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Self-assembly and structural–functional flexibility of oxygenic photosynthetic machineries: personal perspectives

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Abstract

This short review, with a bit of historical aspect and a strong personal bias and emphases on open questions, is focusing on the (macro-)organization and structural–functional flexibilities of the photosynthetic apparatus of oxygenic photosynthetic organisms at different levels of the structural complexity—selected problems that have attracted most my attention in the past years and decades. These include (i) the anisotropic organization of the pigment–protein complexes and photosynthetic membranes—a basic organizing principle of living matter, which can, and probably should be adopted to intelligent materials; (ii) the organization of protein complexes into chiral macrodomains, large self-assembling highly organized but structurally flexible entities with unique spectroscopic fingerprints—structures, where, important, high-level regulatory functions appear to 'reside’; (iii) a novel, dissipation-assisted mechanism of structural changes, based on a thermo-optic effect: ultrafast thermal transients in the close vicinity of dissipation of unused excitation energy, which is capable of inducing elementary structural changes; it makes plants capable of responding to excess excitation with reaction rates proportional to the overexcitation above the light-saturation of photosynthesis; (iv) the 3D ultrastructure of the granum-stroma thylakoid membrane assembly and other multilamellar membrane systems, and their remodelings—associated with regulatory mechanisms; (v) the molecular organization and structural–functional plasticity of the main light-harvesting complex of plants, in relation to their crystal structure and different in vivo and in vitro states; and (vi) the enigmatic role of non-bilayer lipids and lipid phases in the bilayer thylakoid membrane—warranting its high protein content and contributing to its structural flexibility.

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Abbreviations

Chl:

Chlorophyll

CD:

Circular dichroism

DGDG:

Digalactosyl-diacylglycerol

LD:

Linear dichroism

LHCI:

Light-harvesting antenna complex of photosystem I

LHCII:

Light-harvesting protein complex II

MCD:

Magnetic circular dichroism

MGDG:

Monogalactosyl-diacylglycerol

PSI or II:

Photosystem I or II

psi:

Polymer and salt-induced

References

  • Abdourakhmanov I, Chugunov V, Erokhin YE, Ganago AO, Solovev A (1979) Orientation and linear dichroism of the reaction centers from Rhodopseudomonas sphaeroides R-26. Biochim Biophys Acta 546:183–186

    Article  CAS  PubMed  Google Scholar 

  • Akhtar P, Bóta A, Dorogi M, Garab G, Kiss T, Kovács L, Lambrev PH, Pawlak K (2015) Pigment interactions in light-harvesting complex II in different molecular environments. J Biol Chem 290:4877–4886

    Article  CAS  PubMed  Google Scholar 

  • Andersson B, Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427–440

    Article  CAS  PubMed  Google Scholar 

  • Arntzen CJ (1978) Dynamic structural features of chloroplast lamellae. In: Sanadi DR, Vernon LP (eds) Current topics in bioenergetics, vol 8. Academic Press, New York, pp 111–160

    Google Scholar 

  • Arteni AA, Aartsma TJ, Boekema EJ, Liu LN, Zhang YZ, Zhou BC (2008) Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth Res 95:169–174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Austin JR, Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol 155:1601–1611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barber J (1982) Influence of surface charges on thylakoid structure and function. Annu Rev Plant Physiol 33:261–295

    Article  CAS  Google Scholar 

  • Barzda V, Garab G, Mustárdy L (1994) Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. Biochemistry 33:10837–10841

    Article  CAS  PubMed  Google Scholar 

  • Barzda V, Garab G, Istokovics A, Sidimidjiev I (1996) 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

    Article  CAS  PubMed  Google Scholar 

  • Boca S, Chevalier A, Fekete A, Havaux M, Koestler F, Ksas B, Leymarie J, Mueller MJ (2013) Arabidopsis lipocalins AtCHL and AtTIL have distinct but overlapping functions essential for lipid protection and seed longevity. Plant, Cell Environ 37:368–381

    Article  CAS  Google Scholar 

  • Brangeon J, Mustárdy L (1979) The ontogenetic assembly of intra-chloroplastic lamellae viewed in 3-dimension. Biol Cell 36:71–80

