Native catalase expression in Arabidopsis thaliana is more than sufficient to limit excess decarboxylation from photorespiratory intermediates

Abstract

The hydrogen peroxide (H2O2) scavenging enzyme, catalase, plays a critical role in the photorespiratory pathway by maintaining the balance of H2O2, a reactive oxygen species (ROS), in the peroxisome. H2O2 acts as both a signaling molecule and a potential source of ROS depending on its accumulation in the peroxisome. Additionally, H2O2 can also drive non-enzymatic decarboxylation (NED) reactions as well as other decarboxylation reactions, leading to increased CO2 release that is linked to a severe growth phenotype. However, the exact cause of this stunted growth phenotype is not fully understood, and it remains unclear whether the capacity of catalase is critical for minimizing these decarboxylating reactions. Here we elucidate the mechanism behind the decrease in plant growth due to the accumulation of H2O2 from photorespiration using cat2 knock-out lines of Arabidopsis thaliana rescued with transgenic expression lines of Heliobacter pylori catalase. These experiments demonstrated that while one of the three heterologous lines expressing H. pylori catalase isoform (Hp615) had greater catalase activity than cat2-KO and rescued the severe growth and photosynthetic phenotype, its catalase activity was still far below wild type levels. These findings suggest that catalase plays a crucial role in maintaining H2O2 homeostasis within the peroxisome and minimizing decarboxylation reactions, both of which are linked to plant growth. Moreover, once a threshold capacity is reached, increasing catalase capacity further may offer limited benefits in enhancing net carbon fixation. HighlightWe show that peroxisomal catalase is important for maintaining high rates of net carbon fixation associated with plant growth. Native catalase levels in Arabidopsis thaliana are in excess of that which is required to minimize alternative decarboxylation reactions. Therefore, efforts to optimize catalase-mediated degradation of H2O2 may be of limited benefit.