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

Abstract

SUMMARYWnt and Nodal signaling pathways are required for initial patterning of cell fates along anterior-posterior (AP) and dorsal-ventral (DV) axes, respectively, of sea urchin embryos during cleavage and early blastula stages. These mechanisms are connected because expression of nodal depends on early Wnt/-catenin signaling. Here, we show that an important subsequent function of Wnt signaling is to control the shape of the nodal expression domain and maintain correct specification of different cell types along the axes of the embryo. In the absence of Wnt1, the posterior-ventral region of the embryo is severely altered during early gastrulation. Strikingly, at this time, nodal and its downstream target genes gsc and bra are expressed ectopically, extending posteriorly to the blastopore. They override the initial specification of posterior-ventral ectoderm and endoderm fates, eliminating the ventral contribution to the gut and displacing the ciliary band dorsally towards, and occasionally beyond, the blastopore. Consequently, in Wnt1 morphants, the blastopore is located at the border of the re-specified posterior-ventral oral ectoderm and by larval stages it is in the same plane near the stomodeum on the ventral side. In normal embryos, a Nodaldependent process downregulates wnt1 expression in dorsal posterior cells during early gastrulation, focusing Wnt1 signaling to the posterior-ventral region where it suppresses nodal expression. These subsequent interactions between Wnt and Nodal signaling are thus mutually antagonistic, each limiting the range of the other's activity, in order to maintain and stabilize the body plan initially established by those same signaling pathways in the early embryo.

A comprehensive survey of wnt and frizzled expression in the sea urchin Paracentrotuslividus

“…In this study, we have characterized the composition and the spatiotemporal expression of all wnt and fzd genes from the sea urchin P. lividus. This work is complementary to previous analyses conducted on sea urchin wnt and fzd molecules which established (i) the composition of the wnt and fzd complement in the species S. purpuratus (Croce et al, 2006b), (ii) the set of wnt ligands and fzd receptors transcribed maternally in S. purpuratus (Croce et al, 2011;Lhomond et al, 2012;Stamateris et al, 2010), (iii) the biological functions of four wnt ligands (wnt5, wnt6, wnt8, and wnt1) and of two fzd receptors (fzd1/2/7 and fzd5/8) in L. variegatus, S. purpuratus or P. lividus (Croce et al, 2006a(Croce et al, , 2011Lhomond et al, 2012;Range et al, 2013;Sethi et al, 2012;Wei et al, 2012;Wikramanayake et al, 2004), and (iv) the identity of a primary WNT-FZD couple mediating canonical, b-catenin-dependent, WNT signaling during early P. lividus development (Lhomond et al, 2012).…”

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

“…In this regard, wnt1 signaling from the posterior pole suppresses nodal transcription in posterior ventral cells during gastrulation, contributing to sculpt the spatial expression pattern of nodal even at later stages [82]. In wnt1 morphants the nodal expressing territory is expanded posteriorly in the ventral side, provoking DV patterning defects that include a ventral to dorsal shift in the position of the posterior ciliary band [82]. This finding reveals that there is a continuing requirement to restrict Nodal signaling throughout development.…”

“…Large scale studies began to describe the epistatic relationships among these genes [44,81], highlighting that sequential interplay between inductive and suppressive events controlling Nodal signaling is critical for DV patterning. In this regard, wnt1 signaling from the posterior pole suppresses nodal transcription in posterior ventral cells during gastrulation, contributing to sculpt the spatial expression pattern of nodal even at later stages [82]. In wnt1 morphants the nodal expressing territory is expanded posteriorly in the ventral side, provoking DV patterning defects that include a ventral to dorsal shift in the position of the posterior ciliary band [82].…”

Early development of amphioxus links evolutionary events with vertebrates

“…The asymmetrical expression of Bmp2/4 and Chordin on the same side are also found both in cnidarians and deuterosotmes. In sea urchin blastulae, however, the Nodal expression domain appears on the future ventral side and establishes orthogonal coordinates with Wnt/b-Catenin signals from the vegetal side (Yaguchi et al, 2008;Wei et al, 2012;Li et al, 2014). These molecular mechanisms in sea urchin embryos are in turn found in amphioxus embryos, although Wnt/b-Catenin signaling along the animal-vegetal axis has apparently been modified, and this modification has likely given rise to the chordate body plan in this animal (Morov et al, 2016).…”