SpringerLink
Log in

Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes

  • Published:
Photosynthetica

Abstract

The principal function of the thylakoid membrane depends on the integrity of the lipid bilayer, yet almost half of the thylakoid lipids are of non-bilayer-forming type, whose exact functions are not fully understood. Non-bilayer lipids can be extruded from the membrane in the presence of high concentrations of co-solutes. We applied 2 M sucrose to induce lipid phase separation in isolated thylakoid membranes, following consequent structural and physiological effects. Circular dichroism spectroscopy indicated significant changes in the chiral macro-arrangement of the pigment–protein complexes, which were reversed after washing out the co-solute. Similarly, merocyanine-540 fluorescence suggested reversible changes in the lipid phases. The PSII function, as tested by chlorophyll fluorescence induction transients and time-resolved fluorescence, was almost unaffected. However, the presence of sucrose dramatically increased the PSII thermostability, which can partly be explained by a direct osmolyte effect and partly by the lipid phase separation stabilizing the stacked membrane.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CD:

circular dichroism

Chl:

chlorophyll

DAES:

decay-associated emission spectra

DGDG:

digalactosyldiacylglycerol

IRF:

instrument response function

MC540:

merocyanine-540

MGDG:

monogalactosyl-diacylglycerol

PG:

phosphatidylglycerol

psi:

polymer and salt induced

SQDG:

sulfoquinosyl-diacylglycerol

TCSPC:

time-correlated single-photon counting

References

  • Akhtar P., Lingvay M., Kiss T. et al.: Excitation energy transfer between light-harvesting complex II and photosystem I in reconstituted membranes.–Biochim. Biophys. Acta 1857: 462–472, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Barzda V., Istokovics A., Simidjiev I., Garab G.: Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment-protein complexes. Light-induced reversible structural changes associated with energy dissipation.–Biochemistry 35: 8981–8985, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Bernik D., Tymczyszyn E., Daraio M.E., Negri R.M.: Fluorescent dimers of merocyanine 540 (MC540) in the gel phase of phosphatidylcholine liposomes.–Photochem. Photobiol. 70: 40–48, 1999.

    Article  CAS  Google Scholar 

  • Broess K., Trinkunas G., van Hoek A. et al.: Determination of the excitation migration time in Photosystem II consequences for the membrane organization and charge separation parameters.–Biochim. Biophys. Acta 1777: 404–409, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Cseh Z., Rajagopal S., Tsonev T. et al.: Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity.–Biochemistry 39: 15250–15257, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Demé B., Cataye C., Block M.A. et al.: Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids.–FASEB J. 28: 3373–3383, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Douce R., Joyard J.: Biosynthesis of thylakoid membrane lipids.–In: Ort D.R., Yocum C.F. (ed.): Oxygenic Photosynthesis: The Light Reactions. Pp. 69–101. Kluwer Academic Publishers, Dordrecht 1996.

    Google Scholar 

  • Garab G., Faludi-Daniel A., Sutherland J.C., Hind G.: Macroorganization of chlorophyll a/b light-harvesting complex in thylakoids and aggregates - information from circular differential scattering.–Biochemistry 27: 2425–2430, 1988a.

    Article  CAS  Google Scholar 

  • Garab G., Kieleczawa J., Sutherland J.C. et al: Organization of pigment protein complexes into macrodomains in the thylakoid membranes of wild-type and chlorophyll-b-less mutant of barley as revealed by circular-dichroism.–Photochem. Photobiol. 54: 273–281, 1991.

    Article  CAS  Google Scholar 

  • Garab G., Lohner K., Laggner P., Farkas T.: Self-regulation of the lipid content of membranes by non-bilayer lipids: a hypothesis.–Trends Plant Sci. 5: 489–494, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Garab G., Ughy B., Goss R.: Role of MGDG and non-bilayer lipid phases in the structure and dynamics of chloroplast thylakoid membranes.–In: Nakamura Y., Li-Beisson Y. (ed.): Lipids in Plant and Algae Development. Pp. 127–157. Springer, Dordrecht 2016.

    Chapter  Google Scholar 

  • Garab G., Ughy B., Waard P. et al.: Lipid polymorphism in chloroplast thylakoid membranes-as revealed by (31) P-NMR and time-resolved merocyanine fluorescence spectroscopy.–Sci. Rep. 7: 13343, 2017.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garab G., van Amerongen H.: Linear dichroism and circular dichroism in photosynthesis research.–Photosynth. Res. 101: 135–146, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garab G., Wells S., Finzi L., Bustamante C.: Helically organized macroaggregates of pigment protein complexes in chloroplasts - evidence from circular intensity differential scattering.–Biochemistry 27: 5839–5843, 1988b.

    Article  PubMed  CAS  Google Scholar 

  • Goltsev V., Yordanov I., Tsonev T.: Evaluation of relative contribution of initial and variable chlorophyll fluorescence measured at different temperatures.–Photosynthetica 30: 629–643, 1994.

