Probing the role of Valine 185 of the D1 protein in the Photosystem II oxygen evolution

Sugiura, Masahiro; Tibiletti, Tania; Takachi, Itsuki; Hara, Yasutake; Kanawaku, Shin; Sellés, Julien; Boussac, Alain

doi:10.1016/j.bbabio.2018.10.003

Cited by 18 publications

(19 citation statements)

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“…is unusual but has synthetic precedents, for example in the work of Borovik and coworkers [107]. Importantly, detailed EPR studies by Boussac [81,108,109]. This can be considered an experimental demonstration of the gating role of structural bistability in the S 2 state and of the catalytic competence of the high-spin S 2 component, providing strong support for the scheme derived from quantum chemical studies in Figure 5a.…”

Section: S 3 Model [30]mentioning

confidence: 68%

“…A species with a five-coordinate Mn(IV) is unusual but has synthetic precedents, for example in the work of Borovik and coworkers [107]. Importantly, detailed EPR studies by Boussac and coworkers indicate that the multiline signal of the S2 state (attributed here to the open cubane model S2 A ) is formed first and converts to higherspin signals (associated here with the closed cubane topology of S2 B ) in order for the Mn ions to be oxidized by the tyrosyl radical and advance to the S3 state [81,108,109]. This can be considered an experimental demonstration of the gating role of structural bistability in the S2 state and of the catalytic competence of the high-spin S2 component, providing strong support for the scheme derived from quantum chemical studies in Figure 5a.…”

Section: S 3 Model [30]mentioning

confidence: 99%

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The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

Pantazis

2019

Inorganics

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The catalytic cycle of the oxygen-evolving complex (OEC) of photosystem II (PSII) comprises five intermediate states Si (i = 0–4), from the most reduced S0 state to the most oxidized S4, which spontaneously evolves dioxygen. The precise geometric and electronic structure of the Si states, and hence the mechanism of O–O bond formation in the OEC, remain under investigation, particularly for the final steps of the catalytic cycle. Recent advances in protein crystallography based on X-ray free-electron lasers (XFELs) have produced new structural models for the S3 state, which indicate that two of the oxygen atoms of the inorganic Mn4CaO6 core of the OEC are in very close proximity. This has been interpreted as possible evidence for “early-onset” O–O bond formation in the S3 state, as opposed to the more widely accepted view that the O–O bond is formed in the final state of the cycle, S4. Peroxo or superoxo formation in S3 has received partial support from computational studies. Here, a brief overview is provided of spectroscopic information, recent crystallographic results, and computational models for the S3 state. Emphasis is placed on computational S3 models that involve O–O formation, which are discussed with respect to their agreement with structural information, experimental evidence from various spectroscopic studies, and substrate exchange kinetics. Despite seemingly better agreement with some of the available crystallographic interpretations for the S3 state, models that implicate early-onset O–O bond formation are hard to reconcile with the complete line of experimental evidence, especially with X-ray absorption, X-ray emission, and magnetic resonance spectroscopic observations. Specifically with respect to quantum chemical studies, the inconclusive energetics for the possible isoforms of S3 is an acute problem that is probably beyond the capabilities of standard density functional theory.

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Section: S 3 Model [30]mentioning

confidence: 68%

Section: S 3 Model [30]mentioning

confidence: 99%

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

Pantazis

2019

Inorganics

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“…The maximum activities in PsbA3‐thylakoids at pH 7.0 and PsbA3/R323E at pH 6.5 were very similar with ~330–310 μmol O 2 (mg Chl) −1 h −1 . In WT*3 sample, the pH value of 7.0 has been shown to be the pH at which the activity is the highest in the presence of DCBQ whereas it is at pH 6.5 in the presence of PPBQ (discussed in Sugiura et al 2018).…”

Section: Resultsmentioning

confidence: 99%

“…For identifying which amino acids outside the first coordination sphere of the Mn 4 CaO 5 are involved in the networks tuning the properties of the cluster, a great number of site‐directed mutants have been constructed and studied. Among the residues studied and belonging to either D1, or D2 or CP43 or CP47 there are: D1/E65, D2/E312 and D1/E329 (Service et al 2010), D1/R334, D1/Q165, D2/D307, D2/E308, D2/D310, D2/D323 (Service et al 2014) and D2/K317 (Pokhrel et al 2013, Suzuki et al 2013), D1/N181 (Pokhrel et al 2015), D1/N298 (Nagao et al 2017), D1/N87 (Banerjee et al 2018), D1/S169 (Ghosh et al 2019a), D1/P173 (Sugiura et al 2014b), CP43/R357 (Ghosh et al 2019b) and D1/V185 (Bao and Burnap 2015, Sugiura et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Probing the role of arginine 323 of the D1 protein in photosystem II function

Sugiura

Taniguchi

Tango

et al. 2020

Physiologia Plantarum

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The Mn4CaO5 cluster of photosystem II (PSII) advances sequentially through five oxidation states (S0 to S4). Under the enzyme cycle, two water molecules are oxidized, O2 is generated and four protons are released into the lumen. Umena et al. (2011) have proposed that, with other charged amino acids, the R323 residue of the D1 protein could contribute to regulate a proton egress pathway from the Mn4CaO5 cluster and TyrZ via a proton channel identified from the 3D structure. To test this suggestion, a PsbA3/R323E site‐directed mutant has been constructed and the properties of its PSII have been compared to those of the PsbA3‐PSII by using EPR spectroscopy, polarography, thermoluminescence and time‐resolved UV–visible absorption spectroscopy. Neither the oscillations with a period four nor the kinetics and S‐state‐dependent stoichiometry of the proton release were affected. However, several differences have been found: (1) the P680+ decay in the hundreds of ns time domain was much slower in the mutant, (2) the S2QA−/DCMU and S3QA−/DCMU radiative charge recombination occurred at higher temperatures and (3) the S0TyrZ•, S1TyrZ•, S2TyrZ• split EPR signals induced at 4.2 K by visible light from the S0TyrZ, S1TyrZ, S2TyrZ, respectively, and the (S2TyrZ•)' induced by NIR illumination at 4.2 K of the S3TyrZ state differed. It is proposed that the R323 residue of the D1 protein interacts with TyrZ likely via the H‐bond network previously proposed to be a proton channel. Therefore, rather than participating in the egress of protons to the lumen, this channel could be involved in the relaxations of the H‐bonds around TyrZ by interacting with the bulk, thus tuning the driving force required for TyrZ oxidation.

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“…PSII is the light-driven water-splitting enzyme in cyanobacteria, alga, and plants. The main part of PSII consists of about 20 subunits, which bind to many cofactors as X-ray crystal structure revealed (Sugiura et al 2018). And most of these cofactors involving the water oxidation and electron transfer combine with the reaction center subunits, D1 and D2 protein.…”

Section: Gb Stabilizes the Synthesis Of The Structural Components Of mentioning

confidence: 99%

Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses

Huang

Zuo

2020

Planta

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Probing the role of Valine 185 of the D1 protein in the Photosystem II oxygen evolution

Cited by 18 publications

References 91 publications

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

Probing the role of arginine 323 of the D1 protein in photosystem II function

Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses

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