    Google Scholar 

  • Breton J, Verméglio A (1982) Orientation of photosynthetic pigments in vivo. In: Govindjee (ed) Photosynthesis. Academic Press, New York, pp 153–193

    Chapter  Google Scholar 

  • Brown MF (2012) Curvature forces in membrane lipid–protein interactions. Biochemistry 51:9782–9795

    Article  CAS  PubMed  Google Scholar 

  • Büchel C, Garab G (1997) Organization of the pigment molecules in the chlorophyll a/c light-harvesting complex of Pleurochloris meiringensis (Xanthophyceae). Characterization with circular dichroism and absorbance spectroscopy. J Photochem Photobiol, B 37:118–124

    Article  Google Scholar 

  • Bustamante C, Maestre MF, Keller D (1985) Expressions for the interpretation of circular intensity differential scattering of circular aggregates. Biopolymers 24:1595–1612

    Article  CAS  PubMed  Google Scholar 

  • Chappaz-Gillot C, Balaban TS, Blaive BJ, Bürck J, Canard G, Garab G, Hahn H, Jávorfi T, Kelemen L, Krupke R, Marek PL, Mössinger D, Ormos P, Reddy CM, Roussel C, Steinbach G, Szabó M, Ulrich AS, Vanthuyne N, Vijayaraghavan A, Zupcanova A (2011) Anisotropic organization and microscopic manipulation of selfassembling synthetic porphyrin microrods that mimic chlorosomes: bacterial light-harvesting systems. J Am Chem Soc 134:944–954

    Article  PubMed  CAS  Google Scholar 

  • Charuvi D, Adam Z, Farrant JM, Kirchhoff H, Naveh L, Nevo R, Shimoni E, Zia A, Reich Z (2015) Photoprotection conferred by changes in photosynthetic protein levels and organization during dehydration of a homoiochlorophyllous resurrection plant. Plant Physiol 167:1554–1565

    Article  CAS  PubMed  Google Scholar 

  • Chuartzman SG, Brumfeld V, Charuvi D, Kiss Nevo R, Ohad I, Reich Z, Shimoni EV (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20:1029–1039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cseh Z, Busheva M, Garab G, Papp E, Rajagopal S, Tsonev T (2000) Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry 39:15250–15257

    Article  CAS  PubMed  Google Scholar 

  • Cseh Z, Barzda V, Garab G, Jennings R, Kovács L, Krumova S, Papp E, Rajagopal S, Vianelli A (2005) Thermo-optically induced reorganizations in the main light harvesting antenna of plants. I. Non-Arrhenius type of temperature dependence and linear light-intensity dependencies. Photosynth Res 86:263–273

    Article  CAS  PubMed  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1707:12–39

    Article  CAS  Google Scholar 

  • Demé B, Block MA, Cataye C, Jouhet J, Maréchal E (2014) Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J 28:3373–3383

    Article  PubMed  CAS  Google Scholar 

  • Demeter S, Machowicz E, Mustárdy L (1976) The development of the intense circular-dichroic signal during granum formation in greening etiolated maize. Biochem J 156:469–472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams W, Garab G, Govindjee (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Berlin

    Google Scholar 

  • den Brink-van Van, der Laan E, Killian JA, de Kruijff B (2004) Non-bilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim Biophys Acta 1666:275–288

    Article  CAS  Google Scholar 

  • Dobrikova AG, Busheva MC, GarabG Krumova SB, Kovács L, Kostov GK, Todinova SJ, Taneva SG, Várkonyi Z (2003) Structural rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect. Biochemistry 42:11272–11280

    Article  CAS  PubMed  Google Scholar 

  • Enriquez MM, Akhtar P, Garab G, Lambrev PH, Tan H-S, Zhang C (2015) Energy transfer dynamics in trimers and aggregates of light-harvesting complex II probed by 2D electronic spectroscopy. J Chem Phys 142:212432

    Article  PubMed  CAS  Google Scholar 

  • Faludi-Dániel Á, Mustárdy L (1983) Organization of chlorophyll a in the light-harvesting chlorophyll a/b protein complex as shown by circular dichroism. Liquid crystal like domains. Plant Physiol 73:16–19

