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F. Raible and P.R.H. Steinmetz
complexity of the Nematostella and bilaterian genomes in terms of gene content
and architecture supports a morphologically complex cnidarian-bilaterian ancestor.
However, considerable morphological differences of cnidarian and bilaterian body
plans have made comparisons difficult so far. In the following sections, we highlight
several examples where comparing conserved patterning systems shed light on the
origin of putative bilaterian-specific features (e.g. the bilaterian body axes or the
mesoderm) from a cnidarian-bilaterian ancestor.
5.5.2 Cnidarian BMP Patterning and the Evolution
of the Bilaterian Dorso-Ventral Axis
The secreted bone morphogenetic proteins (BMPs) and their antagonists Chordin,
Noggin, Gremlin and Follistatin have prominent and conserved roles in bilaterian
dorso-ventral patterning (Grunz 2004). The neurogenic side of the embryo (ventral
in protostomes and dorsal in vertebrates) expresses BMP antagonists, whereas the
opposite side secretes BMP ligands. In contrast to bilaterians, a spatially antagonistic expression of anthozoan BMP agonists and antagonists along one axis is not
discernable (Arendt and Nübler-Jung 1997, De Robertis and Sasai 1996). Whereas
anthozoan BMP2/4 and BMP5/6/7/8 are expressed asymmetrically along both the
directive axis (on one side of the blastopore and pharynx) and the oral-aboral axis
(restricted to the oral side) in early stages, later expression is only restricted to
one side of the directive axis (Hayward et al. 2002, Matus et al. 2006b, Rentzsch
et al. 2006). Although both Nematostella Chordin and Gremlin proteins can antagonize Nematostella BMP2/4 in the heterologous zebrafish system, they are expressed
inconsistently: while gremlin is the only described antagonist opposing bmp2/4
expression along the directive axis, chordin expression, like that of noggin, largely
overlaps bmp2/4. The radial expression of the follistatin antagonist expession further
refutes a spatially clear agonist-antagonist situation (Matus et al. 2006a, b, Rentzsch
et al. 2006). As most antagonists are also restricted to the oral side of the gastrula –
just as BMPs are – a clear antagonism along the oral-aboral axis is also not observed.
In general, the inconsistent expression with respect to any Nematostella axis suggests a spatially complex regulation of BMP signalling and questions the patterning
of a single anthozoan axis by a clear, bilaterian-like BMP antagonism (Rentzsch
et al. 2006). Rather, the recruitment of BMPs and their antagonists to pattern the
dorso-ventral axis appears to have evolved after the bilaterian-cnidarian split. These
results therefore imply no direct homology between the bilaterian dorso-ventral and
any cnidarian body axis.
5.5.3 Cnidarian Hox Genes and the Evolution
of the Antero-Posterior Axis
Besides the analysis of signalling pathways, the comparison of Hox gene expression may elucidate the relation of cnidarian and bilaterian axes. The Hox cluster is
F. Raible and P.R.H. Steinmetz
complexity of the Nematostella and bilaterian genomes in terms of gene content
and architecture supports a morphologically complex cnidarian-bilaterian ancestor.
However, considerable morphological differences of cnidarian and bilaterian body
plans have made comparisons difficult so far. In the following sections, we highlight
several examples where comparing conserved patterning systems shed light on the
origin of putative bilaterian-specific features (e.g. the bilaterian body axes or the
mesoderm) from a cnidarian-bilaterian ancestor.
5.5.2 Cnidarian BMP Patterning and the Evolution
of the Bilaterian Dorso-Ventral Axis
The secreted bone morphogenetic proteins (BMPs) and their antagonists Chordin,
Noggin, Gremlin and Follistatin have prominent and conserved roles in bilaterian
dorso-ventral patterning (Grunz 2004). The neurogenic side of the embryo (ventral
in protostomes and dorsal in vertebrates) expresses BMP antagonists, whereas the
opposite side secretes BMP ligands. In contrast to bilaterians, a spatially antagonistic expression of anthozoan BMP agonists and antagonists along one axis is not
discernable (Arendt and Nübler-Jung 1997, De Robertis and Sasai 1996). Whereas
anthozoan BMP2/4 and BMP5/6/7/8 are expressed asymmetrically along both the
directive axis (on one side of the blastopore and pharynx) and the oral-aboral axis
(restricted to the oral side) in early stages, later expression is only restricted to
one side of the directive axis (Hayward et al. 2002, Matus et al. 2006b, Rentzsch
et al. 2006). Although both Nematostella Chordin and Gremlin proteins can antagonize Nematostella BMP2/4 in the heterologous zebrafish system, they are expressed
inconsistently: while gremlin is the only described antagonist opposing bmp2/4
expression along the directive axis, chordin expression, like that of noggin, largely
overlaps bmp2/4. The radial expression of the follistatin antagonist expession further
refutes a spatially clear agonist-antagonist situation (Matus et al. 2006a, b, Rentzsch
et al. 2006). As most antagonists are also restricted to the oral side of the gastrula –
just as BMPs are – a clear antagonism along the oral-aboral axis is also not observed.
In general, the inconsistent expression with respect to any Nematostella axis suggests a spatially complex regulation of BMP signalling and questions the patterning
of a single anthozoan axis by a clear, bilaterian-like BMP antagonism (Rentzsch
et al. 2006). Rather, the recruitment of BMPs and their antagonists to pattern the
dorso-ventral axis appears to have evolved after the bilaterian-cnidarian split. These
results therefore imply no direct homology between the bilaterian dorso-ventral and
any cnidarian body axis.
5.5.3 Cnidarian Hox Genes and the Evolution
of the Antero-Posterior Axis
Besides the analysis of signalling pathways, the comparison of Hox gene expression may elucidate the relation of cnidarian and bilaterian axes. The Hox cluster is