Biogenesis of water splitting by photosystem II during de‐etiolation of barley (<i>Hordeum vulgare</i> L.)

Shevela, Dmitriy; Arnold, Janine; Reisinger, Veronika; Berends, Hans-Martin; Kmiec, Karol; Koroidov, Sergey; Bue, Ann Kristin; Messinger, Johannes; Eichacker, Lutz A.

doi:10.1111/pce.12719

Cited by 12 publications

(23 citation statements)

References 67 publications

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“…Then, the de‐etiolation process of the etiolated seedling was induced by continuous illumination with white light (30‐μmol photons m −2 s −1 ; Sylvania GroLux fluorescent tubes, F14W/GRO; Osram) at 25°C for 2, 4 and 8 h. Control (Ctrl) seedlings were grown for 108 h under continuous exposure to while light (30 μmol photons m −2 s −1 ). Isolation of etio−/chloroplasts was carried out immediately after the illumination of etiolated seedlings according to the standard procedures (Robinson et al ) with some modifications described earlier (Shevela et al ). After the final isolation step, the plastids were resuspended in storage/assay SCMNM medium (0.4‐M sucrose, 5‐mM CaCl 2 , 5‐mM MgCl 2 , 15‐mM NaCl and 40‐mM MES‐NaOH, pH 6.5) containing 10% (v/v) glycerol.…”

Section: Methodsmentioning

confidence: 99%

“…Kinetics of light‐induced O 2 production in Ctrl chloroplasts was measured by a time‐resolved MIMS setup (Beckmann et al , Shevela and Messinger ) consisting of an isotope ratio mass spectrometer (Thermo Finnigan DELTA plus XP; Thermo Finnigan), a cooling trap (77 K; liquid nitrogen) and a 150‐μl in‐house‐built membrane‐inlet cell, described in our recent report (Shevela et al ). The measurements were performed at 20°C under continuous stirring of the sample suspensions diluted with the CMNM buffer (pH 6.5) to a desired sample concentration (see below and legend of Fig.…”

Section: Methodsmentioning

confidence: 99%

“…Analysis of O 2 evolution was based on the m/z 34 signals ( 16 O 18 O) according to the procedure described earlier (Shevela et al ).…”

Section: Methodsmentioning

confidence: 99%

“…However, important questions regarding the origin of the impaired turnover efficiency of PSII observed during its de novo photoassembly and maturation of the thylakoid membrane remained unanswered. Thus, the following factors limiting performance of PSII have been suggested: (1) plastoquinone (PQ) Q A / Q B ‐site; (2) low abundance of oxidized PQ molecules in the developing thylakoids before the attachment of the light‐harvesting complex II (LHCII); and (3) further upstream limitations of the electron transport (Shevela et al ). Moreover, in the previous report, we found some indications that the juvenile PSII centers in etiochloroplasts may exhibit higher sensitivity to photodamage than the PSII of mature chloroplasts.…”

Section: Introductionmentioning

confidence: 99%

“…In the present work, we specifically study susceptibility of etiochloroplasts to photodamage and try to identify the limiting factor(s) in functional development of PSII during biogenesis of thylakoid membrane. For this, we focus on the previously established de‐etiolation time points (Shevela et al ), that reflect the key changes in performance of PSII during its de novo assembly and maturation (Scheme ).…”

Section: Introductionmentioning

confidence: 99%

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‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

