Salt Stress Induces Paramylon Accumulation and Fine-Tuning of the Macro-Organization of Thylakoid Membranes in Euglena gracilis Cells

Kanna, Sai Divya; Domonkos, Ildikó; Kóbori, Tímea Ottília; Dergez, Ágnes; Böde, Kinga; Nagyapáti, Sarolta; Zsiros, Ottó; Ünnep, Renáta; Nagy, Gergely; Garab, Gyözö; Szilák, László; Solymosi, Katalin; Kovács, László; Ughy, Bettina

doi:10.3389/fpls.2021.725699

Title: Salt Stress Induces Paramylon Accumulation and Fine-Tuning of the Macro-Organization of Thylakoid Membranes in Euglena gracilis Cells

Journal Article · Tue Nov 16 00:00:00 EST 2021 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2021.725699· OSTI ID:1831604

Kanna, Sai Divya ^[1]; Domonkos, Ildikó ^[2]; Kóbori, Tímea Ottília ^[3]; Dergez, Ágnes ^[4]; Böde, Kinga ^[1]; Nagyapáti, Sarolta ^[1]; Zsiros, Ottó ^[2]; Ünnep, Renáta ^[5];

^[6]; Garab, Gyözö ^[7]; Szilák, László ^[8]; Solymosi, Katalin ^[9]; Kovács, László ^[2]; Ughy, Bettina ^[2]

Eotvos Lorand Research Network, Szeged (Hungary); Univ. of Szeged (Hungary)
Eotvos Lorand Research Network, Szeged (Hungary)
Univ. of Szeged (Hungary); Bay Zoltan Nonprofit Ltd. for Applied Research, Szeged (Hungary)
Bay Zoltan Nonprofit Ltd. for Applied Research, Szeged (Hungary)
Eotvos Lorand Research Network, Budapest (Hungary)
Eotvos Lorand Research Network, Budapest (Hungary); European Spallation Source (ESS), Lund (Sweden); Paul Scherrer Inst. (PSI), Villigen (Switzerland); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Eotvos Lorand Research Network, Szeged (Hungary); University of Ostrava (Czechia)
Szilak Laboratory Ltd., Szeged (Hungary)
ELTE Eotvos Lorand University, Budapest (Hungary)

The effects of salt stress condition on the growth, morphology, photosynthetic performance, and paramylon content were examined in the mixotrophic, unicellular, flagellate Euglena gracilis. We found that salt stress negatively influenced cell growth, accompanied by a decrease in chlorophyll (Chl) content. Circular dichroism (CD) spectroscopy revealed the changes in the macro-organization of pigment-protein complexes due to salt treatment, while the small-angle neutron scattering (SANS) investigations suggested a reduction in the thylakoid stacking, an effect confirmed by the transmission electron microscopy (TEM). At the same time, the analysis of the thylakoid membrane complexes using native-polyacrylamide gel electrophoresis (PAGE) revealed no significant change in the composition of supercomplexes of the photosynthetic apparatus. Salt stress did not substantially affect the photosynthetic activity, as reflected by the fact that Chl fluorescence yield, electron transport rate (ETR), and energy transfer between the photosystems did not change considerably in the salt-grown cells. We have observed notable increases in the carotenoid-to-Chl ratio and the accumulation of paramylon in the salt-treated cells. We propose that the accumulation of storage polysaccharides and changes in the pigment composition and thylakoid membrane organization help the adaptation of E. gracilis cells to salt stress and contribute to the maintenance of cellular processes under stress conditions.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); Czech Science Foundation; Hungarian Ministry for National Economy; National Research Development and Innovation Office of Hungary

Grant/Contract Number:: AC05-00OR22725; GINOP-2.3.2-15-2016-00058; 128679; FK124748; GA CR 19-13637X

