Organization of Plant Photosystem II and Photosystem I Supercomplexes

  • Roman KouřilEmail author
  • Lukáš Nosek
  • Dmitry Semchonok
  • Egbert J. Boekema
  • Petr Ilík
Part of the Subcellular Biochemistry book series (SCBI, volume 87)


In nature, plants are continuously exposed to varying environmental conditions. They have developed a wide range of adaptive mechanisms, which ensure their survival and maintenance of stable photosynthetic performance. Photosynthesis is delicately regulated at the level of the thylakoid membrane of chloroplasts and the regulatory mechanisms include a reversible formation of a large variety of specific protein-protein complexes, supercomplexes or even larger assemblies known as megacomplexes. Revealing their structures is crucial for better understanding of their function and relevance in photosynthesis. Here we focus our attention on the isolation and a structural characterization of various large protein supercomplexes and megacomplexes, which involve Photosystem II and Photosystem I, the key constituents of photosynthetic apparatus. The photosystems are often attached to other protein complexes in thylakoid membranes such as light harvesting complexes, cytochrome b 6 f complex, and NAD(P)H dehydrogenase. Structural models of individual supercomplexes and megacomplexes provide essential details of their architecture, which allow us to discuss their function as well as physiological significance.


Photosystem I Photosystem II Clear native gel electrophoresis Electron microscopy Supercomplex Megacomplex 



This work was supported by the grant project LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I from the Ministry of Education, Youth and Sports, Czech Republic. Dr. Roman Kouřil was supported by a Marie Curie Career Integration Grant call FP7-PEOPLE-2012-CIG (322139). We acknowledge funding by the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 675006.


  1. Albanese P, Nield J, Alejandro J et al (2016) Isolation of novel PSII-LHCII megacomplexes from pea plants characterized by a combination of proteomics and electron microscopy. Photosynth Res 130(1–3):19–31PubMedCrossRefGoogle Scholar
  2. Albertsson PÅ (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6(8):349–354PubMedCrossRefGoogle Scholar
  3. Alboresi A, Caffarri S, Nogue F et al (2008) In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 3:e2033PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335PubMedCrossRefGoogle Scholar
  5. Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63PubMedCrossRefGoogle Scholar
  6. Amunts A, Toporik H, Borovikova A et al (2010) Structure determination and improved model of plant photosystem I. J Biol Chem 285:3478–3486PubMedCrossRefGoogle Scholar
  7. Aro EM, Suorsa M, Rokka A et al (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356PubMedCrossRefGoogle Scholar
  8. Baena-Gonzalez E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Phil Trans R Soc Lond B 357:1451–1460CrossRefGoogle Scholar
  9. Bailey S, Walters RG, Jansson S et al (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801PubMedCrossRefGoogle Scholar
  10. Ballottari M, Dall’Osto L, Morosinotto T et al (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958PubMedCrossRefGoogle Scholar
  11. Balsera M, Arellano JB, Revuelta JL et al (2005) The 1.49 Å resolution crystal structure of PsbQ from photosystem II of Spinacia oleracea reveals a PPII structure in the N-terminal region. J Mol Biol 350:1051–1060PubMedCrossRefGoogle Scholar
  12. Baradaran R, Berrisford JM, Minhas GS et al (2013) Crystal structure of the entire respiratory complex I. Nature 494:443–448PubMedPubMedCentralCrossRefGoogle Scholar
  13. Barera S, Pagliano C, Pape T et al (2012) Characterization of PSII-LHCII supercomplexes isolated from pea thylakoid membrane by one-step treatment with alpha- and beta-dodecyl-D-maltoside. Philos Trans R Soc Lond Ser B Biol Sci 367(1608):3389–3399CrossRefGoogle Scholar
  14. Bellafiore S, Barneche F, Peltier G et al (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895PubMedCrossRefGoogle Scholar
  15. Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269:344–346CrossRefGoogle Scholar
  16. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635PubMedCrossRefGoogle Scholar
  17. Betterle N, Ballottari M, Zorzan S et al (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284(22):15255–15266PubMedPubMedCentralCrossRefGoogle Scholar
