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MBE Advance Access published online on August 24, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi239
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Accepted August 15, 2005

Research Article

Evidence for a Dispersed Hox Gene Cluster in the Platyhelminth Parasite Schistosoma Mansoni

Raymond J. Pierce 1* 10, Wenjie Wu 2 10, Hirohisa Hirai 3, Al Ivens 4, Lee D. Murphy 4, Christophe Noël 5, David A. Johnston 6, François Artiguenave 7, Martin Adams 1, Jocelyne Cornette 1, Eric Viscogliosi 1, Monique Capron 1, and Guillaume Balavoine 8

1 Inserm U 547, Institut Pasteur de Lille, 1 rue du Professeur A. Calmette, 59019 - Lille, France
2 Inserm U 547, Institut Pasteur de Lille, 1 rue du Professeur A. Calmette, 59019 - Lille, France; Present address: Department of Microbiology and Immunology, School of Medicine and Biomedical Sciences, State University of New York, Buffalo, NY 14214, USA
3 Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506 Japan
4 The Welcome Trust Sanger Institute, Hinxton, Cambridge CB101SA, UK
5 School of Biology, Institute for Research on Environment and Sustainability, Devonshire Building, University of Newcastle upon Tyne, NE1 7RU, U.K
6 Experimental Taxonomy Division, Department of Zoology, The Natural History Museum, Cromwell Road, London, UK SW7 5BD
7 Centro de Pesquisas Rene Rachou, Fiocruz, Belo Horizonte, MG, 30190-002, Brasil
8 Centre de Génétique Moléculaire, Centre National de la Recherche Scientifique, UPR 2167, 1 avenue de la terrasse, 91190 Gif sur Yvette, France

* To whom correspondence should be addressed.
Raymond J. Pierce, E-mail: Raymond.Pierce{at}pasteur-lille.fr


  Abstract

In most bilaterian organisms so far studied Hox genes are organised in genomic clusters and determine development along the antero-posterior axis. It has been suggested that this clustering, together with spatial and temporal colinearity of gene expression, represents the ancestral condition. However, in organisms with derived modes of embryogenesis and lineage-dependent mechanisms for the determination of cell fate, temporal colinearity of expression can be lost and Hox cluster organisation disrupted, as is the case for the ecdysozoans Drosophila melanogaster and Caenorhabditis elegans and the urochordates Ciona intestinalis and Oikopleura dioica. We sought to determine whether a lophotrochozoan, the platyhelminth parasite Schistosoma mansoni, possesses a conserved or disrupted Hox cluster. Using a PCR-based strategy we have cloned and characterized three novel S. mansoni genes encoding orthologues of Drosophila lab (SmHox1), Dfd (SmHox4) and Abd-A (SmHox8), as well as the full-length coding sequence of the previously described Smox1, which we identify as an orthologue of ftz. Quantitative RT-PCR showed that the four genes were expressed at all life-cycle stages, but that levels of expression were differentially regulated. Phylogenetic analysis and the conservation of ‘parapeptide’ sequences C-terminal to the homeodomains of SmHox8 and Smox1 support the grouping of platyhelminths within the lophotrochozoan clade. However, BAC library screening followed by genome walking failed to reconstitute a cluster. The BAC clones containing Hox genes were sequenced and in no case were other Hox genes found on the same clone. Moreover, the SmHox4 and SmHox8 genes contained single very large introns (>40 kbp) further indicating that the schistosome Hox cluster is highly extended. Localization of the Hox genes to chromosomes using FISH showed that SmHox4 and SmHox8 are on the long arm of chromosome 4, whereas SmHox1 and Smox1 are on chromosome 3. In silico screening of the available genome sequences corroborated results of Southern blotting and BAC library screening that indicate that there are no paralogues of SmHox1, SmHox4 or SmHox8. The schistosome Hox cluster is therefore not duplicated, but is both dispersed and disintegrated in the genome.

Keywords: Hox gene; Schistosoma mansoni; Lophotrochozoa; genome; chromosomes.

10These authors contributed equally to the project.


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