Molecular characterization of the apical organ of the anthozoan Nematostella vectensis

Chiara Sinigaglia,Henriette Busengdal,Avi Lerner,Paola Oliveri,Fabian Rentzsch

doi:10.1016/j.ydbio.2014.11.019

Chiara Sinigaglia, Henriette Busengdal + Show 3 more

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https://doi.org/10.1016/j.ydbio.2014.11.019

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Abstract

Apical organs are sensory structures present in many marine invertebrate larvae where they are considered to be involved in their settlement, metamorphosis and locomotion. In bilaterians they are characterised by a tuft of long cilia and receptor cells and they are associated with groups of neurons, but their relatively low morphological complexity and dispersed phylogenetic distribution have left their evolutionary relationship unresolved. Moreover, since apical organs are not present in the standard model organisms, their development and function are not well understood. To provide a foundation for a better understanding of this structure we have characterised the molecular composition of the apical organ of the sea anemone Nematostella vectensis. In a microarray-based comparison of the gene expression profiles of planulae with either a wildtype or an experimentally expanded apical organ, we identified 78 evolutionarily conserved genes, which are predominantly or specifically expressed in the apical organ of Nematostella. This gene set comprises signalling molecules, transcription factors, structural and metabolic genes. The majority of these genes, including several conserved, but previously uncharacterized ones, are potentially involved in different aspects of the development or function of the long cilia of the apical organ. To demonstrate the utility of this gene set for comparative analyses, we further analysed the expression of a subset of previously uncharacterized putative orthologs in sea urchin larvae and detected expression for twelve out of eighteen of them in the apical domain. Our study provides a molecular characterization of the apical organ of Nematostella and represents an informative tool for future studies addressing the development, function and evolutionary history of apical organ cells.

Highlights

Apical organs are found in the larval stages of phylogenetically diverse animal groups (Fig. 1A) such as anthozoan cnidarians, protostomes and deuterostomes
In this study we have identified a set of genes that are expressed in the apical organ of the anthozoan N. vectensis, providing a molecular signature for the apical organ cells
Though a bundle of long cilia is considered the hallmark of apical organs both in bilaterian and cnidarian larvae, these aboral cilia can be more or less prominent in different larvae, in particular among cnidarians (e.g. Widersten, 1968)

Summary

Introduction

Apical organs are found in the larval stages of phylogenetically diverse animal groups (Fig. 1A) such as anthozoan cnidarians, protostomes (e.g. molluscs and annelids) and deuterostomes (e.g. echinoderms and hemichordates). The functions of apical organs are not well understood and may vary between taxa Given their temporal restriction to larval stages, apical organs have been proposed to play an important role in the detection of settlement cues and for the induction of metamorphosis, presumably acting as chemosensory and/or mechanosensory structures. Such a function has been confirmed by functional approaches in only few species Apical organs are thought to regulate the activity of ciliary bands and musculature in some bilaterians and likely contribute to their locomotion (Croll and Dickinson, 2004; Goldberg et al, 1994; Satterlie and Cameron, 1985)

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