Photosynthetic Membranes Group

Research

The main goal of our research is to understand the structure and function of the photosynthetic membranes with special attention to the interplay between the dynamic macroorganization of the membranes and the regulation of excitation energy and electron flow. We also design and construct innovative scientific instruments.

Featured research projects

Macroorganization and flexibility of the photosynthetic membranes

By using mainly circular dichroism (CD) spectroscopy, we have established that the protein complexes in the chloroplast thylakoid membranes of higher plants and many algae are assembled into extended arrays with long-range chiral order, which are capable of undergoing sizeable reversible reorganizations upon changes in the environmental conditions (Garab 2014, Lambrev and Akhtar 2019). The macrodomain formation explains the sorting of LHCII:PSII and LHCI:PSI supercomplexes and the stacking of membranes, the basis of the self-assembly of granal ultrastructure (Mustárdy and Garab 2003). Using electron tomography, we revealed the quasi-helical organization of the granum-stroma thylakoid membrane assembly (Mustárdy et al. 2008).

The anisotropic CD (ACD) of macroscopically aligned samples – an extension of the CD spectroscopy – provides additional information about the molecular orientation of the participating pigment dipoles. The plant light-harvesting complex II (LHCII) in isolated form or in the native membrane has a distinct ACD signature that (Miloslavina et al. 2012), which provides geometric constraints helping to identify excitonic states shared between specific chlorophylls (Akhtar et al., 2019b).

Macroorganization of the thylakoid membrane: A. Thin-section electron micrograph of higher-plant chloroplast. B. 3D computer model of the granal thylakoid membrane based on serial-sectioning electron micrographs. C. Psi-type CD spectra of pea chloroplasts, lamellar macroaggregates of LHCII and the excitonic CD spectrum of detergent-solubilized LHCII. D. ACD spectra of LHCII in oriented lipid bilayers (Mustárdy and Garab 2003, Lambrev and Akhtar 2019).

By using the technique of small-angle neutron scattering (SANS) in vitro and in vivo under a large variety of physiologically important conditions and in different mutants, we have also shown that the thylakoid membranes should not be portrayed as simply providing a scaffold for the photosynthetic functions but, by fine-tuning their multilamellar 3D ultrastructure, they actively participate in different regulatory mechanisms (Ünnep et al. 2014). The non-invasive techniques of CD and SANS are routinely used towards the better understanding of the nature and physiological significance of structural dynamics of thylakoid membranes on the mesoscopic size scale.

Small-angle neutron scattering profiles of thylakoid membranes in the dark or after illumination.

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Mechanisms and dynamics of the primary photosynthetic processes

We study the elementary mechanisms, pathways and kinetics of the processes of light absorption, migration of the excitation energy and photochemical charge separation in the photosynthetic apparatus. We apply a variety of optical spectroscopy techniques to study these processes in vivo and in vitro – using isolated pigment-protein complexes, native or reconstituted membranes. One of the most capable techniques to probe the ultrafast excitation dynamics is multidimensional electronic spectroscopy. We have been working in close collaboration with the group of Howe-Siang Tan at NTU, Singapore applying multidimensional electronic spectroscopy to reveal new details on the mechanisms and dynamics of photosynthetic light harvesting (Lambrev et al. 2019). By two-dimensional electronic spectroscopy we could follow simultaneously uphill and downhill energy transfer in light-harvesting complex II (Akhtar et al. 2017) and in Photosystem I (Akhtar et al. 2018). A clear temperature dependence of uphill energy transfer processes was also discerned, consistent with the detailed-balance condition (Akhtar et al. 2019, Akhtar et al. 2020); these uphill pathways ensure fast and efficient energy transfer at physiological temperatures (Do et al. 2019, Leng et al. 2020).

Probing energy transfer in photosynthetic complexes by two-dimensional electronic spectroscopy. A. Relaxation between coupled excitonic transitions appears is visualized as dynamic cross-peaks in the 2D electronic spectra (Lambrev et al. 2020). B. 2D electronic spectra of LHCII from Bryopsis corticulans at 77 K at two different waiting (delay) times (Akhtar et al. 2020b).