OSTI ID:: 1831604

Journal Information:: Frontiers in Plant Science, Vol. 12; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Modification of the thylakoid structure of Euglena gracilis by norflurazon-treatment: consequences for fluorescence quenching Tschiersch, Henning; Ohmann, Erich; Doege, Maria Environmental and Experimental Botany, Vol. 47, Issue 3 https://doi.org/10.1016/S0098-8472(01)00132-0	journal	May 2002
Regulation and function of xanthophyll cycle-dependent photoprotection in algae Goss, Reimund; Jakob, Torsten Photosynthesis Research, Vol. 106, Issue 1-2 https://doi.org/10.1007/s11120-010-9536-x	journal	March 2010
Euglena gracilis growth and cell composition under different temperature, light and trophic conditions Wang, Yanming; Seppänen-Laakso, Tuulikki; Rischer, Heiko PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0195329	journal	April 2018
Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex Murata, N.; Mohanty, P. S.; Hayashi, H. FEBS Letters, Vol. 296, Issue 2 https://doi.org/10.1016/0014-5793(92)80376-R	journal	January 1992
Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells Neelam, Satyabala; Subramanyam, Rajagopal Journal of Photochemistry and Photobiology B: Biology, Vol. 124 https://doi.org/10.1016/j.jphotobiol.2013.04.007	journal	July 2013
The transcriptome of Euglena gracilis reveals unexpected metabolic capabilities for carbohydrate and natural product biochemistry O'Neill, Ellis C.; Trick, Martin; Hill, Lionel Molecular BioSystems, Vol. 11, Issue 10 https://doi.org/10.1039/C5MB00319A	journal	January 2015
Structural and functional changes of PSI-LHCI supercomplexes of Chlamydomonas reinhardtii cells grown under high salt conditions Subramanyam, Rajagopal; Jolley, Craig; Thangaraj, Balakumar Planta, Vol. 231, Issue 4 https://doi.org/10.1007/s00425-009-1097-x	journal	January 2010
Acclimation of Arabidopsis thaliana to the light environment: changes in photosynthetic function Walters, RobinG.; Horton, Peter Planta, Vol. 197, Issue 2 https://doi.org/10.1007/BF00202652	journal	September 1995
The effect of ionic stress on photosynthesis in Dunaliella tertiolecta: Chlorophyll fluorescence kinetics and spectral characteristics Gilmour, D. J.; Hipkins, M. F.; Webber, A. N. Planta, Vol. 163, Issue 2 https://doi.org/10.1007/BF00393515	journal	February 1985
Kinetics of structural reorganizations in multilamellar photosynthetic membranes monitored by small-angle neutron scattering Nagy, Gergely; Kovács, László; Ünnep, Renáta The European Physical Journal E, Vol. 36, Issue 7 https://doi.org/10.1140/epje/i2013-13069-0	journal	July 2013
Analysis of Molecular Masses and Oligomeric States of Protein Complexes by Blue Native Electrophoresis and Isolation of Membrane Protein Complexes by Two-Dimensional Native Electrophoresis Schagger, H.; Cramer, W. A.; Vonjagow, G. Analytical Biochemistry, Vol. 217, Issue 2 https://doi.org/10.1006/abio.1994.1112	journal	March 1994
Photosynthesis in rice under a salt stress Tiwari, B. S.; Bose, A.; Ghosh, B. Photosynthetica, Vol. 34, Issue 2 https://doi.org/10.1023/A:1006857027398	journal	March 1997
Oral administration of Euglena gracilis Z and its carbohydrate storage substance provides survival protection against influenza virus infection in mice Nakashima, Ayaka; Suzuki, Kengo; Asayama, Yuta Biochemical and Biophysical Research Communications, Vol. 494, Issue 1-2 https://doi.org/10.1016/j.bbrc.2017.09.167	journal	December 2017
The role of mitochondrial respiration in salinity tolerance Jacoby, Richard P.; Taylor, Nicolas L.; Millar, A. Harvey Trends in Plant Science, Vol. 16, Issue 11 https://doi.org/10.1016/j.tplants.2011.08.002	journal	November 2011
