On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes

Abstract

The regulation of body axis specification in the common ancestor of bilaterians remains controversial. BMP signaling appears to be an ancient program for patterning the secondary, or dorsoventral, body axis, but any such program for the primary, or anteroposterior, body axis is debated. Recent work in invertebrates indicates that posterior Wnt/b-catenin signaling is such a mechanism and that it evolutionarily predates the cnidarian-bilaterian split. Here, I argue that a Cartesian coordinate system of positional information set up by gradients of perpendicular Wnt and BMP signaling is conserved in bilaterians, orchestrates body axis patterning and contributes to both the relative invariance and diversity of body forms.

The Evolution of the Wnt Pathway

“…The function and localization of Wnt and b-catenin signaling in deuterostome AP-axis formation has been recently reviewed in detail (De Robertis 2010;Niehrs 2010;Holstein et al 2011). The general picture that emerges is that b-catenin plays an important function in the early polarization of the animal -vegetal axis of the embryo (Martin and Kimelman 2009).…”

“…Similarly to the posterior growth zone in amphioxus tail buds (Schubert et al 2001), nuclear b-catenin also forms a posterior-to-anterior gradient in vertebrates. Wnt signaling is involved in tail development in zebrafish (Agathon et al 2003;Shimizu et al 2005;Thorpe et al 2005), where Wnt3a determines the anterior-posterior position of the somite determination front (Aulehla et al 2003;Dunty et al 2008;De Robertis 2010;Niehrs 2010). …”

“…Bilaterian animals are patterned along two major body axes (Niehrs 2010): the anteriorposterior (AP) axis, which is oriented parallel to the gut and, in a perpendicular orientation, the dorsal-ventral (DV) axis. Increasing evidence suggests that the primary body axis is the AP axis, whereas the secondary body axis is the DV axis (Niehrs 2010;Holstein et al 2011).…”

“…Increasing evidence suggests that the primary body axis is the AP axis, whereas the secondary body axis is the DV axis (Niehrs 2010;Holstein et al 2011). A localized Wnt/b-catenin signaling center determines the orientation of the primary body axis in both bilaterians and non-bilaterians, indicating that the conserved Wnt signaling pathway is at the base of polarized development in all metazoans (Petersen and Reddien 2009).…”

-Catenin-Dependent Wnt Signaling in C. elegans: Teaching an Old Dog a New Trick

“…It has been proposed that Wnt signaling may have been used as an ancestral axis specification mechanism with patterning by Hox genes elaborated on top of this more ancestral mechanism (Guder et al 2006;Ryan and Baxevanis 2007;Martin and Kimelman 2009;Petersen and Reddien 2009;Niehrs 2010). Further experiments will need to be performed to determine if specific Hox gene expression along the axis in C. elegans is patterned by the anteriorposterior Wnt gradient.…”