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Molecular interactions in the membranes and excitation quenching

By using CD spectroscopy, we have revealed that the pigment-pigment interactions in LHCII are sensitive to its molecular environment (Lambrev et al. 2007, Akhtar et al. 2015). Extracting of the complexes from the membrane and solubilization with detergents perturbs the native structure. If not bound to the PSII supercomplexes, LHCII units tend to associate into energetically connected domains (Lambrev et al. 2011). Macrostructural rearrangements of a similar kind involve other antenna complexes of the LHC superfamily, such as FCP in diatoms (Miloslavina et al. 2009, Ghazaryan et al. 2016). In model membranes, LHCII forms packed clusters (Tutkus et al. 2019), where the excited-state lifetime is inversely correlated to the protein density (Akhtar et al. 2019a). This type of excitation quenching is accompanied by spectroscopic signatures similar to the photoprotective non-photochemical quenching in vivo, including the formation of chlorophyll-chlorophyll charge-transfer states that can effectively dissipate the excitation energy (Ostroumov et al. 2020).

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Role of non-bilayer lipids in the structure and function of the thylakoid membranes

We are testing the validity of our Dynamic Exchange Model, a membrane model taking into account the presence of non-bilayer lipid phases in addition to the bilayer lipid membrane. To this end, we use fully functional thylakoid membranes as exemplary of energy-converting biological membranes, in which we discovered the co-existence of bilayer and non-bilayer lipid phases. We investigate the role of non-bilayer lipids and non-lamellar lipid phases in the homeostasis, protein-to-lipid ratio and fluidity, of membranes, in controlling their permeability and regulating the activity of the water-soluble, lipocalin-like enzyme, violaxanthin de-epoxidase. We also investigate, in international collaboration, the identity of structural units containing the non-lamellar lipid phases, focusing on the junction and fusion of membranes as well as on membrane-associated lipocalin:lipid assemblies – using combinations of ³¹P-NMR and time-resolved fluorescence spectroscopy and electron microscopy techniques and functional and analytical tools.

Lipid polymorphysm in thylakoid membranes detected by ³¹NMR

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The light-adapted charge-separated state of Photosystem II

We have earlier discovered the existence of light-induced conformational changes and rate-limiting steps in ‘closed’ PSII. In PSII reaction centres in the state of stable charge separation, induced by a single-turnover saturating flash in the presence of PSII electron transport inhibitor, additional excitations have been shown to lead to chlorophyll-a fluorescence increments both in the physiological and cryogenic temperature ranges. In order to characterize this novel state of PSII, we, in collaboration with foreign partners, perform a range of molecular spectroscopic studies in different states of PSII(-containing) samples, including FTIR and low-temperature fluorescence spectroscopy, absorbance transients and fluorescence lifetime measurements. We also analyze the origin of variable chlorophyll-a fluorescence to get a deeper understanding of this parameter, which is arguably the most widely used parameter in photosynthesis research.

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Biotechnological application of microalgae

We consider microalgae from two aspects as model organisms of basic science and as target of industrial use both complement each other. We mainly focus on cell division and stress adaptation of microalgae supporting the high yield of biomass and production of bioactive compounds. We investigate microalgae on gene level, protein level and on supra-individual level and study the membrane structure and function. We deal with commercially available and isolated own microalgae strains from natural sources. The selected microalgal cultures are projects of biotechnological manipulations to increase their yield and the biomass production. Algae often produce different bioactive compounds under stress conditions; therefore we study the connection between their stress adaptation and the production of bioactive compounds. The cell division is the most fundamental process of life. We investigate the cell division with mutational analysis producing different phenotypes and we consider the growth of a culture as a community of millions of single cells. Our scope covers the characterization of the microalgal growth parameters, photosynthetic performance and fatty acid and protein composition.

CLSM image of EGFP signals in Synechococcus phosphatidylglicerol (PG) synthesis mutant live cells grown for 4 days in the presence of PG (A) and during PG depletion on the 4th day (B, b) 8th day (C) and 12th day (D)of the depletion process. (Kobori et al 2018 J Plant Physiol 223: 96–104).

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Technical development projects and applications

We transform confocal laser scanning microscopes (LSMs) into differential-polarization (DP‑)LSMs, which, via measuring pixel-by-pixel different physical quantities allow the mapping of anisotropic molecular organization of biological samples. A DP-LSM and a Re-scan confocal microscope with differential-polarization attachment (DP-RCM) are part of the Euro-BioImaging network.

