Water content, adenylate kinase, and mitochondria drive adenylate balance in dehydrating and imbibing seeds

Water and life are inexorably linked, but some organisms are capable of losing almost all cellular water to enter a non-metabolic state of anhydrobiosis. This raises intriguing questions about how energy metabolism is managed during such transitions. Here, we have investigated adenylate metabolism during seed imbibition and drying using intact or fragmented pea (Pisum sativum L.) seeds. AMP was confirmed as the major adenylate stored in dry seeds, and normal adenylate balance was rapidly restored upon rehydration of the tissues. Conversely, re-drying of fully imbibed seeds reversed the balance toward AMP accumulation. The overall analysis, supported by in vitro enzyme mimicking experiments, shows that during tissue dehydration, when oxidative phosphorylation is no longer efficient because of decreasing water content, the ATP metabolic demand is met by adenylate kinase, resulting in accumulation of AMP. During seed imbibition, adenylate balance is rapidly restored from the AMP stock by the concerted action of adenylate kinase and mitochondria. The adenylate balance in orthodox seeds, and probably in other anhydrobiotes, appears to be simply driven by water content throughout the interplay between ATP metabolic demand, adenylate kinase, and oxidative phosphorylation, which requires mitochondria to be energetically efficient from the onset of imbibition.