chloroplasts into the flowing cytoplasm is largely insensitive to the direction of plasma-membrane H + flows, whereas the events in sink regions where these metabolites are delivered to the acceptor chloroplasts under dim light are controlled by H + fluxes across the plasma membrane. The fluorescence response to local illumination of remote cell regions was best pronounced under weak background light and was also observed in a modified form within 1–2 min after the transfer of cell to darkness. The fluorescence transients in darkened cells were suppressed by antimycin A, an inhibitor of electron transfer from ferredoxin to plastoquinone, whereas the fluorescence response under background light was insensitive to this inhibitor. We conclude that the accumulation of reduced metabolites in the stroma leads to the reduction of photosystem II primary quinone acceptor (Q A ) via two separate (photochemical and non-photochemical) pathways.