Disruption of the Arabidopsis Acyl-Activating Enzyme 3 Impairs Seed Coat Mucilage Accumulation and Seed Germination

The Acyl-activating enzyme (AAE) 3 gene encodes an oxalyl-CoA synthetase that catalyzes the conversion of oxalate to oxalyl-CoA as the first step in the CoA-dependent pathway of oxalate catabolism. Although the role of this enzyme in oxalate catabolism has been established, its biological roles in plant growth and development are less understood. As a step toward gaining a better understanding of these biological roles, we report here a characterization of the Arabidopsis thaliana aae3 (Ataae3) seed mucilage phenotype. Ruthidium red (RR) staining of Ataae3 and wild type (WT) seeds suggested that the observed reduction in Ataae3 germination may be attributable, at least in part, to a decrease in seed mucilage accumulation. Quantitative RT-PCR analysis revealed that the expression of selected mucilage regulatory transcription factors, as well as of biosynthetic and extrusion genes, was significantly down-regulated in the Ataae3 seeds. Mucilage accumulation in seeds from an engineered oxalate-accumulating Arabidopsis and Atoxc mutant, blocked in the second step of the CoA-dependent pathway of oxalate catabolism, were found to be similar to WT. These findings suggest that elevated tissue oxalate concentrations and loss of the oxalate catabolism pathway downstream of AAE3 were not responsible for the reduced Ataae3 seed germination and mucilage phenotypes. Overall, our findings unveil the presence of regulatory interplay between AAE3 and transcriptional control of mucilage gene expression.