Effects of salinity changes on aquatic organisms in a multiple stressor context Velasco, Josefa; Gutiérrez-Cánovas, Cayetano; Botella-Cruz, María Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1764 https://doi.org/10.1098/rstb.2018.0011	journal	December 2018
Reversible changes in macroorganization of the light-harvesting chlorophyll a/b pigment-protein complex detected by circular dichroism Garab, Gyozo; Leegood, Richard C.; Walker, David A. Biochemistry, Vol. 27, Issue 7 https://doi.org/10.1021/bi00407a028	journal	April 1988
Evidence for long-range excitation energy migration in macroaggregates of the chlorophyll ab light-harvesting antenna complexes Barzda, Virginijus; Garab, Gyözö; Gulbinas, Vidas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1273, Issue 3 https://doi.org/10.1016/0005-2728(95)00147-6	journal	March 1996
Salt response of the freshwater microalga Scenedesmus obliquus (Turp.) Kutz is modulated by the algal growth phase El-Katony, Taha Mohamed; El-Adl, Magda Faiz Journal of Oceanology and Limnology, Vol. 38, Issue 3 https://doi.org/10.1007/s00343-019-9067-z	journal	November 2019
An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm Klughammer, Christof; Schreiber, Ulrich Planta, Vol. 192, Issue 2 https://doi.org/10.1007/BF01089043	journal	January 1994
Dynamics of the response of cyanobacteria to salt stress: Deciphering the molecular events Joset, Francoise; Jeanjean, Robert; Hagemann, Martin Physiologia Plantarum, Vol. 96, Issue 4 https://doi.org/10.1111/j.1399-3054.1996.tb00251.x	journal	April 1996
Multiple effects of salinity on photosynthesis of the protist Euglena gracilis Gonzalez-Moreno, Sergio; Gomez-Barrera, Juan; Perales, Hugo Physiologia Plantarum, Vol. 101, Issue 4 https://doi.org/10.1111/j.1399-3054.1997.tb01063.x	journal	December 1997
Toxic effects of individual and combined effects of BTEX on Euglena gracilis Peng, Cheng; Lee, Jong-Wha; Sichani, Homa Teimouri Journal of Hazardous Materials, Vol. 284 https://doi.org/10.1016/j.jhazmat.2014.10.024	journal	March 2015
Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering Nagy, Gergely; Posselt, Dorthe; Kovács, László Biochemical Journal, Vol. 436, Issue 2 https://doi.org/10.1042/BJ20110180	journal	May 2011
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents Lichtenthaler, Hartmut K.; Wellburn, Alan R. Biochemical Society Transactions, Vol. 11, Issue 5 https://doi.org/10.1042/bst0110591	journal	October 1983
Wax ester fermentation in Euglena gracilis Inui, Hiroshi; Miyatake, Kazutaka; Nakano, Yoshihisa FEBS Letters, Vol. 150, Issue 1 https://doi.org/10.1016/0014-5793(82)81310-0	journal	December 1982
Molecular tools and applications of Euglena gracilis : From biorefineries to bioremediation Khatiwada, Bishal; Sunna, Anwar; Nevalainen, Helena Biotechnology and Bioengineering, Vol. 117, Issue 12 https://doi.org/10.1002/bit.27516	journal	August 2020
Thylakoid membrane reorganizations revealed by small-angle neutron scattering of Monstera deliciosa leaves associated with non-photochemical quenching Ünnep, Renáta; Paul, Suman; Zsiros, Ottó Open Biology, Vol. 10, Issue 9 https://doi.org/10.1098/rsob.200144	journal	September 2020
Inactivation of Photosynthetic Oxygen Evolution and Concomitant Release of Three Polypeptides in the Photosystem II Particles of Spinach Chloroplasts Kuwabara, Tomohiko; Murata, Norio Plant and Cell Physiology, Vol. 23, Issue 3 https://doi.org/10.1093/oxfordjournals.pcp.a076378	journal	April 1982
Plant salt tolerance Zhu, Jian-Kang Trends in Plant Science, Vol. 6, Issue 2 https://doi.org/10.1016/S1360-1385(00)01838-0	journal	February 2001
