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Nature. 2015 Aug 27;524(7566):462-5. doi: 10.1038/nature14657. Epub 2015 Aug 10.

The pre-vertebrate origins of neurogenic placodes.

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Center for Integrative Genomics, Division of Genetics, Genomics and Development, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.
Sorbonne Universités, Université Pierre et Marie Curie, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement de Villefranche-sur-mer, Observatoire Océanologique, 06230 Villefranche-sur-mer, France.
Graduate School of Life Science, University of Hyogo, Kamigori, Hyogo 678-1297, Japan.
Institute for Integrative Neurobiology and Department of Biology, Faculty of Science and Engineering, Konan University, Kobe 658-8501, Japan.


The sudden appearance of the neural crest and neurogenic placodes in early branching vertebrates has puzzled biologists for over a century. These embryonic tissues contribute to the development of the cranium and associated sensory organs, which were crucial for the evolution of the vertebrate "new head". A previous study suggests that rudimentary neural crest cells existed in ancestral chordates. However, the evolutionary origins of neurogenic placodes have remained obscure owing to a paucity of embryonic data from tunicates, the closest living relatives to those early vertebrates. Here we show that the tunicate Ciona intestinalis exhibits a proto-placodal ectoderm (PPE) that requires inhibition of bone morphogenetic protein (BMP) and expresses the key regulatory determinant Six1/2 and its co-factor Eya, a developmental process conserved across vertebrates. The Ciona PPE is shown to produce ciliated neurons that express genes for gonadotropin-releasing hormone (GnRH), a G-protein-coupled receptor for relaxin-3 (RXFP3) and a functional cyclic nucleotide-gated channel (CNGA), which suggests dual chemosensory and neurosecretory activities. These observations provide evidence that Ciona has a neurogenic proto-placode, which forms neurons that appear to be related to those derived from the olfactory placode and hypothalamic neurons of vertebrates. We discuss the possibility that the PPE-derived GnRH neurons of Ciona resemble an ancestral cell type, a progenitor to the complex neuronal circuit that integrates sensory information and neuroendocrine functions in vertebrates.

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