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Assembly of Super-Complexes in the Plant Chloroplast
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This entry is adapted from the peer-reviewed paper 10.3390/biom11121839

Increasing evidence has revealed that the enzymes of several biological pathways assemble into larger supramolecular structures called super-complexes. Indeed, those such as association of the mitochondrial respiratory chain complexes play an essential role in respiratory activity and promote metabolic fitness. Dynamically assembled super-complexes are able to alternate between participating in large complexes and existing in a free state.

chloroplast super-complexes structure photosystem ATPase electron transport chain Calvin–Benson cycle de novo purine biosynthesis

1. Introduction

Protein super-complexes are composed of several protein complexes which assemble into a supramolecular structure in order to execute their biological functional such as the well-documented mitochondrial electron transport chain (mETC) complexes containing multi-subunit protein complexes [1]. The association of mETC proton translocating complexes (complex I, III and IV) as well as the mobile electron carriers (ubiquinone and cytochrome c) was revealed by protein structure studies and suggested to possibly mediate the substrate channeling of proton translocation in order to generate a proton-motive force for ATP synthesis [1][2][3]. Although the functional significance of full respirasomes is not fully understood, it has been suggested that the association of respiratory enzymes into super-complexes may increase metabolism efficiency and reduce oxidative damage [4]. It has been demonstrated that that super-complexes comprising Complex IV had higher Complex I and III activities, indicating that the association of Complex IV modifies super-complexes to enhance catalytic activity [5] (Figure 1). Indeed, even increasing evidence has been accumulated to suggest the presence of respirasomes (the super-complex of mETC Complex I, III, and IV) is essential for the stability and function of the Complex II [6]. In addition, the dynamical assembly of super-complex has also be suggested to help the organization of electron flux to optimize the use of substrates [7]. The association of super-complexes increased electron transport by reducing the distance for diffusion of cytochrome c between the cytochrome bc1 complex and cytochrome c oxidase and thereby increases competitive fitness in yeast [8]. However, the evidence of substrate channeling in the super-complexes of mETC remains a matter of debate since it is unclear if structural evidence is consistent with the occurrence of channeling or not [4][9][10][11]. Variations between these super-complexes have been reported across kingdoms, and this super-complex is now widely used as a model for super-complex research.
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Figure 1. Structure of the respiratory chain super-complex. cryo-EM maps of respiratory chain complex from Saccharomyces cerevisiae. (resolution 3.17 Å).

2. Molecular Organization of Different Complexes

2.1. Photosynthesis Complex

2.1.1. Photosystem I Core Complex

Plants and algae have a monomer PSI core complex that connects with different LHCIs to produce the PSI–LHCI super-complex [12][13][14] (Figure 2A).  Almost all Lhca/Lhcb proteins from various photosynthetic species have been described structurally. The antenna size, protein content, and related colors of the LHCI proteins varied greatly among species, according to these structural investigations. [15][16]. The structural similarities and differences among various LHCI proteins are explored in the following sections.

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Figure 2. Structure of the PSI–LHCI and PSII–LHCII super-complex. (A) cryo-EM maps of super-complexes with PSI and LHCI from Bryopsis corticulans. (resolution 3.49 Å). PSaA, raspberry; PSaB, green; PSaF, pink; PSaG, magenta; PSaH, salmon; PSaI, hot pink; PSaJ, blue; PSaK, lime green; PSaL, violet; PSaM, marine; Lhca-a, orange; Lhca-b, split pea; Lhca-c, light pink; Lhca-d, bright orange; Lhca-e, red; Lhca-f, purple blue; Lhca-g, pale cyan; Lhca-h, light blue; Lhca-i, yellow; Lhca-j, cyan. (B) cryo-EM maps of super-complexes with PSII core and LHCII from Pisum sativum. (resolution 2.70 Å). M–LHCII, cyan; S–LHCII, yellow; CP24, slate; CP29, orange; CP26, light pink; PSII core complex, green.
The PSI core of the plant is connected to four LHCI subunits, which create a semispherical belt on the PsaF/PsaJ side. Lhca1–3 are structured as Lhca1–Lhca4 and Lhca2–Lhca3 heterodimers, with Lhca3 and Lhca1 at the two edges and tightly interacting with PsaK/PsaA and PsaG/PsaB, respectively.