    Article  PubMed Central  PubMed  Google Scholar 

  • Faludi-Dániel Á, Demeter S, Garay AS (1973) Circular dichroism spectra of granal and agranal chloroplasts of maize. Plant Physiol 52:54–56

    Article  PubMed Central  PubMed  Google Scholar 

  • Faludi-Dániel Á, Bialek GE, Gregory RP, Horváth G, Rózsa Z (1978) Differential light-scattering of granal and agranal chloroplasts and their fragments. Biochem J 174:647–651

    Article  PubMed Central  PubMed  Google Scholar 

  • Faludi-Dániel Á, Demeter S, Garab G (1981) Organization of pigments in the light-harvesting and antenna complex of chloroplasts. Acta Biol Acad Sci Hung 32:247–258

    Google Scholar 

  • Faludi-Dániel Á, Mustárdy LA, Shubin VV, Sobhi MA (1984) Organization of the light-harvesting chlorophyll-protein complex (LHCP) as shown by difference circular dichroism (dCD) during greening, under light and stepwise degradation. In: Sybesma C (ed) Advances in photosynthesis research, vol 4. Martinus Nijhoff/Dr W Junk, The Hague, pp 733–736

    Chapter  Google Scholar 

  • Finzi L, Bustamante C, Garab G, Juang C-B (1989) Direct observation of large chiral domains in chloroplast thylakoid membranes by differential polarization microscopy. Proc Natl Acad Sci USA 86:8748–8752

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ganago AO, Fock M (1981) Direct and reverse problems in linear dichroism studies. Spectrosc Lett 14:405–414

    Article  CAS  Google Scholar 

  • Garab G (1996) Linear and circular dichroism. In: Amesz J, Hoff AJ (eds) Biophysical techniques in photosynthesis. Advances in photosynthesis, vol 3. Kluwer, Dordrecht, pp 11–40

    Chapter  Google Scholar 

  • Garab G (2014a) Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta 1837:481–494

    Article  CAS  PubMed  Google Scholar 

  • Garab G (2014b) Structural changes and non-photochemical quenching of chlorophyll a fluorescence in oxygenic photosynthetic organisms. In: Demmig-Adams B, Garab G, Adams W, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Berlin, pp 343–371

    Google Scholar 

  • Garab G, Breton J (1976) Polarized light spectroscopy on oriented spinach chloroplasts. Fluorescence emission at low temperature. Biochem Biophys Res Comm 71:1095–1102

    Article  CAS  PubMed  Google Scholar 

  • Garab G, Mustárdy L (1999) Role of LHCII-containing macrodomains in the structure, function and dynamics of grana. Aust J Plant Physiol 26:649–658

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garab G, Faludi-Dániel Á, Hind G, Sutherland JC (1988a) Macroorganizarion of chlorophyll a/b light-harvesting complex in thylakoids and aggregates. Information from circular differential scattering. Biochemistry 27:2425–2430

    Article  CAS  Google Scholar 

  • Garab G, Hind G, Leegood RC, Sutherland JC, Walker DA (1988b) Reversible changes in macroorganization of the light-harvesting chlorophyll a/b pigment-protein complex detected by circular dichroism. Biochemistry 27:2430–2434

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Garab G, Bustamante C, Hind G, Kieleczawa J, Surherland JC (1991) 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

    Article  CAS  Google Scholar 

  • Garab G, Butiuc A, Dér A, Istokovics A, Simidjiev I (1998) Light-induced ion movements in thylakoid membranes and isolated LHCII. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol I. Kluwer, Dordrecht, pp 341–344

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Garab G, Cseh Z, Dér A, Holzenburg A, Horton P, Kovács L, Mustárdy L, Papp E, Rajagopal S, Ruban AV, Várkonyi Z, Wentworth M (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41:15121–15129

    Article  CAS  PubMed  Google Scholar 

  • Goss R, Garab G, Wilhelm C (2000) Organization of the pigment molecules in the chlorophyll a/b/c-containing alga Mantoniella squamata (Prasinophyceae). Studies by means of absorption, circular and linear dichroism spectroscopy. Biochim Biophys Acta 1457:190–199

