Publication Date:
2014-01-30
Description:
Background: Planktonic ciliated larvae are characteristic for the life-cycle of marine invertebrates. Their most prominent feature is the apical organ harbouring sensory cells and neurons of largely undetermined function. An elucidation of the relationships between various forms of primary larvae and apical organs is key to understanding the evolution of animal life-cycles. These relationships have remained enigmatic due to the scarcity of comparative molecular data. Results: To compare apical organs and larval body patterning, we have studied regionalization of the episphere, the upper hemisphere of the trochophore larva of the marine annelid Platynereis dumerilii. We examine the spatial distribution of transcription factors and of Wnt signalling components previously implicated in anterior neural development. Pharmacological activation of Wnt signaling with Gsk3beta antagonists abolishes expression of apical markers, consistent with a repressive role of Wnt signalling in the specification of apical tissue. We refer to this Wnt-sensitive, six3- and foxq2-expressing part of the episphere as 'apical plate'. We also unravel a molecular signature of the apical organ - devoid of six3 but expressing foxj, irx, nkx3 and hox - which is shared with other marine phyla including cnidarians. Finally, we characterize the cell types that form part of the apical organ by PrImR (Profiling by Image Registration), which allows parallel expression profiling of multiple cells. Besides the hox-expressing apical tuft cells this reveals the presence of putative light- and mechanosensory as well as multiple peptidergic cell types that we compare to apical organ cell types of other animal phyla. Conclusions: The similar formation of a six3+, foxq2+ apical plate, sensitive to wnt activity and with an apical tuft in its six3-free centre, are most parsimoniously explained by evolutionary conservation. We propose that a simple apical organ - comprising an apical tuft and a basal plexus innervated by sensory-neurosecretory apical plate cells - was present in the last common ancestors of cnidarians and bilaterians. One of its ancient functions was the control of metamorphosis. Various types of apical plate cells were subsequently added to the apical organ in the divergent bilaterian lineages. Our findings support an ancient and common origin of primary ciliated larvae.
Electronic ISSN:
1741-7007
Topics:
Biology
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