    CAS  Google Scholar 

  • Goss R., Lohr M., Latowski D. et al.: Role of hexagonal structure-forming lipids in diadinoxanthin and violaxanthin solubilization and de-epoxidation.–Biochemistry 44: 4028–4036, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Goss R., Oroszi S., Wilhelm C.: The importance of grana stacking for xanthophyll cycle-dependent NPQ in the thylakoid membranes of higher plants.–Physiol. Plantarum 131: 496–507, 2007.

    Article  CAS  Google Scholar 

  • Holzwarth A.R., Miloslavina Y., Nilkens M., Jahns P.: Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence.–Chem. Phys. Lett. 483: 262–267, 2009.

    Article  CAS  Google Scholar 

  • Jahns P., Latowski D., Strzalka K.: Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids.–BBA-Bioenergetics 1787: 3–14, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Janik E., Bednarska J., Zubik M. et al.: Molecular architecture of plant thylakoids under physiological and light stress conditions: A study of lipid-light-harvesting complex II model membranes.–Plant Cell 25: 2155–2170, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kirchhoff H., Haase W., Wegner S. et al.: Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplast.–Biochemistry 46: 11169–11176, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Kouřil R., Lazár D., Ilík P. et al.: High-temperature induced chlorophyll fluorescence rise in plants at 40–50 °C: Experimental and theoretical approach.–Photosynth. Res. 81: 49–66, 2004.

    Article  PubMed  Google Scholar 

  • Kovács L., Damkjaer J., Kereïche S. et al.: Lack of the lightharvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts.–Plant Cell 18: 3106–3120, 2006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kowalewska L., Mazur R., Suski S. et al.: Three-dimensional visualization of the internal plastid membrane network during runner bean chloroplast biogenesis. Dynamic model of the tubular-lamellar transformation.–Plant Cell 28: 875–891, 2016.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Krishna M., Periasamy N.: Fluorescence of organic dyes in lipid membranes: site of solubilization and effects of viscosity and refractive index on lifetimes.–J. Fluoresc. 8: 81–91, 1998.

    Article  CAS  Google Scholar 

  • Krumova S.B., Dijkema C., de Waard P. et al.: Phase behavior of phosphatidylglycerol in spinach thylakoid membranes as revealed by 31P-NMR.–BBA-Biomembranes 1778: 997–1003, 2008a.

    Article  PubMed  CAS  Google Scholar 

  • Krumova S.B., Koehorst R.B.M., Bóta A. et al.: Temperature dependence of the lipid packing in thylakoid membranes studied by time- and spectrally resolved fluorescence of Merocyanine.–Biochim. Biophys. Acta 1778: 2823–2833, 2008b.

    Article  PubMed  CAS  Google Scholar 

  • Krumova S.B., Laptenok S.P., Kovács L. et al.: Digalactosyldiacylglycerol- deficiency lowers the thermal stability of thylakoid membranes.–Photosynth. Res. 105: 229–242, 2010.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Langner M., Hui S.W.: Merocyanine 540 as a fluorescence indicator for molecular packing stress at the onset of lamellarhexagonal transition of phosphatidylethanolamine bilayers.–Biochim. Biophys. Acta 1415: 323–330, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Latowski D., Akerlund H.E., Strzałka K.: Violaxanthin deepoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity.–Biochemistry 43: 4417–4420, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Miloslavina Y., Wehner A., Lambrev P.H. et al.: Far-red fluorescence: A direct spectroscopic marker for LHCII oligomers forming in non-photochemical quenching.–FEBS Lett. 582: 3625–3631, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Mitchell P.: Chemiosmotic coupling in oxidative and photosynthetic phosphorylation.–Biol. Rev. Camb. Philos. 41: 445–501, 1966.

    Article  CAS  Google Scholar 

  • Nagy G., Szabó M., Ünnep R. et al.: 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.–Photosynth. Res. 111: 71–79, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Nagy G., Ünnep R., Zsiros O. et al.: Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo.–P. Natl. Acad. Sci. USA 111: 5042–5047, 2014.

    Article  CAS  Google Scholar 

  • Pal S.K., Sukul D., Mandal D., Bhattacharyya K.: Solvation dynamics of DCM in lipid.–J. Phys. Chem. B 104: 4529–4531, 2000.

    Article  CAS  Google Scholar 

  • Páli T., Garab G., Horváth L.I., Kóta Z.: Functional significance of the lipid-protein interface in photosynthetic membranes.–Cell Mol. Life Sci. 60: 1591–1606, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Posselt D., Nagy G., Kirkensgaard J.J. et al.: Small-angle neutron scattering study of the ultrastructure of chloroplast thylakoid membranes–periodicity and structural flexibility of the stroma lamellae.–Biochim. Biophys. Acta 1817: 1220–1228, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Pueyo J.J., Alfonso M., Andrés C., Picorel R.: Increased tolerance to thermal inactivation of oxygen evolution in spinach Photosystem II membranes by substitution of the extrinsic 33-kDa protein by its homologue from a thermophilic cyanobacterium.–Biochim. Biophys. Acta 1554: 29–35, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Roelofs T.A., Lee C.-H., Holzwarth A.R.: Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts. A new approach to the characterization of the primary processes in photosystem II α- and β-units.–Biophys. J. 61: 1147–1163, 1992.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simidjiev I., Barzda V., Mustárdy L., Garab G.: Role of thylakoid lipids in the structural flexibility of lamellar aggregates of the isolated light-harvesting chlorophyll a/b complex of photosystem II.–Biochemistry 37: 4169–4173, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Simidjiev I., Stoylova S., Amenitsch H. et al.: Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro.–P. Natl. Acad. Sci. USA 97: 1473–1476, 2000.