The fine structure of Euglena gracilis with special reference to the chloroplasts and pyrenoids Gibbs, Sarah P. Journal of Ultrastructure Research, Vol. 4, Issue 2 https://doi.org/10.1016/S0022-5320(60)90049-6	journal	November 1960
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin Nature, Vol. 428, Issue 6980 https://doi.org/10.1038/nature02373	journal	March 2004
High-salt solutions prevent reactivation of euglenoid movement in detergent-treated cell models ofEuglena gracilis Murata, K.; Suzaki, T. Protoplasma, Vol. 203, Issue 3-4 https://doi.org/10.1007/BF01279468	journal	September 1998
Similarities and Differences in the Effects of Toxic Concentrations of Cadmium and Chromium on the Structure and Functions of Thylakoid Membranes in Chlorella variabilis Zsiros, Ottó; Nagy, Gergely; Patai, Roland Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.01006	journal	July 2020
Effects of abiotic stressors on lutein production in the green microalga Dunaliella salina Fu, Weiqi; Paglia, Giuseppe; Magnúsdóttir, Manuela Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/1475-2859-13-3	journal	January 2014
Effects of NaCl Stress on the Structure, Pigment Complex Composition, and Photosynthetic Activity of Mangrove Bruguiera parviflora Chloroplasts Parida, A. K.; Das, A. B.; Mittra, B. Photosynthetica, Vol. 41, Issue 2 https://doi.org/10.1023/B:PHOT.0000011951.37231.69	journal	June 2003
New Fluorescence Parameters for the Determination of Q _A Redox State and Excitation Energy Fluxes Kramer, David M.; Johnson, Giles; Kiirats, Olavi Photosynthesis Research, Vol. 79, Issue 2 https://doi.org/10.1023/B:PRES.0000015391.99477.0d	journal	January 2004
Effect of salinity and nitrogen on growth, sodium, potassium accumulation, and osmotic adjustment of halophyte Suaeda aegyptiaca (Hasselq.) Zoh Zakery-Asl, Mohammad Amin; Bolandnazar, Sahebali; Oustan, Shahin Archives of Agronomy and Soil Science, Vol. 60, Issue 6 https://doi.org/10.1080/03650340.2013.841889	journal	September 2013
Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max.) under salt stress He, Yi; Yu, Chenliang; Zhou, Li Plant Physiology and Biochemistry, Vol. 74 https://doi.org/10.1016/j.plaphy.2013.11.008	journal	January 2014
Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes Järvi, Sari; Suorsa, Marjaana; Paakkarinen, Virpi Biochemical Journal, Vol. 439, Issue 2 https://doi.org/10.1042/BJ20102155	journal	September 2011
The Role of Glycerol in the Osmotic Regulation of the Halophilic Alga Dunaliella parva Ben-Amotz, Ami; Avron, Mordhay Plant Physiology, Vol. 51, Issue 5 https://doi.org/10.1104/pp.51.5.875	journal	May 1973
Cyanide-sensitive and cyanide-resistant respiration of dark-grown Euglena gracilis Devars, Silvia; Torres-Márquez, M. Eugenia; González-Halphen, Diego Plant Science, Vol. 82, Issue 1 https://doi.org/10.1016/0168-9452(92)90006-8	journal	January 1992
Effect of Mild Salinity Stress on the Growth, Fatty Acid and Carotenoid Compositions, and Biological Activities of the Thermal Freshwater Microalgae Scenedesmus sp. Elloumi, Wiem; Jebali, Ahlem; Maalej, Amina Biomolecules, Vol. 10, Issue 11 https://doi.org/10.3390/biom10111515	journal	November 2020
The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga—Scenedesmus obliquus XJ002 Ji, Xiang; Cheng, Jie; Gong, Donghui Science of The Total Environment, Vol. 633 https://doi.org/10.1016/j.scitotenv.2018.03.240	journal	August 2018