2.1.2. PSII Core Complex

PSII is a large multi-subunit protein complex with a dimeric core and a number of membrane-attached antenna complexes on the periphery. Depending on the organism, the core complex has anywhere from 20 to 23 protein subunits. The reaction center, which is substantially conserved among plants, algae, and cyanobacteria, is the catalytic heart of the core. PsbA (D1), PsbB (CP47), PsbC (CP43), and PsbD (D2), the biggest membrane-intrinsic subunits, make up the reaction center. The photochemical reaction center, made up of PsbA and PsbD, is where charge separation and electron transport across the membrane take place. The subunits bind a total of six chlorophylls (Chls), with two pheophytins which are separately bound to PsbA and PsbD. The internal antenna proteins, PsbB and PsbC, bind multiple chlorophylls. These two subunits are responsible for light gathering and transmitting excitation energy from the antenna’s periphery to the photochemical reaction core [17]. PsbE, PsbF, PsbH, PsbI-M, PsbTc, PsbX, PsbY, and PsbZ are tiny intrinsic subunits that are found in all organisms, in addition to the reaction center. These subunits are physically and functionally preserved; however, they are less closely related between organisms than reaction center subunits. In comparison to its bacterial cousin, plant PsbY possesses one extra membrane-spanning helix. Plants lack the cyanobacterial component Ycf12 but do have the PsbTn and PsbW subunits. Their position in the plant super-complex structure might be determined [18].
The dimeric PSII core is connected with multiple LHCIIs (Lhcb proteins that bind pigments) in plants. The primary light-harvesting complex LHCII, which comprises three apoproteins (Lhcb1, Lhcb2, and Lhcb3) that form Lhcb1/Lhcb2/Lhcb3 heterotrimers in vivo with various stoichiometries [19] or in vitro with homotrimers of Lhcb1 or Lhcb2 [20][21], is the most prevalent antenna complex in vascular plants. Three monomeric minor Lhcbs are linked to the PSII core in addition to the trimeric LHCII. Based on the apparent molecular mass of their apoproteins, they were given the names CP29 (Lhcb4), CP26 (Lhcb5), and CP24 (Lhcb6) [22].
PSII–LHCII super-complexes are formed when the plant PSII core interacts with several LHCIIs. The trimeric LHCII can be characterized as strongly (S), moderately (M), or loosely (L) coupled with the PSII core (C) complex based on their respective affinities [23]. PSII super-complexes modify their antenna size in response to variations in light intensity [24][25] (Figure 2B).
The peripheral antennae of PSII are structured into two layers around the core complex, according to analyses of PSII–LHCII super-complex structures [26][27][28]. The inner layer, which interacts with the dimeric core to produce the C2S2 super-complex, contains two copies of S–LHCII, CP29, and CP26. The C2S2M2 super-complex is formed when two CP24s and two M–LHCIIs attach to the outer layer of C2S2. S–LHCII is near to the core complex of the PSII–LHCII super-complex and connects CP26 and CP29 (from the neighboring monomer) through monomer A and B, respectively. S-third LHCII’s monomer (C) is found at the periphery, where it interacts with M–LHCII′ in the larger C2S2M2 super-complex. In the C2S2M2 super-complex, CP24 interacts extensively with CP29 and forms a CP24–CP29 heterodimer, which closely resembles the Lhca3–Lhca2 and Lhca4–Lhca1 dimers in plant PSI [29][30]. The M–LHCII trimer, which contains Lhcb3 protein, simultaneously binds to the CP24–CP29 heterodimer and S–LHCII′. Both Lhcb3 and CP24 are specific to land plants [31] and are present only in the larger PSII–LHCII super-complexes, such as C2S2M2 [26][32]. M–LHCII is tightly connected with CP24 in the super-complex through Lhcb3. The contacts between M–LHCII and S–LHCII or M–LHCII and CP29, on the other hand, are less extensive and mostly consist of hydrophobic interaction, independently of the enthalpy and entropy rather than intermolecular forces such as der Waals forces or hydrogen bonds. The importance of CP24 in binding M–LHCII to CP29 might explain why knocking out CP24 causes the C2S2M2 super-complex to dissociate, leaving only C2S2. Furthermore, when CP24 dissociates from CP29, M–LHCII may detach from the super-complex, guaranteeing that plant PSII’s antenna size varies rapidly and dynamically in response to high light. [33].
