Photosynthetic free energy transduction related to the electric potential changes across the thylakoid membrane

Abstract

A model based on our present knowledge of photosynthetic energy transduction is presented. Calculated electric potential profiles are compared with microelectrode recordings of the thylakoid electric potential during and after actinic illumination periods of intermediate duration. The information content of the measured electric response is disclosed by a comparison of experimental results with calculations. The proton flux through the ATP synthase complex is seen to markedly influence the electric response. Also the imbalance in maximum turnover rate between the two photosystems, common to obligate shade plants like Peperomia metallica used in the microelectrode experiments, is clearly reflected in the electric potential profile.

The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged

“…As long as the rate of counterion movements is significantly slower than proton movement through the ATPase, the transmembrane ⌬, and thus DIRK ECS , will be linearly affected by the initial proton efflux upon shutter closure. In the cases where the steady-state ⌬ is dissipated by counterion movements, the initial proton efflux (driven by the proton diffusion potential) will establish a ''field inversion,'' where ⌬ will be positive on the stromal side of the membrane, as has been documented in microelectrode experiments (15,74) and in our own measurements of ECS in intact leaves (31). Thus the initial rate of change of ⌬ should still be proportional to the steady-state proton flux.…”

“…If the electrogenicity of postillumination hpc reduction represents a significant fraction of the total pmf, its kinetics would overlap and interfere with the decay of the ECS due to ATPase turnover. On the other hand, the pmf stored as ⌬pH and ⌬ are expected to be well buffered by weak acids (78)(79)(80)(81) and by counterion gradients (15), respectively, and thus the fractional contribution of the small number of turnovers that occur in the dark is expected to be small. This is clear from our previous data, in which the initial decay of the ECS occurs on a time scale of tens of milliseconds, but the field inversion, representing the collapse of the total pmf, decays 1,000-fold more slowly (31,74).…”

“…Because protons are charged, net transthylakoid proton movements will affect the membrane potential and thus can be followed by electrodes (15,74) or by the ECS (65, 75). The ECS is readily measured in higher plants (65,75) and green algae (76) and has been shown to be a linear indicator of transthylakoid electric field or ⌬ (75).…”

“…8-10) to 3 (e.g., refs. 11 and 12), and several groups have suggested that it changes from 3 to 2 with increasing light intensity (1,11,(13)(14)(15)(16)(17). Such indications of variable coupling ratios have led several groups to suggest that the Q cycle or its proton pumping reactions only operate under certain conditions (e.g., 1,10,[16][17][18] Cornic et al (22) argued that because antimycin A, a putative inhibitor of PSI-cyclic electron transfer, inhibits CO 2 fixation in isolated chloroplasts at high, but not low light, cyclic electron transfer is required to supplement the production of ATP at high CO 2 fixation rates.…”

A kinetic model of rapidly reversible nonphotochemical quenching

“…Although there are numerous models of chlorophyll fluorescence kinetics (24)(25)(26), the lumen (27), entire thylakoids (28), and zeaxanthin-dependent NPQ (29), we are not aware of any models simulate the kinetics of the appearance and disappearance of qE at low and high light intensities. Simulating qE in both low and high light intensities is necessary for quantifying the benefit that qE confers to plants in fluctuating light conditions.…”