Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer

Abstract

Upon transition of plants from darkness to light the initiation of photosynthetic linear electron transfer (LET) from H2O to NADP+ precedes the activation of CO2 fixation, creating a lag period where cyclic electron transfer (CET) around photosystem I (PSI) has an important protective role. CET generates ΔpH without net reduced NADPH formation, preventing overreduction of PSI via regulation of the cytochrome b 6 f (cytb 6 f) complex and protecting PSII from overexcitation by inducing non-photochemical quenching. The dark-to-light transition also provokes increased phosphorylation of light-harvesting complex II (LHCII). However, the relationship between LHCII phosphorylation and regulation of the LET/CET balance is not understood. Here, we show that the dark-to-light changes in LHCII phosphorylation profoundly alter thylakoid membrane architecture and the macromolecular organization of the photosynthetic complexes, without significantly affecting the antenna size of either photosystem. The grana diameter and number of membrane layers per grana are decreased in the light while the number of grana per chloroplast is increased, creating a larger contact area between grana and stromal lamellae. We show that these changes in thylakoid stacking regulate the balance between LET and CET pathways. Smaller grana promote more efficient LET by reducing the diffusion distance for the mobile electron carriers plastoquinone and plastocyanin, whereas larger grana enhance the partition of the granal and stromal lamellae plastoquinone pools, enhancing the efficiency of CET and thus photoprotection by non-photochemical quenching.

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Fig. 1: Biochemical and spectroscopic analysis of dark- and growth light-adapted thylakoids.
Fig. 2: Macromolecular organization of grana thylakoids.
Fig. 3: Macromolecular organization of stromal lamellae thylakoids.
Fig. 4: Dimerization of PSI–LHCI supercomplexes in stromal lamellae thylakoids.
Fig. 5: Membrane architectural changes.
Fig. 6: Changes in electron transfer and photoprotection.
Fig. 7: Schematic model of the influence of grana stacking on the balance between LET and CET.

Change history

  • 29 May 2018

    In the version of this Article originally published, the authors incorrectly labelled the timescale in Fig. 6b as milliseconds (ms) on the x axis and the indicated half-life values; the correct units are microseconds (μs). The figure has now been amended in all versions of the Article.

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Acknowledgements

We wish to thank P. Horton (University of Sheffield) and F.-A. Wollman (CNRS, Paris) for fruitful discussions on the manuscript. We also thank J. Walker (University of Cambridge) for providing samples of the bovine ATP synthase complex, E. Murchie (University of Nottingham) for loan of the Dual-PAM and C. Hill (University of Sheffield) for assistance with the electron microscopy. M.P.J. acknowledges funding from the Biotechnology and Biological Sciences Research Council (UK) grant BB/M000265/1, the Leverhulme Trust grant RPG-2016-161, the Krebs Institute, the Grantham Centre for Sustainable Futures and the Kirkwood Memorial Fund. C.N.H. acknowledges the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under Award Number DE-SC0001035. PARC’s role was to partially fund the Multimode VIII AFM system and to provide partial support for C.N.H. The SIM imaging was performed at the University of Sheffield Wolfson Light Microscopy Facility and was partly funded by MRC Grant MR/K015753/1.

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W.W., C.M.C. and M.J. performed the purification of membranes and characterized them by AFM. W.W. and M.J. performed the spectroscopy experiments. W.W. performed the electron microscopy experiments. W.W. performed the AFM, electron microscopy and spectroscopy data analysis, figure preparation and Monte Carlo simulations. G.E.M. assisted with the modelling. S.F.H.B. performed the three-dimensional SIM experiments and data analysis. X.H. performed the AFM experiments on purified ATP synthase. J.H. provided advice and support to the AFM experiments. The work was conceived and written by M.P.J. and C.N.H. All authors discussed the results and commented upon the manuscript.

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Correspondence to Matthew P. Johnson.

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Wood, W.H.J., MacGregor-Chatwin, C., Barnett, S.F.H. et al. Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer. Nature Plants 4, 116–127 (2018). https://doi.org/10.1038/s41477-017-0092-7

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