Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction
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.
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