Preface

Photosynthesis allows the energy of the sun to be used as the driving force for almost all biological processes on earth, and the great oxidation event arising from the appearance of oxygenic photosynthesis about 2.5 billion years ago was arguably the step change that led to the evolution of complex life forms, with consequences for other major global changes. Today, photosynthesis continuously generates the oxygen in the atmosphere, helps drives biogeochemical cycles that maintain the biosphere and provides us with the food, fibre and fuel we need. As humankind searches for ways to provide more food, develop renewable energy and combat the effects of climate change, the need to fully understand the many facets of the photosynthetic process has never been more urgent. Research into photosynthesis in the last 50 years has been remarkably successful. Bringing together the skills of biology, chemistry and physics, inspirational scientists have unravelled considerable details of the molecular mechanisms involved in many of the key steps. We know how the four multisubunit protein complexes located in the thylakoid membrane of the chloroplast work together to use solar energy to drive the electron transport reactions, and how these result in the generation of dioxygen, the reduction of NADP⁺ and conversion of ADP to ATP. These reactions are prerequisites for the fixation of CO₂ to organic molecules.

The four complexes are: photosystem II (PSII), photosystem I (PSI), cytochrome b₆f (Cytb₆f) and ATP synthase (CF₁CF_O). PSII and PSI are serviced by light-harvesting complexes (LHCII and LHCI). Structural and functional studies have revealed a great deal about the molecular details of the individual complexes, and the challenges are now to understand how they are spatially arranged in the thylakoid membrane and efficiently work together to transfer electrons and protons derived from splitting water to NADP⁺. Also, we need to understand how the various complexes are assembled, maintained and regulated in response to changes in environmental conditions. The latter is particularly important—in nature, the environmental conditions, particularly the intensity and spectral quality of sunlight, are continually changing. The dual requirements of maintaining high efficiency when light is limiting but ensuring photoprotection when light is in excess mean adjustments in the quantity and activity of the complexes in the membrane. Details of these processes are beginning to be uncovered. The role of reversible redox-controlled kinases is being revealed, and a number of regulatory genes and proteins have been identified and characterized. Similarly, the series of events associated with the repair and maintenance of the complexes, particularly PSII, are starting to be revealed in considerable detail, with the identification of specific proteases. The phenomenon of photoinhibition occurring when incident light intensities are above the saturation level of photosynthesis triggers protective exciton quenching mechanisms which are associated with chemical (xanthophyll cycle) and physical (conformational) changes in the LHCs. In every case, these regulatory mechanisms appear to involve changes in the interactions between the thylakoid membrane components, and new methods are being developed to study these. For example, advances in electron cryomicroscopy is allowing tomographical images of the intact membrane to be revealed and therefore starting to provide a relatively high-resolution picture of the three-dimensional organization of the various complexes in the thylakoid membrane. Similarly, application of atomic force microscopy promises to reveal new insights into the interactions governing these regulatory processes.

The papers presented in this special edition of Philosophical Transactions of the Royal Society provide a forum for integrating current knowledge in these various aspects of thylakoid membrane structure and dynamics, while at the same time defining new strategies for future experiments. They also represent the research interests of Professor Jan Anderson [1] FRS, FAA to which this special edition is dedicated on the occasion of her 80th birthday. The first article in this issue is Professor Anderson's reflection of the period of her career when it was discovered that each photosynthetic complex was enriched in a particular subfraction of the thylakoid membrane, leading to the fundamental concept of the lateral segregation of these complexes in the granal and stromal thylakoids of plants and green algae [1]. In subsequent years, methods of purification of the complexes have been continually refined, more recently enabling high-resolution structural analysis. The paper by Barera et al. [2] presents the latest efforts to purify a completely intact LHCII–PSII supercomplex that should be suitable for analysis to high-resolution by cryoelectron microscopy and possibly by X-ray crystallography. Studies of the LHCI–PSI complex are much further advanced following the determination of its structure by X-ray crystallography, and the Mazor et al. [3] now consider how the structure found in plants and green algae has evolved, notably by looking at the reservoir of PSI genes found in viruses. Similarly, the availability of high-resolution structures of the cytochrome b₆f complex and its relatives is allowing discussion of novel functional aspects such as the role of bound lipids, as described by Hasan et al. [4]. On the other hand, Semchonok et al. [5] show how electron microscopy and single particle analysis can unravel the structural organization of larger macro-complexes—in this case, the reaction-centre–antenna complexes of photosynthetic bacteria.

