5 Metazoan Complexity
149
The importance of domain rearrangements during the evolution of metazoan proteins is well illustrated by the evolution of Hedgehog ligands (Fig. 5.2). Bilaterian
Hedgehog proteins consist of two functional domains: An N-terminal diffusible
receptor ligand domain, and a C-terminal autocatalytic domain (Bijlsma et al. 2004).
Both domains occur in M. brevicollis, but are encoded by separate genes (King et al.
2008, Snell et al. 2006). Whereas the N-terminal Hedge domain forms part of a
multidomain protein conserved only in sponges and cnidarians (named Hedgling),
the C-terminal Hog/Intein domain occurs in a single domain protein in M. brevicollis (Adamska et al. 2007b, King et al. 2008, Matus et al. 2008). In M. ovata,
not directly related to M. brevicollis, the C-terminal domain occurs on one protein
(Hoglet) together with putative cellulose-binding domains (Carr et al. 2008, Snell
et al. 2006). If separate Hedgehog domains represent an ancestral state, bilaterian
Hedgehog proteins are the result of specific domain duplications and shuffling prior
to the sponge/eumetazoan and the cnidarian/bilaterian split (Fig. 5.2). Accordingly,
Hedgling, the older of the two Hedge-containing proteins in the cnidarian/bilaterian
ancestor, was lost in early bilaterians while only the bona fide Hedgehog was
maintained.
Whereas extracellular and signalling domains are indicative of a considerable
interactive capacity of choanoflagellates, the repertoire of transcription factors
reflects the complexity of regulatory networks and cell type differentiation. The
Monosiga genome contains all major, ubiquitous classes of transcription factor
motifs (e.g. zinc-finger, homeobox or helix-loop-helix proteins) (King et al. 2008).
The few, previously metazoan-specific transcription factors found in Monosiga (e.g.
p53, Myc) have rather general roles in cell cycle or transcriptional control (Nedelcu
and Tan 2007). The existence of only two homeobox genes clustering specifically
with Meis/Prep/TGIF genes (TALE superclass), but not with other TALE class
genes (e.g. Iroqois) (King et al. 2008) indicates the loss of at least the Iroqoisrelated genes and non-TALE homeobox factors as these predate the emergence of
choanoflagellates (Derelle et al. 2007, Mukherjee and Bürglin 2007). Also, M. brevicollis lacks metazoan-specific Ets, Hox, POU or T-box families (King et al. 2008).
In conclusion, the conservation of many metazoan-specific protein domains
associated with cell adhesion and ECM-interacting proteins are indicative of a
surprisingly high capacity of choanoflagellates to interact among themselves and
with the environment, reflected in some choanoflagellate species by colony formation or settlement (Leadbeater 1983, Siewing 1985). However, the absence or
fragmentary presence of metazoan signalling cascade proteins suggests a rather
restricted ability to communicate between cells in a manner similar to metazoans. As
shown for tyrosine-kinase proteins, the present signalling domains appear to function in adapting intracellular processes to changing environmental conditions rather
than in cell–cell interactions. Although the majority of conserved cell adhesion
and signalling domains are present, their unique combinations within multidomain
proteins makes it difficult to deduce their ancestral functions in the choanoflagellatemetazoan ancestor. Extensive rearrangements of protein domains might have led
to novel functions on the evolutionary lines towards metazoans and choanoflagellates. In the few cases where clear orthology between proteins of M. brevicollis or
149
The importance of domain rearrangements during the evolution of metazoan proteins is well illustrated by the evolution of Hedgehog ligands (Fig. 5.2). Bilaterian
Hedgehog proteins consist of two functional domains: An N-terminal diffusible
receptor ligand domain, and a C-terminal autocatalytic domain (Bijlsma et al. 2004).
Both domains occur in M. brevicollis, but are encoded by separate genes (King et al.
2008, Snell et al. 2006). Whereas the N-terminal Hedge domain forms part of a
multidomain protein conserved only in sponges and cnidarians (named Hedgling),
the C-terminal Hog/Intein domain occurs in a single domain protein in M. brevicollis (Adamska et al. 2007b, King et al. 2008, Matus et al. 2008). In M. ovata,
not directly related to M. brevicollis, the C-terminal domain occurs on one protein
(Hoglet) together with putative cellulose-binding domains (Carr et al. 2008, Snell
et al. 2006). If separate Hedgehog domains represent an ancestral state, bilaterian
Hedgehog proteins are the result of specific domain duplications and shuffling prior
to the sponge/eumetazoan and the cnidarian/bilaterian split (Fig. 5.2). Accordingly,
Hedgling, the older of the two Hedge-containing proteins in the cnidarian/bilaterian
ancestor, was lost in early bilaterians while only the bona fide Hedgehog was
maintained.
Whereas extracellular and signalling domains are indicative of a considerable
interactive capacity of choanoflagellates, the repertoire of transcription factors
reflects the complexity of regulatory networks and cell type differentiation. The
Monosiga genome contains all major, ubiquitous classes of transcription factor
motifs (e.g. zinc-finger, homeobox or helix-loop-helix proteins) (King et al. 2008).
The few, previously metazoan-specific transcription factors found in Monosiga (e.g.
p53, Myc) have rather general roles in cell cycle or transcriptional control (Nedelcu
and Tan 2007). The existence of only two homeobox genes clustering specifically
with Meis/Prep/TGIF genes (TALE superclass), but not with other TALE class
genes (e.g. Iroqois) (King et al. 2008) indicates the loss of at least the Iroqoisrelated genes and non-TALE homeobox factors as these predate the emergence of
choanoflagellates (Derelle et al. 2007, Mukherjee and Bürglin 2007). Also, M. brevicollis lacks metazoan-specific Ets, Hox, POU or T-box families (King et al. 2008).
In conclusion, the conservation of many metazoan-specific protein domains
associated with cell adhesion and ECM-interacting proteins are indicative of a
surprisingly high capacity of choanoflagellates to interact among themselves and
with the environment, reflected in some choanoflagellate species by colony formation or settlement (Leadbeater 1983, Siewing 1985). However, the absence or
fragmentary presence of metazoan signalling cascade proteins suggests a rather
restricted ability to communicate between cells in a manner similar to metazoans. As
shown for tyrosine-kinase proteins, the present signalling domains appear to function in adapting intracellular processes to changing environmental conditions rather
than in cell–cell interactions. Although the majority of conserved cell adhesion
and signalling domains are present, their unique combinations within multidomain
proteins makes it difficult to deduce their ancestral functions in the choanoflagellatemetazoan ancestor. Extensive rearrangements of protein domains might have led
to novel functions on the evolutionary lines towards metazoans and choanoflagellates. In the few cases where clear orthology between proteins of M. brevicollis or