Guard cell‐specific glycine decarboxylase manipulation affects Arabidopsis photosynthesis, growth and stomatal behavior

Abstract

Summary Photorespiration is a mandatory metabolic repair shunt of carbon fixation by the Calvin–Benson cycle in oxygenic phototrophs. Its extent depends mainly on the CO2 : O2 ratio in chloroplasts, which is regulated via stomatal movements. Despite a comprehensive understanding of the role of photorespiration in mesophyll cells, its role in guard cells (GC) is unknown. Therefore, a key enzyme of photorespiration, glycine decarboxylase (GDC), was specifically manipulated by varying glycine decarboxylase H‐protein (GDC‐H) expression in Arabidopsis GC. Multiple approaches were used to analyze the transgenic lines growth, their gas exchange and Chl fluorescence, alongside metabolomics and microscopic approaches. We observed a positive correlation of GC GDC‐H expression with growth, photosynthesis and carbohydrate biosynthesis, suggesting photorespiration is involved in stomatal regulation. Gas exchange measurements support this view, as optimized GC photorespiration improved plant acclimation toward conditions requiring a high photorespiratory capacity. Microscopic analysis revealed that altered photorespiratory flux also affected GC starch accumulation patterns, eventually serving as an underlying mechanism for altered stomatal behavior. Collectively, our data suggest photorespiration is involved in the regulatory circuit that coordinates stomatal movements with CO2 availability. Thus, the manipulation of photorespiration in GC has the potential to engineer crops maintaining growth and photosynthesis under future climates.