Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2021
Publication Date: 3/23/2021
Citation: Foster, J., Cheng, N., Paris, V., Wang, L., Wang, J., Wang, X., Nakata, P.A. 2021. An arabidopsis oxalyl-CoA decarboxylase, AtOXC, is important for oxalate catabolism in plants. International Journal of Molecular Sciences. 22(6):3266. https://doi.org/10.3390/ijms22063266.
DOI: https://doi.org/10.3390/ijms22063266

Interpretive Summary: Plant scientists have been avidly working to discover new strategies to increase crop resistance to oxalate-secreting fungal pathogens. These fungal pathogens produce oxalate as a plant toxin that is required by the fungus for plant infection. Such fungi are responsible for major crop losses each year. In this study we report the discovery of oxalyl-CoA decarboxylase which is an enzyme that catalyzes the second step in a previously uncharacterized pathway of oxalate degradation. Biochemical analysis showed that this enzyme converts oxalyl-CoA into formyl-CoA and CO2. Biological analysis revealed that the plants lacking a functional copy of the enzyme could not break down oxalate into CO2 and were more susceptible to the deleterious effects of oxalate exposure. Thus, the identification and isolation of this enzyme is an important advancement in our understanding of oxalate metabolism. It also provides us with a new strategy that may help protect crop plants from oxalate-secreting phytopathogens which would have a beneficial impact on crop yields.

Technical Abstract: Considering the widespread occurrence of oxalate in nature and its broad impact on a host of organisms, it is surprising that so little is known about the turnover of this important acid. In plants, oxalate oxidase is the most well studied enzyme capable of degrading oxalate, but not all plants possess this activity. Recently, an Acyl Activating Enzyme 3 (AAE3), encoding an oxalyl-CoA synthetase, was identified in Arabidopsis. This enzyme has been proposed to catalyze the first step in an alternative pathway of oxalate degradation. Since this initial discovery, this enzyme and proposed pathway has been found to be important to other plants and yeast as well. In this study we identify, in Arabidopsis, an oxalyl-CoA decarboxylase (AtOXC) that is capable of catalyzing the second step in this proposed pathway of oxalate catabolism. This enzyme breaks down oxalyl-CoA, the product of AtAAE3, into formyl-CoA and CO2. AtOXC:GFP localization suggested that this enzyme functions within the cytosol of the cell. An Atoxc knock-down mutant showed a reduction in the ability to degrade oxalate into CO2. This reduction in AtOXC activity resulted in an increase in the accumulation of oxalate and the enzyme substrate, oxalyl-CoA. Size exclusion studies suggest that the enzyme functions as a dimer. Computer modeling of the AtOXC enzyme structure identified amino acids of predicted importance in co-factor binding and catalysis. Overall, these results suggest that AtOXC catalyzes the second step in this alternative pathway of oxalate catabolism.