Although the high-resolution structure of the PSII–LHCII super-complex comprising L–LHCII has yet to be determined, prior negatively stained electron microscopy investigations indicated that L–LHCII interacts with the core complex near CP26 or at the periphery of S- and M-trimers [23][34][35]. Unlike S–LHCII and M–LHCII, which are usually attached to PSII, L-mobile LHCII’s LHCII can associate with PSI core under appropriate conditions. According to previous research, the mobile LHCII is mostly made up of the Lhcb1–Lhcb1–Lhcb2 trimer and may switch between PSI and PSII during state transitions. [36][37][38]. pLhcb2 is responsible for the interaction between mobile LHCII and PSI, despite the fact that Lhcb1 can also be phosphorylated. [36][37]. The entire structure of Lhcb2 and its phosphorylated Thr3 residue in the N-terminal region of maize PSI–LHCI–LHCII were first disclosed in the cryo-EM structure of maize PSI–LHCI–LHCII [39]. The PSI core subunits engage with the N-terminal region of pLhcb2, particularly the phosphate group of phosphorylated Thr3 (pThr3) and two basic residues, in the complex (Arg1 and Arg2). Furthermore, the protein sequence of Lhcb2’s N-terminal region is somewhat shorter than that of Lhcb1, suggesting that the interaction between Lhcb2 and PSI core is more specialized [39].
Plant Lhcb proteins are members of the LHC superfamily and share comparable sequences and structural characteristics. Lhcb proteins’ N- and C-termini are found on the stromal and luminal sides, respectively. Helix B, C, and A are the three transmembrane helices found in all Lhcb proteins (from the N-terminus to the C-terminus). Except for CP24, which has a very short helix E but no helix D due to its short C-terminal fragment, all Lhcbs have two amphipathic helices with identical lengths (D and E) at the luminal surfaces. In the center of the membrane, helices A and B interlock to generate a left-handed supercoil. Helix C is approximately perpendicular to the membrane plane, with a BC loop and an AC loop connecting it to helices B and A, respectively. Despite the general resemblance of their apoprotein folds, there are considerable variances in their loop regions.
In terms of sequence and structure, CP26 is the most similar to Lhcb1 of the three minor Lhcb proteins, with conformational variations being confined to their loop regions. Specifically, the N-terminal segment of CP26 adopts a shape similar to that of Lhcb1, which is consistent with a previous research indicating that CP26 may form a trimer in lieu of Lhcb1 and Lhcb2 in Arabidopsis thaliana when these proteins are absent. [40][41]. In the Lhcb family, the CP29 component possesses the biggest apoprotein and the longest N-terminal domain. In the PSII–LHCII super-complex, its N-terminal region forms a lengthy hairpin loop that practically covers the whole core component CP47 at the stromal surface. As a result, of all the main and minor Lhcb proteins in the super-complex, the antenna complex’s CP29 is the most intimately connected with the PSII core. The N-terminal loop of CP29 was not defined in the previously established crystal structure of CP29 due to proteolysis during crystallization. Based on these structural observations, the N-terminal portion of CP29 in the super-complex may be maintained by interactions with PSII core subunits [42], When CP29 is detached from the core, it may be quite flexible. CP24 is the smallest of the Lhcb proteins, with a short BC loop and C-terminal tail. It, on the other hand, has the longest AC loop, which contains two extra segments required for CP24–Lhcb3 and CP24–CP29 interactions. On the stromal side, CP24 has a longer helix C than the other Lhcbs, which aids in the connection with the nearby CP29 protein.

