Unexpected complexity of the Wnt gene family in a sea anemone

Abstract

The Wnt gene family encodes secreted signalling molecules that control cell fate in animal development and human diseases. Despite its significance, the evolution of this metazoan-specific protein family is unclear. In vertebrates, twelve Wnt subfamilies were defined, of which only six have counterparts in Ecdysozoa (for example, Drosophila and Caenorhabditis). Here, we report the isolation of twelve Wnt genes from the sea anemone Nematostella vectensis, a species representing the basal group within cnidarians. Cnidarians are diploblastic animals and the sister-group to bilaterian metazoans. Phylogenetic analyses of N. vectensis Wnt genes reveal a thus far unpredicted ancestral diversity within the Wnt family. Cnidarians and bilaterians have at least eleven of the twelve known Wnt gene subfamilies in common; five subfamilies appear to be lost in the protostome lineage. Expression patterns of Wnt genes during N. vectensis embryogenesis indicate distinct roles of Wnts in gastrulation, resulting in serial overlapping expression domains along the primary axis of the planula larva. This unexpectedly complex inventory of Wnt family signalling factors evolved in early multi-cellular animals about 650 million years (Myr) ago, predating the Cambrian explosion by at least 100 Myr (refs 5, 8). It emphasizes the crucial function of Wnt genes in the diversification of eumetazoan body plans.

RBR Ubiquitin Ligases: Diversification and Streamlining in Animal Lineages

“…After that, the story reverses, with losses of genes occurring in many lineages and only a few new genes appearing. With the available data, cnidarians and mammals are the only groups that conserve a set of RBR genes that is similar to that of their common ancestors, while other lineages, both protostomates and deuterostomates, have lost several or even most of those genes, a result observed before for other gene families (e.g., Kusserow et al 2005;Marín 2008) This streamlining process was especially extreme in nematodes and dipteran insects. However, after this occurred, some of the organisms with less RBR genes have generated some or even many new genes, duplicates of the few that were still left, thus secondarily increasing the number of RBR genes available.…”

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

“…Recent molecular evidence suggests that these diverse groups use many of the same signal transduction pathways and transcription factors during early development (Kusserow et al 2005;Miller et al 2005;Technau et al 2005;Technau and Scholz 2003). Two recent studies have examined the FGF signaling pathway in Cnidaria.…”

The Wnt code: cnidarians signal the way

“…Recent work revealed that almost all bilaterian wnt gene subfamilies are present in cnidarians (Kusserow et al, 2005;Lee et al, 2006 unpublished work from the HR Bode, B Hobmayer and TW Holstein labs) suggesting that the main genes of the Wnt pathways are present in cnidarians.…”

“…An analysis of wnt sequences from various lophotrochozoan representatives revealed an additional wnt gene (wntA) that is not present in vertebrates (Prud'homme et al, 2002). From Nematostella a total of 14 different wnt genes was isolated (Kusserow et al, 2005;Lee et al, 2006, M Ritthaler, A Kusserow and TW Holstein, unpublished), representing 12 of the 13 wnt subfamilies (Table 1). The Nematostella genome only lacks the wnt9 subfamily.…”