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Open Access Highly Accessed Research article

Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes

Jerome HL Hui17, Florian Raible23, Natalia Korchagina1, Nicolas Dray48, Sylvie Samain5, Ghislaine Magdelenat5, Claire Jubin5, Béatrice Segurens5, Guillaume Balavoine49, Detlev Arendt2 and David EK Ferrier16*

Author Affiliations

1 Department of Zoology, University of Oxford, Oxford, UK

2 EMBL, 69117 Heidelberg, Germany

3 MFPL, Vienna, Austria

4 CNRS-CGM, Gif-sur-Yvette, France

5 Génoscope, Centre National de Séquençage, Evry, France

6 The Scottish Oceans Institute, University of St Andrews, St Andrews, UK

7 Faculty of Life Sciences, Michael Smith Building, University of Manchester, Manchester, UK

8 Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, USA

9 Institut Jacques Monod, UMR 7592 CNRS/Université Denis Diderot – Paris VII, Paris, France

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BMC Biology 2009, 7:43  doi:10.1186/1741-7007-7-43

Published: 23 July 2009

Abstract

Background

The ParaHox gene cluster is the evolutionary sister to the Hox cluster. Whilst the role of the Hox cluster in patterning the anterior-posterior axis of bilaterian animals is well established, and the organisation of vertebrate Hox clusters is intimately linked to gene regulation, much less is known about the more recently discovered ParaHox cluster. ParaHox gene clustering, and its relationship to expression, has only been described in deuterostomes. Conventional protostome models (Drosophila melanogaster and Caenorhabditis elegans) are secondarily derived with respect to ParaHox genes, suffering gene loss and cluster break-up.

Results

We provide the first evidence for ParaHox gene clustering from a less-derived protostome animal, the annelid Platynereis dumerilii. Clustering of these genes is thus not a sole preserve of the deuterostome lineage within Bilateria. This protostome ParaHox cluster is not entirely intact however, with Pdu-Cdx being on the opposite end of the same chromosome arm from Pdu-Gsx and Pdu-Xlox. From the genomic sequence around the P. dumerilii ParaHox genes the neighbouring genes are identified, compared with other taxa, and the ancestral arrangement deduced.

Conclusion

We relate the organisation of the ParaHox genes to their expression, and from comparisons with other taxa hypothesise that a relatively complex pattern of ParaHox gene expression existed in the protostome-deuterostome ancestor, which was secondarily simplified along several invertebrate lineages. Detailed comparisons of the gene content around the ParaHox genes enables the reconstruction of the genome surrounding the ParaHox cluster of the protostome-deuterostome ancestor, which existed over 550 million years ago.