The pre-vertebrate origins of neurogenic placodes

Philip Barron Abitua, T. Blair Gainous, Angela N. Kaczmarczyk, Christopher J. Winchell, Clare Hudson, Kaori Kamata, Masashi Nakagawa, Motoyuki Tsuda, Takehiro G. Kusakabe, Michael Levine

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Abstract

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.

Original languageEnglish (US)
Pages (from-to)462-465
Number of pages4
JournalNature
Volume524
Issue number7566
DOIs
StatePublished - Aug 27 2015

All Science Journal Classification (ASJC) codes

  • General

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    Abitua, P. B., Gainous, T. B., Kaczmarczyk, A. N., Winchell, C. J., Hudson, C., Kamata, K., Nakagawa, M., Tsuda, M., Kusakabe, T. G., & Levine, M. (2015). The pre-vertebrate origins of neurogenic placodes. Nature, 524(7566), 462-465. https://doi.org/10.1038/nature14657