Temperature-dependent regulation of electron transport and ATP synthesis in chloroplasts in vitro and in silico
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ORIGINAL ARTICLE
Temperature‑dependent regulation of electron transport and ATP synthesis in chloroplasts in vitro and in silico Alexander N. Tikhonov1,2 · Alexey V. Vershubskii1 Received: 15 April 2020 / Accepted: 21 July 2020 © Springer Nature B.V. 2020
Abstract The significance of temperature-dependent regulation of photosynthetic apparatus (PSA) is determined by the fact that plant temperature changes with environmental temperature. In this work, we present a brief overview of temperature-dependent regulation of photosynthetic processes in class B chloroplasts (thylakoids) and analyze these processes using a computer model that takes into account the key stages of electron and proton transport coupled to ATP synthesis. The rate constants of partial reactions were parametrized on the basis of experimental temperature dependences of partial photosynthetic processes: (1) photosystem II (PSII) turnover and plastoquinone (PQ) reduction, (2) the plastoquinol ( PQH2) oxidation by the cytochrome (Cyt) b6f complex, (3) the ATP synthase activity, and (4) the proton leak from the thylakoid lumen. We consider that PQH2 oxidation is the rate-limiting step in the intersystem electron transport. The parametrization of the rate constants of these processes is based on earlier experimental data demonstrating strong correlations between the functional and structural properties of thylakoid membranes that were probed with the lipid-soluble spin labels embedded into the membranes. Within the framework of our model, we could adequately describe a number of experimental temperature dependences of photosynthetic reactions in thylakoids. Computer modeling of electron and proton transport coupled to ATP synthesis supports the notion that P QH2 oxidation by the Cyt b6f complex and proton pumping into the lumen are the basic temperature-dependent processes that determine the overall electron flux from PSII to molecular oxygen and the net ATP synthesis upon variations of temperature. The model describes two branches of the temperature dependence of the post-illumination reduction of P+700 characterized by different activation energies (about 60 and ≤ 3.5 kJ mol−1). The model predicts the bell-like temperature dependence of ATP formation, which arises from the balance of several factors: (1) the thermo-induced acceleration of electron transport through the Cyt b6f complex, (2) deactivation of PSII photochemistry at sufficiently high temperatures, and (3) acceleration of the passive proton outflow from the thylakoid lumen bypassing the ATP synthase complex. The model describes the temperature dependence of experimentally measured parameter P/2e, determined as the ratio between the rates of ATP synthesis and pseudocyclic electron transport (H2O → PSII → PSI → O2). Keywords Photosynthesis · Chloroplasts · Electron transport · Thylakoid membranes · Temperature-dependent regulation · Computer modeling Abbreviations CBC Calvin–Benson cycle DGDG Digalactosyldiacylglycerol EPR Electron paramagnetic resonance ETC Electron transport chai
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