    Article  CAS  PubMed  Google Scholar 

  • Goss R, Lohr M, Latowski D, Grzyb J, Vieler A, Wilhelm C, Strzalka K (2005) Role of hexagonal structure-forming lipids in diadinoxanthin and violaxanthin solubilization and de-epoxidation. Biochemistry 44:4028–4036

    Article  CAS  PubMed  Google Scholar 

  • Goss R, Grzyb J, Latowski D, Lohr M, Strzalka K, Vieler A, Wilhelm C (2007) Lipid dependence of diadinoxanthin solubilization and de-epoxidation in artificial membrane systems resembling the lipid composition of the natural thylakoid membrane. Biochim Biophys Acta 1768:67–75

    Article  CAS  PubMed  Google Scholar 

  • Gregory RPF (1975) Evidence that circularly dichroic chlorophyll forms a-682 and a-710 are oriented at right angles to the thylakoid membranes of whole chloroplasts, and that the circular dichroism is light-dependent. Biochem J 148:487–497

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gregory RPF, Demeter S, Faludi-Dániel Á (1980) Macromolecular organization of chlorophyll a in aggregated chlorophyll a/b protein complex as shown by circular dichroism at room and cryogenic temperatures. Biochim Biophys Acta 591:356–360

    Article  CAS  PubMed  Google Scholar 

  • Gulbinas V, Garab G, Karpicz R, Valkunas L (2006) Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochemistry 45:9559–9565

    Article  CAS  PubMed  Google Scholar 

  • Gussakovsky EE, Barzda V, Garab G, Shahak Y (1997) Irreversible disassembly of chiral macrodomains in thylakoids due to photoinhibition. Photosynth Res 51:119–126

    Article  CAS  Google Scholar 

  • Gussakovsky EE, Barzda V, Shahak Y, van Amerongen H (2000) Circular polarized chlorophyll luminescence reflects the macroorganization of grana in pea chloroplasts. Photosynth Res 65:83–92

    Article  CAS  PubMed  Google Scholar 

  • Hakala M, Keränen M, Tuominen I, Tyystjärvi E, Tyystjärvi T (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta 1706:68–80

    Article  CAS  PubMed  Google Scholar 

  • Haranczyk H, Blicharski JS, Dietrich W, Strzalka K (1995) 31P-NMR observation of the temperature and glycerol induced non-lamellar phase-formation in wheat thylakoid membranes. J Biol Phys 21:125–139

    Article  CAS  Google Scholar 

  • Hind G, Izawa S, Nakatani HY (1974) Light-dependent redistribution of ions in suspensions of chloroplast thylakoid membranes. Proc Natl Acad Sci USA 71:1484–1488

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hind G, Garab G, Istokovics A, Lambrev PG, Várkonyi Z, Wall JS (2014) Membrane crystals of plant light-harvesting complex II disassemble reversibly in light. Plant Cell Physiol 55:1296–1303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Istokovics A, Garab G, Lajkó F, Simidjiev I (1997) Characterization of the light-induced reversible changes in the chiral macroorganization of the chromophores in chloroplast thylakoid membranes. Temperature dependence and effect of inhibitors. Photosynth Res 54:45–53

    Article  CAS  Google Scholar 

  • Iwai M, Minagawa J, Takahashi Y (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20:2177–2189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwai M, Nakano A, Yokono M (2014) Visualizing structural dynamics of thylakoid membranes. Sci Rep 4:3768

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Janik E, Bednarska J, Zubik M, Puzio M, Luchowski R, Grudzinski W, Mazur R, Garstka M, Maksymiec W, Kulik A, Dietler G, Gruszecki WI (2013) 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Johnson MP, Brain AP, Duffy CD, Goral TK, Mullineaux CW, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Junge W (1977) Membrane potentials in photosynthesis. Ann Rev Plant Physiol 28:503–536

    Article  CAS  Google Scholar 

  • Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Ünnep R, Zsiros O, Nagy G, Garab G, Aronsson H, Versaw WK, Spetea C (2015) The Arabidopsis thylakoid transporter PHT4; 1 influences phosphate availability for ATP synthesis and plant growth. Plant J. doi:10.1111/tpj.12962

    Google Scholar 

  • Keller D, Buslamante C (1986) Theory of the interaction of light with large inhomogeneous molecular aggregates. I. Absorption. J Chem Phys 84:2961–2971

