Aspects of PSI were discovered in the s, but the significances of these discoveries was not yet known. PsaA and PsaB are both integral membrane proteins of to amino acids that contain 11 transmembrane segments. The two cysteines in each are proximal and located in a loop between the ninth and tenth transmembrane segments. Photoexcitation of the pigment molecules in the antenna complex induces electron transfer.
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Oxygenic photosynthesis is indispensable both for the development and maintenance of life on earth by converting light energy into chemical energy and by producing molecular oxygen and consuming carbon dioxide.
This latter process has been responsible for reducing the CO2 from its very high levels in the primitive atmosphere to the present low levels and thus reducing global temperatures to levels conducive to the development of life. Photosystem I and photosystem II are the two multi-protein complexes that contain the pigments necessary to harvest photons and use light energy to catalyse the primary photosynthetic endergonic reactions producing high energy compounds. Both photosystems are highly organised membrane supercomplexes composed of a core complex, containing the reaction centre where electron transport is initiated, and of a peripheral antenna system, which is important for light harvesting and photosynthetic activity regulation.
If on the one hand both the chemical reactions catalysed by the two photosystems and their detailed structure are different, on the other hand they share many similarities.
In this review we discuss and compare various aspects of the organisation, functioning and regulation of plant photosystems by comparing them for similarities and differences as obtained by structural, biochemical and spectroscopic investigations. Oxygenic photosynthesis is thought to have begun around 2.
The first oxygenic organisms, the ancestor of modern cyanobacteria, acquired the ability to oxidise water through the evolution of more ancient not-oxygenic photosystems through a process that is only partially understood [ 2 ]. Almost all forms of life today depend on the ability of photosynthetic oxygenic organisms to convert light energy into chemical energy and to produce molecular oxygen.
Photosynthesis also played and plays a major role in the control of atmospheric CO 2 concentration through carbon fixation,which is also of fundamental importance for life on the planet. Moreover, modern economies are heavily dependent on photosynthetically produced fossil fuels, which contain sunlight energy harvested millions years ago. They are electronically connected by an intermediate membrane supercomplex called Cytochrome b 6 f Cyt b 6 f [ 3 , 4 ] and two electron carriers, a liposoluble quinone molecule plastoquinone that transports electrons between PSII and Cyt b 6 f , and the luminal copper-containing soluble protein plastocyanin, which links Cyt b 6 f to PSI.
However, for almost 2 billion years life remained mainly confined in the water and land plants appeared only about 0. The first land plants had to challenge new environmental constraints and stresses: an atmosphere rich in oxygen, an environment rapidly fluctuating in terms of light quantity and quality, temperature, nutrients and water. In green organisms Viridiplantae , most of the light is absorbed by the photosynthetic pigments chlorophyll a and b , which have remarkable physicochemical properties allowing efficient light harvesting and ultra fast excitation energy transfer amongst antenna chlorophylls, leading to the quantum and thermodynamic efficiencies which are the highest known.
Thus, all these factors a rapidly fluctuating environment and a high reactivity of excited Chls with oxygen were important for the evolution of the photosynthetic process and its regulations before and during land colonisation. The two photosystems have a common organisation and are functionally organised in two main moieties: a core complex, containing the reaction centre where the photochemical reactions occur, and a peripheral antenna system that increases the light harvesting capability, but that is also involved in regulation of the photosynthetic process [ 10 , 11 ].
The core complexes have been well conserved during the evolution, as most of the subunits are similar in prokaryotic and eukaryotic photosystems and only a few are specific to each group [ 12 ]. On the contrary, the peripheral antenna system displays great variability, being composed of peripheral associated membrane proteins in cyanobacteria, the phycobilisomes, and integral Lhc membrane proteins in eukaryotic cells.
