Animal multicellularity and polarity without Wnt signaling

Quentin Schenkelaars,André Le Bivic,Emmanuelle Renard,Laura Fierro-Constain,Laurent Kodjabachian,Carole Borchiellini,Marine Pratlong,Jean Vacelet

doi:10.1038/s41598-017-15557-5

Abstract

Acquisition of multicellularity is a central event in the evolution of Eukaryota. Strikingly, animal multicellularity coincides with the emergence of three intercellular communication pathways – Notch, TGF-β and Wnt – all considered as hallmarks of metazoan development. By investigating Oopsacas minuta and Aphrocallistes vastus, we show here that the emergence of a syncytium and plugged junctions in glass sponges coincides with the loss of essential components of the Wnt signaling (i.e. Wntless, Wnt ligands and Disheveled), whereas core components of the TGF-β and Notch modules appear unaffected. This suggests that Wnt signaling is not essential for cell differentiation, polarity and morphogenesis in glass sponges. Beyond providing a comparative study of key developmental toolkits, we define here the first case of a metazoan phylum that maintained a level of complexity similar to its relatives despite molecular degeneration of Wnt pathways.

Highlights

The emergence of multicellularity was a critical step in the origin of life diversity[1]
Adult glass sponges mainly consist of a multinucleated syncytium as well, which is connected to different cell types via plugged junctions (Fig. 1e–g)[19]
In order to test the universality of the classical cell-to-cell communication modules of animal development (i.e. Notch, TGF-β and Wnt pathways), we analyzed the transcriptomes of two distantly related glass sponges Oopsacas minuta Topsent, 1927 (Hexactinellida, Lyssacinosida) and Aphrocallistes vastus Schulze, 1886 (Hexactinellida, Hexactinosida) and compared them to those of other sponge lineages (i.e. Calcarea, Demospongiae and Homoscleromorpha) and of other metazoans (Fig. 1a)

Summary

Introduction

The emergence of multicellularity was a critical step in the origin of life diversity[1]. Adult glass sponges mainly consist of a multinucleated syncytium as well (the trabecular syncytium), which is connected to different cell types (i.e. archeocytes, choanoblasts and collar bodies) via plugged junctions (Fig. 1e–g)[19]. This unique syncytial feature, acquired more than 545 million years ago in the last common ancestor of glass sponges[21], raises exciting questions regarding its consequences on the developmental toolkit of extant species. In order to test the universality of the classical cell-to-cell communication modules of animal development (i.e. Notch, TGF-β and Wnt pathways), we analyzed the transcriptomes of two distantly related glass sponges Oopsacas minuta Topsent, 1927 (Hexactinellida, Lyssacinosida) and Aphrocallistes vastus Schulze, 1886 (Hexactinellida, Hexactinosida) and compared them to those of other sponge lineages (i.e. Calcarea, Demospongiae and Homoscleromorpha) and of other metazoans (Fig. 1a)

Methods

Results

Conclusion