Solid-like PAR protein assemblies encode long-term spatial memory of cell polarity during suspended animation

Abstract

During suspended animation, organisms must preserve cellular organization despite the collapse of the active biochemical processes that normally maintain it. Here we show that anoxia-induced suspended animation drives cell polarity proteins into a poised, memory-like state that preserves spatial information and templates rapid resumption of morphogenesis upon reanimation. In C. elegans embryos, anoxia drives progressive assembly of the polarity protein PAR-3 into solid-like clusters that preserve the polarity axis during metabolic arrest despite inactivation of patterning reactions normally required to maintain PAR asymmetry. Embryos expressing cluster-defective PAR-3 fail to maintain asymmetry during arrest and consequently exhibit polarity axis defects upon reanimation, demonstrating that arrested PAR-3 clusters function as physical templates for re-establishment of polarity. Our data suggest that cells cope with transient metabolic arrest by reversibly converting actively maintained biochemical patterns into stable physical templates that preserve spatial information for later reactivation.