We formulate a biochemical reaction mechanism for the damped oscillations in the chlorophyll fluorescence, oxygen evolution, and carbon dioxide assimilation observed in leaves of higher (C-3) plants when a leaf in an atmosphere containing a high CO2 concentration is suddenly subjected to strong illumination. The mechanism is based on the type of gating behavior responsible for the rapid firing of nerve cells : the ATP-synthetase of the thylakoid membrane has a similar gating property that is responsive to changes in the Delta pH across the thylakoid membrane. The negative resistance of the gating behavior is used to create a positive feedback cycle in the rate of change of the Delta pH across the thylakoid membrane. The positive feedback cycle in conjunction with a slow, proton-gated, leak leads to oscillations in the Delta pH across the thylakoid membrane. There is no need to introduce a delay in the availability of inorganic phosphate to the enzymes of the Calvin cycle, as was done in earlier approaches of modeling damped oscillations. The kinetics of the proposed reaction mechanism is described by three differential equations which are solved numerically. Despite its simplicity, the model predicts oscillations (either to a stable focus or on a limit cycle) in the Delta pH across the thylakoid membrane (and consequently chlorophyll fluorescence) that are on the same time scale of the pH changes in the lumen under nonoscillatory conditions. The predicted damped oscillations in transthylakoid Delta pH are qualitatively similar to the changes to chlorophyll fluorescence quenching observed experimentally. The model also predicts an increase in the amplitude of oscillations under supersaturating CO2 conditions and a resonance when the activity of the Calvin cycle is perturbed periodically, observed for the first time as reported in a companion article. The model does not predict the dependence of the resonance response on the phase of the perturbation nor the alteration in average nonphotochemical quenching and average photochemical efficiency reported in the companion article.