    Article  CAS  Google Scholar 

  • Keller D, Bustamante C (1986) Theory of the interaction of light with large inhomogeneous molecular aggregates. II. Psi-type circular dichroism. J Chem Phys 84:2972–2979

    Article  CAS  Google Scholar 

  • Kim M, Bustamante C (1991) Differential polarization imaging. Images in higher Born approximations. Biophys J 59:1171–1182

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim M, Bustamante C, Keller D, Maestre MF, Ulibarri L (1986) The psi-type circular dichroism of large molecular aggregates. III. Calculations. J Chem Phys 84:2981–2989

    Article  CAS  Google Scholar 

  • Kirchhoff H, Charuvi D, Hall C, Herbstová M, Nevo R, Reich Z, Shimoni E, Tsabari O, Wood M (2011) Dynamic control of protein diffusion within the granal thylakoid lumen. Proc Natl Acad Sci USA 108:20248–20253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kirchhoff H, Edwards GE, Herbstova M, Sharpe RM, Yarbrough R (2013) Differential mobility of pigment-protein complexes in granal and agranal thylakoid membranes of C-3 and C-4 plants. Plant Physiol 161:497–507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kiss JG, Faludi-Dániel Á, Garab G, Tóth Z (1986) The light-harvesting chlorophyll a/b protein acts as a torque aligning chloroplasts in a magnetic field. Photosynth Res 10:217–222

    Article  CAS  PubMed  Google Scholar 

  • Knox PP, Faludi-Dániel Á, Garab G, Kononenko AA, Venediktov PS (1984) Role of electric polarization in the thermoluminescence of chloroplasts. Photochem Photobiol 40:119–125

    Article  CAS  Google Scholar 

  • Kouřil R, Boekema EJ, Bultema JB, Croce R, Wientjes E (2013) High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta 1827:411–419

    Article  PubMed  CAS  Google Scholar 

  • Kovács L, Boekema EJ, Damkjaer J, Ilioaia C, Jansson S, Horton P, Kereiche S, Ruban AV (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Krüger TPJ, Croce R, van Grondelle R, Wientjes E (2011) Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA 108:13516–13521

    Article  PubMed Central  PubMed  Google Scholar 

  • Krumova SB, Dijkema C, de Waard P, van As H, Garab G, van Amerongen H (2008a) Phase behaviour of phosphatidylglycerol in spinach thylakoid membranes as revealed by P-31-NMR. Biochim Biophys Acta 1778:997–1003

    Article  CAS  PubMed  Google Scholar 

  • Krumova SB, Koehorst RBM, Bota A, Páli T, van Hoek A, Garab G, van Amerongen H (2008b) Temperature dependence of the lipid packing in thylakoid membranes studied by time- and spectrally resolved fluorescence of Merocyanine 540. Biochim Biophys Acta 1778:2823–2833

    Article  CAS  PubMed  Google Scholar 

  • Krumova SB, Laptenok SP, Kovács L, Tóth T, van Hoek A, Garab G, van Amerongen H (2010) Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Photosynth Res 105:229–242

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krumova SB, Busheva MC, Garab G, Kovács L, Lambrev PH, Todinova SJ, Taneva SG, Várkonyi Z (2014) Heat- and light-induced detachment of the light-harvesting antenna complexes of photosystem I in isolated stroma thylakoid membranes. J Photochem Photobiol 137:4–12

    Article  CAS  Google Scholar 

  • Lambrev PH, Garab G, Holzwarth AR, Kovács L, Krumova S, Miloslavina Y, Várkonyi Z (2007) Importance of trimer-trimer interactions for the native state of the plant light-harvesting complex II. Biochim Biophys Acta 1764:847–853

    Article  CAS  Google Scholar 

  • Lambrev PH, Fiedor J, Fiedor L, Garab G, van Grondelle R, Groot ML, Huhn G, Miloslavina Y, Michalik M, Stahl AD, van Stokkum IHM, Susz A, Tworzydło J (2013) Excitation energy trapping and dissipation by Ni-substituted bacteriochlorophyll a in reconstituted LH1 complexes from Rhodospirillum rubrum. J Phys Chem B 117:11260–11271