Understanding how these large, multisubunit complexes are assembled in a functional thylakoid is a major research challenge, and the paper by Chi et al. [6] summarizes the vast and growing array of regulatory factors involved. An important question is how the relative quantity of each particular complex is determined, and the paper by Mitra et al. [7] describes investigation of the TLA1 gene, which is thought to regulate the overall chlorophyll antenna size. The PSII complex is in a continual state of disassembly and reassembly as part of the repair cycle that replaces photo-damaged D1 subunits. Boehm et al. [8] have used mutants of Synechocystis to characterize a reaction-centre-CP47 complex, one the various intermediate sub-complexes that are involved in this repair cycle.

A number of papers deal with the dynamic aspects of the structure and function of the thylakoid membranes, and how these are integrated into the physiology of the whole plant. The central issue of reconciling the requirement for efficient harvesting of sunlight with that of ensuring safe dissipation of excess potentially damaging radiation is summarized by Horton [9], focusing how dynamic changes in the organization of the thylakoid membrane controls non-photochemical quenching, and how this is integrated into the wider aspects of plant function. Rochaix et al. [10] describe the role of the redox-controlled thylakoid protein kinases and associated phosphatases, which regulate the phosphorylation state of LHCII proteins and so maintain redox poise and optimize distribution of energy between the PSII and PSI under fluctuating light, a key part of the acclimation of the thylakoid to changing light conditions. Queval & Foyer [11] extend this discussion, focusing on how the cellular redox potential also regulates the expression of genes encoding the components of photosynthetic complexes, thereby providing a way to control photosynthetic electron transport. The short-term regulation of electron transport in fluctuating light conditions is the subject of the paper by Tikkanen et al. [12]; here, a theory is presented that the regulatory processes, including non-photochemical quenching and thylakoid protein phosphorylation, all serve to reduce the flow of electrons to the acceptor side of PSI, thereby preventing the production of reactive oxygen and thus the irreversible damage to PSI.

The acclimation and adaption of the thylakoid membrane is further considered in the final three papers. Firstly, Jia et al. [13] consider the forces that regulate the stacking of thylakoid membranes into grana; in limiting light the extent of stacking increases and large grana are formed, and it is hypothesized that the dominant attractive force in thylakoid stacking is entropy-driven, and that these increase in low light because of the changes in thylakoid composition. The paper by Matsubara et al. [14] focuses on the huge biological diversity of the response of thylakoid structure and function to light conditions, illustrating this concept by discussion of the lutein epoxide cycle, which appears to provide added photoprotection in shade-adapted species. The final paper in this issue is fittingly provided by Jan Anderson. This paper, by Anderson et al. [15], shows how changes in thylakoid membrane architecture resembling the long-term acclimation exhibited in sun and shade plants are induced within minutes of transitions in irradiance. The regulatory mechanisms discussed earlier such as non-photochemical quenching and protein phosphorylation are most likely the processes controlling the dynamic changes that occur during the normal day-to-day operating mode of this remarkable membrane system.

‘Structure and Dynamics of the Thylakoid Membrane’ Royal Society Meeting at Chicheley Hall, 3–4 May, 2012 to honour Jan Anderson and her achievements in research.Chicheley Meadow: Anthriscus sylvestris, Lamium purpureum, Carex flacca, Myosotis pratensis, Primula odorata, Luzula campestris, Glechoma hederacea, Claytonia serfoliata. Print of original watercolour painting by Cornelia Büchen-Osmond, 2012.