    Article  CAS  Google Scholar 

  • Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient.–J. Photoch. Photobio. B 104: 236–257, 2011.

    Article  CAS  Google Scholar 

  • Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient.–In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 463–495. Springer, Dordrecht 2004.

    Google Scholar 

  • Stratt R.M., Maroncelli M.: Nonreactive dynamics in solution: The emerging molecular view of solvation dynamics and vibrational relaxation.–J. Phys. Chem. 100: 12981–12996, 1996.

    Article  CAS  Google Scholar 

  • Tóth T.N., Rai N., Solymosi K. et al.: Fingerprinting the macroorganisation of pigment-protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy.–BBA-Bioenergetics 1857: 1479–1489, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Tsvetkova N.M., Apostolova E.L., Brain A.P. et al.: Factors influencing PSII particle array formation in Arabidopsis thaliana chloroplasts and the relationship of such arrays to the thermostability of PS II.–BBA-Bioenergetics 1228: 201–210, 1995.

    Article  Google Scholar 

  • Ünnep R., Zsiros O., Solymosi K. et al.: The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering.–BBA-Bioenergetics 1837: 1572–1580, 2014.

    Article  PubMed  CAS  Google Scholar 

  • van der Weij-de Wit C.D., Ihalainen J.A., van Grondelle R., Dekker J.P.: Excitation energy transfer in native and unstacked thylakoid membranes studied by low temperature and ultrafast fluorescence spectroscopy.–Photosynth. Res. 93: 173–182, 2007.

    Article  PubMed  CAS  Google Scholar 

  • van Eerden F.J., de Jong D.H., de Vries A.H. et al.: Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations.–Biochim. Biophys. Acta 1848: 1319–1330, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Williams W., Brain A., Dominy P.: Induction of non-bilayer lipid phase separations in chloroplast thylakoid membranes by compatible co-solutes and its relation to therthermal stability of Photosystem II.–BBA-Bioenergetics 1099: 137–144, 1992.

    Article  CAS  Google Scholar 

  • Williams W., Gounaris K.: Stabilisation of PS-II-mediated electron transport in oxygen-evolving PS II core preparations by the addition of compatible co-solutes.–Biochim. Biophys. Acta 1100: 92–97, 1992.

    Article  PubMed  CAS  Google Scholar 

  • Williams W.P.: The physical properties of thylakoid membrane lipids and their relation to photosynthesis.–In: Siegenthaler P.-A., Murata N. (ed.): Lipids in Photosynthesis: Structure, Function and Genetics. Pp. 103–118. Springer, Dordrecht 1998.

    Google Scholar 

  • Yamamoto H.Y., Higashi R.: Violaxanthin de-epoxidase: lipid composition and substrate specificity.–Arch. Biochem. Biophys. 190: 514–522, 1978.

    Article  PubMed  CAS  Google Scholar 

  • Yancey P.H.: Compatible and counteracting solutes.–In: Strange K. (ed.): Cellular and Molecular Physiology of Cell Volume Regulation. Pp. 81–109. CRC Press, Boca Raton 1994.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Plant Biology, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, H-6726, Szeged, Hungary

    C. Kotakis, P. Akhtar, O. Zsiros, G. Garab & P. H. Lambrev

  2. Doctoral School in Biology, Faculty of Science and Informatics, University of Szeged, Aradi vértanúk tere 1, H-6720, Szeged, Hungary

    P. Akhtar

  3. Department of Physics, Faculty of Science, University of Ostrava, Chittussiho 10, CZ-710 00, Ostrava, Czech Republic

    G. Garab

Authors
  1. C. Kotakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Zsiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Garab
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. H. Lambrev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. H. Lambrev.

Additional information

Acknowledgements: This work benefitted of grants from the Hungarian Ministry for National Economy (GINOP-2.3.2-15-2016-00001 and GINOP-2.3.2-15-2016-00058) and the National Research Development and Innovation Office of Hungary (OTKA K 112688 to G.G.). C.K. was supported by a postdoctoral fellowship from the Hungarian Academy of Sciences. G.G. acknowledges partial support from Moravian-Silesian Region (Project 01211/2016/RRC).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kotakis, C., Akhtar, P., Zsiros, O. et al. Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes. Photosynthetica 56, 254–264 (2018). https://doi.org/10.1007/s11099-018-0782-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-018-0782-z

Additional key words

Search

Navigation