Expanding the collaboration with the ELI-ALPS laser centre (www.eli-alps.hu), we are developing a user end station for multidimensional optical spectroscopy employing ultrashort, ultrabroadband pulses at very high repetition rates that will be available to the broad research community.

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Instrumentation and methodology

Optical spectroscopy

• UV-VIS absorption spectroscopy (Thermo Evolution 500 double-beam spectrophotometer)

• Circular and linear dichroism spectroscopy (Jasco J-815 spectropolarimeter with temperature control, MCD, ACD)

• Fluorescence emission and excitation spectra (Jasco FP-8500 spectrofluorometer)

Chlorophyll fluorescence induction

• Pulse-amplitude modulated fluorometer (Walz)

• Fast fluorescence induction measurements (Hansatech, PSI)

• Flash-induced fluorescence changes, pump-probe fluorescence measurements and relaxation kinetics with a custom apparatus

Time-resolved spectroscopy

• Time-correlated single-photon counting spectrometer (PicoQuant FT200 + PicoHarp 300, tunable excitation and emission 400-750 nm, 40 ps IRF FWHM, custom data analysis allowing resolution of fluorescence lifetimes <10 ps)

• Microsecond-resolution transient absorption and fluorescence measurements – electrochromic shift, P700, C550

Techniques at external facilities

• Small-angle neutron scattering (www.psi.ch, www.ill.eu, mlz-garching.de)

• Synchrotron-radiation circular dichroism (www.diamond.ac.uk)

• Nuclear magnetic resonance spectroscopy (www.ceric-eric.eu)

• Ultrafast spectroscopy (www.laserlab-europe.eu, www.eli-alps.hu, www.eli-beams.eu)

Biochemistry lab

• We run a wet lab for protein purification, reconstitution of protein complexes and membranes, gel electrophoresis, etc.

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Publications

Featured publications

Lambrev PH, Akhtar P, Tan H-S (2020) Insights into the mechanisms and dynamics of energy transfer in plant light-harvesting complexes from two-dimensional electronic spectroscopy. Biochim Biophys Acta 1861 (4):148050. 

Akhtar P, Lindorfer D, Lingvay M, Pawlak K, Zsiros O, Siligardi G, Javorfi T, Dorogi M, Ughy B, Garab G, Renger T, Lambrev PH (2019) Anisotropic Circular Dichroism of Light-Harvesting Complex II in Oriented Lipid Bilayers: Theory Meets Experiment. J Phys Chem B 123 (5):1090–1098. 

Lambrev PH, Akhtar P (2019) Macroorganisation and flexibility of thylakoid membranes. Biochem J 476 (20):2981–3018. 

Ughy B, Schmidthoffer I, Szilak L (2019) Heparan sulfate proteoglycan (HSPG) can take part in cell division: inside and outside. Cell Mol Life Sci 76 (5):865–871. 

Magyar M, Sipka G, Kovács L, Ughy B, Zhu Q, Han G, Špunda V, Lambrev PH, Shen J-R, Garab G (2018) Rate-limiting steps in the dark-to-light transition of Photosystem II - revealed by chlorophyll-a fluorescence induction. Scientific Reports 8 (1):2755. 

Akhtar P, Zhang C, Do TN, Garab G, Lambrev PH, Tan H-S (2017) Two-dimensional spectroscopy of chlorophyll a excited-state equilibration in light-harvesting complex II. J Phys Chem Lett 8 (1):257–263. 

Garab G, Ughy B, de Waard P, Akhtar P, Javornik U, Kotakis C, Sket P, Karlicky V, Materova Z, Spunda V, Plavec J, van Amerongen H, Vigh L, Van As H, Lambrev PH (2017) Lipid polymorphism in chloroplast thylakoid membranes - as revealed by 31P-NMR and timeresolved merocyanine fluorescence spectroscopy. Scientific Reports 7 (1):13343. 

Zhang Z, Lambrev PH, Wells KL, Garab G, Tan HS (2015) Direct observation of multistep energy transfer in LHCII with fifth-order 3D electronic spectroscopy. Nat Commun 6:7914. 

