Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Visualizing the dynamic structure of the plant photosynthetic membrane

Nature Plants volume 1, Article number: 15161 (2015) Cite this article

Subjects

Abstract

The chloroplast thylakoid membrane is the site for the initial steps of photosynthesis that convert solar energy into chemical energy, ultimately powering almost all life on earth. The heterogeneous distribution of protein complexes within the membrane gives rise to an intricate three-dimensional structure that is nonetheless extremely dynamic on a timescale of seconds to minutes. These dynamics form the basis for the regulation of photosynthesis, and therefore the adaptability of plants to different environments. High-resolution microscopy has in recent years begun to provide new insights into the structural dynamics underlying a number of regulatory processes such as membrane stacking, photosystem II repair, photoprotective energy dissipation, state transitions and alternative electron transfer. Here we provide an overview of the essentials of thylakoid membrane structure in plants, and consider how recent advances, using a range of microscopies, have substantially increased our knowledge of the thylakoid dynamic structure. We discuss both the successes and limitations of the currently available techniques and highlight newly emerging microscopic methods that promise to move the field beyond the current ‘static’ view of membrane organization based on frozen snapshots to a ‘live’ view of functional membranes imaged under native aqueous conditions at ambient temperature and responding dynamically to external stimuli.

The plant chloroplast thylakoid is the site of the photosynthetic electron transfer chain that converts absorbed solar energy into chemical energy in the form of ATP and NADPH mainly for use in CO2 fixation (for a recent review see ref. 1). The thylakoid is one of the most complex biological structures in nature, forming a continuous three-dimensional membrane structure consisting of stacked regions (grana) interconnected by unstacked regions (stromal lamellae); together these enclose a single aqueous compartment, the lumen. Because the early steps of photosynthesis depend upon excitation energy as well as electron and proton transfers (all of which have distinct distance dependencies), the organization of the macromolecular protein complexes within the thylakoid is a critical determinant of their function. The thylakoid membrane shows a hierarchical organization in which individual proteins assemble into complexes, which in turn form looser associations in ‘supercomplexes’ that further organize themselves into distinct domains within the membrane leading to a lateral heterogeneity. This organization has been honed by evolution to improve the efficiency of these energy- and electron-transfer processes while simultaneously offering the flexibility to allow the protein components to be dynamically redistributed, such that the plant can perform vital self-protective and repair processes that enable rapid responses to its environment. Hence, knowledge of the structure and dynamics of the thylakoid membrane is crucial to the understanding of its multiple functions.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure of the plant chloroplast thylakoid membrane.
Figure 2: Dynamics in thylakoid structure associated with unstacking and state transitions.
Figure 3: Dynamics of PSII and LHCII organization associated with photoprotective energy dissipation (qE) in plants.
Figure 4: Dynamics of PSII organization and lumen expansion associated with possible regulation of electron transfer in plants.

References

  1. Nelson, N. & Ben-Shem, A. The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell. Biol. 5, 971–982 (2004).

    Article  CAS  PubMed  Google Scholar 

  2. Kausche, G. A. & Ruska, H. Zur Frage der Chloroplastenstruktur. Naturwissenschaften 28, 303–304 (1940).

    CAS  Google Scholar 

  3. Gibbs, S. P. The fine structure of Euglena gracilis with special reference to the chloroplasts and pyrenoids. J. Ultrastruct. Res. 4, 127–148 (1960).

    Article  Google Scholar 

  4. Menke, W. Structure and chemistry of plastids. Annu. Rev. Plant. Physiol. 13, 27–44 (1962).

    Article  Google Scholar 

  5. Shimoni, E., Rav-Hon, O., Ohad, I., Brumfeld, V. & Reich, Z. Three-dimensional organisation of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17, 2580–2586 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Austin, J. R. II & Staehelin, L. A. Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol. 155, 1601–1611 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Paolillo, D. J. The three dimensional arrangement of intergranal lamellae in chloroplasts. J. Cell Sci. 6, 243–255 (1970).