2.1.3. ATPase

The F1F0-ATP synthase, also known as the ATPase synthase complex of green plant chloroplasts, is a member of the F-type ATP synthase family. Prokaryotes and eukaryotes both have mitochondria with similar sorts of complexes. Through evolution, the ATP synthase enzymes have remained impressively conserved. Bacterial enzymes are structurally and functionally similar to those found in the mitochondria of animals, plants, and fungus, as well as the chloroplasts of plants. They are always made up of three parts: a hydrophilic, almost spherical headpiece (F1) connected to a smaller membrane-bound F0 moiety by a stalk region. A central stalk connects to a peripheral stator connection in the stalk area. Three noncatalytic a-subunits and three catalytic h-subunits of around 55 kDa alternate in a hexagon to make up the majority of the bulk of the F1 headpiece. The isolated F1-ATPase produces ATP, which drives the rotation, and subunit g of 35 kDa covers most of the middle shaft. The F1F0 complex’s g subunit is linked to an 8-kDa c subunit made up of two membrane-bound a-helices arranged in a hairpin. Subunit c exists as a multimer at all times [43]. The chloroplast subunit III, the equivalent of c, forms a fixed ring of 14 subunits [44].
Rotation of the c component multimer in undamaged chloroplasts is caused by the proton motive force acting across the thylakoid membrane. This causes g to rotate, which leads to the production of ATP via rotational catalysis. A second stalk, or stator, links the F1 headpiece and F0 to prevent fruitless spinning. Green plant subunits I, II, and IV, as well as y, are engaged in the stator, and a ninth component, q, controls catalytic activity by binding to g, bringing the total number of subunits to nine. Three tiny subunits and one inhibitor protein are found in vertebrate mitochondrial ATPase.
The three catalytic h-subunits vary in conformation and bound nucleotide in the crystal structure of bovine mitochondrial F1-ATPase measured at 2.8 Å resolution [45]. In intact ATP synthase, the structure supports a catalytic mechanism in which the three catalytic subunits are in distinct phases of the catalytic cycle at any one time. Interconversion of states is accomplished by rotating the α-helical subunit’s domain relative to the a3–h3 subassembly. Based on the homologous structure of the bovine mitochondrial enzyme, the structure of the F (1)—ATPase from spinach chloroplasts was determined to 3.2 Å resolution by molecular replacement [46]. The a- and h-subunits display a structure that was quite similar to the mitochondrial and thermophilic subunits. NMR has established the structures of several minor subunits (δ, ε), but no entire ATP synthase complex has yet been crystallized. It is possible that the stator is too delicate to crystallize. As a result, we do not know the specific structure of the plant component IV (named in prokaryotes and mitochondria). Despite this, the general locations of all subunits are quite well established.
For a long time, the F-type ATP synthase was thought to be a monomeric membrane complex. The enzyme from yeast mitochondria, however, was discovered to be dimeric, utilizing the technique of blue native gel electrophoresis [47]. In comparison to the monomer, the dimer’s subunit makeup indicated the existence of three more small proteins. The creation of the dimeric state required two of these dimer-specific subunits of the ATP synthase. Because other respiratory chain complexes such as cytochrome reductase (Complex III) and cytochrome oxidase (Complex IV) also create particular types of associates, the mitochondrial ATPase dimer is not a unique large super-complex.

2.1.4. Cytochrome b6/f

The cytochrome b6/f complex is a dimeric integral membrane protein complex with eight-to-nine polypeptide subunits that has a molecular weight of around 220 kDa [48]. The four largest have well defined roles. Together with the 17-kDa subunit IV, which has three transmembrane helices and two b-type hemes, the 24-kDa cytochrome b6 subunit has four transmembrane α-helices and contains two b-type hemes. The N- and C-terminal portions of cytochrome b of the bc1 complex from the respiratory chain in mitochondria are homologous to cytochrome b6 and subunit IV. The 19-kDa Rieske iron–sulfur protein, consisting of an N-terminal single transmembrane α-helix domain and a 140-residue soluble extrinsic domain with a linker region connecting these two domains, has an overall function similar to that of the iron–sulfur protein in the bc1 complex, deprotonating the membrane-bound quinol and transferring electrons from the quinol to the membrane-bound c-type cytochrome. The 31-kDa c-type cytochrome f subunit is functionally related to, but structurally completely different from, the cytochrome c1 in the bc1 complex. In addition to these four large subunits four smaller subunits, PetG, PetL, PetM and PetN, are each bound the complex with one membrane-spanning α-helix (Figure 3B). They have no counterparts in the cytochrome bc1 complex.
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Figure 3. Structure of the ATPase, cytob6f. (A) cryo-EM maps of ATPase from Spinacia oleracea. (resolution 3.35 Å). α, limon, light pink and light blue; β, magenta, pale green and split pea; γ, green; ε, slate; δ,purple blue; c14, yellow and cyan gradual part; bb’, blue and marine. (B) cryo-EM maps of super-complexes with cytob6 and cytof from Spinacia oleracea. (resolution 3.58 Å). cytob6, light pink; cytof, cyan; ISP, yellow; IV, orange; PetG, pale green; PetM, wheat; PetL, magenta; PetN, green.

