Comparison of differentiation gene batteries for migratory mechanosensory neurons across bilaterians

In embryos of distantly related bilaterian phyla, their lateral neural borders give rise to the peripheral nervous system elements, including various mechanosensory cells derived from migratory precursors, such as hair cells and dorsal root ganglion (DRG) neurons in vertebrates, bipolar tail neuron (BTN) in Ciona, chordotonal organ in Drosophila, and AVM/PVM in Caenorhabditis elegans. Developmental genetics studies had revealed a couple of transcription factors (TFs) regulating differentiation of mechanosensory cells shared by vertebrates and arthropods. However, unbiased systematic profiling of regulators is needed to demonstrate conservation of differentiation gene batteries for mechanosensory cells across bilaterians. At first, we observed that in both C. elegans Q neuroblasts and Drosophila lateral neuroectoderm, conserved NPB specifier Msx/vab-15 regulates Atoh1/lin-32, supporting the homology of mechanosensory neuron development in lateral neural border lineage of Ecdysozia. So we used C. elegans as a protostomia model. Single-cell resolution expression profiling of TFs and genetic analysis revealed a differentiation gene battery (Atonh1/lin-32, Drg11/alr-1, Gfi1/pag-3, Lhx5/mec-3, and Pou4/unc-86) for AVM/PVM mechanosensory neurons. The worm-gene battery significantly overlaps with both that of placode-derived Atonh1/lin-32-dependent hair cells and that of NPB-derived Neurogenin-dependent DRG neurons in vertebrates, supporting the homology of molecular mechanisms underlying the differentiation of neural border-derived mechanosensory cells between protostome and deuterostome. At last, Ciona BTN, the homolog of vertebrate DRG, also expresses Atonh1/lin-32, further supporting the homology notion and indicating a common origin of hair cells and DRG in vertebrate lineage.