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Anderson, J. M. & Andersson, B. The architecture of photosynthetic membranes: lateral and transverse organization. Trends Biochem. Sci. 7, 288–292 (1982).

    Article  CAS  Google Scholar 

  11. Albertsson, P.-Å. A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6, 349–354 (2001).

    Article  CAS  PubMed  Google Scholar 

  12. Dekker, J. P. & Boekema, E. J. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706, 12–39 (2005).

    Article  CAS  PubMed  Google Scholar 

  13. Olive, J. & Vallon, O. Structural organization of the thylakoid membrane: Freeze-fracture and immunocytochemical analysis. J. Electron Micr. Tech. 18, 360–374 (1991).

    Article  CAS  Google Scholar 

  14. Staehelin, L. A. Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth. Res. 76, 185–196 (2003).

    Article  CAS  PubMed  Google Scholar 

  15. Goral, T. K. et al. Light-harvesting antenna composition controls the macromolecular organization and dynamics of thylakoid membranes in Arabidopsis. Plant J. 69, 289–301 (2012).

    Article  CAS  PubMed  Google Scholar 

  16. Boekema, E. J., van Breemen, J. F. L., van Roon, H. & Dekker, J. P. Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J. Mol. Biol. 301, 1123–1133 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Boekema, E. J., van Roon, H., Calkoen, F., Bassi, R. & Dekker, J. P. Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38, 2233–2239 (1999).

    Article  CAS  PubMed  Google Scholar 

  18. Staehelin, L. A. Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J. Cell Biol. 71, 136–158 (1976).

    Article  CAS  PubMed  Google Scholar 

  19. Kouřil, R., Oostergetel, G. T. & Boekema, E. J. Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim. Biophys. Acta 1807, 368–374 (2011).

    Article  PubMed  CAS  Google Scholar 

  20. Sznee, K. et al. Jumping mode atomic force microscopy on grana membranes from spinach. J. Biol. Chem. 286, 39164–39171 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Johnson, M. P., Vasilev, C., Olsen, J. D. & Hunter, C. N. Nanodomains of cytochrome b6f and photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26, 3051–3061 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Phuthong, W. et al. The use of contact mode atomic force microscopy in aqueous medium for structural analysis of spinach photosynthetic complexes. Plant Physiol. 169, 1318–1332 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Vasilev, C. et al. Nano-mechanical mapping of the interactions between surface-bound RC-LH1-PufX core complexes and cytochrome c2 attached to an AFM probe. Photosynth. Res. 120, 169–180 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. van Roon, H., van Breemen, J. F. L., de Weerd, F. L., Dekker, J. P. & Boekema, E. J. 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 b6f complexes. Photosynth. Res. 64, 155–166 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Boekema, E. J., Jensen, P. E., Schlodder, E., van Breemen, J. F. L., van Roon, H., Scheller, H. V. & Dekker, J. P. Green plant photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40, 1029–1036 (2001).

    Article  CAS  PubMed  Google Scholar 

  26. Kouřil, R. et al. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44, 10935–10940 (2005).

    Article  PubMed  CAS  Google Scholar 

  27. Kouřil, R. et al. Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J. 77, 568–576 (2014).

    Article  PubMed  CAS  Google Scholar 

  28. Bell, A. J., Frankel, L. K. & Bricker, T. M. High yield non-detergent isolation of photosystem I-light harvesting chlorophyll II membranes from spinach thylakoids: implications for the organization of the PSI antennae in higher plants. J. Biol. Chem. 290, 18429–18437 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Peng, L., Fukao, Y., Fujiwara, M., Takami, T. & Shikanaia, T. Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21, 3623–3640 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Armbuster, U. et al. Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25, 2661–2678 (2013).

