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First published online November 9, 2007
doi: 10.1242/10.1242/dev.010173

Development 134, 4187-4197 (2007)
Published by The Company of Biologists 2007
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Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction

Holger Bielen1, Sabine Oberleitner2, Sylvain Marcellini3,4, Lydia Gee5, Patrick Lemaire3, Hans R. Bode5, Ralph Rupp2,* and Ulrich Technau1,*

1 Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt. 55, 5008 Bergen, Norway.
2 Adolf-Butenandt-Institut, Ludwig-Maximilians-Universität, Schillerstrase 44, D-80336 München, Germany.
3 IBDM/LGPD Case 907, Campus de Luminy, 13288 Marseille, France.
4 Departamento de Bioquimica y Biologia Molecular, Facultad de Ciencias Biológicas, Universidad de Concepción, Casilla 160-C, Concepción, Chile.
5 Developmental Biology Center and Developmental and Cell Biology Department, University of California at Irvine, Irvine, CA 92697, USA.

* Authors for correspondence (e-mails: ralph.rupp{at}med.uni-muenchen.de; ulrich.technau{at}sars.uib.no)

Accepted 4 September 2007

Homologues of the T-box gene Brachyury play important roles in mesoderm differentiation and other aspects of early development in all bilaterians. In the diploblast Hydra, the Brachyury homologue HyBra1 acts early in the formation of the hypostome, the location of the organiser in adult Hydra. We now report the isolation and characterisation of a second Brachyury gene, HyBra2. Sequence analysis suggests that HyBra1 and HyBra2 are paralogues, resulting from an ancient lineage-specific gene duplication. We show that both paralogues acquired novel functions, both at the level of their cis-regulation as well as through significant divergence of the coding sequence. Both genes are expressed in the hypostome, but HyBra1 is predominantly endodermal, whereas HyBra2 transcripts are found primarily in the ectoderm. During bud formation, both genes are activated before any sign of evagination, suggesting an early role in head formation. During regeneration, HyBra1 is an immediate-early response gene and is insensitive to protein synthesis inhibition, whereas the onset of expression of HyBra2 is delayed and requires protein synthesis. The functional consequence of HyBra1/2 protein divergence on cell fate decisions was tested in Xenopus. HyBra1 induces mesoderm, like vertebrate Brachyury proteins. By contrast, HyBra2 shows a strong cement-gland and neural-inducing activity. Domain-swapping experiments show that the C-terminal domain of HyBra2 is responsible for this specific phenotype. Our data support the concept of sub- and neofunctionalisation upon gene duplication and show that divergence of cis-regulation and coding sequence in paralogues can lead to dramatic changes in structure and function.

Key words: Brachyury, Hydra, Gene duplication, Head formation, Regeneration, Mesoderm, Evolution, Structure function analysis, Xenopus, Animal cap






© The Company of Biologists Ltd 2007