An old dog with new tricks – the value of photorespiration as a central metabolic hub with implications for environmental acclimation

Abstract

Photorespiration serves as a metabolic repair system that safeguards photosynthetic carbon fixation in photoautotrophic organisms thriving in today’s oxygen-rich atmosphere. This essential process detoxifies the inhibitory metabolite 2-phosphoglycolate (2PG), an unavoidable byproduct of ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) activity in the light. If not efficiently metabolized, 2PG impairs key enzymatic processes involved in carbon assimilation and utilization thereby inhibiting growth in oxygenic phototrophs. Decades of research have unraveled the biochemical and genetic intricacies of photorespiration, establishing it as the second-highest carbon flux in illuminated leaves. Here, we discuss recent developments that have expanded our understanding of the pathway, revealing novel metabolic players, intricate inter-organelle interactions, and new regulatory networks. Isotope labeling studies and reverse genetics have identified further interactions of the classical photorespiratory cycle with central carbon and nitrogen metabolism. In order to enhance photosynthetic efficiency, synthetic biology approaches have reengineered photorespiration, either by integrating bypass pathways or optimizing native enzymes. These interventions highlight the vast potential of optimized photorespiration to boost photosynthetic yield and enhance plant adaptation to future climates. Very recently, the importance of active photorespiration in guard cells was discovered, linking it to the regulation of stomatal metabolism and behavior. Collectively, these recent findings reinforce the immense promise of continued photorespiratory research in developing innovative strategies for improving plant yield and resilience.