    Article  CAS  Google Scholar 

  31. Wollenberger, L., Stefansson, H., Yu, S. G. & Albertsson, P. A. Isolation and characterization of vesicles originating from the chloroplast grana margins. Biochim. Biophys. Acta 1184, 93–102 (1994).

    Article  CAS  Google Scholar 

  32. Puthiyaveetil, S. et al. Compartmentalization of the protein repair machinery in photosynthetic membranes. Proc. Natl Acad. Sci. USA 111, 15839–15844 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Grieco, M., Suorsa, M., Jajoo, A., Tikkanen, M. & Aro, E. M. Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery - including both photosystems II and I. Biochim. Biophys. Acta 1847, 607–619 (2015).

    Article  CAS  PubMed  Google Scholar 

  34. Anderson, J. M., Horton, P., Kim, E.-H. & Chow, W. S. Towards elucidation of dynamic structural changes of plant thylakoid architecture. Phil. Trans. Roy. Soc. London 367, 3515–3524 (2012).

    Article  CAS  Google Scholar 

  35. Izawa, S. & Good, N. E. Effects of salts and electron transport on the conformation of isolated chloroplasts. II. Electron microscopy. Plant Physiol. 41, 544–552 (1966).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Barber, J. Influence of surface charges on thylakoid structure and function. Ann. Rev. Plant Physiol. 33, 261–295 (1982).

    Article  CAS  Google Scholar 

  37. Kim, E. H., Chow, W. S., Horton, P. & Anderson, J. M. Entropy-assisted stacking of thylakoid membranes. Biochim. Biophys. Acta 1708, 187–195 (2005).

    Article  CAS  PubMed  Google Scholar 

  38. Murakami, S. & Packer, L. The role of cations in the organization of chloroplast membranes. Arch. Biochem. Biophys. 146, 337–347 (1971).

    Article  CAS  PubMed  Google Scholar 

  39. Rubin, B. T., Chow, W. S. & Barber, J. Experimental and theoretical considerations of mechanisms controlling cation effects on thylakoid membrane stacking and chlorophyll fluorescence. Biochim. Biophys. Acta 634, 174–190 (1981).

    Article  CAS  PubMed  Google Scholar 

  40. Kaftan, D., Brumfeld, V., Nevo, R., Scherz, A. & Reich, Z. From chloroplasts to photosystems: In situ scanning force microscopy on intact thylakoid membranes. EMBO J. 21, 6146–6153 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rumak, I. et al. 3-D modelling of chloroplast structure under (Mg2+) magnesium ion treatment. Relationship between thylakoid membrane arrangement and stacking. Biochim. Biophys. Acta 1797, 1736–1748 (2010).

    Article  CAS  PubMed  Google Scholar 

  42. Emerson, R. & Arnold, W. The photochemical reaction in photosynthesis. J. Gen. Physiology 16, 191–205 (1932).

    Article  CAS  Google Scholar 

  43. Haldrup, A., Jensen, P. E., Lunde, C. & Scheller, H. V. Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci. 6, 301–305 (2001).

    Article  CAS  PubMed  Google Scholar 

  44. Wollman, F. A. State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20, 3623–3630 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ruban, A. V. & Johnson, M. P. Dynamics of the photosystems cross-section associated with the state transitions in higher plants. Photosynth. Res. 99, 173–183 (2009).

    Article  CAS  PubMed  Google Scholar 

  46. Horton, P. & Black, M. T. Activation of adenosine 5′-triphosphate induced quenching of chlorophyll fluorescence by reduced plastoquinone. The basis of state I–state II transitions in chloroplasts. FEBS Lett. 119, 141–144 (1980).

    Article  CAS  Google Scholar 

  47. Allen, J. F., Bennett, J., Steinback, K. E. & Arntzen, C. J. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291, 25–29 (1981).

    Article  CAS  Google Scholar 

  48. Bellafiore S., Barneche F., Peltier G. & Rochaix J.-D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892–895 (2005).

