To survive extreme desiccation, seeds enter a period of dormancy that can last millennia. Seed dormancy involves the accumulation of protective storage proteins through unknown adjustments in proteasomal degradation. Mutating all six type II metacaspase (MCA-II) proteases in Arabidopsis thaliana revealed their essential roles in modulating proteasomal degradation. MCA-II mutant seeds fail to target the AAA ATPase CELL DIVISION CYCLE 48 (CDC48) at the endoplasmic reticulum to discard misfolded proteins, compromising their storability. Moreover, we show that MCA-IIs cleave a PUX (ubiquitination regulatory X domain-containing) adaptor, which is responsible for the localization of CDC48 to lipid droplets. This cleavage enables the shuttling of CDC48 between lipid droplets and the endoplasmic reticulum, constituting an important step in the regulation of spatiotemporal proteolysis. In summary, we uncovered a proteolytic pathway conferring seed longevity.