Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO₂ Availability

The photorespiratory pathway or photorespiration is an essential process in oxygenic photosynthetic organisms, which can reduce the efficiency of photosynthetic carbon assimilation and is hence frequently considered as a wasteful process. By comparing the response of the wild-type plants and mutants impaired in photorespiration to a shift in ambient CO₂ concentrations, we demonstrate that photorespiration also plays a beneficial role during short-term acclimation to reduced CO₂ availability. The wild-type plants responded with few differentially expressed genes, mostly involved in drought stress, which is likely a consequence of enhanced opening of stomata and concomitant water loss upon a shift toward low CO₂. In contrast, mutants with impaired activity of photorespiratory enzymes were highly stressed and not able to adjust stomatal conductance to reduced external CO₂ availability. The transcriptional response of mutant plants was congruent, indicating a general reprogramming to deal with the consequences of reduced CO₂ availability, signaled by enhanced oxygenation of ribulose-1,5-bisphosphate and amplified by the artificially impaired photorespiratory metabolism. Central in this reprogramming was the pronounced reallocation of resources from growth processes to stress responses. Taken together, our results indicate that unrestricted photorespiratory metabolism is a prerequisite for rapid physiological acclimation to a reduction in CO₂ availability.