    Article  CAS  PubMed  Google Scholar 

  49. Galka P. et al. 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, 2963–2978 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Iwai, M., Pack, C., Takenaka, Y., Sako, Y. & Nakano, A. Photosystem II antenna phosphorylation-dependent protein diffusion determined by fluorescence correlation spectroscopy. Sci. Rep. 3, 2833 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Iwai, M., Yokono, M., Inada, N. & Minagawa, J. Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc. Natl Acad. Sci. USA 107, 2337–2342 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R. & Leister, D. Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Shapiguzov, A. et al. The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc. Natl Acad. Sci. USA. 107, 4782–4787 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kyle, D. J., Staehelin, L. A. & Arntzen, C. J. Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch. Biochem. Biophys. 222, 527–541 (1983).

    Article  CAS  PubMed  Google Scholar 

  55. Vallon, O. et al. Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc. Natl Acad. Sci. USA 88, 8262–8266 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Rozak, P. R., Seiser, R. M., Wacholtz, W. F. & Wise, R. R. Rapid, reversible alterations in spinach thylakoid appression upon changes in light intensity. Plant Cell Environ. 25, 421–429 (2002).

    Article  Google Scholar 

  57. Chuartzman, S. G. et al. Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20, 1029–1039 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Hasegawa, M., Shiina, T., Terazima, M. & Kumazaki, S. Selective excitation of photosystems in chloroplasts inside plant leaves observed by near-infrared laser-based fluorescence spectral microscopy. Plant Cell Physiol. 51, 225–238 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Kim, E., Ahn, T. K. & Kumazak, S. Changes in antenna sizes of photosystems during state transitions in granal and stroma-exposed thylakoid membrane of intact chloroplasts in Arabidopsis mesophyll protoplasts. Plant Cell Physiol. 56, 759–768 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Tikkanen, M. et al. Phosphorylation-dependent regulation of excitation energy distribution between the two photosystems in higher plants. Biochim. Biophys. Acta 1777, 425–432 (2008).

    Article  CAS  PubMed  Google Scholar 

  62. Mekala, N. R., Suorsa, M., Rantala, M., Aro, E. M. & Tikkanen M. Plants actively avoid state-transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light. Plant Physiol. 168, 721–734 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Goral . et al. Visualising the mobility and distribution of chlorophyll-proteins in higher plant thylakoid membranes: effects of photoinhibition and protein phosphorylation. Plant J. 62, 948–959 (2010).

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  65. Holt, N. E., Fleming, G. R. & Niyogi, K. K. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43, 8281–8289 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Ruban, A. V., Johnson, M. P. & Duffy, C. D. P. Photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta 1817, 167–181 (2012).

    Article  CAS  PubMed  Google Scholar 

  67. Johnson, M. P. et al. Photoprotective energy dissipation involves the reorganization of photosystem II light harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23, 1468–1479 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Horton P. et al. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll–protein complex. FEBS Lett. 292, 1–4 (1991).

    Article  CAS  PubMed  Google Scholar 

  69. Betterle, N. et al. Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284, 15255–15266 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kiss, A., Crouchman, S., Ruban, A. V. & Horton, P. The PsbS protein controls the organisation of the photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem. 283, 3972–3978 (2008).

    Article  CAS  PubMed  Google Scholar 

  71. Belgio, E., Johnson, M. P., Jurić, S. & Ruban, A. V. Higher plant photosystem II light harvesting antenna, not the reaction center, determines the excited state lifetime—both the maximum and the non-photochemically quenched. Biophys. J. 102, 2761–2771 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Belgio, E., Ungerer, P. & Ruban, A. V. Light harvesting superstructures of green plant chloroplasts lacking photosystems. Plant Cell Env. 38, 2035‐2047 (2015).