    Article  CAS  PubMed  Google Scholar 

  • Latowski D, Akerlund HE, Strzalka K (2004) Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 43:4417–4420

    Article  CAS  PubMed  Google Scholar 

  • Liberton M, Mamontov E, O’Neill H, O’Dell WB, Page LE, Pakrasi HB, Urban VS (2013) Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. J Biol Chem 288:3632–3640

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu ZF, An XM, Chang WR, Gui LL, Kuang TY, Yan HC, Wang KB, Zhang JP (2004) Crystal structure of spinach major light-harvesting complex at 2.72 ångstrom resolution. Nature 428:287–292

    Article  CAS  PubMed  Google Scholar 

  • Miloslavina Y, Wehner A, Wientjes E, Reus M, Lambrev P, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomers forming in non-photochemical quenching. FEBS Lett 582:3625–3631

    Article  CAS  PubMed  Google Scholar 

  • Miloslavina Y, Garab G, Hind G, Jávorfi T, Karlicky V, Lambrev PH, Várkonyi Z, Wall JS (2012) Anisotropic circular dichroism signatures of oriented thylakoid membranes and lamellar aggregates of LHCII. Photosynth Res 111:29–39

    Article  CAS  PubMed  Google Scholar 

  • Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148

    Article  CAS  PubMed  Google Scholar 

  • Murakami S, Packer L (1970) Protonation and chloroplast membrane structure. J Cell Biol 47:332–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mustárdy L, Garab G (2003) Granum revisited. A three-dimensional model: where things fall into place. Trends Plant Sci 8:117–122

    Article  PubMed  CAS  Google Scholar 

  • Mustárdy L, Buttle K, Garab G, Steinbach G (2008) The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant Cell 20:2552–2557

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nagy G (2012) Structure and dynamics of photosynthetic membranes as revealed by Neutron Scattering. PhD Thesis. Université de Grenoble, Eötvös University, Grenoble, Budapest

  • Nagy L, Maróti P, Terazima M (2008) Spectrally silent light induced conformation change in photosynthetic reaction centers. FEBS Lett 582:3657–3662

    Article  CAS  PubMed  Google Scholar 

  • Nagy G, Posselt D, Kovács L, Holm JK, Szabó M, Ughy B, Rosta L, Peters J, Timmins P, Garab G (2011) Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering. Biochem J 436:225–230

    Article  CAS  PubMed  Google Scholar 

  • Nagy G, Szabó M, Ünnep R, Káli G, Miloslavina Y, Lambrev PH, Zsiros O, Porcar L, Timmins P, Rosta L, Garab G (2012) 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

    Article  CAS  PubMed  Google Scholar 

  • Nagy G, Kovács L, Ünnep R, Zsiros O, Almásy L, Rosta L, Timmins P, Peters J, Posselt D, Garab G (2013) Kinetics of structural reorganizations in multilamellar photosynthetic membranes monitored by small angle neutron scattering. Eur Phys J E 36:69

    Article  PubMed  CAS  Google Scholar 

  • Nagy G, Garab G, Pieper J (2014a) Neutron scattering in photosynthesis research. In: Allakhverdiev SI, Rubin AB, Shuvalov VA (eds) Contemporary problems of photosynthesis, vol 1. Izhevsk Institute of Computer Science, Moscow, pp 69–121

    Google Scholar 

  • Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G, Minagawa J (2014b) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proc Natl Acad Sci USA 111:5042–5047

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Naqvi KR, Jávorfi T, Melo TB, Garab G (1999) More on the catalysis of internal conversion in chlorophyll a by an adjacent carotenoid in light-harvesting complex (Chl a/b LHCII) of higher plants: time-resolved triplet-minus-singlet spectra of detergent-perturbed complexes. Spectrochim Acta A 55:193–204

    Article  Google Scholar 

  • Nellaepalli S, Zsiros O, Tóth T, Yadavalli V, Garab G, Subramanyam R, Kovács L (2014) Heat- and light-induced detachment of the light harvesting complex from isolated photosystem I supercomplexes. J Photochem Photobiol, B 137:13–20

