Comparative Omics Reveals Unanticipated Metabolic Rearrangements in a High-Oil Mutant of Plastid Acetyl-CoA Carboxylase

Heteromeric acetyl-CoA carboxylase (ACCase) catalyzes the ATP-dependent carboxylation of acetyl-CoA to produce malonyl-CoA, which is 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 accumulated more protein. The metabolic consequences from both higher oil and protein were investigated in developing badc1/3 seed using global transcriptomics, translatomics, proteomics, metabolomics, and other biomass measurements. Changes included increased storage proteins and lipid droplet-packaging proteins, increased SDP1 lipase, altered organic acid metabolism, and reduced extracellular lipid synthesis perhaps offsetting the increase in TAG. We present a model of how Arabidopsis adapted to deregulated ACCase, resulting in more oil, and altered flux through pathways that partition carbon and propose targets for future bioengineering of seed storage reserves.