    Article  CAS  Google Scholar 

  73. Ware, M. A., Giovagnetti, V., Belgio, E. & Ruban, A. V. PsbS protein modulates non-photochemical chlorophyll fluorescence quenching in membranes depleted from photosystems. J. Photochem. Photobiol. Bhttp://dx.doi.org/10.1016/j.jphotobiol.2015.07.016 (2015).

  74. Haferkamp, S., Haase, W., Pascal, A. A., van Amerongen, H. & Kirchhoff, H. Efficient light harvesting by photosystem II requires an optimized protein packing density in grana thylakoids. J. Biol. Chem. 285, 17020–17028 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kirchhoff, H., Tremmel, I., Haase, W. & Kubitscheck, U. Supramolecular photosystem II organization in grana thylakoid membranes: Evidence for a structured arrangement. Biochemistry 43, 9204–9213 (2004).

    Article  CAS  PubMed  Google Scholar 

  76. Blackwell, M. F., Gibas, C., Gygax, S., Roman, D. & Wagner B. The plastoquinone diffusion coefficient in chloroplasts and its mechanistic implications. Biochim. Biophys. Acta. 1183, 533–543 (1994).

    Article  CAS  Google Scholar 

  77. Tremmel, I. G., Kirchhoff, H., Weis, E. & Farquhar, G.D. Dependence of plastoquinol diffusion on the shape, size, and density of integral proteins. Biochim. Biophys. Acta 1607, 97–109 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. Joliot, P., Lavergne, J. & Béal, D. Plastoquinone compartmentation in chloroplasts. I. Evidence for domains with different rates of photo-reduction. Biochim. Biophys. Acta 1101, 1–12 (1992).

    Article  CAS  Google Scholar 

  79. Kirchhoff, H., Horstmann, S. & Weis, E. Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim. Biophys. Acta 1459, 148–168 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. de Bianchi, S., Dall'Osto, L., Tognon, G., Morosinotto, T. & Bassi, R. 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, 1012–1028 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Kovacs, L. et al. Lack of the light harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18, 3106–3120 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Tietz, S. et al. Functional implications of photosystem II crystal formation in photosynthetic membranes. J. Biol. Chem. 290, 14091–14106 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kirchhoff, H. et al. Dynamic control of protein diffusion within the granal thylakoid lumen. Proc. Natl Acad. Sci. USA 108, 20248–20253 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Murakami, S. & Packer, L. Light-induced changes in the conformation and configuration of the thylakoid membrane of Ulva and Porphyra chloroplasts in vivo. Plant Physiol. 45, 289–299 (1970).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Danielsson, R., Albertsson, P. Å., Mamedov, F. & Styring, S. Quantification of photosystem I and II in different parts of the thylakoid membrane from spinach. Biochim. Biophys. Acta 1608, 53–61 (2004).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

A.V.R. would like to acknowledge The Royal Society for the Wolfson Research Merit Award. M.P.J. acknowledges funding from the Leverhulme Trust, the Krebs Institute, University of Sheffield and Project Sunshine, University of Sheffield. We would like to acknowledge Prof. N. Hunter FRS for the critical reading of the manuscript. This work is dedicated to the memory of Prof. Jan Anderson FRS.

Author information

Authors and Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary, University of London, Mile End Road, London, E1 4NS, UK

    Alexander V. Ruban

  2. Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield, S10 2TN, UK

    Matthew P. Johnson

Authors
  1. Alexander V. Ruban
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew P. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.V.R. conceived the idea of this publication, planned the original structure, drafted the manuscript and prepared Figs 1a,b,c,d; 2c,d; 3a,b,e,f. M.P.J. performed freeze-fracture and AFM experiments, helped to write and finalize the manuscript, prepared Figs 1e; 2a,b,d; 3c,d and 4.

Corresponding author

Correspondence to Alexander V. Ruban.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruban, A., Johnson, M. Visualizing the dynamic structure of the plant photosynthetic membrane. Nature Plants 1, 15161 (2015). https://doi.org/10.1038/nplants.2015.161

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.161

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing