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Modeling of the redox state dynamics in photosystem II of Chlorella pyrenoidosa Chick cells and leaves of spinach and Arabidopsis thaliana from single flash-induced fluorescence quantum yield changes on the 100 ns–10 s time scale

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Abstract

The time courses of the photosystem II (PSII) redox states were analyzed with a model scheme supposing a fraction of 11–25 % semiquinone (with reduced \({\text{Q}}_{\text{B}}^{ - }\)) RCs in the dark. Patterns of single flash-induced transient fluorescence yield (SFITFY) measured for leaves (spinach and Arabidopsis (A.) thaliana) and the thermophilic alga Chlorella (C.) pyrenoidosa Chick (Steffen et al. Biochemistry 44:3123−3132, 2005; Belyaeva et al. Photosynth Res 98:105–119, 2008, Plant Physiol Biochem 77:49–59, 2014) were fitted with the PSII model. The simulations show that at high-light conditions the flash generated triplet carotenoid 3Car(t) population is the main NPQ regulator decaying in the time interval of 6–8 μs. So the SFITFY increase up to the maximum level \(F_{\text{m}}^{\text{STF}}\)/F 0 (at ~50 μs) depends mainly on the flash energy. Transient electron redistributions on the RC redox cofactors were displayed to explain the SFITFY measured by weak light pulses during the PSII relaxation by electron transfer (ET) steps and coupled proton transfer on both the donor and the acceptor side of the PSII. The contribution of non-radiative charge recombination was taken into account. Analytical expressions for the laser flash, the 3Car(t) decay and the work of the water-oxidizing complex (WOC) were used to improve the modeled P680+ reduction by YZ in the state S 1 of the WOC. All parameter values were compared between spinach, A. thaliana leaves and C. pyrenoidosa alga cells and at different laser flash energies. ET from \({\text{Q}}_{\text{A}}^{ - } \;{\text{to}}\;{\text{Q}}_{\text{B}}^{( - )}\) slower in alga as compared to leaf samples was elucidated by the dynamics of \({\text{Q}}_{\text{A}}^{ - } ,{\text{ Q}}_{\text{B}}^{ - }\) fractions to fit SFITFY data. Low membrane energization after the 10 ns single turnover flash was modeled: the ∆Ψ(t) amplitude (20 mV) is found to be about 5-fold smaller than under the continuous light induction; the time-independent lumen pHL, stroma pHS are fitted close to dark estimates. Depending on the flash energy used at 1.4, 4, 100 % the pHS in stroma is fitted to 7.3, 7.4, and 7.7, respectively. The biggest ∆pH difference between stroma and lumen was found to be 1.2, thus pH- dependent NPQ was not considered.

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Abbreviations

Chl:

Chlorophyll

PSII:

Photosystem II

RC:

Reaction center (PSII)

P680, P680 :

Chlorophyll a acting as the electron donor in PSII

Phe, Ph:

Primary electron acceptor, pheophytin

QA and QB :

Primary and secondary plastoquinone electron acceptors of PSII

3Car:

Triplet carotenoid state

YZ :

Tyrosine 161 of the PSII D1 polypeptide

WOC:

Water oxidizing complex

PQ:

Plastoquinone

PQH2 :

Plastoquinol

\({\text{H}} _{\text{L}}^{ + } ,{\text{ H}}_{\text{S}}^{ + }\) :

Protons in lumen, in stroma

pHL, pHS :

pH in lumen, in stroma

∆Ψ :

Electrical potential across the thylakoid membrane

EET:

Excitation energy transfer

ET:

Electron transfer

PT:

Proton transfer

FL:

Fluorescence

ETC:

Electron transport chain

Cyt b 6 f :

Cytochrome b 6 f complex

k L :

Light excitation rate (time dependent)

k 3Car :

Rate constant of quenching by triplet carotenoids

k F :

Rate constant of fluorescence emission

k WOC :

Rate constant of the electron donation to the oxidized P680+•

LED:

Light emitting diode

PFD:

Photon flux density

F 0 :

Minimal FL yield

F m :

Maximal FL yield induced by multiturnover light

\(F_{\text{m}}^{\text{STF}}\) :

Maximal FL yield excited by single turnover flash

SFITFY:

Single flash-induced transient fluorescence yield

STF:

Single turnover flash

FWHM, fwhm:

Full width at half-maximum

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Acknowledgments

This work was supported by the RFBR 11-04-01268-a, 14-04-01536, by BMBF RUS 10/026, 11/014, BMBF project “Quantum” (FKZ 13N10076) and by COST action MP1205. We are grateful to Prof. A.A. Bulychev for fruitful discussions.

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  1. Department of Biophysics, Biology Faculty, M.V. Lomonosov Moscow State University, 119992, Moscow, Russia

    N. E. Belyaeva, V. Z. Paschenko, G. Yu. Riznichenko & A. B. Rubin

  2. Max-Volmer-Laboratory of Biophysical Chemistry, Institute of Chemistry, Technical University Berlin, Straβe des 17. Juni 135, 10623, Berlin, Germany

    F.-J. Schmitt

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  1. N. E. Belyaeva
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Belyaeva, N.E., Schmitt, FJ., Paschenko, V.Z. et al. Modeling of the redox state dynamics in photosystem II of Chlorella pyrenoidosa Chick cells and leaves of spinach and Arabidopsis thaliana from single flash-induced fluorescence quantum yield changes on the 100 ns–10 s time scale. Photosynth Res 125, 123–140 (2015). https://doi.org/10.1007/s11120-015-0163-4

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