A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation

Many organisms evolved strategies to survive desiccation. Plant seeds protect dehydrated embryos from various stressors and can lay dormant for millennia. Hydration is the key trigger to initiate germination, but the mechanism by which seeds sense water remains unresolved. We identified an uncharacterized Arabidopsis thaliana prion-like protein we named FLOE1, which phase separates upon hydration and allows the embryo to sense water stress. We demonstrate that biophysical states of FLOE1 condensates modulate its biological function in vivo in suppressing seed germination under unfavorable environments. We find intragenic, intraspecific, and interspecific natural variation in FLOE1 expression and phase separation and show that intragenic variation is associated with adaptive germination strategies in natural populations. This combination of molecular, organismal, and ecological studies uncovers FLOE1 as a tunable environmental sensor with direct implications for the design of drought-resistant crops, in the face of climate change. [Display omitted] •FLOE1 is a plant-specific gene that regulates seed germination under water stress•FLOE1 undergoes reversible hydration-dependent phase separation•Ecological data suggest that FLOE1 variation is involved in local adaptation•FLOE1 can be engineered to tune seed germination with potential use for agriculture A previously uncharacterized protein, FLOE1, functions in seeds as a water potential sensor and can undergo reversible phase separation.