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Induction Changes of Chlorophyll Fluorescence in Chara Cells Related to Metabolite Exchange between Chloroplasts and Cytoplasmic Flow

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Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract—

Induction changes in chlorophyll fluorescence are associated with photosynthetic electron transfer, generation of the transmembrane proton gradient, and production of carbohydrates in the CO2 fixation cycle. The reactions of photosynthesis are also accompanied by the outflow of photoproducts from illuminated chloroplasts and their long-distance transport. The exchange of metabolites across the chloroplast envelope membranes is carried out by transporters that are active in the light and cease to operate in darkness. Inactivation of light-dependent envelope transporters in Chara cells interrupts spatial signaling manifested as a transient fluorescence rise in response to illumination of a distant cell area. The dark adaptation was found to down-regulate the entry of metabolites from the streaming cytoplasm into shaded chloroplasts but had rather low influence on metabolite export from illuminated plastids. Fluorescence induction curves were quite sensitive to illumination or darkening of the sample area residing outside the region of photometric assay. The amplitude of slow fluorescence changes observed under dim illumination of the whole Chara internode was substantially larger than under narrow-field illumination of the fluorescence assay region. The results indicate that the slow increase in fluorescence during the induction period in characean cells results not only from photosynthetic activity of chloroplasts in the examined cell region but also from interactions between the analyzed and neighboring cell areas. When the cytoplasmic streaming was arrested by cytochalasin D, similar induction changes were induced by local and global illumination, indicating a disruption of long-range interactions. The results suggest that the liquid flow not only carries metabolites from illuminated to shaded cell parts but also facilitates the export of photometabolites from chloroplasts to the cytoplasm.

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REFERENCES

  1. Papageorgiou G.C., Govindjee. 2014. The non-photochemical quenching of the electronically excited state of chlorophyll a in plants: Definitions, timelines, viewpoints, open questions. In: Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Eds. Demmig-Adams B., Garab G., Adams III W., Govindjee. Dordrecht: Springer, p. 531–550.

  2. Stirbet A., Riznichenko G.Y., Rubin A.B., Govindjee. 2014. Modeling chlorophyll a fluorescence transient: Relation to photosynthesis, Biochemistry (Moscow). 79, 291–323.

    Article  CAS  Google Scholar 

  3. Siebke K., Weis E. 1995. Imaging of chlorophyll-a-fluorescence in leaves: Topography of photosynthetic oscillations in leaves of Glechoma hederacea. Photosynth. Res. 45, 225–237.

    Article  CAS  Google Scholar 

  4. Pieruschka R., Schurr U., Jensen M., Wolff W.F., Jahnke S. 2006. Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves. New Phytol. 169, 779–788.

    Article  Google Scholar 

  5. Pieruschka R., Chavarría-Krauser A., Schurr U., Jahnke S. 2010. Photosynthesis in lightfleck areas of homobaric and heterobaric leaves, J. Exp. Bot. 61, 1031–1039.

    Article  CAS  Google Scholar 

  6. Kaňa R., Kotabová E., Komárek O., Šedivá B., Papageorgiou G.C., Govindjee, Prášil O. 2012. The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim. Biophys. Acta. 1817, 1237–1247.

  7. Kodru S., Malavath T., Devadasu E., Nellaepalli S., Stirbet A., Subramanyam R., Govindjee. 2015. The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth. Res. 125, 219–231.

    Article  CAS  Google Scholar 

  8. Bernát G., Steinbach G., Kaňa R., Govindjee, Misra A.N., Prašil O. 2018. On the origin of the slow M–T chlorophyll a fluorescence decline in cyanobacteria: Interplay of short-term light-responses. Photosynth. Res. 136, 183–198.

    Article  Google Scholar 

  9. Bulychev A., Vredenberg W. 2003. Spatio-temporal patterns of photosystem II activity and plasma-membrane proton flows in Chara corallina cells exposed to overall and local illumination. Planta. 218, 143–151.

    Article  CAS  Google Scholar 

  10. Bulychev A.A., Dodonova S.O. 2011. Effects of cyclosis on chloroplast-cytoplasm interactions revealed with localized lighting in characean cells at rest and after electrical excitation. Biochim. Biophys. Acta. 1807, 1221–1230.

    Article  CAS  Google Scholar 

  11. Bulychev A.A., Komarova A.V. 2015. Photoinduction of cyclosis-mediated interactions between distant chloroplasts. Biochim. Biophys. Acta. 1847, 379–389.

