UC Berkeley

The sudden appearance of 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 head. The evolution of neural crest and neurogenic placodes has been postulated as a key event leading to the appearance of new cell types that fostered the transition from filter feeding to active predation in ancestral vertebrates. However, the evolutionary origin of neural crest and neurogenic placodes has remained obscure due to the lack of embryonic data from tunicates, the closest living relative to the vertebrates. We provide evidence that the tunicate Ciona intestinalis possesses a cephalic melanocyte lineage (a9.49) similar to neural crest that can be reprogrammed into migrating ectomesenchyme by the targeted misexpression of Twist. Our results suggest that the neural crest melanocyte regulatory network predated the divergence of tunicates and vertebrates. We propose that the co-option of mesenchyme determinants, such as Twist, into the neural plate ectoderm was crucial for the emergence of the vertebrate “new head”.

Furthermore, we show that Ciona intestinalis possesses a preplacodal ectoderm (PPE) that is specified by a BMP antagonist and expresses the key regulatory determinant Six1/2, a developmental program conserved across vertebrates. The Ciona PPE is shown to produce ciliated neurons that express gonadotropin-releasing hormone (GnRH), a G protein-coupled receptor for relaxin-3 (RXFP3), and a functional cyclic nucleotide gated channel (CNGA), suggestive of dual chemosensory and neurosecretory activities. These observations provide the first evidence that Ciona possesses a neurogenic placode, which produces multifunctional sensory and neurosecretory cells related to those derived from olfactory placodes of vertebrates. In vertebrates, GnRH neuroblasts are first formed in the olfactory placode and use the axon tracts of chemosensory neurons to guide them to their final destination in the hypothalamus. Tracing experiments have shown that olfactory and GnRH neurons form a direct neuronal circuit. We speculate that the PPE-derived neurons in Ciona resemble an ancestral cell type, a progenitor to the complex neuronal circuit that integrates sensory information and neuroendocrine control in vertebrates.