Neural plate morphogenesis and pre-patterning enable specification of intermediate progenitors in the spinal cord

Spinal cord organization begins with the specification of a series of neural progenitor domains along the dorsal-ventral axis of the neural tube. Patterning at the dorsal and ventral ends is established by canonical morphogen gradients. Intermediate progenitor domains are located distally to morphogen sources yet display similar organization. How this is achieved is unclear and the relevant positional cues have not been identified. Here we show that intermediate progenitor domains are established through a distinct mechanism that operates in the preceding neural plate stage and leverages its multiple signaling inputs and morphogenesis. An integrated spatial atlas of transcription factor expression, signaling activity, and cell movement reveals that the neural plate comprises an array of cell states, defined by combinatorial signaling and morphogenesis-driven transitions between local signaling environments. Specifically, we find that p0 and p1 intermediate progenitors, located immediately outside the morphogen-patterned region, arise from specific precursor states that are established in the posterior neural plate by tailbud-derived Wnt signaling. Convergent-extension movements subsequently drive progenitor specification by displacing precursors out of Wnt/FGF signaling fields while shaping them into stripe-like domains. Thus, by controlling signaling exposure, tissue dynamics convert positional information encoded by signaling history into downstream fate specification. This mode of patterning may operate broadly across developmental contexts, with implications for tissue engineering and patterning-related disorders.