Double assurance in the induction of axial development by egg dorsal determinants in <i>Xenopus</i> embryos.

Abstract

We recently reported that microinjection of <i>Xenopus nodal-related</i> (<i>xnr</i>) mRNAs into β-catenin-depleted <i>Xenopus</i> embryos rescued a complete dorsal axis. Xnrs mediate the signal of the Nieuwkoop center that induces the Spemann-Mangold organizer in the overlying mesoderm, a process inhibited by the Nodal antagonist Cerberus-short (CerS). However, β-catenin also induces a second signaling center in the dorsal prospective ectoderm, designated the Blastula Chordin and Noggin Expression (BCNE) center, in which the homeobox gene <i>siamois</i> (<i>sia</i>) plays a major role. In this study, we asked whether the Xnrs and Sia depend on each other or function on parallel pathways. Expression of both genes induced β-catenin-depleted embryos to form complete axes with heads and eyes via the activation of similar sets of downstream organizer-specific genes. Xnrs did not activate <i>siamois</i>, and, conversely, Sia did not activate <i>xnrs</i>, although both were induced by β-catenin stabilization. Depletion with morpholinos revealed a robust role for the downstream target Chordin. Remarkably, Chordin depletion prevented all ectopic effects resulting from microinjection of the mRNA encoding the maternal cytoplasmic determinant <i>Huluwa</i>, including the radial expansion of brain tissue and the ectopic expression of the ventral gene <i>sizzled</i>. The main conclusion was that the BCNE and Nieuwkoop centers provide a double assurance mechanism for axial formation by independently activating similar downstream transcriptional target gene repertoires. We suggest that Siamois likely evolved from an ancestral Mix-type homeodomain protein called Sebox as a <i>Xenopus</i>-specific adaptation for the rapid differentiation of the anterior neural plate in the ectoderm.