2.2. The Chloroplast Electron Transport Chain

In the primary reactions of photosynthesis, there are two modes of electron flow: linear or non-cyclic electron flow (LEF) and cyclic electron flow (CEF). In LEF, both PSI and PSII are involved, together with the cyt b6/f complex. LEF is more important under normal conditions than CEF, in which PSI and cyt b6/f are the main relevant players, without the involvement of PSII. The LEF produces both ATP and NADPH, but the CEF pathway generates extra ATP. For a balanced CO2 fixation and other metabolic processes LEF does not provide enough ATP (vs NADPH). By tuning the levels of LEF and CEF, the ATP/NADPH ratio can be adjusted to meet cellular demands [49][50]. Under certain conditions CEF appears to contribute substantially to photosynthetic electron flow, for instance during induction of photosynthesis and under stressful conditions such as drought, high light and extreme temperatures [49].
A super-complex involved in both electron transport and photosynthesis is the PSI–LHCI–LHCII–FNR–cyt b6/f–PGRL1 super-complex, named here the PSI-cyt b6/f super-complex, for the sake of simplicity. This super-complex was isolated from the green alga C. reinhardtii in state 2 by sucrose gradient centrifugation and has an approximate mass of 1200–1400 kDa [51]. The main components are PSI and the cyt b6/f complex.

2.3. Calvin–Benson Cycle (CBC)

Oxygenic phototrophs such as cyanobacteria, algae, and land plants convert carbon dioxide and water into carbohydrates and release the by-product oxygen, a process that can be divided into the light reactions and the CBC (light-independent reactions). ATP and NADPH are produced in the light reaction process before being utilized by the enzymes of the CBC responsible for CO2 assimilation [52]. The CBC is regulated by light/dark transitions through the redox states of the chloroplast stroma. Chloroplast thioredoxins (TRXs), including TRX f and TRX m, are reduced by PSI upon illumination through ferredoxin and the ferredoxin thioredoxin reductase system [53][54] and further reduce and activate the enzymes of the CBC, including phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH). In addition, the small chloroplast protein CP12, which is central for the regulation of the CBC and usually possesses two Cys pairs at both N- and C-terminal regions, is redox-regulated by TRXs [17][55][56].
The GAPDH/CP12/PRK complex is formed when oxidized CP12 interacts with the GAPDH tetramer and then assembles with the oxidized PRK dimer [57][58][59][60] (Figure 4A). Both GAPDH and PRK have been found to have their enzymatic activities inhibited when they form a complex, and the activity of PRK in the complex is even lower than the free oxidized PRK dimer [61]. The activation of PRK in the complex occurs quickly, while the transition of free oxidized PRK to its active state is slower [58]. However, the mechanism for this divergence remains unknown.
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Figure 4. Structure of the GAPDH-CP12-PRK complex and the purinosome formation. (A) cryo-EM maps of complexes with GAPDH, CP12 and PRK from Thermosynechococcus vestitus. (resolution 3.90 Å). GAPDH, green; CP12, yellow; PRK, cyan. (B) Enzymes of de novo purine biosynthesis assemble into purinosome in purine depleted conditions in Hela cells. PPAT: amidophosphoribosyl transferase, purple; FGAMS: phoshoribosylformylglycinimidine transferase, red; PAICS: bifunctional phosphoribosylaminoimidazole carboxylase and phosphoribosyl aminoimidazole (CAIR synthetase, and SAICAR synthetase), yellow; ATIC: bifunctional 5-aminoimidazole-4-carboxamide nucleotide formyltransferase/IMP cyclohydroxylase (IMPCH), blue; ADSL: bifunctional adenylosuccinate lyase, orange; GART: trifunctional phosphoribosylglycinamide formyltransferase (GAR synthetase, GAR formyltransferase, and AIR synthetase), green.

2.4. A Chloroplast Purinosome

The purinosome is a multi-enzyme complex that carries out de novo purine biosynthesis within the cell [62]. Six identified enzymes were postulated to directly participate in a ten-step biosynthetic pathway converting phosphoribosyl pyrophosphate to inosine monophosphate [63]. In human cells, the de novo purine biosynthesis pathway has been proved to form a multi-enzyme complex to facilitate substrate channeling between each enzyme of the pathway [63][64][65]. Remarkably, under cellular circumstances that lead to a high demand for purines, the enzymes of de novo purine biosynthesis cluster together into multi-enzyme complexes that have been dubbed purinosomes [64] (Figure 4B). Proteomics has subsequently been used to define the nature of protein–protein interactions within the cluster demonstrating that a core complex which assembles in a step-wise fashion includes the first three enzymes in the pathway. Subsequent study of the mutants of other enzymes in the pathway revealed a decreased purinosome formation suggesting that these proteins likely affect complex stability [66].

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Youjun Zhang
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