Publications by year

2020

Akhtar P, Biswas A, Petrova N, Zakar T, van Stokkum IHM, Lambrev PH (2020a) Time-resolved fluorescence study of excitation energy transfer in the cyanobacterium Anabaena PCC 7120. Photosynth Res 144 (2):247–259.

Akhtar P, Nowakowski PJ, Wang W, Do TN, Zhao S, Siligardi G, Garab G, Shen JR, Tan HS, Lambrev PH (2020b) Spectral tuning of light-harvesting complex II in the siphonous alga Bryopsis corticulans and its effect on energy transfer dynamics. Biochim Biophys Acta Bioenerg 1861 (7):148191.

Bernula D, Benkő P, Kaszler N, Domonkos I, Valkai I, Szőllősi R, Ferenc G, Ayaydin F, Fehér A, Gémes K (2020) Timely removal of exogenous cytokinin and the prevention of auxin transport from the shoot to the root affect the regeneration potential of Arabidopsis roots. Plant Cell, Tissue and Organ Culture (PCTOC) 140 (2):327–339.

Biswas A, Huang X, Lambrev PH, van Stokkum IHM (2020) Modelling excitation energy transfer and trapping in the filamentous cyanobacterium Anabaena variabilis PCC 7120. Photosynth Res 144 (2):261–272.

Lambrev PH, Akhtar P, Tan H-S (2020) Insights into the mechanisms and dynamics of energy transfer in plant light-harvesting complexes from two-dimensional electronic spectroscopy. Biochim Biophys Acta 1861 (4):148050.

Leng X, Do TN, Akhtar P, Nguyen HL, Lambrev P, Tan HS (2020) Hierarchical Equations of Motion Simulation of Temperature-Dependent Two-Dimensional Electronic Spectroscopy of the Chlorophyll a Manifold in LHCII. Chem Asian J in press.

Ostroumov EE, Gotze JP, Reus M, Lambrev PH, Holzwarth AR (2020) Characterization of fluorescent chlorophyll charge-transfer states as intermediates in the excited state quenching of light-harvesting complex II. Photosynth Res 144 (2):171–193.

Ünnep R, Paul S, Zsiros O,Kovács L, Székely NK, Steinbach G, Appavou M-S, Porcar L, Holzwarth AR, Garab G, Nagy G (2020) Thylakoid membrane reorganizations revealed by small-angle neutron scattering of Monstera deliciosa leaves associated with non-photochemical quenching. Open biol 200144 , 12 p.

Wientjes E, Lambrev P (2020) Ultrafast processes in photosynthetic light-harvesting. Photosynth Res 144 (2):123–125.

Zsiros O,Ünnep R,Nagy G,Almasy L,Patai R,Szekely NK,Kohlbrecher J,Garab G,Der A,Kovacs L (2020) Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes-As Revealed by the Effectsof Hofmeister Salts. Front Plant Sci 1257 (11):14 p.

2019

Akhtar P, Do TN, Nowakowski PJ, Huerta-Viga A, Khyasudeen MF, Lambrev PH, Tan HS (2019a) Temperature Dependence of the Energy Transfer in LHCII Studied by Two-Dimensional Electronic Spectroscopy. J Phys Chem B 123 (31):6765–6775.

Akhtar P, Gorfol F, Garab G, Lambrev PH (2019b) Dependence of chlorophyll fluorescence quenching on the lipid-to-protein ratio in reconstituted light-harvesting complex II membranes containing lipid labels. Chem Phys 522:242–248.

Akhtar P, Lindorfer D, Lingvay M, Pawlak K, Zsiros O, Siligardi G, Javorfi T, Dorogi M, Ughy B, Garab G, Renger T, Lambrev PH (2019c) Anisotropic Circular Dichroism of Light-Harvesting Complex II in Oriented Lipid Bilayers: Theory Meets Experiment. J Phys Chem B 123 (5):1090–1098.

Bocsik A, Grof I, Kiss L, Otvos F, Zsiros O, Daruka L, Fulop L, Vastag M, Kittel A, Imre N, Martinek TA, Pal C, Szabo-Revesz P, Deli MA (2019) Dual Action of the PN159/KLAL/MAP Peptide: Increase of Drug Penetration across Caco-2 Intestinal Barrier Model by Modulation of Tight Junctions and Plasma Membrane Permeability. Pharmaceutics 11 (2):73.

