Formation of the Ascidian Epidermal Sensory Neurons: Insights into the Origin of the Chordate Peripheral Nervous System

Abstract

The vertebrate peripheral nervous system (PNS) originates from neural crest and placodes. While its developmental origin is the object of intense studies, little is known concerning its evolutionary history. To address this question, we analyzed the formation of the larval tail PNS in the ascidian Ciona intestinalis. The tail PNS of Ciona is made of sensory neurons located within the epidermis midlines and extending processes in the overlying tunic median fin. We show that each midline corresponds to a single longitudinal row of epidermal cells and neurons sharing common progenitors. This simple organization is observed throughout the tail epidermis, which is made of only eight single-cell rows, each expressing a specific genetic program. We next demonstrate that the epidermal neurons are specified in two consecutive steps. During cleavage and gastrula stages, the dorsal and ventral midlines are independently induced by FGF9/16/20 and the BMP ligand ADMP, respectively. Subsequently, Delta/Notch–mediated lateral inhibition controls the number of neurons formed within these neurogenic regions. These results provide a comprehensive overview of PNS formation in ascidian and uncover surprising similarities between the fate maps and embryological mechanisms underlying formation of ascidian neurogenic epidermis midlines and the vertebrate median fin.

Hemichordate neurulation and the origin of the neural tube

“…In contrast, in the chordate lineage, the hedgehog-positive cells are only retained ventrally. The ventral PNS of amphioxus 33 and ascidians 34 may be evolutionary remnants, homologous to the dorsal nerve cord of hemichordates.…”

Nodal signaling regulates specification of ascidian peripheral neurons through control of the BMP signal

“…The cell bodies of ESNs lie in the rostral-dorsal epidermis of the trunk and midline epidermis of the tail with long processes extending to the cuticular fin (Ohtsuka et al, 2001b;Takamura, 1998). Previous studies on Ciona intestinalis have shown that caudal ESNs are derived from the b4.2 and that caudal ESN formation is controlled by FGF, Nodal, anti-dorsalizing morphogenetic protein (ADMP) and Delta/Notch (Hudson and Lemaire, 2001;Pasini et al, 2006). However, it was not determined when and where these signaling pathways play roles in ESN specification.…”

The involvement of three signal transduction pathways in botryllid ascidian astogeny, as revealed by expression patterns of representative genes

“…Negative (or very low) p-Smad1/5/8 staining was observed in buds and embryos. The weak p-Smad1/5/8 staining in embryos contradicted the well documented BMP input to the heart and nervous systems specifications, described in other ascidians (Pasini et al, 2006;Christiaen et al, 2010). Therefore, functions in the B. schlosseri BMP pathways should be further studied.…”

“…In solitary ascidian species, STP expression and functions during ontogenic stages have been elucidated for Wnt/b-catenin (Niwano et al, 2009;Hudson et al, 2013), TGF-b (Kobayashi et al, 1999;Kobayashi and Makabe, 2001;Hino et al, 2003;Kawashima et al, 2005;Christiaen et al, 2010;Nishide et al, 2012) and MAPK/ ERK (Bertrand et al, 2003;Hudson et al, 2003;Nishida, 2003;Pasini et al, 2006;Chambon et al, 2007;Sakabe et al, 2006) pathways alone, or in combination with other STPs (Hudson et al, 2007;Lemaire, 2009;Pasini et al, 2012;Sasakura et al, 2012;Squarzoni et al, 2011). This has not been extensively studied in colonial species where astogenic and ontogenic pathways are developing side by side and in concert.…”