Understanding plant resilience by putting photosynthesis and photorespiration in the metabolic context

Photorespiration is a dynamic metabolic process that contributes to energy balance, stress resilience, and nutrient flux, warranting its integration into genome-scale models to enhance plant productivity and climate adaptation. Photorespiration, sometimes referred to as a wasteful byproduct of rubisco's oxygenation activity, is increasingly recognized as a vital and multifaceted component of plant metabolism. This perspective explores three underappreciated roles of photorespiration: as an alternative energy sink, a marker of stress resilience, and a metabolic hub. Photorespiration consumes significant ATP and reducing equivalents, potentially serving as a photoprotective mechanism under environmental stress. However, its role in energy dissipation remains debated, particularly in relation to non-photochemical quenching. Stress conditions such as drought and heat elevate photorespiratory flux due to Rubisco kinetics and stomatal responses, yet the link between photorespiration and resilience is complex and species-dependent. Metabolites like serine and glycine, key intermediates in photorespiration, correlate with stress responses and may exit the canonical pathway, contributing to one-carbon metabolism and amino acid biosynthesis. Calculations suggest that serine export from photorespiration could explain nitrate assimilation rates, yet protein synthesis alone cannot account for this flux, indicating unknown metabolic sinks. Genome-scale metabolic models (GSMMs) and resource allocation models (RAMs) offer promising tools to integrate photorespiration into broader metabolic frameworks. These models can simulate open-loop versus closed-loop photorespiration, assess energy dissipation capacity, and track amino acid fate. Future research should focus on refining GSMMs to include accurate photorespiratory pathways and leveraging them to understand photorespiration's role in plant resilience and nutrition, especially under realistic field conditions. This integrated approach is essential for reimagining photorespiration not as a metabolic burden, but as a central player in plant adaptation and productivity.