Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

Abstract

Two embryonic tissues-the neural crest and the cranial placodes-give rise to most evolutionary novelties of the vertebrate head. These two tissues develop similarly in several respects: they originate from ectoderm at the neural plate border, give rise to migratory cells and develop into multiple cell fates including sensory neurons. These similarities, and the joint appearance of both tissues in the vertebrate lineage, may point to a common evolutionary origin of neural crest and placodes from a specialized population of neural plate border cells. However, a review of the developmental mechanisms underlying the induction, specification, migration and cytodifferentiation of neural crest and placodes reveals fundamental differences between the tissues. Taken together with insights from recent studies in tunicates and amphioxus, this suggests that neural crest and placodes have an independent evolutionary origin and that they evolved from the neural and non-neural side of the neural plate border, respectively.

WNT/β-catenin signaling mediates human neural crest induction via a pre-neural border intermediate

“…The 'binary competence' model of neural crest/cranial placode induction proposed a segregation of NC and cranial placode competence at the neural plate border stage (Schlosser, 2008). Contrary to this model, we found that WNT directs a segregation of early NC and cranial placode cell fates prior to the induction of the neural plate border markers; pB genes such as GBX2, ZEB2, SP5 and ZIC3 are induced by WNT/CTNNB1 signaling 1 or 2 days prior to induction of the NB genes PAX3, PAX7 and MSX1.…”

“…3D,E; Leung et al, 2013) further supporting the idea that segregation of NC and cranial placode fates occurs very early in our cultures. It has been suggested that NC competence segregates with the neuralized domain of the ectoderm (Pieper et al, 2012;Schlosser, 2008). We have examined the expression dynamics of a number of neural-related transcripts, including LHX2, PAX6, SOX1, SOX2, OTX2 and HES5 (Greber et al, 2011;Hou et al, 2013;Zhang et al, 2010).…”

“…The 'new head' model (Gans and Northcutt, 1983) proposed that the NC was an evolutionary advancement that distinguished vertebrates from other chordates, and linked the derivatives of NC and cranial placodes to the predatory life style of vertebrates. Interestingly, NC and cranial placodes were further proposed to derive from single precursors (Baker and BronnerFraser, 1997;Gans and Northcutt, 1983), and phylogenetic studies suggested that their lineages diverted after the neural-epidermal segregation in the early ectoderm (Groves and LaBonne, 2014;Patthey and Gunhaga, 2014;Schlosser, 2008). In avian embryos, neural induction is thought to initiate slightly before or during gastrulation (Streit et al, 2000;Wilson et al, 2000Wilson et al, , 2001, and specification and lineage assays identified the lateral epiblast at early gastrula stages as poised to form NC independently of neural fate (Basch et al, 2006;Patthey et al, 2009).…”

Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis

“…7A-C, E,M). Since placodal and neural crest cells both originate from the ectoderm at the neural plate border and give rise to migratory cells developing into multiple cell fates (Schlosser, 2008), they may also share their response to semaphorin signals.…”

Conserved gene regulatory module specifies lateral neural borders across bilaterians

“…The NPB and PPE give rise to the neural crest and placode, respectively, both of which undergo epithelial-to-mesenchymal transition/delamination, migrate in prototypical paths, and give rise to the peripheral nervous system (PNS) and many other cell types (3,4). However, the NPB and PPE also have many different features (5). 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.…”