Migratory neuronal progenitors arise from the neural plate borders in tunicates

Alberto Stolfi, Kerrianne Ryan, Ian A. Meinertzhagen, Lionel Christiaen

Research output: Contribution to journalArticle

Abstract

The neural crest is an evolutionary novelty that fostered the emergence of vertebrate anatomical innovations such as the cranium and jaws. 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 cells, 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 several cell types. 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.

Original languageEnglish (US)
Pages (from-to)371-374
Number of pages4
JournalNature
Volume527
Issue number7578
DOIs
StatePublished - Nov 19 2015

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Neural Plate
Urochordata
Neural Crest
Vertebrates
Neurons
Invertebrates
Larva
Tail
Ciona intestinalis
Afferent Neurons
Neural Tube
Melanins
Spinal Ganglia
Motor Neurons
Mesoderm
Sensory Receptor Cells
Jaw
Skull
Embryonic Development
Cell Differentiation

ASJC Scopus subject areas

  • General

Cite this

Migratory neuronal progenitors arise from the neural plate borders in tunicates. / Stolfi, Alberto; Ryan, Kerrianne; Meinertzhagen, Ian A.; Christiaen, Lionel.

In: Nature, Vol. 527, No. 7578, 19.11.2015, p. 371-374.

Research output: Contribution to journalArticle

Stolfi, Alberto ; Ryan, Kerrianne ; Meinertzhagen, Ian A. ; Christiaen, Lionel. / Migratory neuronal progenitors arise from the neural plate borders in tunicates. In: Nature. 2015 ; Vol. 527, No. 7578. pp. 371-374.
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