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      The structure of plant photosystem I super-complex at 2.8 Å resolution

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          Abstract

          Most life forms on Earth are supported by solar energy harnessed by oxygenic photosynthesis. In eukaryotes, photosynthesis is achieved by large membrane-embedded super-complexes, containing reaction centers and connected antennae. Here, we report the structure of the higher plant PSI-LHCI super-complex determined at 2.8 Å resolution. The structure includes 16 subunits and more than 200 prosthetic groups, which are mostly light harvesting pigments. The complete structures of the four LhcA subunits of LHCI include 52 chlorophyll a and 9 chlorophyll b molecules, as well as 10 carotenoids and 4 lipids. The structure of PSI-LHCI includes detailed protein pigments and pigment–pigment interactions, essential for the mechanism of excitation energy transfer and its modulation in one of nature's most efficient photochemical machines.

          DOI: http://dx.doi.org/10.7554/eLife.07433.001

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          Most plants, green algae and some bacteria use a process called photosynthesis to convert energy from sunlight into the chemical energy they need to survive and grow. With this energy, these organisms use carbon dioxide and water to create organic matter and release oxygen into the atmosphere. Therefore, photosynthesis plays a major role in providing the basis for life on earth.

          During photosynthesis, molecules of pigments known as chlorophyll and carotenoid capture the light energy. These pigments are contained within large groups (or ‘complexes’) of proteins that sit in membrane structures within cells. Two of the protein complexes—called photosystem I and LHCI—interact with each other to form a ‘supercomplex’ that transfers energy to a small protein called ferredoxin. To achieve this, the light energy captured by pigment molecules is transferred to other pigment molecules so that the energy is funneled towards the center of photosystem I.

          Mazor et al. used a technique called X-ray crystallography to create a very detailed three-dimensional model of photosystem I and LHCI from pea plants. The model shows how the twelve proteins of photosystem I are arranged in relation to the four proteins of the LHCI complex. The super-complex contains more than 200 other molecules, which are mostly chlorophylls and carotenoids. Of these, 61 chlorophyll molecules and ten carotenoid molecules are found in LHCI.

          The model also provides detailed information about how the pigments interact with each other and with the proteins in the supercomplex. Mazor et al.'s detailed model may help us to understand how these interactions allow photosystem I to harvest light energy with almost 100% efficiency, and aid efforts to develop new technologies that harness light.

          DOI: http://dx.doi.org/10.7554/eLife.07433.002

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          Most cited references42

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          Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II.

          Oxygenic photosynthesis in plants, algae and cyanobacteria is initiated at photosystem II, a homodimeric multisubunit protein-cofactor complex embedded in the thylakoid membrane. Photosystem II captures sunlight and powers the unique photo-induced oxidation of water to atmospheric oxygen. Crystallographic investigations of cyanobacterial photosystem II have provided several medium-resolution structures (3.8 to 3.2 A) that explain the general arrangement of the protein matrix and cofactors, but do not give a full picture of the complex. Here we describe the most complete cyanobacterial photosystem II structure obtained so far, showing locations of and interactions between 20 protein subunits and 77 cofactors per monomer. Assignment of 11 beta-carotenes yields insights into electron and energy transfer and photo-protection mechanisms in the reaction centre and antenna subunits. The high number of 14 integrally bound lipids reflects the structural and functional importance of these molecules for flexibility within and assembly of photosystem II. A lipophilic pathway is proposed for the diffusion of secondary plastoquinone that transfers redox equivalents from photosystem II to the photosynthetic chain. The structure provides information about the Mn4Ca cluster, where oxidation of water takes place. Our study uncovers near-atomic details necessary to understand the processes that convert light to chemical energy.
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            State transitions and light adaptation require chloroplast thylakoid protein kinase STN7.

            Photosynthetic organisms are able to adjust to changing light conditions through state transitions, a process that involves the redistribution of light excitation energy between photosystem II (PSII) and photosystem I (PSI). Balancing of the light absorption capacity of these two photosystems is achieved through the reversible association of the major antenna complex (LHCII) between PSII and PSI (ref. 3). Excess stimulation of PSII relative to PSI leads to the reduction of the plastoquinone pool and the activation of a kinase; the phosphorylation of LHCII; and the displacement of LHCII from PSII to PSI (state 2). Oxidation of the plastoquinone pool by excess stimulation of PSI reverses this process (state 1). The Chlamydomonas thylakoid-associated Ser-Thr kinase Stt7, which is required for state transitions, has an orthologue named STN7 in Arabidopsis. Here we show that loss of STN7 blocks state transitions and LHCII phosphorylation. In stn7 mutant plants the plastoquinone pool is more reduced and growth is impaired under changing light conditions, indicating that STN7, and probably state transitions, have an important role in response to environmental changes.
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              The complex architecture of oxygenic photosynthesis.

              Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on earth. The primary step in this process - the conversion of sunlight into chemical energy - is driven by four, multisubunit, membrane-protein complexes that are known as photosystem I, photosystem II, cytochrome b(6)f and F-ATPase. Structural insights into these complexes are now providing a framework for the exploration not only of energy and electron transfer, but also of the evolutionary forces that shaped the photosynthetic apparatus.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                15 June 2015
                2015
                : 4
                : e07433
                Affiliations
                [1 ]deptDepartment of Biochemistry, The George S. Wise Faculty of Life Sciences , Tel Aviv University , Tel Aviv, Israel
                Max Planck Institute of Biophysics , Germany
                Max Planck Institute of Biophysics , Germany
                Author notes
                Article
                07433
                10.7554/eLife.07433
                4487076
                26076232
                2d107203-0839-4caf-b6bb-da6fb39102ce
                © 2015, Mazor et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 11 March 2015
                : 14 June 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council (ERC);
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003977, Israel Science Foundation (ISF);
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Biophysics and Structural Biology
                Plant Biology
                Custom metadata
                2.3
                The crystal structure of higher plant PSI-LHCI complex reveals intricate details responsible for light harvesting.

                Life sciences
                pisum sativum,membrane structure,light adaptation,non photochemical quenching,light harvesting,other

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