  18. Boekema EJ, Dekker JP, van Heel MG et al (1987) Evidence for a trimeric organization of the photosystem I complex from the thermophililc cyanobacterium Synechococcus sp. FEBS Lett 217(2):283–286CrossRefGoogle Scholar
  19. Boekema EJ, Hankamer B, Bald D et al (1995) Supramolecular structure of the photosystem-II complex from green plants and cyanobacteria. Proc Natl Acad Sci U S A 92(1):175–179PubMedPubMedCentralCrossRefGoogle Scholar
  20. Boekema EJ, van Roon H, Dekker JP (1998) Specific association of photosystem II and light-harvesting complex II in partially solubilized photosystem II membranes. FEBS Lett 424:95–99PubMedCrossRefGoogle Scholar
  21. Boekema EJ, van Roon H, Calkoen F et al (1999a) Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38:2233–2239PubMedCrossRefGoogle Scholar
  22. Boekema EJ, van Roon H, van Breemen JFL et al (1999b) Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur J Biochem 266:444–452PubMedCrossRefGoogle Scholar
  23. Boekema EJ, van Breemen JFL, van Roon H et al (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301:1123–1133PubMedCrossRefGoogle Scholar
  24. Boekema EJ, Jensen PE, Schlodder E et al (2001) Green plant photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40:1029–1036PubMedCrossRefGoogle Scholar
  25. Boekema EJ, Folea M, Kouřil R (2009) Single particle electron microscopy. Photosynth Res 102:189–196PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383PubMedCrossRefGoogle Scholar
  27. Broess K, Trinkunas G, van Hoek A et al (2008) Determination of the excitation migration time in photosystem II – consequences for the membrane organization and charge separation parameters. Biochim Biophys Acta 1777:404–409PubMedCrossRefGoogle Scholar
  28. Büchel C (2015) Evolution and function of light harvesting proteins. J Plant Physiol 172:62–75PubMedCrossRefGoogle Scholar
  29. Burrows PA, Sazanov LA, Svab Z et al (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876PubMedPubMedCentralCrossRefGoogle Scholar
  30. Busch A, Hippler M (2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807:864–877PubMedCrossRefGoogle Scholar
  31. Caffarri S, Kouřil R, Kereïche S et al (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063PubMedPubMedCentralCrossRefGoogle Scholar
  32. Caffarri S, Tibiletti T, Jennings RC (2014) A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sci 15(4):296–331PubMedPubMedCentralCrossRefGoogle Scholar
  33. Calderone V, Trabucco M, Vujicić A et al (2003) Crystal structure of the PsbQ protein of photosystem II from higher plants. EMBO Rep 4(9):900–905PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chen F, Dong G, Wu L et al (2016) A nucleus-encoded chloroplast protein YL1 is involved in chloroplast development and efficient biogenesis of chloroplast ATP synthase in rice. Sci Rep 6:32295PubMedPubMedCentralCrossRefGoogle Scholar
  35. Correa-Galvis V, Poschmann G, Melzer M et al (2016) PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nat Plants 2:15225PubMedCrossRefGoogle Scholar
  36. Crepin A, Santabarbara S, Caffarri S (2016) Biochemical and spectroscopic characterization of highly stable photosystem II supercomplexes from Arabidopsis. J Biol Chem 291(36):19157–19171PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dainese P, Bassi R (1991) Subunit stoichiometry of the chloroplast photosystem-II antenna system and aggregation state of the component chlorophyll-a/b binding-proteins. J Biol Chem 266:8136–8142PubMedGoogle Scholar
  38. Daum B, Nicastro D, Austin J et al (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22:1299–1312PubMedPubMedCentralCrossRefGoogle Scholar
  39. de Bianchi S, Dall’Osto L, Tognon G et al (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 20:1012–1028PubMedPubMedCentralCrossRefGoogle Scholar
  40. Dekker JP, Boekema EJ (2005) Supermolecular organization of the thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39PubMedCrossRefGoogle Scholar
  41. Dietzel L, Bräutigam K, Steiner S et al (2011) Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in Arabidopsis. Plant Cell 23(8):2964–2977PubMedPubMedCentralCrossRefGoogle Scholar
  42. Drop B, Webber-Birungi M, Fusetti F et al (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286(52):44878–44887PubMedPubMedCentralCrossRefGoogle Scholar
  43. Drop B, Webber-Birungi M, Yadav SKN et al (2014) Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta 1837:63–72PubMedCrossRefGoogle Scholar
  44. Dudkina NV, Oostergetel GT, Braun HP et al (2010a) Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochim Biophys Acta 1797:272–277PubMedCrossRefGoogle Scholar
