Comparative omics reveals unanticipated metabolic rearrangements in a high-oil mutant of plastid acetyl-CoA carboxylase

ABSTRACT Heteromeric acetyl-CoA carboxylase (ACCase) catalyzes the ATP-dependent carboxylation of acetyl-CoA to produce malonyl-CoA, the committed step for de novo fatty acid synthesis. In plants, ACCase activity is controlled at multiple levels, including negative regulation by biotin attachment domain-containing (BADC) proteins, of which the badc1/3 double mutant leads to increased seed triacylglycerol accumulation. Unexpectedly, the Arabidopsis badc1/3 mutant also accumulates more protein. The metabolic consequences from both higher oil and protein was investigated in developing badc1/3 seed using global transcriptomics, translatomics, proteomics, and metabolomics. Changes include: reduced plastid pyruvate dehydrogenase; increased acetyl-CoA synthetase; increased storage and lipid-droplet packaging proteins; increased lipases; and increased β-oxidation fatty acid catabolism. We present a model of how Arabidopsis adapted to deregulated ACCase, limiting total oil accumulation, and altering flux through pathways of carbon accumulation that presents possible targets for future bioengineering of valuable seed storage reserves.