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.