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Open Access Research article

Larval body patterning and apical organs are conserved in animal evolution

Heather Marlow1*, Maria Antonietta Tosches1, Raju Tomer12, Patrick R Steinmetz13, Antonella Lauri14, Tomas Larsson15 and Detlev Arendt1*

Author Affiliations

1 European Molecular Biology Laboratory, Development Biology Unit, EMBL Heidelberg, Meyerhofstraße 1, 69117 Heidelberg, Germany

2 Present address: Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA

3 Present address: Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, A-1090 Vienna, Austria

4 Present address: Institute for Biological and Medical Imaging, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764 München, Germany

5 European Molecular Biology Laboratory, Structural and Computational Biology Unit, Meyerhofstraße 1, 69117 Heidelberg, Germany

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BMC Biology 2014, 12:7  doi:10.1186/1741-7007-12-7

Published: 29 January 2014

Abstract

Background

Planktonic ciliated larvae are characteristic for the life cycle of marine invertebrates. Their most prominent feature is the apical organ harboring 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 examined the spatial distribution of transcription factors and of Wnt signaling components previously implicated in anterior neural development. Pharmacological activation of Wnt signaling with Gsk3β antagonists abolishes expression of apical markers, consistent with a repressive role of Wnt signaling in the specification of apical tissue. We refer to this Wnt-sensitive, six3- and foxq2-expressing part of the episphere as the ‘apical plate’. We also unraveled a molecular signature of the apical organ - devoid of six3 but expressing foxj, irx, nkx3 and hox - that is shared with other marine phyla including cnidarians. Finally, we characterized the cell types that form part of the apical organ by profiling by image registration, which allows parallel expression profiling of multiple cells. Besides the hox-expressing apical tuft cells, this revealed the presence of putative light- and mechanosensory as well as multiple peptidergic cell types that we compared 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 center, is 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 would have been the control of metamorphosis. Various types of apical plate cells would then have subsequently been added to the apical organ in the divergent bilaterian lineages. Our findings support an ancient and common origin of primary ciliated larvae.

Keywords:
Apical-blastoporal axis; Apical organ; Body plan; Larval evolution