A photorespiratory glyoxylate shunt in the cytosol supports photosynthesis and plant growth under high light conditions in Arabidopsis

Abstract

Photorespiration, a central aspect of plant metabolism that is tightly connected to photosynthesis, functions in part to support photosynthetic performance, especially under stress conditions such as high light. However, our understanding of the mechanisms underlying the role and regulation of photorespiration in plant response to high light is limited. To identify modulators of photorespiration under high light, we isolated genetic suppressors of the photorespiratory mutant hpr1, which is defective in the peroxisomal hydroxypyruvate reductase 1. A suppressor that partially rescued hpr1 under high light was mapped to GLYR1, which encodes the cytosolic glyoxylate reductase 1 enzyme that converts glyoxylate to glycolate. Independent GLYR1 loss-of-function mutants also partially rescued hpr1 and another photorespiratory mutant, catalase 2. Our genetic, transcriptomic and metabolic profiling analyses together suggested a novel connection between cytosolic glyoxylate and a non-canonical photorespiratory route mediated by the cytosolic HPR2 enzyme, which we named the photorespiratory glyoxylate shunt. This shunt is especially critical under high light intensities when a high rate of photorespiratory flux is required and in the absence of a properly functional major photorespiratory pathway. Our findings support the metabolic flexibility of photorespiration and may help future efforts to improve crop performance under stress.