  45. Dudkina NV, Kouřil R, Bultema JB et al (2010b) Imaging of organelles by electron microscopy reveals protein-protein interactions in mitochondria and chloroplasts. FEBS Lett 584:2510–2515PubMedCrossRefGoogle Scholar
  46. Fernandez-Leiro R, Scheres SH (2016) Unravelling biological macromolecules with cryo-electron microscopy. Nature 537:339–346PubMedPubMedCentralCrossRefGoogle Scholar
  47. Galka P, Santabarbara S, Thi THK et al (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24:2963–2978PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gerotto C, Franchin C, Arrigoni G et al (2015) In vivo identification of photosystem II light harvesting complexes interacting with photosystem II subunit S. Plant Physiol 168:1747–1761PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hankamer B, Barber J, Boekema EJ (1997) Structure and membrane organization of photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48:641–671PubMedCrossRefGoogle Scholar
  50. Harrer R (2003) Associations between light-harvesting complexes and photosystem II from Marchantia polymorpha L. determined by two- and three-dimensional electron microscopy. Photosynth Res 75:249–258PubMedCrossRefGoogle Scholar
  51. Ifuku K, Nakatsu T, Kato H et al (2004) Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum. EMBO Rep 5(4):362–367PubMedPubMedCentralCrossRefGoogle Scholar
  52. Iwai M, Takizawa K, Tokutsu R et al (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464(7292):1210–1203PubMedCrossRefGoogle Scholar
  53. Jansson S (1994) The light–harvesting chlorophyll a/b binding-proteins. Biochim Biophys Acta 1184:1–19PubMedCrossRefGoogle Scholar
  54. Jansson S, Andersen B, Scheller HV (1996) Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol 112:409–420PubMedPubMedCentralCrossRefGoogle Scholar
  55. Jarvi S, Suorsa M, Paakkarinen V et al (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214PubMedCrossRefGoogle Scholar
  56. Järvi S, Suorse M, Aro EM (2015) Photosystem II repair in plant chloroplasts – regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim Biophys Acta 1847:900–909PubMedCrossRefGoogle Scholar
  57. Jensen PE, Rosgaard L, Knoetzel J et al (2002) Photosystem I activity is increased in the absence of the PSI-G subunit. J Biol Chem 277(4):2798–2803PubMedCrossRefGoogle Scholar
  58. Johnson MP, Goral TK, Duffy CD et al (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23(4):1468–1479PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jordan P, Fromme P, Witt HT et al (2001) Three-dimensional structure of photosystem I at 2.5 Å resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  60. Kirchhoff H (2013) Architectural switches in plant thylakoid membranes. Photosynth Res 116:481–487PubMedCrossRefGoogle Scholar
  61. Kirchhoff H, Haase W, Wegner S et al (2007) Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplasts. Biochemistry 46:11169–11176PubMedCrossRefGoogle Scholar
  62. Kirchhoff H, Lenhert S, Büchel C et al (2008) Probing the organization of photosystem II in photosynthetic membranes by atomic force microscopy. Biochemistry 47:431–440PubMedCrossRefGoogle Scholar
  63. Klimmek F, Sjodin A, Noutsos C et al (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140:793–804PubMedPubMedCentralCrossRefGoogle Scholar
  64. Knispel RW, Kofler C, Boicu M et al (2012) Blotting protein complexes from native gels to electron microscopy grids. Nat Methods 9:182–184PubMedCrossRefGoogle Scholar
  65. Kofer W, Koop HU, Wanne G et al (1998) Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol Gen Genet 258:166–173PubMedCrossRefGoogle Scholar
  66. Kouřil R, van Oosterwijk N, Yakushevska AE et al (2005a) Photosystem I: a search for green plant trimers. Photochem Photobiol Sci 4:1091–1094PubMedCrossRefGoogle Scholar
  67. Kouřil R, Zygadlo A, Arteni AA et al (2005b) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940PubMedCrossRefGoogle Scholar
  68. Kouřil R, Oostergetel GT, Boekema EJ (2011) Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta 1807:368–374PubMedCrossRefGoogle Scholar
  69. Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12PubMedCrossRefGoogle Scholar
  70. Kouřil R, Wientjes E, Bultema JB et al (2013) High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta 1827:411–419PubMedCrossRefGoogle Scholar
  71. Kouřil R, Strouhal O, Nosek L et al (2014) Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J 77:568–576PubMedCrossRefGoogle Scholar
