Effects of chloroplast-cytoplasm exchange and lateral mass transfer on slow induction of chlorophyll fluorescence in Characeae.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Dec 2021
Dec 2021
Historique:
revised:
09
08
2021
received:
24
06
2021
accepted:
17
08
2021
pubmed:
21
8
2021
medline:
1
12
2021
entrez:
20
8
2021
Statut:
ppublish
Résumé
Rapid cytoplasmic streaming in characean algae mediates communications between remote cell regions exposed to uneven irradiance. The metabolites exported from brightly illuminated chloroplasts spread along the internode with the liquid flow and cause transient changes in chlorophyll fluorescence at cell areas that are exposed to dim light or placed shortly in darkness. The largest distance to which the photometabolites can be transported has not yet been determined. Neither is it known if lateral transport has an influence on the induction of chlorophyll fluorescence. In this study, the relations between spatial connectivity of anchored chloroplasts in characean internodes and fluorescence induction curves were examined. Connectivity between remote cell parts was pronounced upon illumination of a cell spot at a distance up to 10 mm from the area of fluorescence measurement, provided the spot was located upstream in the cytoplasmic flow. Spatial interactions between distant cell sites were also manifested in strikingly different slow stages of fluorescence induction caused by narrow- and wide-field illumination. Cytochalasin D, cooling of bath solution, and inactivation of light-dependent envelope transporters were used to disturb cyclosis-mediated spatial interactions. Although fluorescence induction curves induced by narrow- and wide-field illumination differed greatly under control conditions, they became similar after the inhibition of cyclosis with cytochalasin D. The results indicate that cytoplasmic streaming not only drives the lateral translocation of photometabolites but also promotes the export of reducing power from illuminated chloroplasts due to flushing the chloroplast surface and keeping sharp concentration gradients.
Substances chimiques
Chlorophyll
1406-65-1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1901-1913Subventions
Organisme : Russian Foundation for Basic Research
ID : 20-54-12015 NNIO_а
Informations de copyright
© 2021 Scandinavian Plant Physiology Society.
Références
Baker, N.R. (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89-113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Beilby, M.J. & Casanova, M.T. (2014) The physiology of characean cells. Berlin-Heidelberg: Springer.
Bräutigam, A. & Weber, A.P.M. (2011) Do metabolite transport processes limit photosynthesis? Plant Physiology, 155, 43-48. https://doi.org/10.1104/pp.110.164970
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. https://doi.org/10.1007/s00425-003-1084-6
Bulychev, A.A. (2020) Transient depletion of transported metabolites in the streaming cytoplasm of Chara upon shading the long-distance transmission pathway. Biochimica et Biophysica Acta-Bioenergetics, 1861, 148257. https://doi.org/10.1016/j.bbabio.2020.148257
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. Biochimica et Biophysica Acta-Bioenergetics, 1807, 1221-1230. https://doi.org/10.1016/j.bbabio.2011.06.009
Bulychev, A.A. & Foissner, I. (2020) Inhibition of endosomal trafficking by brefeldin A interferes with long-distance interaction between chloroplasts and plasma membrane transporters. Physiologia Plantarum, 169, 122-134. https://doi.org/10.1111/ppl.13058
Bulychev, A.A. & Komarova, A.V. (2015) Photoinduction of cyclosis-mediated interactions between distant chloroplasts. Biochimica et Biophysica Acta-Bioenergetics, 1847, 379-389. https://doi.org/10.1016/j.bbabio.2015.01.004
Bulychev, A.A. & Krupenina, N.A. (2019) Interchloroplast communications in Chara are suppressed under the alkaline bands and are relieved after the plasma membrane excitation. Bioelectrochemistry, 129, 62-69. https://doi.org/10.1016/j.bioelechem.2019.05.006
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. https://doi.org/10.1007/s00709-018-1255-8
Foissner, I. & Wasteneys, G.O. (2012) The characean internodal cell as a model system for studying wound healing. Journal of Microscopy, 247, 10-22. https://doi.org/10.1111/j.1365-2818.2011.03572.x
Elanskaya, I.V., Bulychev, A.A., Lukashev, E.P. & Muronets, E.M. (2021) Deficiency in flavodiiron protein Flv3 promotes cyclic electron flow and state transition under high light in the cyanobacterium Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta-Bioenergetics, 1862, 148318. https://doi.org/10.1016/j.bbabio.2020.148318
Elsässer, M., Feitosa-Araujo, E., Lichtenauer, S., Wagner, S., Fuchs, P., Giese, J. et al. (2020) Photosynthetic activity triggers pH and NAD redox signatures across different plant cell compartments. bioRxiv. https://doi.org/10.1101/2020.10.31.363051
Goldstein, R.E. & van de Meent, J.W. (2015) A physical perspective on cytoplasmic streaming. Interface Focus, 5, 20150030. https://doi.org/10.1098/rsfs.2015.0030
Kamiya, N. (1959) Protoplasmic streaming. Wien: Springer.