These important topics have been presented in several recent reviews and we suggest reading the following papers for a greater understanding [ 13 - 15 ]. A large body of investigation has been dedicated to the comprehension of photosynthesis in plants over several decades. Although many aspects of the photosynthetic process are nowadays substantially elucidated, several details, specific regulations, and even structural details about photosynthesis in plants are still little known.
We will discuss about the functioning, organisation, regulation of photosystems under different environmental conditions, by analysing common and specific aspects of each photosystem and by presenting open questions that requires further investigation in order to better understand their functioning. Both families of RC are present in membranes of oxygenic photosynthetic organism. On the other hand, non-oxygenic phototrophic organisms generally harbour either a Type-II reaction centre i.
Non-oxygenic bacterial photosystems usually operate a cyclic electron transport involving the photosystem and a cytochrome complex, which is analogous to the respiratory complex Cyt bc 1 [ 3 ] as well as other diffusible electron carrier proteins, with the most common electron donor to the RCs being small soluble c- type cytochromes.
Photosynthetic reaction centres are most commonly hetero-dimer pigment-protein complexes and this is the case for all known oxygenic photosystems. Structural, biochemical and biophysical analyses reveal a high degree of similarity between the two subunits composing the RC, suggesting that this common organisation originated from an ancient non-oxygenic homodimeric complex [ 2 , 16 ].
In the past decades crystallographic models of several photosynthetic reaction centres have been presented with sufficient resolution to discern not only the overall structural organisation of the complexes, but also the positions of most of the cofactors. However, whereas crystallographic models have been obtained for both higher plant PSI 3.
Nevertheless, due to the great similarity between the plant and cyanobacteria RC proteins, the high resolution structures of the cyanobacterium Thermosynechococcus elongatus 2. By comparing the low resolution structure of plant PSII cores [ 23 , 24 ] to PSII from cyanobacteria, a slightly different organisation of the eukaryotic and prokaryotic reaction centres has however been observed [ 24 , 25 ].
The core of PSII is a multi-subunit complex composed of about subunits. The precise number is still unknown, since in recent years advances in purification and mass spectrometry analyses led to the discovery of new subunits, some of which are probably only transiently bound to PSII [ 26 ]. Moreover the exact number of subunits appears also to be species-specific.
Their function is only partially understood and apparently they are mainly involved in PSII assembly, repair and regulation [ 26 , 27 ]. Yet, most of the chromophores involved in light-harvesting, as well as electron transfer reactions, are bound to four main subunits, known as D1, D2, CP43 and CP47, all of which are membrane proteins containing several trans-membrane helices TMH.
The D1-D2 complex together with Cyt b composed of the PsbE and PsbF subunits is often referred to as the PSII RC because it binds most of the cofactors in the photo-catalytic activity of this photosystem this will be discussed further in the successive paragraph. Each of these subunits, containing 6 TMH, is associated with one of the RC heterodimer, the binding of CP43 being slightly more labile based on detergent effects [ 31 ].
Collectively CP43 and CP47 bind a total of 29 Chls a molecules based on the cyanobacterial structural model that function as internal antenna and allow excitation energy transfer from the peripheral antenna system to the RC see below for further discussion on pigment stoichiometry in plant PSII.
The Chls a composing the internal light harvesting system appear to be organised predominantly in two layers parallel to the membrane plane, and approximately localised in proximity of the luminal and stromal sides of the membrane Fig. On the other hand the cofactors involved in electron transfer ET reactions are organised in two parallel chains or branches that are perpendicular to the membrane plane Fig.
This configuration allows the transfer of electrons across the membrane and the formation of a photochemically generated electrochemical potential. A Simplified model of plant thylakoid membranes. The four photosynthetic complexes involved in the electron transport and ATP synthesis are shown.
PSI and ATP synthase are located in the stroma-exposed membranes, which are the last layers of the grana and the stroma lamellae. Location of Cytochrome b6f is more controversial: this complex is considered evenly distributed in the two kinds of membranes, but highly purified appressed grana membranes called BBY do not contain Cyt b6f [61, 85, ]. Thylakoids are dynamic membranes which are subjected to reorganization for the number and size of the stacks, volume of the lumen and location of the complexes.
