The largest stable photosystem II (PSII) supercomplex in land plants (C2S2M2) consists of a core complex dimer (C2), two strongly (S2) and two moderately (M2) bound light-harvesting protein (LHCB) trimers attached to C2 via monomeric antenna proteins LHCB4-6. Recently, we have shown that LHCB3 and LHCB6, presumably essential for land plants, are missing in Norway spruce (Picea abies), which results in a unique structure of its C2S2M2 supercomplex. Here, we performed structure-function characterization of PSII supercomplexes in Arabidopsis (Arabidopsis thaliana) mutants lhcb3, lhcb6, and lhcb3 lhcb6 to examine the possibility of the formation of the "spruce-type" PSII supercomplex in angiosperms. Unlike in spruce, in Arabidopsis both LHCB3 and LHCB6 are necessary for stable binding of the M trimer to PSII core. The "spruce-type" PSII supercomplex was observed with low abundance only in the lhcb3 plants and its formation did not require the presence of LHCB4.3, the only LHCB4-type protein in spruce. Electron microscopy analysis of grana membranes revealed that the majority of PSII in lhcb6 and namely in lhcb3 lhcb6 mutants were arranged into C2S2 semi-crystalline arrays, some of which appeared to structurally restrict plastoquinone diffusion. Mutants without LHCB6 were characterized by fast induction of non-photochemical quenching and, on the contrary to the previous lhcb6 study, by only transient slowdown of electron transport between PSII and PSI. We hypothesize that these functional changes, associated with the arrangement of PSII into C2S2 arrays in thylakoids, may be important for the photoprotection of both PSI and PSII upon abrupt high-light exposure.

Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University 783 71 Olomouc Czech Republic

Department of Physics Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic

Electron Microscopy Group Groningen Biomolecular Sciences and Biotechnology Institute University of Groningen Nijenborgh 7 9747 AG Groningen The Netherlands

Global Change Research Institute of the Czech Academy of Sciences 603 00 Brno Czech Republic

Institute of Experimental Botany of the Czech Academy of Sciences Centre of the Region Haná for Biotechnological and Agricultural Research 783 71 Olomouc Czech Republic

Erratum In

Plant Physiol. 2022 Jan 20;188(1):671. doi: 10.1093/plphys/kiab505. PubMed

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Adamiec M, Gibasiewicz K, Luciński R, Giera W, Chełminiak P, Szewczyk S, Sipińska W, van Grondelle R, Jackowski G (2015) Excitation energy transfer and charge separation are affected in PubMed

Albanese P, Manfredi M, Meneghesso A, Marengo E, Saracco G, Barber J, Morosinotto T, Pagliano C (2016a) Dynamic reorganization of photosystem II supercomplexes in response to variations in light intensities. Biochim Biophys Acta 1857 PubMed

Albanese P, Nield J, Tabares JAM, Chiodoni A, Manfredi M, Gosetti F, Marengo E, Saracco G, Barber J, Pagliano C (2016b) Isolation of novel PSII-LHCII megacomplexes from pea plants characterized by a combination of proteomics and electron microscopy. Photosynth Res 130 PubMed

Albanese P, Melero R, Engel BD, Grinzato A, Berto P, Manfredi M, Chiodoni A, Vargas J, Sorzano CÓS, Marengo E, et al. (2017) Pea PSII–LHCII supercomplexes form pairs by making connections across the stromal gap. Sci Rep. 7 PubMed PMC

Albanese P, Manfredi M, Re A, Marengo E, Saracco G, Pagliano C (2018) Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non-model organism aided by transcriptomic data integration. Plant J 96 PubMed

Albanese P, Manfredi M, Marengo E, Saracco G, Pagliano C (2019) Structural and functional differentiation of the light‐harvesting protein Lhcb4 during land plant diversification. Physiol Plant 166 PubMed

Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T (2008) PubMed PMC

Allahverdiyeva Y, Isojärvi J, Zhang P, Aro E-M (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life Basel Switz 5 PubMed PMC

Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: New links in the chain. Trends Plant Sci 8 PubMed

Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282 PubMed

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

Belgio E, Kapitonova E, Chmeliov J, Duffy CDP, Ungerer P, Valkunas L, Ruban AV (2014) Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nat Commun 5 PubMed

Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall’Osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284 PubMed PMC

van Bezouwen LS, Caffarri S, Kale RS, Kouřil R, Thunnissen A-MWH, Oostergetel GT, Boekema EJ (2017) Subunit and chlorophyll organization of the plant photosystem II supercomplex. Nat. Plants 3 PubMed

de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23 PubMed PMC

de Bianchi S, Dall’Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20 PubMed PMC

Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of PubMed

Björkman O, Demmig B (1987) Photon yield of O PubMed

Boekema EJ, van Roon H, Calkoen F, Bassi R, Dekker JP (1999) Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38 PubMed

Boekema EJ, van Breemen JFL, van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301 PubMed

Bratt CE, Arvidsson PO, Carlsson M, Akerlund HE (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res 45 PubMed

Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: Differential analysis of the Lhcb1 − 3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43 PubMed

Caffarri S, Kouřil R, Kereïche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28 PubMed PMC

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

Chen Y-E, Ma J, Wu N, Su Y-Q, Zhang Z-W, Yuan M, Zhang H-Y, Zeng X-Y, Yuan S (2018) The roles of Arabidopsis proteins of Lhcb4, Lhcb5 and Lhcb6 in oxidative stress under natural light conditions. Plant Physiol Biochem 130 PubMed

Dall’Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R (2017) Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat Plants 3 PubMed

Damkjær JT, Kereiche S, Johnson MP, Kovács L, Kiss AZ, Boekema EJ, Ruban AV, Horton P, Jansson S (2009) The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. Plant Cell 21 PubMed PMC

Dau H, Andrews JC, Roelofs TA, Latimer MJ, Liang W, Yachandra VK, Sauer K, Klein MP (1995) Structural consequences of ammonia binding to the manganese center of the photosynthetic oxygen-evolving complex: An X-ray absorption spectroscopy study of isotropic and oriented photosystem II particles. Biochemistry 34 PubMed

Daum B, Nicastro D, Austin J, McIntosh JR, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22 PubMed PMC

Deák Z, Sass L, Kiss É, Vass I (2014) Characterization of wave phenomena in the relaxation of flash-induced chlorophyll fluorescence yield in cyanobacteria. Biochim Biophys Acta 1837 PubMed

Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706 PubMed

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

Garab G, Kieleczawa J, Sutherland JC, Bustamante C, Hind G (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

Garab G, van Amerongen H (2009) Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res 101 PubMed PMC

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990

Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69 PubMed

Grebe S, Trotta A, Bajwa AA, Suorsa M, Gollan PJ, Jansson S, Tikkanen M, Aro E-M (2019) The unique photosynthetic apparatus of Pinaceae: Analysis of photosynthetic complexes in PubMed PMC

Grinzato A, Albanese P, Marotta R, Swuec P, Saracco G, Bolognesi M, Zanotti G, Pagliano C (2020) High-light versus low-light: Effects on paired photosystem II supercomplex structural rearrangement in pea plants. Int J Mol Sci 21 PubMed PMC

Günther G, Thiele A, Laasch H (1994) A new method for the determination of the transthylakoid pH gradient in isolated chloroplasts: The pH-dependent activity of violaxanthin de-epoxidase. Plant Sci 102

Haferkamp S, Haase W, Pascal AA, van Amerongen H, Kirchhoff H (2010) Efficient light harvesting by photosystem II requires an optimized protein packing density in grana thylakoids. J Biol Chem 285 PubMed PMC

Ilík P, Kotabová E, Spundová M, Novák O, Kana R, Strzałka K (2010) Low-light-induced violaxanthin de-epoxidation in shortly preheated leaves: uncoupling from Delta pH-dependent nonphotochemical quenching. Photochem Photobiol 86 PubMed

Ilík P, Pavlovič A, Kouřil R, Alboresi A, Morosinotto T, Allahverdiyeva Y, Aro E-M, Yamamoto H, Shikanai T (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol 214 PubMed

Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4 PubMed

Johnson MP (2020) Just the essentials: Photoprotective energy dissipation pared-down. J Exp Bot 71 PubMed

Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99 PubMed PMC

Kereïche S, Kiss AZ, Kouřil R, Boekema EJ, Horton P (2010) The PSBS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584 PubMed

Kirchhoff H (2008) Significance of protein crowding, order and mobility for photosynthetic membrane functions. Biochem Soc Trans 36 PubMed

Kirchhoff H, Haase W, Wegner S, Danielsson R, Ackermann R, Albertsson P-A (2007) Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplasts. Biochemistry 46 PubMed

Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376 PubMed

Klimmek F, Sjödin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed LHC protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140 PubMed PMC

Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1

Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ (2013) High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in PubMed

Kouřil R, Strouhal O, Nosek L, Lenobel R, Chamrád I, Boekema EJ, Šebela M, Ilík P (2014) Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J 77 PubMed

Kouřil R, Nosek L, Bartoš J, Boekema EJ, Ilík P (2016) Evolutionary loss of light-harvesting proteins Lhcb6 and Lhcb3 in major land plant groups—break-up of current dogma. New Phytol 210 PubMed

Kouřil R, Nosek L, Semchonok D, Boekema EJ, Ilík P (2018) Organization of plant photosystem II and photosystem I supercomplexes. PubMed

Kouřil R, Nosek L, Opatíková M, Arshad R, Semchonok DA, Chamrád I, Lenobel R, Boekema EJ, Ilík P (2020) Unique organization of photosystem II supercomplexes and megacomplexes in Norway spruce. Plant J 104 PubMed PMC

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

Kurasova I, Kalina J, Urban O, Stroch M, Spunda V (2003) Acclimation of two distinct plant species, Spring Barley and Norway Spruce, to combined effect of various irradiance and CO

Lazár D (1999) Chlorophyll a fluorescence induction 1. Biochim Biophys Acta 1412 PubMed

Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33 PubMed

Lazár D, Nauš J (1998) Statistical properties of chlorophyll fluorescence induction parameters. Photosynthetica 35

Lazár D, Tomek P, Ilík P, Nauš J (2001) Determination of the antenna heterogeneity of photosystem II by direct simultaneous fitting of several fluorescence rise curves measured with DCMU at different light intensities. Photosynth Res 68 PubMed

Li X-P, Gilmore AM, Niyogi KK (2002) Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. J Biol Chem 277 PubMed

Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes.

Lípová L, Krchnák P, Komenda J, Ilík P (2010) Heat-induced disassembly and degradation of chlorophyll-containing protein complexes in vivo. Biochim Biophys Acta 1797 PubMed

Malkin S, Armond PA, Mooney HA, Fork DC (1981) Photosystem II photosynthetic unit sizes from fluorescence induction in leaves : Correlation to photosynthetic capacity. Plant Physiol 67 PubMed PMC

McKenzie SD, Ibrahim IM, Aryal UK, Puthiyaveetil S (2020) Stoichiometry of protein complexes in plant photosynthetic membranes. Biochim Biophys Acta 1861 PubMed

Miller KR, Miller GJ, Mclntyre KR (1976) The light-harvesting chlorophyll–protein complex of photosystem II. Its location in the photosynthetic membrane. J Cell Biol 71: 624–638 PubMed PMC

Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: Molecular mechanisms and physiological functions. Plant Cell Physiol 51 PubMed

Miyake C (2020) Molecular mechanism of oxidation of P700 and suppression of ROS production in photosystem I in response to electron–sink limitations in C3 plants. Antioxidants 9 PubMed PMC

Morosinotto T, Caffarri S, Dall’Osto L, Bassi R (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol Plant 119

Morosinotto T, Bassi R, Frigerio S, Finazzi G, Morris E, Barber J (2006) Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barley. FEBS J 273 PubMed

Munekage Y, Takeda S, Endo T, Jahns P, Hashimoto T, Shikanai T (2001) Cytochrome b(6)f mutation specifically affects thermal dissipation of absorbed light energy in Arabidopsis. Plant J 28 PubMed

Nosek L, Semchonok D, Boekema EJ, Ilík P, Kouřil R (2017) Structural variability of plant photosystem II megacomplexes in thylakoid membranes. Plant J 89 PubMed

Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, et al. (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497 PubMed

Onoa B, Schneider AR, Brooks MD, Grob P, Nogales E, Geissler PL, Niyogi KK, Bustamante C (2014) Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids. PLoS ONE 9 PubMed PMC

van Oort B, Alberts M, de Bianchi S, Dall’Osto L, Bassi R, Trinkunas G, Croce R, van Amerongen H (2010) Effect of antenna-depletion in photosystem II on excitation energy transfer in PubMed PMC

Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components—calculation of qP and