  72. Kouřil R, Nosek L, Bartoš J et al (2016) Evolutionary loss of light-harvesting proteins Lhcb6 and Lhcb3 in major land plant groups – break-up of current dogma. New Phytol 210:808–814PubMedCrossRefGoogle Scholar
  73. Kovacs L, Damkjær J, Kereïche S (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120PubMedPubMedCentralCrossRefGoogle Scholar
  74. Koziol AG, Borza T, Ishida KI et al (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kramer DM, Avenson TJ, Edwards GE (2004) Dynamics flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357PubMedCrossRefGoogle Scholar
  76. Krauss N, Schubert WD, Klukas O et al (1996) Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nat Struct Biol 3(11):965–973PubMedCrossRefGoogle Scholar
  77. Kurisu G, Zhang H, Smith JL et al (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014PubMedCrossRefGoogle Scholar
  78. Li XP, BjörkmanO Shich C et al (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395Google Scholar
  79. Liu Z, Yan H, Wang K et al (2004) Crystal structure of spinach light-harvesting complex at 2.72 Å resolution. Nature 428:287–292PubMedCrossRefGoogle Scholar
  80. Lunde C, Jensen PE, Haldrup A et al (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408:613–615PubMedCrossRefGoogle Scholar
  81. Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 Å resolution. Elife 4:e07433PubMedPubMedCentralCrossRefGoogle Scholar
  82. Minagawa J (2011) State transitions – the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807:897–905PubMedCrossRefGoogle Scholar
  83. Morosinotto T, Bassi R, Frigerio S et al (2006) Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barely. Consequences of a chronic over-reduction of the plastoquinone pool. FEBS J 273:4616–4630PubMedCrossRefGoogle Scholar
  84. Munekage Y, Hashimoto M, Miyake C et al (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582PubMedCrossRefGoogle Scholar
  85. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Ann Rev Plant Biol 57:521–565CrossRefGoogle Scholar
  86. Nield J, Barber J (2006) Refinement of the structural model for the photosystem II supercomplex of higher plants. Biochim Biophys Acta 1757:353–361PubMedCrossRefGoogle Scholar
  87. Nield J, Orlova EV, Morris EP et al (2000) 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 7(1):44–47PubMedCrossRefGoogle Scholar
  88. Nosek L, Semchonok D, Boekema EJ et al (2017) Structural variability of plant photosystem II megacomplexes in thylakoid membranes. Plant J 89:104–111PubMedCrossRefGoogle Scholar
  89. Pagliano C, Barera S, Chimirri F et al (2012) Comparison of the alpha and beta isomeric forms of the detergent n-dodecyl-D-maltoside for solubilizing photosynthetic complexes from pea thylakoid membranes. Biochim Biophys Acta 1817:1506–1515PubMedCrossRefGoogle Scholar
  90. Pagliano C, Saracco G, Barber J (2013) Structural, functional and auxiliary proteins of photosystem II. Photosynth Res 116:167–188PubMedCrossRefGoogle Scholar
  91. Pagliano C, Nield J, Marsano F et al (2014) Proteomic characterization and three-dimensional electron microscopy study of PSII-LHCII supercomplexes from higher plants. Biochim Biophys Acta 1837:1454–1462PubMedCrossRefGoogle Scholar
  92. Pan X, Li M, Wan T et al (2011) Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat Struct Mol Biol 18:309–315PubMedCrossRefGoogle Scholar
  93. Peng LW, Shikanai T (2011) Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol 155:1629–1639PubMedPubMedCentralCrossRefGoogle Scholar
  94. Peng LW, Shimizu H, Shikanai T (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J Biol Chem 283:34873–34879PubMedPubMedCentralCrossRefGoogle Scholar
  95. Peng LW, Fukao Y, Fujiwara M et al (2009) Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21:3623–3640PubMedPubMedCentralCrossRefGoogle Scholar
  96. Peter GF, Thornber JP (1991) Biochemical-composition and organization of higher-plant photosystem-II light-harvesting pigment-proteins. J Biol Chem 266:16745–16754PubMedGoogle Scholar
  97. Pribil M, Pesaresi P, Hertle A et al (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8:e1000288PubMedPubMedCentralCrossRefGoogle Scholar
  98. Qin X, Suga M, Kuang T et al (2015) Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348(6238):989–995PubMedCrossRefGoogle Scholar
  99. Schubert WD, Klukas O, Krauss N et al (1997) Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysis. J Mol Biol 272(5):741–769PubMedCrossRefGoogle Scholar
  100. Semchonok DA, Li M, Bruce BD et al (2016) Cyro-EM structure of a tetrameric cyanobacterial photosystem I complex reveals novel subunit interactions. Biochim Biophys Acta 1857:1619–1626PubMedCrossRefGoogle Scholar