    Article  CAS  Google Scholar 

  • Nevo R, Charuvi D, Shimoni E, Schwarz R, Kaplan A, Ohad I, Reich Z (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO J 26:1467–1473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts. J Cell Sci 6:243–255

    PubMed  Google Scholar 

  • Pearlstein RM (1991) Theoretical interpretation of antenna spectra. In: Scheer H (ed) Chlorophylls. CRC Press, Boca Raton, pp 1047–1078

    Google Scholar 

  • Pearlstein RM, Davis RC, Ditson SL (1982) Giant circular dichroism of high molecular weight chlorophyllide-apomyoglobin complexes. Proc Natl Acad Sci USA 79:400–402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Philipson KD, Sauer K (1973) Light–scattering effect on the circular dichroism of chloroplasts. Biochemistry 12:3454–3458

    Article  CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, Kovács L, Holzwarth AR, Garab G (2011) Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise. Biochim Biophys Acta 1807:1032–1043

    Article  CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the Q(A) model. Photosynth Res 120:43–58

    Article  CAS  PubMed  Google Scholar 

  • Simidjev I, Barzda V, Mustárdy L, Garab G (1997) Isolation of lamellar aggregates of light-harvesting chlorophyll a/b protein complex of photosystem II with long range chiral order and structural flexibility. Anal Biochem 250:169–175

    Article  Google Scholar 

  • Simidjiev I, Barzda V, Mustárdy L, Garab G (1998) 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

    Article  CAS  PubMed  Google Scholar 

  • Simidjiev I, Stoylova S, Amenitsch H, Jávorfi T, Mustárdy L, Laggner P, Holzenburg A, Garab G (2000) Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro. Proc Natl Acad Sci USA 97:1473–1476

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Simidjiev I, Várkonyi Z, Lambrev PH, Garab G (2011) Isolation and characterization of lamellar aggregates of LHCII and LHCII-lipid macro-assemblies with light-inducible structural transitions. In: Carpentier R (ed) Photosynthesis research protocols, methods in molecular biology 684: 127–138

  • Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    Article  CAS  PubMed  Google Scholar 

  • Standfuss J, van Scheltinga ACT, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J 24:919–928

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steinbach G, Pawlak K, Pomozi I, Tóth EA, Molnár A, Matkó J, Garab G (2014) Mapping microscopic order in plant and mammalian cells and tissues: novel differential polarization attachment for new generation confocal microscopes (DP-LSM). Methods Appl Fluoresc 2:015005

    Article  Google Scholar 

  • Stoitchkova K, Zsiros O, Jávorfi T, Páli T, Andreeva A, Gombos Z, Garab G (2007) Heat- and light-induced reorganizations in the phycobilisome antenna of Synechocystis sp. PCC 6803. Thermo-optic effect. Biochim Biophys Acta 1767:750–756

    Article  CAS  PubMed  Google Scholar 

  • Szabó M, Lepetit B, Goss R, Wilhelm C, Mustárdy L, Garab G (2008) Structurally flexible macro-organization of the pigment-protein complexes of the diatom Phaeodactylum tricornutum. Photosynth Res 95:237–245

    Article  PubMed  CAS  Google Scholar 

  • Tapie P, Haworth P, Hervo G, Breton J (1982) Orientation of the pigments in the thylakoid membrane and in the isolated chlorophyll-protein complexes of higher plants. III. A quantitative comparison of the low-temperature linear dichroism spectra of thylakoids and isolated pigment-protein complexes. Biochim Biophys Acta 682:339–344

    Article  CAS  Google Scholar 

  • Tinoco IJ, Mickols W, Maestre MF, Bustamante C (1987) Absorption, scattering, and imaging of biomolecular structures with polarized light. Ann Rev Biophys Biophys Chem 16:319–349

    Article  CAS  Google Scholar 

  • Ünnep R, Nagy G, Markó M, Garab G (2014a) Monitoring thylakoid ultrastructural changes in vivo using small-angle neutron scattering. Plant Physiol Biochem 81:197–207

    Article  PubMed  CAS  Google Scholar 

  • Ünnep R, Zsiros O, Solymosi K, Kovács L, Lambrev PH, Tóth T, Schweins R, Posselt D, Székely NK, Rosta L, Nagy G, Garab G (2014b) The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering. Biochim Biophys Acta 1837:1572–1580

