β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

Abstract

SUMMARYThe canonical Wnt/b-catenin pathway is a key regulator of body plan organization and axis formation in metazoans, being involved in germ layer specification, posterior growth and patterning of the anteroposterior axis. Results from animals spanning a wide phylogenetic range suggest that a unifying function of b-catenin in metazoans is to define the posterior/vegetal part of the embryo. Although the specification of vegetal territories (endoderm) by b-catenin has been demonstrated in distantly related animals (cnidarians, a protostome, echinoderms and ascidians), the definition of the posterior part of the embryo is well supported only for vertebrates and planarians. To gain insights into b-catenin functions during deuterostome evolution, we have studied the early development of the direct developing hemichordate Saccoglossus kowalevskii. We show that the zygote is polarized after fertilization along the animal-vegetal axis by cytoplasmic rearrangements resembling the ascidian vegetal contraction. This early asymmetry is translated into nuclear accumulation of b-catenin at the vegetal pole, which is necessary and sufficient to specify endomesoderm. We show that endomesoderm specification is crucial for anteroposterior axis establishment in the ectoderm. The endomesoderm secretes as yet unidentified signals that posteriorize the ectoderm, which would otherwise adopt an anterior fate. Our results point to a conserved function at the base of deuterostomes for b-catenin in germ layer specification and to a causal link in the definition of the posterior part of the embryonic ectoderm by way of activating posteriorizing endomesodermal factors. Consequently, the definition of the vegetal and the posterior regions of the embryo by b-catenin should be distinguished and carefully re-examined.

Dose-dependent nuclear β-catenin response segregates endomesoderm along the sea star primary axis

“…It has been proposed that a gradient of nβ-catenin is the ancestral mechanism used to pattern the primary axis (Niehrs, 2010). However, no evidence for a long-range gradient of nβ-catenin has been found in any invertebrate (Darras et al, 2011;Röttinger et al, 2012). Although we demonstrate a dose-dependent response to nβ-catenin activity in territory specification in sea star embryos, this does not arise through a response to a long-range spatial gradient.…”

“…Detailed GRNs explaining the genesis of this territory have been described for the invertebrates Nematostella vectensis, Caenorhabditis elegans and Strongylocentrotus purpuratus, and for vertebrates, such as Xenopus laevis and Danio rerio (Chan et al, 2009;Loose and Patient, 2004;Maduro, 2009;Peter and Davidson, 2011;Röttinger et al, 2012). In these and other, less well-studied organisms (Darras et al, 2011;Henry et al, 2008;Imai et al, 2000), nuclear β-catenin (nβ-catenin) is required for endomesoderm specification, or, in vertebrates, for the specification of anterior endomesoderm (Logan and Nusse, 2004). Therefore, the polar nuclearization of β-catenin is an ancestral mechanism among the metazoa used to establish endomesoderm.…”

“…Niehrs, 2010). As yet, there is no evidence in any invertebrate for a long-range nβ-catenin gradient being used to establish different territories, although differential accumulation has been observed within restricted domains (Darras et al, 2011;Henry et al, 2008;Imai et al, 2000;Logan et al, 1999;Miyawaki et al, 2003;Röttinger et al, 2012).…”

The Evolution of the Wnt Pathway

“…b-catenin signaling marks the vegetal pole of the sea urchin embryo (Wikramanayake et al 1998(Wikramanayake et al , 2004Logan et al 1999) and is required for the formation of the endoderm and mesoderm. Overactivation of bcatenin with LiCl results in vegetalized embryos with ectopic endoderm (Darras et al 2011). Furthermore, in many chordates, a peak expression of b-catenin at the vegetal and blastoporal side defines a gradient along the AP axis.…”

Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis

“…Thus, β-catenin acts as a master regulatory gene, responsible for the control of multiple processes. During early animal embryogenesis, β-catenin specifies the site of endoderm internalization and promotes posterior fates in most studied systems (Byrum and Wikramanayake, 2013;Darras et al, 2011;Haegel et al, 1995;Henry et al, 2008;Lee et al, 2006;Logan et al, 1999;Srivastava et al, 2014;Wikramanayake et al, 2003). In later stages of development, the canonical Wnt pathway influences the formation of multiple cell types, tissues and organ systems (Aulehla et al, 2008;Grigoryan et al, 2008;Hari et al, 2002;Holland et al, 2005;Kiecker and Niehrs, 2001; Lewis et al, 2004;Petersen and Reddien, 2009a;Schneider and Bowerman, 2007;Tan et al, 2006;Watanabe et al, 2014), and most prominently, the anteroposterior (AP) patterning of the vertebrate central nervous system (Ciani and Salinas, 2005).…”