Do TN, Huerta-Viga A, Akhtar P, Nguyen HL, Nowakowski PJ, Khyasudeen MF, Lambrev PH, Tan H-S (2019) Revealing the excitation energy transfer network of Light-Harvesting Complex II by a phenomenological analysis of two-dimensional electronic spectra at 77 K. J Chem Phys 151 (20):205101.

Hudak A, Kusz E, Domonkos I, Josvay K, Kodamullil AT, Szilak L, Hofmann-Apitius M, Letoha T (2019) Contribution of syndecans to cellular uptake and fibrillation of alpha-synuclein and tau. Scientific Reports 9:16543.

Lambrev PH, Akhtar P (2019) Macroorganisation and flexibility of thylakoid membranes. Biochem J 476 (20):2981–3018.

Letoha T, Hudak A, Kusz E, Pettko-Szandtner A, Domonkos I, Josvay K, Hofmann-Apitius M, Szilak L (2019) Contribution of syndecans to cellular internalization and fibrillation of amyloid-beta(1-42). Scientific Reports 9 (1):1393.

Patty CHL, ten Kate IL, Buma WJ, van Spanning RJM, Steinbach G, Ariese F, Snik F (2019) Circular Spectropolarimetric Sensing of Vegetation in the Field: Possibilities for the Remote Detection of Extraterrestrial Life. Astrobiology 19 (10):1221–1229.

Sipka G, Muller P, Brettel K, Magyar M, Kovacs L, Zhu QJ, Xiao YA, Han GY, Lambrev PH, Shen JR, Garab G (2019) Redox transients of P680 associated with the incremental chlorophyll-a fluorescence yield rises elicited by a series of saturating flashes in diuron-treated photosystem II core complex of Thermosynechococcus vulcanus. Physiol Plant 166 (1):22–32.

Steinbach G, Nagy D, Sipka G, Manders E, Garab G, Zimanyi L (2019) Fluorescence-detected linear dichroism imaging in a re-scan confocal microscope equipped with differential polarization attachment. Eur Biophys J 48 (5):457–463.

Ughy B, Karlicky V, Dlouhy O, Javornik U, Materova Z, Zsiros O, Sket P, Plavec J, Spunda V, Garab G (2019a) Lipid-polymorphism of plant thylakoid membranes. Enhanced non-bilayer lipid phases associated with increased membrane permeability. Physiol Plant 166 (1):278–287.

Ughy B, Schmidthoffer I, Szilak L (2019b) Heparan sulfate proteoglycan (HSPG) can take part in cell division: inside and outside. Cell Mol Life Sci 76 (5):865–871.

Zsiros O, Nagy V, Párducz Á, Nagy G, Ünnep R, El-Ramady H, Prokisch J, Lisztes-Szabó Z, Fári M, Csajbók J, Tóth SZ, Garab G, Domokos-Szabolcsy É (2019) Effects of selenate and red Se-nanoparticles on the photosynthetic apparatus of Nicotiana tabacum. Photosynth Res 139 (1):449-460.

2018

Akhtar P, Zhang C, Liu Z, Tan HS, Lambrev PH (2018) Excitation transfer and trapping kinetics in plant photosystem I probed by two-dimensional electronic spectroscopy. Photosynth Res 135 (1–3):239–250.

Domokos-Szabolcsy É, Fári M, Márton L, Czakó M, Veres S, Elhawat N, Antal G, El-Ramady H, Zsíros O, Garab G (2018) Selenate tolerance and selenium hyperaccumulation in the monocot giant reed (Arundo donax), a biomass crop plant with phytoremediation potential. Environ Sci Pollut Res 25 (31):31368–31380.

Erdei AI, Borbely A, Magyar A, Taricska N, Perczel A, Zsiros O, Garab G, Szucs E, Otvos F, Zador F, Balogh M, Al-Khrasani M, Benyhe S (2018) Biochemical and pharmacological characterization of three opioid-nociceptin hybrid peptide ligands reveals substantially differing modes of their actions. Peptides 99:205–216.

Kis M, Sipka G, Ayaydin F, Maroti P (2018) The biophysics of a critical phenomenon: colonization and sedimentation of the photosynthetic bacteria Rubrivivax gelatinosus. Eur Biophys J 47 (2):139–149.