Involvement of the Lhcx protein Fcp6 of the diatom Cyclotella meneghiniana in the macro-organisation and structural flexibility of thylakoid membranes Ghazaryan, Artur; Akhtar, Parveen; Garab, Győző Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 9 https://doi.org/10.1016/j.bbabio.2016.04.288	journal	September 2016
Bioproducts From Euglena gracilis: Synthesis and Applications Gissibl, Alexander; Sun, Angela; Care, Andrew Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00108	journal	May 2019
β-Glucan in Foods and Its Physiological Functions Nakashima, Ayaka; Yamada, Koji; Iwata, Osamu Journal of Nutritional Science and Vitaminology, Vol. 64, Issue 1 https://doi.org/10.3177/jnsv.64.8	journal	January 2018
Fingerprinting the macro-organisation of pigment–protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy Tóth, Tünde N.; Rai, Neha; Solymosi, Katalin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 9 https://doi.org/10.1016/j.bbabio.2016.04.287	journal	September 2016
The psi‐type circular dichroism of large molecular aggregates. III. Calculations Kim, Myeong‐Hee; Ulibarri, Laura; Keller, David The Journal of Chemical Physics, Vol. 84, Issue 6 https://doi.org/10.1063/1.450279	journal	March 1986
Structurally flexible macro-organization of the pigment–protein complexes of the diatom Phaeodactylum tricornutum Szabó, Milán; Lepetit, Bernard; Goss, Reimund Photosynthesis Research, Vol. 95, Issue 2-3 https://doi.org/10.1007/s11120-007-9252-3	journal	September 2007
Photorespiration: metabolic pathways and their role in stress protection Wingler, Astrid; Lea, Peter J.; Quick, W. Paul Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0712	journal	October 2000
Osmoregulation in the Extremely Euryhaline Marine Micro-Alga Chlorella autotrophica Ahmad, Iftikhar; Hellebust, Johan A. Plant Physiology, Vol. 74, Issue 4 https://doi.org/10.1104/pp.74.4.1010	journal	April 1984
Theory of the interaction of light with large inhomogeneous molecular aggregates. I. Absorption Keller, David; Bustamante, Carlos The Journal of Chemical Physics, Vol. 84, Issue 6 https://doi.org/10.1063/1.450277	journal	March 1986
Changes of the Photosynthetic Apparatus in Spirulina Cyanobacterium by Sodium Stress Verma, Kavita; Mohanty, Prasanna Zeitschrift für Naturforschung C, Vol. 55, Issue 1-2 https://doi.org/10.1515/znc-2000-1-205	journal	February 2000
Carotenoids, versatile components of oxygenic photosynthesis Domonkos, Ildikó; Kis, Mihály; Gombos, Zoltán Progress in Lipid Research, Vol. 52, Issue 4 https://doi.org/10.1016/j.plipres.2013.07.001	journal	October 2013
Responses of morphological, physiological, and biochemical parameters in Euglena gracilis to 7-days exposure to two commonly used fertilizers DAP and urea Azizullah, Azizullah; Richter, Peter; Häder, Donat-Peter Journal of Applied Phycology, Vol. 24, Issue 1 https://doi.org/10.1007/s10811-010-9641-4	journal	January 2011
The light-harvesting system of Euglena gracilis during the cell cycle Brandt, Peter; Wilhelm, Christian Planta, Vol. 180, Issue 2 https://doi.org/10.1007/BF00194010	journal	January 1990
Salinity stress effects on direct and indirect defence metabolites in maize Forieri, Ilaria; Hildebrandt, Ulrich; Rostás, Michael Environmental and Experimental Botany, Vol. 122 https://doi.org/10.1016/j.envexpbot.2015.09.007	journal	February 2016
The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering Ünnep, R.; Zsiros, O.; Solymosi, K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 9 https://doi.org/10.1016/j.bbabio.2014.01.017	journal	September 2014
Differential synthesis of sucrose and trehalose in Euglena gracilis cells during growth and salt stress Porchia, Andrea C.; Fiol, Diego F.; Salerno, Graciela L. Plant Science, Vol. 149, Issue 1 https://doi.org/10.1016/S0168-9452(99)00142-9	journal	November 1999
