The activation state of Rubisco directly limits photosynthesis at low CO2 and low O2 partial pressures

Using gas exchange, enzyme assays, and theoretical modeling of photosynthetic responses to light and CO2, we investigated whether decarbamylation of the active site of Rubisco at low CO2 and low light leads to a condition where the activation state of Rubisco directly limits the rate of net CO2 assimilation. Photosynthetic limitation by a reduction in the activation state of Rubisco would be indicated as a decline in the initial slope of the photosynthetic CO2 response relative to what is predicted using theoretical models. In bean (Phaseolus vulgaris) and oat (Avena sativa), we saw no discrepancy between predicted and observed initial slope values at 200 and 400 mbar O2, indicating no limitation by the carbamylation state of Rubisco. At 30 mbar O2 and light saturation, we also saw no discrepancy between predicted and observed initial slope values; however, at subsaturating light intensity, our observed initial slope values were less than the modeled initial slope values that corresponded to an RuBP regeneration limitation. Moreover, significant reduction of the Rubisco activation state occurred in both species at 30 mbar O2 and 30 μbar CO2. When the model was reprogrammed to account for observed levels of Rubisco deactivation, the predicted and measured initial slope values at low O2 and low PPFD were similar, indicating the reduction in carbamylation state accounted for the discrepancy. We interpret this as evidence for a direct limitation of the carbamylation state of Rubisco, probably because of a CO2 limitation for carbamate formation. This limitation was only observed at intercellular CO2 levels below what is encountered in vivo. At physiologically relevant CO2 levels in situ, the leaves maintained sufficient Rubisco activity to avoid cabamylation state limitations in the steady state.