Photoinduction of cyclosis-mediated interactions between distant chloroplasts

Abstract

Communications between chloroplasts and other organelles based on the exchange of metabolites, including redox active substances, are recognized as a part of intracellular regulation, chlororespiration, and defense against oxidative stress. Similar communications may operate between spatially distant chloroplasts in large cells where photosynthetic and respiratory activities are distributed unevenly under fluctuating patterned illumination. Microfluorometry of chlorophyll fluorescence in vivo in internodal cells of the alga Chara corallina revealed that a 30-s pulse of localized light induces a transient increase (~25%) in F' fluorescence of remote cell parts exposed to dim background light at a 1.5-mm distance on the downstream side from the illuminated spot in the plane of unilateral cytoplasmic streaming but has no effect on F' at equal distance on the upstream side. An abrupt arrest of cytoplasmic streaming for about 30s by triggering the action potential extended either the ascending or descending fronts of the F' fluorescence response, depending on the exact moment of streaming cessation. The response of F' fluorescence to localized illumination of a distant cell region was absent in dark-adapted internodes, when the localized light was applied within the first minute after switching on continuous background illumination of the whole cell, but it appeared in full after longer exposures to continuous background light. These results and the elimination of the F' response by methyl viologen known to redirect electron transport pathways beyond photosystem I indicate the importance of photosynthetic induction and the stromal redox state for long-distance communications of chloroplasts in vivo.

Inhibition of endosomal trafficking by brefeldin A interferes with long‐distance interaction between chloroplasts and plasma membrane transporters

“…Such experiments have previously revealed that chloroplast electron transport can be modified by reducing equivalents released from illuminated regions and transported to non‐illuminated chloroplasts via the streaming endoplasm (Fig. S1C; Bulychev et al , Bulychev and Komarova , ).…”

Pathways for external alkalinization in intact and in microwounded Chara cells are differentially sensitive to wortmannin

“…When a small portion of the internodal cell is shortly exposed to local illumination, a transient increase in actual chlorophyll fluorescence ( F' ) can be observed after a lag period on mm-scale distances, provided the analyzed cell area is positioned downstream of the illuminated region. 16, 17 This fluorescence transient is mediated by cytoplasmic streaming. It vanishes after the cessation of cyclosis in the presence of 25 μM cytochalasin D and reappears after the recovery of cyclosis in washed cells ( Fig.…”

“…At low irradiance (8–10 µmol quanta m −2 s −1 ) long-distance communications between chloroplasts, manifested as F’ changes in response to a bright pulse of local light, are pronounced to the highest extent. 16 Low intensity background light is needed to maintain light-dependent photosynthetic enzymes in the active state. On the other hand, at high intensity of background light, the analyzed F' transients are masked by strong fluorescence quenching.…”

Effects of chloroplast–cytoplasm exchange and lateral mass transfer on slow induction of chlorophyll fluorescence in Characeae

“…Previous studies with Chara revealed very slow stages of F′ fluorescence induction under the exposure of internodal cells to dim light (approximately 10 μmol m −2 s −1 ) (Bulychev & Komarova, 2015; Bulychev & Krupenina, 2019). The appearance of this S‐M‐T fluorescence transient correlated with the development of spatial connectivity, as observed from longitudinal propagation of the F′ fluorescence wave.…”