Structure Determination and Improved Model of Plant Photosystem I

Abstract

Photosystem I functions as a sunlight energy converter, catalyzing one of the initial steps in driving oxygenic photosynthesis in cyanobacteria, algae, and higher plants. Functionally, Photosystem I captures sunlight and transfers the excitation energy through an intricate and precisely organized antenna system, consisting of a pigment network, to the center of the molecule, where it is used in the transmembrane electron transfer reaction. Our current understanding of the sophisticated mechanisms underlying these processes has profited greatly from elucidation of the crystal structures of the Photosystem I complex. In this report, we describe the developments that ultimately led to enhanced structural information of plant Photosystem I. In addition, we report an improved crystallographic model at 3.3-Å resolution, which allows analysis of the structure in more detail. An improved electron density map yielded identification and tracing of subunit PsaK. The location of an additional ten ␤-carotenes as well as five chlorophylls and several loop regions, which were previously uninterpretable, are now modeled. This represents the most complete plant Photosystem I structure obtained thus far, revealing the locations of and interactions among 17 protein subunits and 193 non-covalently bound photochemical cofactors. Using the new crystal structure, we examine the network of contacts among the protein subunits from the structural perspective, which provide the basis for elucidating the functional organization of the complex.During oxygenic photosynthesis, solar energy is converted into chemical energy for all higher forms of life on Earth. This process is driven by a photosynthetic apparatus within the thylakoid membranes of cyanobacteria, algae, and plants. The photochemical functions are performed by two photosystems: Photosystems I (PSI) and II (PSII). 4 These photosystems are multisubunit complexes that consist of protein and non-protein components, and drive light-dependent electron transfer reactions, resulting in the formation of high energy products: ATP and NADPH (1, 2). PSII catalyzes light-driven oxidation of water, providing electrons to PSI via the plastoquinone pool, the cytochrome b 6 f complex, and the water-soluble electron carrier plastocyanin. This electron transfer is coupled to the increase of a transmembrane electrochemical potential gradient (proton motive force), which powers ATP-synthase for phosphorylation of ADP to ATP. PSI catalyzes light-driven electron transport from plastocyanin at the inner face of the membrane (lumen) to ferredoxin on the outside of the membrane (stroma). The reduced ferredoxin is subsequently used for NADPH production, which provides the reducing power for the conversion of carbon dioxide to organic molecules. Although PSII is unique in its ability to extract electrons from water, PSI is arguably the most efficient photoelectric apparatus in nature, exhibiting a quantum efficiency of almost 100% in its utilization of light for electron transport (3). The ability of PS to...

The Arabidopsis nox Mutant Lacking Carotene Hydroxylase Activity Reveals a Critical Role for Xanthophylls in Photosystem I Biogenesis

“…However, the mutant accumulates normal amounts of other [2Fe-2S] and [4Fe-4S] cluster-containing proteins, such as ferredoxin and the NDH complex (see Supplemental Figure 6 online). Finally, ribosomal loading of psaC is similar in wild-type and nox chloroplasts (Figure 7), despite the fact that the PsaC protein contains two [4Fe-4S] clusters (Amunts et al, 2010).…”

“…Moreover, PSI is one of the most elaborate macromolecular complexes of the chloroplast, having 17 protein subunits and nearly 200 cofactors (Amunts et al, 2010) that need to be assembled in a concerted manner. Although a number of auxiliary factors involved in these tasks have been described, a complete understanding on how the molecular machinery works is still lacking.…”

Characterization and Evolution of Tetrameric Photosystem I from the Thermophilic Cyanobacterium Chroococcidiopsis sp TS-821

“…Some reviews have pointed out that the modification of PsaL C terminus and the emergence of PsaH in plant PSI led to the monomeric form of PSI in plants (Ben-Shem et al, 2004;Nelson and Ben-Shem, 2005;Amunts and Nelson, 2008). In plant PSI monomer, according to the available crystal structure (Amunts et al, 2010), the longer insertion between transmembrane helix 2 and transmembrane helix 3 in PsaL is in close vicinity of PsaH, which indicates their potential interaction that stabilizes the monomeric form of PSI. This insertion, along with short C terminus, is also found in PsaL of tetrameric PSI ( Figure 8; Supplemental Figure 5), which further indicates that tetrameric PSI may be an intermediate form during the evolution of the PSI in plants and green algae.…”

15N Photo-CIDNP MAS NMR To Reveal Functional Heterogeneity in Electron Donor of Different Plant Organisms

“…The X-ray structure of cyanobacterial PSI has been solved with 2.5 Å resolution and shows high resemblance to plant PSI [5,6]. From plant PSI currently only X-ray structures of near-atomic resolution (down to 3.4 Å [7]) are available, leaving the exact electronic structure of plant P700 a matter of debate. All PSI systems, as other RCs, have two symmetric branches consisting of six chlorine molecules and two quinones (Fig.…”