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Architectural switches in plant thylakoid membranes

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Abstract

Recent progress in elucidating the structure of higher plants photosynthetic membranes provides a wealth of information. It allows generation of architectural models that reveal well-organized and complex arrangements not only on whole membrane level, but also on the supramolecular level. These arrangements are not static but highly responsive to the environment. Knowledge about the interdependency between dynamic structural features of the photosynthetic machinery and the functionality of energy conversion is central to understanding the plasticity of photosynthesis in an ever-changing environment. This review summarizes the architectural switches that are realized in thylakoid membranes of green plants.

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References

  • Albertsson PA (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6:349–354

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2003) State transitions—a question of balance. Science 299:1530–1532

    Article  PubMed  CAS  Google Scholar 

  • Amunts A, Nelson N (2008) Functional organization of plant Photosystem I: evolution of a highly efficient photochemical machine. Plant Physiol Biochem 46:228–237

    Article  PubMed  CAS  Google Scholar 

  • Anderson JM (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Structure-function of the Cytochrome b6f complex. Photochem Photobiol 84:1349–1358

    Article  PubMed  CAS  Google Scholar 

  • Barros T, Royant A, Standfuss J, Dreuw A, Kühlbrandt W (2009) Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J 28:298–306

    Article  PubMed  CAS  Google Scholar 

  • 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 284:15255–15266

    Article  PubMed  CAS  Google Scholar 

  • Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063

    Article  PubMed  CAS  Google Scholar 

  • Chow WS (1999) Grana formation: entropy-assisted local order in chloroplasts? Aust J Plant Physiol 26:641–647

    Article  CAS  Google Scholar 

  • Daum B, Kühlbrandt W (2011) Electron tomography of plant thylakoid membranes. J Exp Bot 62:2393–2402

    Article  PubMed  CAS  Google Scholar 

  • Daum B, Nicastro D, Austin J II, McIntosh R, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22:1299–1312

    Article  PubMed  CAS  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    Article  PubMed  CAS  Google Scholar 

  • Ettinger FE, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca++/H+ antiport in plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1385

    Article  PubMed  CAS  Google Scholar 

  • Fristed R, Willig A, Granath P, Crèvecoeur M, Rochaix J-D, Vener AV (2009) Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21:3950–3964

    Article  Google Scholar 

  • Fristed R, Granath P, Vener AV (2010) A protein phosphorylation threshold for functional stacking of plant photosynthetic membranes. PLoS ONE 5:e10963

    Article  Google Scholar 

  • Garber MP, Steponkus PL (1976) Alterations in chloroplast thylakoids during cold acclimation. Plant Physiol 57:681–686

    Article  PubMed  CAS  Google Scholar 

  • Goodchild DJ, Björkman O, Pyliotis NA (1972) Chloroplast ultrastructure, leaf anatomy, and soluble protein in rainforest species. Carnegie Inst Wash Yearb 71:102–107

    Google Scholar 

  • Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289–301

    Article  PubMed  CAS  Google Scholar 

  • Herbstová M, Tietz S, Kinzel C, Turkina MV, Kirchhoff H (2012) Architectural switch in plant photosynthetic membranes induced by light stress. Proc Natl Acad Sci USA 109:20130–20135

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    Article  PubMed  CAS  Google Scholar 

  • Johnson MP, Goral TK, Duffy CD, Brain AP, 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  CAS  Google Scholar 

  • Junge W, Sielaff H, Engelbrecht S (2009) Torque generation and elastic power transmission in the rotary FoF1-ATPase. Nature 459:364–370

    Article  PubMed  CAS  Google Scholar 

  • Kargul J, Barber J (2008) Photosynthetic acclimation: structural reorganization of light harvesting-antenna – role of redox-dependent phosphorylation of major and minor chlorophyll a/b binding proteins. FEBS Lett 275:1056–1068

    CAS  Google Scholar 

  • Kereïche S, Kiss AZ, Kouril R, Boekema E, Horton P (2010) The PsbS protein controls the macro-organization of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:754–764

    Article  Google Scholar 

  • Khatoon M, Inagawa K, Pospísil P, Yamashita A, Yoshioka M, Lundin B, Horie J, Morita N, Jajoo A, Yamamoto Y, Yamamoto Y (2009) Quality control of photosystem II. J Biol Chem 284:2543–2552

    Article  Google Scholar 

  • Kirchhoff H (2013) Structural constraints for protein repair in plant photosynthetic membranes. Plant Signal Behav 8(4):e23634

    Google Scholar 

  • Kirchhoff H, Haase W, Wegner S, Danielsson R, Ackermann R, Albertsson PA (2007) Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplasts. Biochem 46:11169–11176

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kleine T, Voigt C, Leister D (2009) Plastid signaling to the nucleus: messengers still lost in the mists? Trends Gen 25:185–192

