Precraniate origin of cranial motoneurons.
The craniate head is innervated by cranial sensory and motor neurons. Cranial sensory neurons stem from the neurogenic placodes and neural crest and are seen as evolutionary innovations crucial in fulfilling the feeding and respiratory needs of the craniate "new head." In contrast, cranial motoneurons that are located in the hindbrain and motorize the head have an unclear phylogenetic status. Here we show that these motoneurons are in fact homologous to the motoneurons of the sessile postmetamorphic form of ascidians. The motoneurons of adult Ciona intestinalis, located in the cerebral ganglion and innervating muscles associated with the huge "branchial basket," express the transcription factors CiPhox2 and CiTbx20, whose vertebrate orthologues collectively define cranial motoneurons of the branchiovisceral class. Moreover, Ciona's postmetamorphic motoneurons arise from a hindbrain set aside during larval life and defined as such by its position (caudal to the prosensephalic sensory vesicle) and coexpression of CiPhox2 and CiHox1, whose orthologues collectively mark the vertebrate hindbrain. These data unveil that the postmetamorphic ascidian brain, assumed to be a derived feature, in fact corresponds to the vertebrate hindbrain and push back the evolutionary origin of cranial nerves to before the origin of craniates.
Dufour
Héloïse D
HD
Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8542, Ecole Normale Supérieure, 46 Rue d'Ulm, 75005 Paris, France.
Chettouh
Zoubida
Z
Deyts
Carole
C
de Rosa
Renaud
R
Goridis
Christo
C
Joly
Jean-Stéphane
JS
Brunet
Jean-François
JF
D000818:Animals; D002938:Ciona intestinalis / Q000166:cytology* / Q000196:embryology / Q000254:growth & development; D004625:Embryo, Nonmammalian / Q000166:cytology; D045888:Ganglion Cysts / Q000378:metabolism; D006257:Head / Q000294:innervation*; D018398:Homeodomain Proteins / Q000378:metabolism; D007814:Larva / Q000254:growth & development / Q000378:metabolism; D008675:Metamorphosis, Biological; D051379:Mice; D008969:Molecular Sequence Data; D009046:Motor Neurons / Q000166:cytology*; D020825:T-Box Domain Proteins / Q000378:metabolism
D018398:Homeodomain Proteins; D020825:T-Box Domain Proteins