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Open Access Research article

Intact cluster and chordate-like expression of ParaHox genes in a sea star

Rossella Annunziata1, Pedro Martinez23 and Maria Ina Arnone1*

Author affiliations

1 Stazione Zoologica Anton Dohrn di Napoli, Cellular and Developmental Biology, Villa Comunale, 80121 Napoli, Italy

2 Departament de Genètica, Universitat de Barcelona, Av. Diagonal, 643, 08028 Barcelona, Spain

3 Institució Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluís Companys, 23 08010, Barcelona, Spain

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Citation and License

BMC Biology 2013, 11:68  doi:10.1186/1741-7007-11-68

Published: 27 June 2013

Abstract

Background

The ParaHox genes are thought to be major players in patterning the gut of several bilaterian taxa. Though this is a fundamental role that these transcription factors play, their activities are not limited to the endoderm and extend to both ectodermal and mesodermal tissues. Three genes compose the ParaHox group: Gsx, Xlox and Cdx. In some taxa (mostly chordates but to some degree also in protostomes) the three genes are arranged into a genomic cluster, in a similar fashion to what has been shown for the better-known Hox genes. Sea urchins possess the full complement of ParaHox genes but they are all dispersed throughout the genome, an arrangement that, perhaps, represented the primitive condition for all echinoderms. In order to understand the evolutionary history of this group of genes we cloned and characterized all ParaHox genes, studied their expression patterns and identified their genomic loci in a member of an earlier branching group of echinoderms, the asteroid Patiria miniata.

Results

We identified the three ParaHox orthologs in the genome of P. miniata. While one of them, PmGsx is provided as maternal message, with no zygotic activation afterwards, the other two, PmLox and PmCdx are expressed during embryogenesis, within restricted domains of both endoderm and ectoderm. Screening of a Patiria bacterial artificial chromosome (BAC) library led to the identification of a clone containing the three genes. The transcriptional directions of PmGsx and PmLox are opposed to that of the PmCdx gene within the cluster.

Conclusions

The identification of P. miniata ParaHox genes has revealed the fact that these genes are clustered in the genome, in contrast to what has been reported for echinoids. Since the presence of an intact cluster, or at least a partial cluster, has been reported in chordates and polychaetes respectively, it becomes clear that within echinoderms, sea urchins have modified the original bilaterian arrangement. Moreover, the sea star ParaHox domains of expression show chordate-like features not found in the sea urchin, confirming that the dynamics of gene expression for the respective genes and their putative regulatory interactions have clearly changed over evolutionary time within the echinoid lineage.

Keywords:
Patiria miniata; Asteroid; ParaHox; Cluster; Gsx; Xlox; Cdx; Colinearity; Gut