For more information, we suggest referring to the following reviews and references therein [85, 92]. Image modified from . In the upper of the two monomers composing the dimeric core of PSII, the D1 and D2 reaction center subunits and the internal antenna proteins of the core complex CP43 and CP47 are indicated in color and other core proteins are shown in transparent grey.
In the PSI model the PsaA and PsaB core subunits are indicated, as well as the Lhca antenna complexes and other subunits visible from the luminal view. Lhca3 and Lhca4 are in red to highlight the fact that these complexes harbor the lowest energy Chls red forms. The position of Chls and carotenoids is also shown. For PSI, the low resolution of the crystal structure in the Lhca region, where Chls b are, does not allow assigning their position and thus all Chls are indicated only in blue.
Carotenoids are drawn using the following colors: b-carotene, brown; lutein, orange; violaxanthin, violet; neoxanthin, yellow. Several carotenoids are not resolved in the PSI crystal structure in particular in the Lhca region and at the interface Lhca-core and thus they are not shown. Note also that the proteins on the PSI side docking LHCII are only partially resolved, thus in this region other peptides and likely some Chls do not appear in the crystal structure and in this figure.
An iron atom Fe is in between the two quinones. See text for further discussion on ET mechanism and reaction sequence. As in the case of PSII, the Chl a molecules involved in proximal light harvesting are organised in two layers parallel to each other and located close to the luminal and stromal sides of the membrane, respectively, whereas the cofactors involved in the ET reactions form two parallel branches, related by pseudo-C2 symmetry, perpendicular to the membrane plane Fig.
In cyanobacteria, some of the small subunits are involved in the super-structural organisation of the core complex that will be described in further detail below.
The high turnover of D1 subunit [ 35 , 36 ] might explain the reason why the core pigments of PSII are located on separated proteins CP43 and CP47 with respect to the reaction center proteins D1 and D2. D1 is indeed very sensitive to oxidative stresses and plant needs to partially disassemble PSII and substitute D1 at a high rate, while other subunits are recycled [ 37 ].
This is simpler and energetically more efficient if the PSII core is composed by modular smaller subunits. It is likely that these subunits originated to optimise the assembly and catalytic activity of PSI and PSII and to adapt to new environmental niches and environmental conditions, such as an atmosphere getting richer in molecular oxygen.
Extensive reviews concerning the evolution of photosynthesis have been recently published and we recommend them for more detailed information on these issues [ 2 , 38 ]. All the structural models of photosynthetic RCs with sufficient resolution, i.
Other cofactors are specific to each ET chain. In recent years, in both oxygenic reaction centres, it has been suggested that the so-called accessory Chls play the role of electron transfer intermediates, possibly being the primary donor [ 40 - 44 ]. This is known as monodirectional or asymmetric ET. The latter is known as bidirectional or symmetrical electron transfer [ 44 , 45 ]. The remaining quinone, Q B, is reduced to the semi-quinone Q B — by Q A — as a result of one charge separation event, and to the fully reduced quinole form Q B 2— which is then protonated to become Q B H 2 , after a second charge separation event, which is a process known as the two electron gate.
Q B represents the terminal electron acceptor of PSII, which in a reduced and protonated form can diffuse out of the RC binding site and acts as a lipophilic electron carrier within the thylakoid membranes. Moreover, the PhQs are not the terminal electron acceptors, as their semi-quinone form is oxidised by the iron sulphur cluster F X which is coordinated at the interface of the PsaA and PsaB subunits and is a common cofactor to both ET chains.
Subsequent energy losses are useful to stabilize the primary charge separation and make the reaction directional low reversibility. A similar situation is found for PSI. As a result of the difference in operational potential between PSII and PSI, also the donor side of the latter is significantly more reducing than that of PSII; for instance the potential of the primary acceptors, A 0 , is estimated at about —1.
