Abstract
BackgroundThe Planar Cell Polarity pathway (PCP) has been described as the main feature involved in patterning cell orientation in bilaterian tissues. Recently, a similar phenomenon was revealed in cnidarians, in which the inhibition of this pathway results in the absence of cilia orientation in larvae, consequently proving the functional conservation of PCP signaling between Cnidaria and Bilateria. Nevertheless, despite the growing accumulation of databases concerning basal lineages of metazoans, very few information concerning the existence of PCP components have been gathered outside of Bilateria and Cnidaria. Thus, the origin of this module or its prevalence in early emerging metazoans has yet to be elucidated.ResultsThe present study addresses this question by investigating the genomes and transcriptomes from all poriferan lineages in addition to Trichoplax (Placozoa) and Mnemiopsis (Ctenophora) genomes for the presence of the core components of this pathway. Our results confirm that several PCP components are metazoan innovations. In addition, we show that all members of the PCP pathway, including a bona fide Strabismus ortholog (Van gogh), are retrieved only in one sponge lineage (Homoscleromorpha) out of four. This highly suggests that the full PCP pathway dates back at least to the emergence of homoscleromorph sponges. Consequently, several secondary gene losses would have occurred in the three other poriferan lineages including Amphimedon queenslandica (Demospongiae). Several proteins were not retrieved either in placozoans or ctenophores leading us to discuss the difficulties to predict orthologous proteins in basally branching animals. Finally, we reveal how the study of multigene families may be helpful to unravel the relationships at the base of the metazoan tree.ConclusionThe PCP pathway antedates the radiation of Porifera and may have arisen in the last common ancestor of animals. Oscarella species now appear as key organisms to understand the ancestral function of PCP signaling and its potential links with Wnt pathways.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0641-0) contains supplementary material, which is available to authorized users.
Highlights
The Planar Cell Polarity pathway (PCP) has been described as the main feature involved in patterning cell orientation in bilaterian tissues
Fy, Dgo and the PET family arose in the last common ancestor of Metazoa and Choanoflagellata As previously reported [11], few members of the core PCP pathway were identified in the genome of the choanoflagellate Salpingoeca rosetta (Table 1 and Additional file 1)
We show here that several of these ancient genes may have been secondarily lost during animal evolution: no dgo orthologous gene was found in the genomes of Mnemiopsis leidyi and Trichoplax adhaerens, and no fy was identified in either of the glass sponge transcriptomes (Oopsacas minuta and Aphrocalistes vastus), whereas it is present in all other sponges studied here, including the Amphimedon queenslandica genome in which it had previously been considered as missing (Table 1 and Additional file 1) [24]
Summary
The Planar Cell Polarity pathway (PCP) has been described as the main feature involved in patterning cell orientation in bilaterian tissues. As recently reviewed by Hale and Strutt (2015) [12], the function of the PCP core proteins in epithelial cell orientation is well documented in various developmental processes across planulozoans (bilaterians + cnidarians) [14, 15]. Among those commonly used to study the planar polarized tissues in Drosophila are the alignment of actin hairs on the abdomen, the alignment of wing sensory bristles, and the arrangement of eye facet systems [16,17,18].
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