Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer

Abstract

The importance of polarity-the possession of a primary body axis-is evident in the functional features of animals, such as feeding, and therefore must have arisen simultaneously with the evolution of multicellular animal body plans. Sponges are thought to represent the most ancient extant lineage of multicellular animals and whereas adult sponges do not possess obvious polarity, they are useful study organisms in which to examine the origin and evolution of body polarity. We tested the effect of pharmacological agents known to disrupt the polarity of a wide variety of animals on sponge organization during development. Lithium chloride and alsterpaullone, which mimic canonical Wnt signaling in other animals, caused formation of ectopic oscula and disrupted the ability of the sponge to feed. Transplanted oscula were able to attach to and induce canal reorganization in host sponges suggesting that the osulum has inductive capabilities. This work suggests that canonical Wnt signaling is responsible for setting up the aquiferous system, which acts as an organizing center polarizing the sponge.

Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans

“…One of the three Amphimedon Wnt ligands is specifically expressed in the posterior pole of the embryos and larvae, and one of the eight Amphimedon Tgfb ligands is expressed in the outer embryonic layer, and then restricted to the posterior pole 7,48 . Nothing is known about the expression of relevant genes in juvenile or adult demosponges, but transplantation experiments performed with Ephydatia mulleri demonstrated organizer properties of the osculum, and that this activity is likely conveyed by canonical Wnt signalling 59 . We have not been able to replicate this result in Sycon, possibly because Ephydatia, like the overwhelming majority of sponges, produces multiple oscula as it grows, while Sycon evolved mechanisms preserving a single body axis throughout its life.…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Among cnidarians, cWNT signalling has been shown to facilitate the establishment of embryonic [65,77,78] and adult [29,72] organizing centres in both anthozoan and hydrozoan model systems. Although functional studies in sponges are lacking, studies of WNT gene expression in situ suggest that this pathway is also asymmetrically expressed along the larval swimming axis and during development of the adult axis (defined by the aquiferous system) [36,79,80]. Treatment with pharmacological activators of cWNT signalling (e.g.…”

The Evolution of the Wnt Pathway

“…In Oscarella, Wnt-I is also expressed at the canal openings (ostia), and b-catenin activation induces ectopic ostia (Lapebie et al 2009). This is reminiscent of the blastoporal organizer in cnidarians (Windsor and Leys 2010), and future work must reveal to what extent these Wnt genes also contribute to noncanonical Wnt function.…”