  101. Shapiguzov A, Ingelsson B, Samol I et al (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci U S A 107:4782–4787PubMedPubMedCentralCrossRefGoogle Scholar
  102. Shikanai T (2016) Chloroplast NDH: a different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochim Biophys Acta 1857:1015–1022PubMedCrossRefGoogle Scholar
  103. Shikanai T, Endo T, Hashimoto T et al (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci U S A 95:9705–9709PubMedPubMedCentralCrossRefGoogle Scholar
  104. Standfuss R, van Scheltinga ACT, Lamborghini M et al (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light harvesting complex at 2.5 Å resolution. EMBO J 24:919–928PubMedPubMedCentralCrossRefGoogle Scholar
  105. Stroebel D, Choquet Y, Popot JL et al (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418PubMedCrossRefGoogle Scholar
  106. Tietz S, Puthiyaveetil S, Enlow HM et al (2015) Functional implications of photosystem II crystal formation in photosynthetic membranes. J Biol Chem 290:14091–14106PubMedPubMedCentralCrossRefGoogle Scholar
  107. Tokutsu R, Kato N, Bui KH et al (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581PubMedPubMedCentralCrossRefGoogle Scholar
  108. van Oort B, Alberts M, de Bianchi S et al (2010) Effect of antenna-depletion in photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophys J 98:922–931PubMedPubMedCentralCrossRefGoogle Scholar
  109. van Roon H, van Breemen JFL, de Werd FL et al (2000) Solubilization of green plant thylakoid membranes with n-dodecyl-α,D-maltoside. Implications for the structural organization of the photosystem II, photosystem I, ATP synthase and cytochrome b 6 f complexes. Photosynth Res 64:155–166PubMedCrossRefGoogle Scholar
  110. Varotto C, Pesaresi P, Jahns P et al (2002) Single and double knockouts of the genes for photosystem I subunits G, K, and H of Arabidopsis. Effects on photosystem I composition, photosynthetic electron flow, and state transitions. Plant Physiol 129:616–624PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wei X, Su X, Cao P et al (2016) Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature 534(7605):69–74PubMedCrossRefGoogle Scholar
  112. Wientjes E, Oostergetel GT, Jansson S et al (2009) The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J Biol Chem 284:7803–7810PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wientjes E, Drop B, Kouřil R et al (2013) During state 1 to state 2 transition in Arabidopsis thaliana, the photosystem II supercomplex gets phosphorylated but does not disassemble. J Biol Chem 288:32821–32826PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wittig I, Schägger H (2005) Advantages and limitations of clear-native PAGE. Proteomics 5:4338–4346PubMedCrossRefGoogle Scholar
  115. 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 6:1215–1225PubMedCrossRefGoogle Scholar
  116. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630PubMedPubMedCentralCrossRefGoogle Scholar
  117. Yadav KNS, Semchonok DA, Nosek L et al (2017) Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH. Biochim Biophys Acta 1858:12–20PubMedCrossRefGoogle Scholar
  118. Yakushevska AE, Jensen PE, Keegstra W et al (2001a) Supermolecular organization of photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana. Eur J Biochem 268:6020–6021PubMedCrossRefGoogle Scholar
  119. Yakushevska AE, Ruban AV, Jensen PE et al (2001b) Supermolecular organization of photosystem II and its associated light-harvesting antenna in the wild- type and npq4 mutant of Arabidopsis thaliana. In: PS2001 proceedings: 12th international congress on photosynthesis. CSIRO Publishing, Melbourne, p S5Google Scholar
  120. Yakushevska AE, Keegstra W, Boekema EJ et al (2003) The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42:806–813CrossRefGoogle Scholar
  121. Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106PubMedCrossRefGoogle Scholar
  122. Yokono M, Takabayashi A, Akimoto S et al (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Roman Kouřil
    • 1
    Email author
  • Lukáš Nosek
    • 1
  • Dmitry Semchonok
    • 2
  • Egbert J. Boekema
    • 2
  • Petr Ilík
    • 1
  1. 1.Department of Biophysics, Faculty of Science, Centre of the Region Haná for Biotechnological and Agricultural ResearchPalacký UniversityOlomoucCzech Republic
  2. 2.Electron Microscopy Group, Groningen Biomolecular Sciences and Biotechnology InstituteUniversity of GroningenGroningenThe Netherlands

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