Effects of increased salinity on gravitaxis inEuglena gracilis Richter, Peter; Börnig, Anke; Streb, Christine Journal of Plant Physiology, Vol. 160, Issue 6 https://doi.org/10.1078/0176-1617-00828	journal	January 2003
Simultaneous Intake of Euglena gracilis and Vegetables Exerts Synergistic Anti-Obesity and Anti-Inflammatory Effects by Modulating the Gut Microbiota in Diet-Induced Obese Mice Okouchi, Ran; E., Shuang; Yamamoto, Kazushi Nutrients, Vol. 11, Issue 1 https://doi.org/10.3390/nu11010204	journal	January 2019
Modulation of the multilamellar membrane organization and of the chiral macrodomains in the diatom Phaeodactylum tricornutum revealed by small-angle neutron scattering and circular dichroism spectroscopy Nagy, Gergely; Szabó, Milán; Ünnep, Renáta Photosynthesis Research, Vol. 111, Issue 1-2 https://doi.org/10.1007/s11120-011-9693-6	journal	October 2011
Signification structurale et fonctionnelle des enveloppes chloroplastiques d'Euglena: Etude immunocytologique et en cryofracture Lefort-Tran, M.; Pouphile, M.; Freyssinet, G. Journal of Ultrastructure Research, Vol. 73, Issue 1 https://doi.org/10.1016/0022-5320(80)90115-X	journal	October 1980
The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii Kodru, Sireesha; Malavath, Tirupathi; Devadasu, Elsinraju Photosynthesis Research, Vol. 125, Issue 1-2 https://doi.org/10.1007/s11120-015-0084-2	journal	February 2015
Halotolerance studies onChlamydomonas reinhardtii: glycerol excretion by free and immobilized cells León, R.; Galván, F. Journal of Applied Phycology, Vol. 6, Issue 1 https://doi.org/10.1007/BF02185898	journal	February 1994
Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Stirbet, A.; Lazár, D.; Kromdijk, J. Photosynthetica, Vol. 56, Issue 1 https://doi.org/10.1007/s11099-018-0770-3	journal	January 2018
Comparative assessment of the Euglena gracilis var. saccharophila variant strain as a producer of the β‐1,3‐glucan paramylon under varying light conditions Sun, Angela; Hasan, Mafruha Tasnin; Hobba, Graham Journal of Phycology, Vol. 54, Issue 4 https://doi.org/10.1111/jpy.12758	journal	July 2018
Accumulation of Trehalose as a Compatible Solute under Osmotic Stress in Euglena gracilis Z Takenaka, Shigeo; Kondo, Tomohiro; Nazeri, Sonbol Journal of Eukaryotic Microbiology, Vol. 44, Issue 6 https://doi.org/10.1111/j.1550-7408.1997.tb05967.x	journal	November 1997
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence Genty, Bernard; Briantais, Jean-Marie; Baker, Neil R. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 990, Issue 1 https://doi.org/10.1016/S0304-4165(89)80016-9	journal	January 1989
Enrichment of the Light-Harvesting Complex in Diadinoxanthin and Implications for the Nonphotochemical Fluorescence Quenching in Diatoms Lavaud, Johann; Rousseau, Bernard; Etienne, Anne-Lise Biochemistry, Vol. 42, Issue 19 https://doi.org/10.1021/bi027112i	journal	April 2003
The Effects of Salt Stress on Photosynthetic Electron Transport and Thylakoid Membrane Proteins in the Cyanobacterium Spirulina platensis Sudhir, Putty-Reddy; Pogoryelov, Denys; Kovacs, Laszlo BMB Reports, Vol. 38, Issue 4 https://doi.org/10.5483/BMBRep.2005.38.4.481	journal	July 2005

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59 BASIC BIOLOGICAL SCIENCES
salt stress
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paramylon
microalgae
photosynthesis

Title: Salt Stress Induces Paramylon Accumulation and Fine-Tuning of the Macro-Organization of Thylakoid Membranes in Euglena gracilis Cells

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