However, whereas in the latter case the difference is also due to the different chemical species, PhQ being more reducing than PQ even in bulk organic solvents, the modulation of the redox properties of Chls a induced by the interaction with the protein subunits is rather remarkable and highlights the flexibility of these molecules as redox as well as light harvesting cofactors as well as the impressive influence of protein-cofactor interactions in sustaining the catalytic activity of both photosystems.
The oligomeric state of PSI has been investigated in various papers in recent years [ 46 - 48 ]. In plants, after purification, other than the most common monomeric form, dimers, trimers and tetramers of PSI have been detected [ 47 ]. However, an in depth investigation by single particle analysis of electron microscope images [ 46 , 47 ] showed that all the oligomers contain PSI units in inverted positions. This configuration is not compatible with the functionality of the photosystem in vivo , because electron transfer is vectorial in the membranes, as required to set up an ionic gradient, and indicates that such oligomeric states are very likely artefacts observed in vitro after purification.
Indeed, it has been demonstrated that oligomeric forms of PSI can be also induced in vitro from purified monomeric PSI [ 48 ]. Taken together, biochemical and electron microscopy data strongly suggest that plant PSI is a monomeric complex in vivo , differently from the case of cyanobacteria, where PSI is found predominantly as a trimer, even though a possible equilibrium between trimers and monomers has been suggested in some cyanobacterial strains [ 49 ].
This difference is probably caused by the evolution in plants of the PsaH subunit, which is necessary for LHCII docking, but which impairs formation of trimers in plants. In plants, such low energy Chl states are instead associated with the LHCI antenna [ 52 - 55 ], which is not present in cyanobacteria. On the other hand, PSII is generally found as a homodimer where each monomer is the heterodimeric complex described above associated with Lhc antennas Fig.
Even though in a recent report it was suggested that PSII in cyanobacteria is a monomer in vivo and dimerisation is induced by delipidation after a detergent treatment [ 56 ], most of the findings indicate that both in plants as well as in cyanobacteria, the dimeric conformation is the most common and that monomers should be considered mainly as an intermediate step of PSII assembly and disassembly, which is necessary during its repairing as a result of photoinhibition [ 35 ].
This conclusion is supported by the evidence that PSII dimers are observed by electron microscopy analysis in intact thylakoid membranes [ 57 - 59 ], which are purified without the aid of detergents, and that the topography of such dimers matches that of isolated plant PSII supercomplexes [ 21 , 60 , 61 ], which require a detergent treatment of thylakoid membranes for their purification. In both cases, most of the plant PSII complexes are present as dimers.
A reason for the dimeric conformation of PSII could be the fact that PSII has a slow turnover mainly determined by PQ replacement at the Q B site and in a dimeric conformation there is the possibility of an efficient excitation energy transfer between adjacent RC, thus optimising energy utilisation Fig. As example, it can be calculated that under full sunlight in a temperate environment i.
Similarly, in the presence of one photo-inactivated D1 protein and before PSII monomerization necessary for repairing, which can be delayed and controlled by core complex proteins phosphorylation [ 63 , 64 ], the second intact core could use the energy harvested by the Lhc antennas associated to the damaged PSII core. Comparison of the overall PSII photosynthetic yield in dimeric or monomeric conformation in relationship with the fraction of open RC.
Photosynthetic yield of open and closed RC is taken accordingly to : 0. This effect increase when the population of open RC decreases dotted line. A similar curve has been measured in vivo already long time ago dotted lined, retraced from [65, ] and an even higher convexity of the overall PSII yield was found. This indicates that interconnectivity between PSII dimeric units extends that one between monomers in a single PSII dimer see text for further discussion.
Complejo del citocromo b6f
A Comparison Between Plant Photosystem I and Photosystem II Architecture and Functioning