The trade-off function of photorespiration in a changing environment

Abstract

The photorespiratory pathway in plants comprises metabolic reactions distributed across several cellular compartments. It emerges from the dual catalytic function of Rubisco, i.e. ribulose-1,5-bisphosphate carboxylase/oxygenase. Rubisco either carboxylates or oxygenates ribulose-1,5-bisphosphate. Carboxylation reactions produce 3-phosphoglycerate molecules which are substrates for the central carbohydrate metabolism. However, oxygenation reactions additionally form 2-phosphoglycolate molecules which are (i) substrate for a multicompartmental recovery process, and (ii) inhibit several enzymes of the Calvin–Benson–Bassham cycle. Here, an approach of structural kinetic modelling is presented to investigate the extent of stabilization of the Calvin–Benson–Bassham cycle and carbohydrate metabolism by photorespiration. This method is based on a parametric representation of the Jacobian matrix of a metabolic system which offers a robust strategy for handling uncertainties associated with in vitro kinetic constants. Our findings indicate that oxygenation of ribulose-1,5-bisphosphate by Rubisco significantly stabilizes the Calvin–Benson–Bassham cycle. Hence, a trade-off function of photorespiration is suggested which reduces carbon assimilation rates but simultaneously stabilizes metabolism by increasing plasticity of metabolic regulation within the chloroplast. Furthermore, our analysis indicates that increasing carbon flux towards sucrose biosynthesis has a stabilizing effect. Finally, our findings shed light on the role of a multicompartmental metabolic pathway in stabilizing plant metabolism against perturbation induced by a dynamic environment.