Condensates act as translation hubs to coordinate multinucleate cell growth

Coordination between growth and division is a fundamental feature of cells. In many syncytia, cell growth must couple with multiple nuclear divisions in one cytoplasm. In the fungus, Ashbya gossypii, cell-cycle progression and hyphal elongation require condensates formed by the protein Whi3 in complex with distinct mRNA species. We hypothesized the condensates may act through local translation regulation and find that Whi3 target mRNAs show distinct spatial biases in translation in vivo. Whi3-RNA condensates can both promote and repress RNA translation in an RNA- and condensate size-dependent manner in vitro. Interestingly, we observe a sub-condensate enrichment of translation that is tunable by RNA valency and protein phospho-state. Together, these data suggest that Whi3 condensates generate a continuum of translation states, resulting in asynchronous nuclear divisions coordinated with growth. This local regulation requires a minimal complement of molecular components at the nano scale to support global coordination at the cell scale.