Temperature-dependent regulation of electron transport and ATP synthesis in chloroplasts in vitro and in silico

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 (PQH(2)) oxidation by the cytochrome (Cyt) b(6)f complex, (3) the ATP synthase activity, and (4) the proton leak from the thylakoid lumen. We consider that PQH(2) 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 PQH(2) oxidation by the Cyt b(6)f 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 b(6)f 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 -> O-2).