Stoichiometric analysis of the energetics and metabolic impact of photorespiration in C3 plants

Summary Analysis of the impact of photorespiration on plant metabolism is usually based on manual inspection of small network diagrams. Here we create a structural metabolic model that contains the reactions that participate in photorespiration in the plastid, peroxisome, mitochondrion and cytosol, and the metabolite exchanges between them. This model was subjected to elementary flux modes analysis, a technique that enumerates all the component, minimal pathways of a network. Any feasible photorespiratory metabolism in the plant will be some combination of the elementary flux modes (EFMs) that contain the Rubisco oxygenase reaction. Amongst the EFMs we obtained was the classic photorespiratory cycle, but there were also modes that involve photorespiration coupled with mitochondrial metabolism and ATP production, the glutathione‐ascorbate cycle and nitrate reduction to ammonia. The modes analysis demonstrated the underlying basis of the metabolic linkages with photorespiration that have been inferred experimentally. The set of reactions common to all the elementary modes showed good agreement with the gene products of mutants that have been reported to have a defective phenotype in photorespiratory conditions. Finally, the set of modes provided a formal demonstration that photorespiration itself does not impact on the CO2:O2 ratio (assimilation quotient), except in those modes associated with concomitant nitrate reduction. Significance Statement A comprehensive identification of the alternative pathways of photorespiratory metabolism using elementary modes analysis demonstrates that photorespiration itself does not have an impact on the CO2:O2 ratio (or assimilation quotient), but can dissipate ATP and reductant resulting from excess light input. The stoichiometric requirement for redox and ATP balancing in the chloroplast is met in some pathways by linkage to nitrate reduction, and it is the latter that changes the assimilation quotient in photorespiratory conditions.