Dehydration-induced condensation of AGO1 modulates miRNA functionality

Abstract Recent studies have shown that microRNA (miRNA) functions are associated with plant responses to water deficiency. Mature miRNAs are loaded onto a complex that includes the ARGONAUTE 1 (AGO1) protein; this complex then cleaves mRNAs or inhibits their translation. Here, we demonstrate that the prion-like domain of AGO1 is responsible for topological changes in AGO1 under dehydration in Arabidopsis thaliana. AGO1 undergoes liquid-liquid phase separation (LLPS), which is driven by intrinsically disordered protein domains and plays diverse roles in cellular processes. LLPS of AGO in the cytoplasm influences miRNA regulatory activity, a process related to cytoplasmic calcium levels. We found that dehydration-induced AGO1 condensation influences AGO1 activity, while contributing to dehydration tolerance in plants. Upon rehydration, the condensation-driven accumulation of AGO1 is resolved, restoring its protein levels to normal. Overall, we propose that AGO1 phase separation acts as an emergent property in response to dehydration, attenuating the energy-consuming miRNA regulatory pathway in young seedlings.