Migratory neuronal progenitors arise from the neural plate borders in tunicates

Abstract

The neural crest is an evolutionary novelty that fostered the emergence of vertebrate anatomical innovations such as the cranium and jaws1. During embryonic development, multipotent neural crest cells are specified at the lateral borders of the neural plate before delaminating, migrating, and differentiating into various cell types. In invertebrate chordates (cephalochordates and tunicates), neural plate border cells express conserved factors such as Msx, Snail, and Pax3/7 and generate melanin-containing pigment cells2-4, a derivative of the neural crest in vertebrates. However, invertebrate neural plate border cells have not been shown to generate homologues of other neural crest derivatives. Thus, proposed models of neural crest evolution postulate vertebrate-specific elaborations on an ancestral neural plate border program, through acquisition of migratory capabilities and the potential to generate multiple cell types5-7. Here we show that a particular neuronal cell type in the tadpole larva of the tunicate Ciona intestinalis, the bipolar tail neuron, shares a set of features with neural crest-derived spinal ganglia neurons in vertebrates. Bipolar tail neuron precursors derive from caudal neural plate border cells, delaminate, and migrate along the paraxial mesoderm on either side of the neural tube, eventually differentiating into afferent neurons that form synaptic contacts with both epidermal sensory cells and motor neurons. We propose that the neural plate borders of the chordate ancestor already produced migratory peripheral neurons and pigment cells, and that the neural crest evolved through the acquisition of a multipotent progenitor regulatory state upstream of multiple, pre-existing neural plate border cell differentiation programs.

Nodal and FGF coordinate ascidian neural tube morphogenesis

“…We are also curious about the final fate of A10.64 derivatives, which migrate anteriorly along the neural tube as the tail extends. It is conceivable that these cells respond to the same migratory cues as the BTN cells, which possess some of the properties of neural crest derivatives (Stolfi et al, 2015). It is also possible that A10.64 cells correspond to Islet-positive neurons of the visceral ganglion (Stolfi and Levine, 2011) rather than A10.57.…”

Conserved gene regulatory module specifies lateral neural borders across bilaterians

“…Another example of more lateral Msx/ vab-15 expression exists in the urochordate C. intestinalis. Two NPB cells (b8.18 and b8.21) give rise to BTNs, which are likely the counterparts to vertebrate dorsal root ganglion (DRG) mechanosensory neurons (9) (Fig. 4C).…”

“…The laterally located V5 and Q neuroblasts give rise to PNS neurons; that is, V5 neuroblasts give rise to the mechanosensory neuron PVD, whereas QL and QR neuroblasts give rise to the migratory mechanosensory neurons AVM and PVM, respectively (10). Furthermore, Q neuroblasts undergo delamination and migrate along prototypical paths while dividing and differentiating (10), similar to the neural crest in vertebrates and mechanosensory bipolar tail neurons (BTNs) in tunicate (3,9). At the molecular level, Msx/vab-15 establishes the identity of the lateral boundary of the neuroectoderm in fly, annelids, amphioxus, lamprey, and higher vertebrates.…”

“…For example, the PPE is confined to the anterior half of embryos and does not contribute to the central nervous system (CNS), whereas the NPB is the lateral border of the whole neural plate and consists not only of progenitors for the PNS but also those for the CNS in the dorsal neural tube. The juxtaposed localization of the CNS neuroectoderm and PNS progenitors also occurs in the trunk of invertebrate embryos such as nematodes, arthropods, annelids, and urochordates (6)(7)(8)(9), reminiscent of vertebrate NPB. In Caenorhabditis elegans, lateral neuroblasts (P, Q, and V5 cells) are located between the embryonic CNS and skin from the birth of these cells (10).…”

Aquatic Model Organisms in Neurosciences: The Genome-Editing Revolution

“…Bill Jeffery identified migratory pigment cells in ascidians (Jeffery et al 2004;Jeffery 2006) and, more recently, Lionel Christiaen's group identified migrating neuron precursors in the ascidian Ciona intestinalis. Interestingly, these precursors were shown to arise from the border of the neural plate, a hallmark of the neural crest in vertebrates (Stolfi et al 2015).…”