Kóbori TO, Uzumaki T, Kis M, Kovács L, Domonkos I, Itoh S, Krynická V, Kuppusamy SG, Zakar T, Dean J, Szilák L, Komenda J, Gombos Z, Ughy B (2018) Phosphatidylglycerol is implicated in divisome formation and metabolic processes of cyanobacteria. J Plant Physiol 223:96–104.

Kotakis C, Akhtar P, Zsiros O, Garab G, Lambrev PH (2018) 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.

Magyar M, Sipka G, Kovács L, Ughy B, Zhu Q, Han G, Špunda V, Lambrev PH, Shen J-R, Garab G (2018) Rate-limiting steps in the dark-to-light transition of Photosystem II - revealed by chlorophyll-a fluorescence induction. Scientific Reports 8 (1):2755.

Nedzved A, Mitrović AL, Savić A, Mutavdžić D, Radosavljević JS, Pristov JB, Steinbach G, Garab G, Starovoytov V, Radotić K (2018) Automatic image processing morphometric method for the analysis of tracheid double wall thickness tested on juvenile Picea omorika trees exposed to static bending. Trees 32 (5):1347–1356.

Patty CL, Luo DA, Snik F, Ariese F, Buma WJ, Ten Kate IL, van Spanning RJ, Sparks WB, Germer TA, Garab G (2018) Imaging linear and circular polarization features in leaves with complete Mueller matrix polarimetry. Biochimica et Biophysica Acta (BBA) - General Subjects 1862 (6):1350–1363.

Sipka G, Kis M, Maroti P (2018a) Characterization of mercury(II)-induced inhibition of photochemistry in the reaction center of photosynthetic bacteria. Photosynth Res.

Sipka G, Kis M, Smart JL, Maróti P (2018b) Fluorescence induction of photosynthetic bacteria. Photosynthetica 56 (1):125–131.

Sipka G, Maroti P (2018) Photoprotection in intact cells of photosynthetic bacteria: quenching of bacteriochlorophyll fluorescence by carotenoid triplets. Photosynth Res 136 (1):17–30.

Stefanov D, Milanov G, Lambrev P, Kurteva M, Abumhadi N, Goltsev V, Kapchina V (2018) Delayed fluorescence measurements show increased S₂Q_B⁻ charge recombination in PS2 of tobacco pigment-deficient aurea mutant. Comptes Rendus de L'Academie Bulgare des Sciences 71 (8):1052–1061.

Tutkus M, Akhtar P, Chmeliov J, Görföl F, Trinkunas G, Lambrev PH, Valkunas L (2018) Fluorescence Microscopy of Single Liposomes with Incorporated Pigment–Proteins. Langmuir 34 (47):14410–14418.

2017

Akhtar P, Zhang C, Do TN, Garab G, Lambrev PH, Tan H-S (2017) Two-dimensional spectroscopy of chlorophyll a excited-state equilibration in light-harvesting complex II. J Phys Chem Lett 8 (1):257–263.

Bar Eyal L, Ranjbar Choubeh R, Cohen E, Eisenberg I, Tamburu C, Dorogi M, Unnep R, Appavou MS, Nevo R, Raviv U, Reich Z, Garab G, van Amerongen H, Paltiel Y, Keren N (2017) Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria. Proceedings of the National Academy of Sciences 114 (35):9481–9486.

Garab G, Ughy B, de Waard P, Akhtar P, Javornik U, Kotakis C, Sket P, Karlicky V, Materova Z, Spunda V, Plavec J, van Amerongen H, Vigh L, Van As H, Lambrev PH (2017) Lipid polymorphism in chloroplast thylakoid membranes - as revealed by ³¹P-NMR and timeresolved merocyanine fluorescence spectroscopy. Scientific Reports 7 (1):13343.

Keller-Pinter A, Ughy B, Domoki M, Pettko-Szandtner A, Letoha T, Tovari J, Timar J, Szilak L (2017) The phosphomimetic mutation of syndecan-4 binds and inhibits Tiam1 modulating Rac1 activity in PDZ interaction-dependent manner. PLoS One 12 (11):e0187094.

Radosavljevic JS, Pristov JB, Mitrovic AL, Steinbach G, Mouille G, Tufegdzic S, Maksimovic V, Mutavdzic D, Janosevic D, Vukovic M, Garab G, Radotic K (2017) Parenchyma cell wall structure in twining stem of Dioscorea balcanica. Cellulose 24 (11):4653–4669.

Szabo T, Cseko R, Hajdu K, Nagy K, Sipos O, Galajda P, Garab G, Nagy L (2017) Sensing photosynthetic herbicides in an electrochemical flow cell. Photosynth Res 132 (2):127–134.

Unnep R, Zsiros O, Horcsik Z, Marko M, Jajoo A, Kohlbrecher J, Garab G, Nagy G (2017) Low-pH induced reversible reorganizations of chloroplast thylakoid membranes - As revealed by small-angle neutron scattering. Bba-Bioenergetics 1858 (5):360–365.

2016

Akhtar P, Lingvay M, Kiss T, Deák R, Bóta A, Ughy B, Garab G, Lambrev PH (2016) Excitation energy transfer between light-harvesting complex II and photosystem I in reconstituted membranes. Biochim Biophys Acta 1857 (4):462–472.

Garab G (2016) Self-assembly and structural–functional flexibility of oxygenic photosynthetic machineries: personal perspectives. Photosynth Res 127 (1):131-150.

Garab G, Ughy B, Goss R (2016) Role of MGDG and Non-bilayer Lipid Phases in the Structure and Dynamics of Chloroplast Thylakoid Membranes. In: Nakamura Y, Li-Beisson Y (eds) Lipids in Plant and Algae Development. Springer, Dordrecht, pp 127–157. doi:10.1007/978-3-319-25979-6

Ghazaryan A, Akhtar P, Garab G, Lambrev PH, Buchel C (2016) Involvement of the Lhcx protein Fcp6 of the diatom Cyclotella meneghiniana in the macro-organisation and structural flexibility of thylakoid membranes. Biochim Biophys Acta 1857 (9):1373–1379.

Herdean A, Nziengui H, Zsiros O, Solymosi K, Garab G, Lundin B, Spetea C (2016a) The Arabidopsis Thylakoid Chloride Channel AtCLCe Functions in Chloride Homeostasis and Regulation of Photosynthetic Electron Transport. Front Plant Sci 7:115.

Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON, Unnep R, Nagy G, Zsiros O, Dana S, Solymosi K, Garab G, Szabo I, Spetea C, Lundin B (2016b) A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun 7:11654.

Nielsen JT, Kulminskaya NV, Bjerring M, Linnanto JM, Ratsep M, Pedersen MO, Lambrev PH, Dorogi M, Garab G, Thomsen K, Jegerschold C, Frigaard NU, Lindahl M, Nielsen NC (2016) In situ high-resolution structure of the baseplate antenna complex in Chlorobaculum tepidum. Nat Commun 7:12454.

Tóth TN, Rai N, Solymosi K, Zsiros O, Schröder WP, Garab G, van Amerongen H, Horton P, Kovács L (2016) Fingerprinting the macro-organisation of pigment-protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy. Biochimica et Biophysica Acta-Bioenergetics 1857 (9):1479–1489.

2015

Akhtar P, Dorogi M, Pawlak K, Kovacs L, Bota A, Kiss T, Garab G, Lambrev PH (2015) Pigment interactions in light-harvesting complex II in different molecular environments. J Biol Chem 290 (8):4877–4886.

Bricker WP, Shenai PM, Ghosh A, Liu Z, Enriquez MG, Lambrev PH, Tan HS, Lo CS, Tretiak S, Fernandez-Alberti S, Zhao Y (2015) Non-radiative relaxation of photoexcited chlorophylls: theoretical and experimental study. Sci Rep 5:13625.

Enriquez MM, Akhtar P, Zhang C, Garab G, Lambrev PH, Tan HS (2015) Energy transfer dynamics in trimers and aggregates of light-harvesting complex II probed by 2D electronic spectroscopy. J Chem Phys 142 (21):212432.

Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Unnep 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 84 (1):99–110.

Nagy L, Kiss V, Brumfeld V, Osvay K, Borzsonyi A, Magyar M, Szabo T, Dorogi M, Malkin S (2015) Thermal Effects and Structural Changes of Photosynthetic Reaction Centers Characterized by Wide Frequency Band Hydrophone: Effects of Carotenoids and Terbutryn. Photochem Photobiol 91 (6):1368–1375.