    Article  CAS  Google Scholar 

  12. Komarova A.V., Sukhov V.S., Bulychev A.A. 2018. Cyclosis-mediated long distance communications of chloroplasts in giant cells of Characeae. Funct. Plant Biol. 45, 236–246.

    Article  CAS  Google Scholar 

  13. Bulychev A.A., Foissner I. 2020. Inhibition of endosomal trafficking by brefeldin A interferes with long-distance interaction between chloroplasts and plasma membrane transporters. Physiol. Plant. 169, 122–134.

    Article  CAS  Google Scholar 

  14. Tseng Y.C., Chu S.W. 2017. High spatio-temporal-resolution detection of chlorophyll fluorescence dynamics from a single chloroplast with confocal imaging fluorometer. Plant Methods. 13, 1–11.

    Article  Google Scholar 

  15. Bulychev A.A. 2020. Transient depletion of transported metabolites in the streaming cytoplasm of Chara upon shading the long-distance transmission pathway. Biochim. Biophys. Acta. 1861, 148257.

    Article  CAS  Google Scholar 

  16. Bulychev A.A., Foissner I. 2017. Pathways for external alkalinization in intact and in microwounded Chara cells are differentially sensitive to wortmannin. Plant Signal. Behav. 12, e1362518.

    Article  Google Scholar 

  17. Foissner I., Wasteneys G.O. 2012. The characean internodal cell as a model system for studying wound healing. J. Microsc. 247, 10–22.

    Article  CAS  Google Scholar 

  18. Goldstein R.E., Van de Meent J.W. 2015. A physical perspective on cytoplasmic streaming. Interface Focus. 5, 20150030.

    Article  Google Scholar 

  19. Scheibe R. 2004. Malate valves to balance cellular energy supply. Physiol. Plant. 120, 21–26.

    Article  CAS  Google Scholar 

  20. Taniguchi M., Miyake H. 2012. Redox-shuttling between chloroplast and cytosol: Integration of intra-chloroplast and extra-chloroplast metabolism. Curr. Opin. Plant Biol. 15, 252–260.

    Article  CAS  Google Scholar 

  21. Selinski J., Scheibe R. 2019. Malate valves: Old shuttles with new perspectives. Plant Biol. 21, 21–30.

    Article  CAS  Google Scholar 

  22. Vaseghi M.J., Chibani K., Telman W., Liebthal M.F., Gerken M., Schnitzer H., Mueller S.M., Dietz K.J. 2018. The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism. Elife. 7, e38194.

    Article  Google Scholar 

  23. Howard T.P., Metodiev M., Lloyd J.C., Raines C.A. 2008. Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc. Natl. Acad. Sci. USA. 105, 4056–4061.

    Article  CAS  Google Scholar 

  24. Bulychev A.A., Komarova A.V. 2017. Photoregulation of photosystem II activity mediated by cytoplasmic streaming in Chara and its relation to pH bands. Biochim. Biophys. Acta. 1858, 386–395.

    Article  CAS  Google Scholar 

  25. Bulychev A.A., Rybina A.A. 2018. Long-range interactions of Chara chloroplasts are sensitive to plasma-membrane H+ flows and comprise separate photo- and dark-operated pathways. Protoplasma. 255, 1621–1634.

    Article  CAS  Google Scholar 

  26. Heineke D., Riens B., Grosse H., Hoferichter P., Peter U., Flügge U.I., Heldt H.W. 1991. Redox transfer across the inner chloroplast envelope membrane. Plant Physiol. 95, 1131–1137.

    Article  CAS  Google Scholar 

  27. Lim S.L., Voon C.P., Guan X., Yang Y., Gardeström P., Lim B.L. 2020. In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD+ fluorescent protein sensors. Nat. Commun. 11, 3238.

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

The study was supported by the Russian Foundation for Basic Research (project no. 20-54-12 015).

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  1. Lomonosov Moscow State University, Faculty of Biology, 119991, Moscow, Russia

    A. A. Bulychev

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  1. A. A. Bulychev
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Correspondence to A. A. Bulychev.

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Translated by A. Bulychev

Abbreviations: AOI, area of fluorescence inspection; BGL, background lighting of the whole cell; BGLAOI, background light directed locally to AOI; Chl, chlorophyll; D, dark incubation; LL, local light (pulse).

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Bulychev, A.A. Induction Changes of Chlorophyll Fluorescence in Chara Cells Related to Metabolite Exchange between Chloroplasts and Cytoplasmic Flow. Biochem. Moscow Suppl. Ser. A 15, 184–194 (2021). https://doi.org/10.1134/S199074782103003X

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  • DOI: https://doi.org/10.1134/S199074782103003X

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