Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos

Abstract

The animal plate of the sea urchin embryo becomes the apical organ, a sensory structure of the larva. In the absence of vegetal signaling, an expanded and unpatterned apical organ forms. To investigate the signaling that restricts the size of the animal plate and patterns neurogenesis, we have expressed molecules that regulate specification of ectoderm in embryos and chimeras. Enhancing oral ectoderm suppresses serotonergic neuron differentiation, whereas enhancing aboral or ciliary band ectoderm increases differentiation of serotonergic neurons. In embryos in which vegetal signaling is blocked, Nodal expression does not reduce the size of the thickened animal plate; however, almost no neurons form. Expression of BMP in the absence of vegetal signaling also does not restrict the size of the animal plate, but abundant serotonergic neurons form. In chimeras in which vegetal signaling is blocked in the entire embryo, and one half of the embryo expresses Nodal,serotonergic neuron formation is suppressed in both halves. In similar chimeras in which vegetal signaling is blocked and one half of the embryo expresses Goosecoid (Gsc), serotonergic neurons form only in the half of the embryo not expressing Gsc. We propose that neurogenesis is specified by a maternal program that is restricted to the animal pole by signaling that is dependent on nuclearization of β-catenin and specifies ciliary band ectoderm. Subsequently, neurogenesis in the animal plate is patterned by suppression of serotonergic neuron formation by Nodal. Like other metazoans,echinoderms appear to have a phase of neural development during which the specification of ectoderm restricts and patterns neurogenesis.

Axial patterning interactions in the sea urchin embryo: suppression of nodal by Wnt1 signaling

“…These functions have been particularly well elucidated in the sea urchin embryo. A series of Wnt signals specifies mesoderm and endoderm at one end of the primary (animal-vegetal) axis (Logan et al, 1999;Sherwood and McClay, 1999;Wikramanayake et al, 1998;Wikramanayake et al, 2004;Croce et al, 2011) and restricts anterior neuroectoderm to the opposite end (Wei et al, 2009;Yaguchi et al, 2008;Yaguchi et al, 2006). In this way, Wnt/-catenin-dependent patterning of the primary axis is like that along the anterior-posterior (AP) axis of most bilaterians; consequently, here we refer to the primary axis of the sea urchin embryo as the AP axis.…”

“…Nodal signaling is necessary and sufficient to impose DV polarity to cells in all three germ layers of the embryo Duboc et al, 2004) and its influence extends in a broad band imposing DV polarity on tissues that develop from anterior to posterior poles of the embryo Yaguchi et al, 2006). Where it is expressed, Nodal signaling specifies oral ectoderm on the ventral side and is required for the production of BMP2/4, which acts as a relay to specify aboral ectoderm, most of which covers the dorsal side (Duboc et al, 2004;Lapraz et al, 2009).…”

Direct development of neurons within foregut endoderm of sea urchin embryos

“…1). During embryogenesis, the anterior neuroectoderm is localized to the animal pole by controlled canonical Wnt-dependent processes (3,4), and the ciliary band is positioned by TGF-β signaling through nodal and bone morphogenetic protein pathways (5)(6)(7)(8). However, the mechanisms regulating development of pharyngeal neurons have not been explored.…”

Ciliogenesis, Ciliary Function, and Selective Isolation

“…Development of this "apical tuft" coincides with the acquisition of directional swimming and, thus, the tuft is thought to have a sensory function. In fact, specific cells of the apical plate later develop into the larval nervous system (11).…”