    Article  PubMed  CAS  Google Scholar 

  • Van Amerongen H, Struve WS (1995) Polarized optical spectroscopy of chromoproteins. Meth Enzymol 246:259–283

    Article  CAS  PubMed  Google Scholar 

  • Van Amerongen H, Valkunas L, van Grondelle R (2000) Photosynthetic excitons. World Scientific, Singapore

    Book  Google Scholar 

  • Van Eerden FJ, de Jong DH, de Vries AH, Wassenaar TA, Marrink SJ (2015) Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations. Biochim Biophys Acta 1848:1319–1330

    Article  PubMed  CAS  Google Scholar 

  • Van Oort B, Marechal A, Ruban AV, Robert B, Pascal AA, de Ruijter NCA, van Grondelle R, van Amerongen H (2011) Different crystal morphologies lead to slightly different conformations of light-harvesting complex II as monitored by variations of the intrinsic fluorescence lifetime. Phys Chem Chem Phys 13:12614–12622

    Article  PubMed  CAS  Google Scholar 

  • Wendling M, Przyjalgowski MA, Gulen D, Vulto SIE, Aartsma TJ, van Grondelle R, van Amerongen H (2002) The quantitative relationship between structure and polarized spectroscopy in the FMO complex of Prosthecochloris aestuarii: refining experiments and simulations. Photosynth Res 71:99–123

    Article  CAS  PubMed  Google Scholar 

  • Williams WP (1998) The physical properties of thylakoid membrane lipids and their relation to photosynthesis. In: Siegenthaler P-A, Murata N (eds) Advances in Photosynthesis. Lipids in Photosynthesis. Kluwer, Dordrecht, pp 103–118

    Google Scholar 

  • Witt HT (1971) Coupling quanta, electrons, fields, ions and phosphorylation in the functional membrane of photosynthesis. Q Rev Biophys 4:365–477

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto HY, Higashi RM (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190:514–522

    Article  CAS  PubMed  Google Scholar 

  • Yang DH, Paulsen H, Andersson B (2000) The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett 466:385–388

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Lambrev P, Cheng Z, Jávorfi T, Kiss AZ, Paulsen H, Garab G (2008) The negatively charged amino acids in the lumenal loop influence the pigment binding and conformation of the major light-harvesting chlorophyll a/b complex of photosystem II. Biochim Biophys Acta 1777:1463–1470

    Article  CAS  PubMed  Google Scholar 

  • Zer H, Vink M, Keren N, Dilly-Hatrwig H, Paulsen H, Herrmann RG, Andersson B, Ohad I (1999) Regulation of thylakoid protein phosphorylation at the substrate level: reversible light-induced conformational changes expose the phosphorylation site of the light-harvesting complex II. Proc Natl Acad Sci USA 96:8277–8282

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zer H, Vink M, Shochat S, Herrmann RG, Andersson B, Ohad I (2003) Light affects the accessibility of the thylakoid light harvesting complex II (LHCII) phosphorylation site to the membrane protein kinase(s). Biochemistry 42:728–738

    Article  CAS  PubMed  Google Scholar 

  • Zimányi L, Garab G (1989) Configuration of the electric field and distribution of ions in energy transducing biological membranes: model calculations in a vesicle containing discrete charges. J Theor Biol 138:59–76

    Article  Google Scholar 

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Acknowledgments

I am greatly indebted to all my coworkers of the past more than four decades; it was a privilege for me to work together with them on problems what we mutually found important or exciting, or just interesting for one reason or another. On the present subjects, the List of References is thus also a way to acknowledge most warmly their contributions, often guidance, and their dedicated and hard works; specifically, in cases when their eagerness and enthusiasm were absolutely essential to address enigmatic or too hard-to-answer questions. The financial supports from OTKA (K112688) and TÁMOP (422D-15/1/KONV-2015-0024) are also acknowledged.

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Garab, G. Self-assembly and structural–functional flexibility of oxygenic photosynthetic machineries: personal perspectives. Photosynth Res 127, 131–150 (2016). https://doi.org/10.1007/s11120-015-0192-z

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