mRNA concentration-dependent translation enables rapid and sharp patterning in resource-constrained Drosophila embryos

One of the fundamental challenges in protein expression during embryogenesis is the establishment of dynamic protein patterns under the resource constraint. This constraint is particularly stringent in enclosed Drosophila early embryogenesis, where protein synthesis relies exclusively on maternally supplied resources, yet its zygotic protein patterns still exhibit sharp boundaries and dynamic abundance changes for body plan development. Here, by integrating single-molecule imaging with mathematical modeling, we reveal that an mRNA concentration-dependent translation enables sharp and dynamics patterning even under resource constraint in embryos. Firstly, we reveal pronounced spatial heterogeneity in the fraction of hunchback (hb) mRNAs engaged in translation, challenging the conventional assumption of uniform translation rates. We further demonstrate that hb mRNA concentration is a dominant predictor of this heterogeneity, showing an increasing-saturation relationship between this translating fraction and mRNA abundance. This regulatory strategy enables combination of sharp Hb protein boundaries and close tracking of protein level to mRNA concentration decline under slow protein turnover rates, correlated to the resource efficiency in embryos. Together, our findings identify a translational control strategy that links molecular-scale regulation to embryonic pattern formation under resource constraints and highlight mRNA concentration-dependent translation as an effective way simultaneously enabling dynamic and economical spatial gene expression in biological systems.