Visualizing the dynamic structure of the plant photosynthetic membrane

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.

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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.

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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.

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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.

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Correspondence to Alexander V. Ruban.

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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

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