Park RB, Biggins J (1964) Quantasome: size and composition. Science 144 PubMed

Peter GF, Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment–proteins. J Biol Chem 266 PubMed

de la Rosa-Trevín JM, Quintana A, Del Cano L, Zaldívar A, Foche I, Gutiérrez J, Gómez-Blanco J, Burguet-Castell J, Cuenca-Alba J, Abrishami V, et al. (2016) Scipion: A software framework toward integration, reproducibility and validation in 3D electron microscopy. J Struct Biol 195 PubMed

Ruban AV, Johnson MP (2009) Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth Res 99 PubMed

Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421 PubMed

Ruban AV, Wilson S (2020). The mechanism of non-photochemical quenching in plants: Localisation and driving forces. Plant Cell Physiol (doi: 10.1093/pcp/pcaa155) PubMed

Saccon F, Giovagnetti V, Shukla MK, Ruban AV (2020) Rapid regulation of photosynthetic light harvesting in the absence of minor antenna and reaction centre complexes. J Exp Bot 71 PubMed PMC

Schägger H (2006) Tricine-SDS-PAGE. Nat Protoc 1 PubMed

Scheres SHW (2012) RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180 PubMed PMC

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9 PubMed PMC

Semenova GA (1995) Particle regularity on thylakoid fracture faces is influenced by storage conditions. Can J Bot 73

Simpson DJ (1979) Freeze–fracture studies on barley plastid membranes. III. Location of the light-harvesting chlorophyll-protein. Carlsberg Res Commun 44

Standfuss J, Kühlbrandt W, (2004) The three isoforms of the light-harvesting complex II: Spectroscopic features, trimer formation, and functional roles. J Biol Chem 279 PubMed

Stirbet A, Lazár D, Kromdijk J, Govindjee (2018) Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56

Stoylova S, Flint TD, Ford RC, Holzenburg A (2000) Structural analysis of photosystem II in far-red-light-adapted thylakoid membranes: New crystal forms provide evidence for a dynamic reorganization of light-harvesting antennae subunits. Eur J Biochem 267 PubMed

Strasser RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient.

Su X, Ma J, Wei X, Cao P, Zhu D, Chang W, Liu Z, Zhang X, Li M (2017) Structure and assembly mechanism of plant C PubMed

Sznee K, Dekker JP, Dame RT, van Roon H, Wuite GJL, Frese RN (2011) Jumping mode atomic force microscopy on grana membranes from Spinach. J Biol Chem 286 PubMed PMC

Tietz S., Puthiyaveetil S, Enlow HM, Yarbrough R, Wood M, Semchonok DA, Lowry T, Li Z, Jahns P, Boekema EJ, et al. (2015) Functional implications of photosystem II crystal formation in photosynthetic membranes. J Biol Chem 290 PubMed PMC

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. Biochim Biophys Acta 1857 PubMed

Townsend AJ, Saccon F, Giovagnetti V, Wilson S, Ungerer P, Ruban AV (2018) The causes of altered chlorophyll fluorescence quenching induction in the Arabidopsis mutant lacking all minor antenna complexes. Biochim Biophys Acta 1859 PubMed

Tremmel IG, Kirchhoff H, Weis E, Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Biophys Acta 1607 PubMed

Tsvetkova NM, Apostolova EL, Brain APR, Patrick Williams W, Quinn PJ (1995) Factors influencing PS II particle array formation in

Vass I, Kirilovsky D, Etienne AL (1999) UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium PubMed

Wang YH (2008) How effective is T-DNA insertional mutagenesis in Arabidopsis? J Biochem Technol 1

Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II—LHCII supercomplex at 3.2 Å resolution. Nature 534 PubMed

Wientjes E, Drop B, Kouřil R, Boekema EJ, Croce R (2013) During state 1 to state 2 transition in PubMed PMC

Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6 PubMed

Wittig I, Karas M, Schägger H (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 6 PubMed

Yakushevska AE, Jensen PE, Keegstra W, van Roon H, Scheller HV, Boekema EJ, Dekker JP (2001) Supermolecular organization of photosystem II and its associated light-harvesting antenna in PubMed

Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV, Horton P (2003) The structure of photosystem II in PubMed

Yamamoto H, Shikanai T (2019) PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides. Plant Physiol 179 PubMed PMC

Photosystem II supercomplexes lacking light-harvesting antenna protein LHCB5 and their organization in the thylakoid membrane

Spruce versus Arabidopsis: different strategies of photosynthetic acclimation to light intensity change