Guard cell photorespiration has a major impact on photosynthesis, growth and stomatal behavior in Arabidopsis

Photorespiration is a mandatory metabolic repair shunt of carbon fixation by the Calvin-Benson (CB) cycle in oxygenic phototrophs. Its extent depends mainly on the CO2/O2 ratio in chloroplasts, which is regulated via stomatal movements. However, despite comprehensive understanding on the role of photorespiration in mesophyll cells (MC), its role in guard cells (GC) is yet unknown. To analyze this issue, the key enzyme of photorespiration, glycine decarboxylase (GDC), was manipulated through overexpression and antisense suppression of the GDC H-protein gene. A positive correlation of GDC-H expression with growth, photosynthesis and carbohydrate biosynthesis was observed in the transgenic lines, demonstrating active photorespiration is involved in stomatal regulation. This view is supported by gas exchange measurements showing that optimized GC photorespiration improves plant acclimation towards conditions requiring a high photorespiratory capacity, including high light. Microscopic analysis revealed that altered photorespiratory flux also affected starch accumulation patterns in GC, eventually serving as the underlying mechanistic for altered stomatal behavior. Collectively, our data suggest that photorespiration is a key component of the regulatory circuit that coordinates stomatal movements with external and internal CO2 availability. Thus, manipulation of photorespiration in GC has the potential to engineer crops maintaining growth and photosynthesis under future climates. One-sentence summaryGuard-cell-specific manipulation of photorespiratory glycine decarboxylase reveals photorespiration is active in guard cells and makes a major contribution to stomatal metabolism and movements.