Kaňa, R. & Govindjee, G. (2016) Role of ions in the regulation of light harvesting. Frontiers in Plant Science, 7, 1849. https://doi.org/10.3389/fpls.2016.01849
Kaňa, R., Kotabová, E., Komárek, O., Šedivá, B., Papageorgiou, G.C., Govindjee, G. & Prášil, O. (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochimica et Biophysica Acta-Bioenergetics, 1817, 1237-1247. https://doi.org/10.1016/j.bbabio.2012.02.024
Kodru, S., Malavath, T., Devadasu, E., Nellaepalli, S., Stirbet, A., Subramanyam, R. et al. (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. Photosynthesis Research, 125, 219-231. https://doi.org/10.1007/s11120-015-0084-2
Komarova, A.V., Sukhov, V.S. & Bulychev, A.A. (2018) Cyclosis-mediated long distance communications of chloroplasts in giant cells of Characeae. Functional Plant Biology, 45, 236-246. https://doi.org/10.1071/FP16283
Kramer, D.M. & Evans, J.R. (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiology, 155, 70-78. https://doi.org/10.1104/pp.110.166652
Lazar, D. (2015) Parameters of photosynthetic energy partitioning. Journal of Plant Physiology, 175, 131-147. https://doi.org/10.1016/j.jplph.2014.10.021
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. Nature Communications, 11, 3238. https://doi.org/10.1038/s41467-020-17056-0
Marri, L., Zaffagnini, M., Collin, V., Issakidis-Bourguet, E., Lemaire, S.D., Pupillo, P. et al. (2009) Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Molecular Plant, 2, 259-269. https://doi.org/10.1093/mp/ssn061
Mishra, K.B., Mishra, A., Kubásek, J., Urban, O., Heyer, A.G. & Govindjee. (2019) Low temperature induced modulation of photosynthetic induction in non-acclimated and cold-acclimated Arabidopsis thaliana: chlorophyll a fluorescence and gas-exchange measurements. Photosynthesis Research, 139, 123-143. https://doi.org/10.1007/s11120-018-0588-7
Papageorgiou, G.C. & Govindjee (Eds.). (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Dordrecht: Springer Netherlands.
Pieruschka, R., Chavarría-Krauser, A., Schurr, U. & Jahnke, S. (2010) Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany, 61, 1031-1039. https://doi.org/10.1093/jxb/erp368
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. The New Phytologist, 169, 779-788. https://doi.org/10.1111/j.1469-8137.2005.01605.x
Satoh, K. (1982) Mechanism of photoactivation of electron transport in intact Bryopsis chloroplasts. Plant Physiology, 70, 1413-1416. https://doi.org/10.1104/pp.70.5.1413
Schansker, G., Tóth, S.Z. & Strasser, R.J. (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochimica et Biophysica Acta-Bioenergetics, 1706, 250-261. https://doi.org/10.1016/j.bbabio.2004.11.006
Scheibe, R. (2004) Malate valves to balance cellular energy supply. Physiologia Plantarum, 120, 21-26. https://doi.org/10.1111/j.0031-9317.2004.0222.x
Scheibe, R. & Dietz, K.J. (2012) Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant, Cell and Environment, 35, 202-216. https://doi.org/10.1111/j.1365-3040.2011.02319.x
Scheibe, R. & Stitt, M. (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiology and Biochemistry, 26, 473-481.
Selinski, J. & Scheibe, R. (2019) Malate valves: old shuttles with new perspectives. Plant Biology, 21, 21-30. https://doi.org/10.1111/plb.12869
Shimmen, T. & Yoshida, S. (1993) Analysis of temperature dependence of cytoplasmic streaming using tonoplast-free cells of Characeae. Protoplasma, 176, 174-177. https://doi.org/10.1007/BF01378954
Siebke, K. & Weis, E. (1995) Imaging of chlorophyll-a-fluorescence in leaves: topography of photosynthetic oscillations in leaves of Glechoma hederacea. Photosynthesis Research, 45, 225-237. https://doi.org/10.1007/BF00015563
Sommer, A., Hoeftberger, M., Hoepflinger, M.C., Schmalbrock, S., Bulychev, A. & Foissner, I. (2015) Convoluted plasma membrane domains in the green alga Chara are depleted of microtubules and actin filaments. Plant & Cell Physiology, 56, 1981-1996. https://doi.org/10.1093/pcp/pcv119
Stirbet, A., Lazar, D., Papageorgiou, G.C. & Govindjee G. (2019) Chlorophyll a fluorescence in cyanobacteria: relation to photosynthesis. In: Mishra, A.K., Tiwari, D.N. & Rai, A.N. (Eds.) Cyanobacteria: from basic science to applications. London: Acadeimc Press, Elsevier Inc., pp. 79-130.
Stirbet, A., Lazar, D., Guo, Y. & Govindjee, G. (2020) Photosynthesis: basics, history and modelling. Annals of Botany, 126, 511-537. https://doi.org/10.1093/aob/mcz171
Stirbet, A., Riznichenko, G.Y., Rubin, A.B. & Govindjee. (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow), 79, 291-323. https://doi.org/10.1134/S0006297914040014
Taniguchi, M. & Miyake, H. (2012) Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Current Opinion in Plant Biology, 15, 252-260. https://doi.org/10.1016/j.pbi.2012.01.014
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, 43. https://doi.org/10.1186/s13007-017-0194-2
Tsuchiya, Y., Yamazaki, H. & Aoki, T. (1991) Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell. Biophysical Journal, 59, 249-251. https://doi.org/10.1016/S0006-3495(91)82215-9