Shevela

Ananyev

Vatland

et al. 2019

Physiologia Plantarum

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High solar flux is known to diminish photosynthetic growth rates, reducing biomass productivity and lowering disease tolerance. Photosystem II (PSII) of plants is susceptible to photodamage (also known as photoinactivation) in strong light, resulting in severe loss of water oxidation capacity and destruction of the water‐oxidizing complex (WOC). The repair of damaged PSIIs comes at a high energy cost and requires de novo biosynthesis of damaged PSII subunits, reassembly of the WOC inorganic cofactors and membrane remodeling. Employing membrane‐inlet mass spectrometry and O2‐polarography under flashing light conditions, we demonstrate that newly synthesized PSII complexes are far more susceptible to photodamage than are mature PSII complexes. We examined these ‘PSII birth defects’ in barley seedlings and plastids (etiochloroplasts and chloroplasts) isolated at various times during de‐etiolation as chloroplast development begins and matures in synchronization with thylakoid membrane biogenesis and grana membrane formation. We show that the degree of PSII photodamage decreases simultaneously with biogenesis of the PSII turnover efficiency measured by O2‐polarography, and with grana membrane stacking, as determined by electron microscopy. Our data from fluorescence, QB‐inhibitor binding, and thermoluminescence studies indicate that the decline of the high‐light susceptibility of PSII to photodamage is coincident with appearance of electron transfer capability QA− → QB during de‐etiolation. This rate depends in turn on the downstream clearing of electrons upon buildup of the complete linear electron transfer chain and the formation of stacked grana membranes capable of longer‐range energy transfer.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

“…Analysis of O 2 evolution was based on the m/z 34 signals ( 16 O 18 O) according to the procedure described earlier (Shevela et al ).…”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

Shevela

Ananyev

Vatland

et al. 2019

Physiologia Plantarum

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Photoassembly of the CaMn ₅ O ₅ Catalytic Core and Its Inorganic Mutants in Photosystem II

Gates

Ananyev

Dismukes

2017

Encyclopedia of Inorganic and Bioinorganic Chemistry

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“What I cannot create (build), I do not understand”—Richard Feynman The ability to take apart and reassemble atom by atom the elements of the water‐oxidizing complex (WOC) of photosynthetic enzymes and substitute each cofactor, while monitoring the consequences on photolytic charge separation and catalytic activity, has given deep insights into how photosynthetic water oxidation works, equal to any other method or technique. Here we summarize the literature covering the reconstitution of the inorganic core (Mn 4 CaO 5 ) of photosystem II water‐oxidizing complexes (PSII‐WOCs), called photoassembly, and the consequences of substitution of the inorganic cofactors with nonnative cofactors. We give the evidence that explains the universal utilization of manganese as the sole redox‐active element for O 2 evolution by all native PSII‐WOCs. The selection of Mn 2+ over other more abundant transition metals during uptake and photooxidation by apo‐WOC‐PSII is shown to be achieved by a combination of thermodynamic advantage (bicarbonate stabilization of Mn 3+ photoproduct) and kinetic advantage favoring slow charge recombination from its intermediates. Manganese is shown to be favored over other transition metals because it can operate over a wider range of turnover rates produced by solar fluxes from morning to midday to dusk. The speciation of aqueous manganese in cells in equilibrium with air and bicarbonate is described from thermodynamic data and used to explain how (bi)carbonate stabilizes Mn 2+ → Mn 3+ photooxidation and provides the core oxo bridges that build the Mn 4 CaO 5 cluster. The oxidation states of manganese obtained from photoassembly experiments are described and compared to spectroscopic results. The functional role of Ca 2+ in photoassembly and catalysis is revealed by substitution with Sr 2+ and Cd 2+ . These properties are advanced in order to understand how it is that evolution of only a single enzymatic blueprint for photosynthetic water oxidation has emerged, despite the access to every ecological niche on Earth and over 3 billion years of evolutionary history.

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Barley Proteomics

Mock¹,

Finnie²,

Witzel³

et al. 2018

Compendium of Plant Genomes

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Biogenesis of water splitting by photosystem II during de‐etiolation of barley (Hordeum vulgare L.)

Cited by 12 publications

References 67 publications

‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

Photoassembly of the CaMn ₅ O ₅ Catalytic Core and Its Inorganic Mutants in Photosystem II

Barley Proteomics

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Biogenesis of water splitting by photosystem II during de‐etiolation of barley (Hordeum vulgare L.)

Cited by 12 publications

References 67 publications

‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

Photoassembly of the CaMn 5 O 5 Catalytic Core and Its Inorganic Mutants in Photosystem II

Barley Proteomics

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Photoassembly of the CaMn ₅ O ₅ Catalytic Core and Its Inorganic Mutants in Photosystem II