    Article  CAS  Google Scholar 

  • Kley J, Schmidt B, Boyanov B, Stolt-Berger PC, Kirk R, Ehrmann M, Knopf RR, Naveh L, Adam Z, Clausen T (2011) Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat Struct Mol Biol 18:728–731

    Article  PubMed  CAS  Google Scholar 

  • Kouřil R, Oostergetel GT, Boekema EJ (2011) Fine structure of grana thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta 1807:368–374

    Article  PubMed  Google Scholar 

  • Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12

    Article  PubMed  Google Scholar 

  • Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid protein gradient. Trends Plant Sci 8:27–32

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosy Res 98:551–564

    Article  CAS  Google Scholar 

  • Kyle DJ, Staehelin LA, Arntzen CJ (1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222:527–541

    Article  PubMed  CAS  Google Scholar 

  • Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 181:4070–4074

    Article  Google Scholar 

  • Lemeille S, Rochaix JD (2010) State transition at the crossroad of thylakoid signaling pathways. Photosyn Res 106:33–46

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  PubMed  CAS  Google Scholar 

  • Marr KM, McFeeters RL, Lyon MK (1996) Isolation and structural anaylsis of two-dimensional crystals of photosystem II from Hordeum viridis zb. J Struct Biol 117:86–98

    Article  PubMed  CAS  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • Miller KR, Miller GJ, McIntyre KR (1976) The light-harvesting chlorophyll-protein complex of photosystem II. J Cell Biol 71:624–638

    Article  PubMed  CAS  Google Scholar 

  • Mullet JE (1983) The amino acid sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts. J Biol Chem 258:9941–9948

    PubMed  CAS  Google Scholar 

  • Mulo P, Sirpio S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosyn Res 98:489–501

    Article  PubMed  CAS  Google Scholar 

  • Nevo R, Charuvi D, Tsabari O, Reich Z (2012) Composition, architecture and dynamics of the photosynthetic apparatus in higher plants. Plant J 70(1):157–176

    Article  PubMed  CAS  Google Scholar 

  • Nield J, Barber J (2006) Refinement of the structural model for the photosystem II supercomplex of higher plants. Biochim Biophys Acta 1757:353–361

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes. J Cell Biol 99:481–485

    Article  PubMed  CAS  Google Scholar 

  • Pfalz J, Liebers M, Hirth M, Grübler B, Holtzegel U, Schröter Y, Dietzel L, Pfannschmidt T (2012) Environmental control of plant nuclear gene expression by chloroplast redox signals. Frontier Plant Sci. doi:10.3389/fpls.2012.00257

    Google Scholar 

  • Puthiyaveetil S, Ibrahim IM, Jelicić B, Tomasić A, Fulgosi H, Allen JF (2010) Transcriptional control of photosynthesis genes: the evolutionary conserved regulatory mechanism in plastid genome function. Genome Biol Evol 2:888–896

    Article  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CD (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    Article  PubMed  CAS  Google Scholar 

  • Schönknecht G, Hedrich R, Junge W, Raschke K (1988) A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant. Nature 336:589–592

    Article  Google Scholar 

  • Schuhmann H, Adamska I (2012) Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. Physiol Plant 145:224–234

    Article  PubMed  CAS  Google Scholar 

  • Semenova GA (1995) Particle regularity on thylakoid fracture faces is influenced by storage conditions. Can J Bot 73:1676–1682

    Article  Google Scholar 

  • Simpson DJ (1978) Freeze-fracture studies on barley plastid membranes II. Wild-type chloroplasts. Carlsberg Res Commun 43:365–389

    Article  Google Scholar 

  • Spetea C, Schoefs B (2010) Solute transporter in plant thylakoid membranes. Commun Integr Biol 3:122–129

    Article  PubMed  Google Scholar 

  • Staehelin LA (1986) Chloroplast structure and supramolecular organization of photosynthetic membranes. In: Staehelin LA, Arntzen CJ (eds) Photosynthesis III: photosynthetic membranes and light-harvesting systems. Springer-Verlag, Berlin, pp 1–84

    Google Scholar 

  • Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–61

    Article  PubMed  CAS  Google Scholar 

  • Wagner R, Aigner H, Funk C (2012) FtsH proteases located in the plant chloroplast. Physiol Plant 145:203–214

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Our research is supported by grants from the National Science Foundation (NSF-MCB115871), the United States-Israel Binational Agricultural Research and Development Fund (BARD US-4334-10), the US Department of Agriculture (ARC grant WNP00775), and Washington State University.

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  1. Institute of Biological Chemistry, Washington State University, Pullman, WA, USA

    Helmut Kirchhoff

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  1. Helmut Kirchhoff
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Correspondence to Helmut Kirchhoff.

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Kirchhoff, H. Architectural switches in plant thylakoid membranes. Photosynth Res 116, 481–487 (2013). https://doi.org/10.1007/s11120-013-9843-0

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