Szabo T, Magyar M, Hajdu K, Dorogi M, Nyerki E, Toth T, Lingvay M, Garab G, Hernadi K, Nagy L (2015) Structural and Functional Hierarchy in Photosynthetic Energy Conversion-from Molecules to Nanostructures. Nanoscale Res Lett 10 (1):458.

Toth TN, Chukhutsina V, Domonkos I, Knoppova J, Komenda J, Kis M, Lenart Z, Garab G, Kovacs L, Gombos Z, van Amerongen H (2015) Carotenoids are essential for the assembly of cyanobacterial photosynthetic complexes. Biochim Biophys Acta 1847 (10):1153–1165.

Zhang Z, Lambrev PH, Wells KL, Garab G, Tan HS (2015) Direct observation of multistep energy transfer in LHCII with fifth-order 3D electronic spectroscopy. Nat Commun 6:7914.

2000–2015

Demmig-Adams, B., Garab, G. & Adams III, W. (Eds) (2014) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Adv. Photosynth. Respir., Vol. 40, Springer Science+Business Media, Dordrecht

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

Hind, G., Wall, J.S., Várkonyi, Z., Istokovics, A., Lambrev, P.H. & Garab, G. (2014) Membrane crystals of plant light-harvesting complex II disassemble reversibly in light. Plant Cell Physiol. 55: 1296-303.

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

Ünnep, R., Zsiros, O., Solymosi, K., Kovács, L., Lambrev, P.H., Tóth, T., Schweins, R., Posselt, D., Székely, N.K., Rosta, L., Nagy, G. & Garab G. (2014) 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.

Wells, K.L., Lambrev, P.H., Zhang, Z., Garab, G. & Tan, H.S. (2014) Pathways of energy transfer in LHCII revealed by room-temperature 2D electronic spectroscopy, Phys. Chem. Chem. Phys. 16: 1463-9076.

Lambrev, P.H., Miloslavina, Y., Van Stokkum, I.H.M., Stahl, A.D., Michalik, M., Susz, A., Tworzydło, J., Fiedor, J., Huhn, G., Groot, M.L., Van Grondelle, R., Garab, G. & Fiedor, L. (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.

Lambrev, P.H. & Miloslavina, Y. (2012) On the relationship between non-photochemical quenching and photoprotection of Photosystem II. Biochim. Biophys. Acta 1817: 760–769.

Nagy, G., Szabó, M., Ünnep, R., Káli, G., Miloslavina, Y., Lambrev, P.H., 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 revealed by small-angle neutron scattering and circular dichroism spectroscopy. Photosynth. Res. 111: 71-79.

Lambrev, P.H., Schmitt, F.J., Kussin, S., Schoengen, M., Várkonyi, Zs., Eichler, H.J., Garab, G. & Renger G. (2011) Functional domain size in aggregates of light-harvesting complex II and thylakoid membranes. Biochim. Biophys. Acta 1807: 1022-1031.

Miloslavina, Y., Lambrev, P.H., Jávorfi, T., Várkonyi, Zs., Karlický, V., Wall, J.S., Hind, G. & Garab, G. (2011) Anisotropic circular dichroism signatures of oriented thylakoid membranes and lamellar aggregates of LHCII. Photosynth. Res. 111: 29-39.

Schansker, G., Tóth, S.Z., Kovács, L., Holzwarth, A.R. & 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.

Krumova, S.B., Laptenok, S.P., 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.

Miloslavina, Y., Grouneva, I., Lambrev, P.H., Lepetit, B., Goss, R., Wilhelm, C. & Holzwarth, A.R. (2009) Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim. Biophys. Acta 1787: 1189-1197.

Krumova, S.B., Koehorst, R.B.M., Bóta, A., Páli, T., van Hoek, A., Garab, G. & van Amerongen, H. (2008) 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.

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

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

Lambrev, P.H., Várkonyi, Zs., Krumova, S., Kovács, L., Miloslavina, Y., Holzwarth, A.R. & Garab, G. (2007) Importance of trimer–trimer interactions for the native state of the plant light-harvesting complex II. Biochim. Biophys. Acta 1767: 847-853.

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

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