Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements

Abstract

Recent molecular phylogenies support that the non-bilaterian Cnidaria is the sister group to bilaterians (4,5) and are therefore informative to reconstruct the early history of bilaterian homeobox gene complements. Earlier searches for cnidarian homeobox genes have revealed the presence of anterior-like Hox genes as well as Gsx, so that the ProtoHox cluster must have been duplicated prior to the cnidarian-bilaterian split. Earlier reports (6-13) have proposed that posterior Hox genes but not central genes or Hox3 are also present in cnidarians. We used publicly available high coverage genome shotgun sequence to identify the complete set of homeobox genes of two distantly related cnidarians, the freshwater polyp Hydra magnipapillata (Hydrozoa) and the sea anemone Nematostella vectensis (Anthozoa).Nematostella is particularly informative as it is considered to represent the basal group within the Cnidaria (14,15 (Fig. 1b and SOM). Instead, they formed an independent and strongly supported branch. Finally, one of the two divergent genes showed conflicting affinities in network analyses with Cdx and Xlox (Fig. 1b) and is therefore most likely a ParaHox gene. (Fig. 2c), and Gsx was the only ParaHox gene detected.As lineage-specific duplications in the Hox cluster are rare within bilaterians, we wanted to know whether or not those found in Nematostella are limited to the Hox genes. For this we examined potential linkages between all other homeobox genes. Including the nine Hox-like genes mentioned above, we found a total of 139 homeobox genes, a surprisingly high number compared to other invertebrates (Table 1 and SOM). Phylogenetic analyses allowed placing at least 87 of those into 58 known groups of homeobox genes, out of 76 groups known for 5 bilaterians. They also suggested that 42 unclassified genes have arisen through recent amplifications of maximally ten genes. By comparison, Hydra has a considerably smaller number of homeobox genes and gene groups. Since all Hydra homeobox gene groups have representatives in the Nematostella genome, we assume that the homeobox complement has been dramatically reduced in the Hydra lineage (Table 1). Comparisons between the extended homeobox sequences of Nematostella allowed the detection of an additional 13 physical clusters ( Fig. 2b and SOM). Four of these clusters may have a more ancient origin, either because they have been identified in the genomes of bilaterians or because they associate distantly related genes. The other nine clusters are undoubtedly the result of recent tandem duplications. We also did not detect obvious synteny conservation between the environments of well related but unlinked homeobox genes, as might be expected after whole genome duplication (not shown). Hence, the gene duplications observed among the Nematostella Hox genes represent a general phenomenon for the homeobox gene complement.From our data, the most parsimonious scenario for the evolution of Hox/ParaHox clusters is as follows (Fig. 3): two ProtoHox genes (P1/2 and P3) gave rise to the ...

The Wnt code: cnidarians signal the way

“…One hypothesis is that hox/parahox clusters originated from the duplication of an ancient protohox cluster with anterior and posterior hox/parahox genes (Brooke et al, 1998;Ferrier and Holland, 2001;Brooke and Holland, 2003;Garcia-Fernandez, 2005a, b). However, other findings propose the protohox cluster may have only consisted of two anterior genes, while the non-anterior genes most probably appeared independently in the hox and parahox clusters after the separation of bilaterians and cnidarians (Chourrout et al, 2006;Kamm et al, 2006). …”

“…However, new data reveal that no complete hox code exists in cnidarians. Although some if not all cnidarians possess a limited number of bilaterian-like anterior hox genes, many of these genes are paralogs and they do not represent equivalents of the hox cluster (Chourrout et al, 2006;Kamm et al, 2006). One hypothesis is that hox/parahox clusters originated from the duplication of an ancient protohox cluster with anterior and posterior hox/parahox genes (Brooke et al, 1998;Ferrier and Holland, 2001;Brooke and Holland, 2003;Garcia-Fernandez, 2005a, b).…”

Ancient linkage of a POU class 6 and an anterior hox‐like gene in cnidaria: implications for the evolution of homeobox genes

“…Compared with representatives from Bilateria both appear to be relatively derived, whereas the other cnidarian sequence, the Acropora POU3 protein seems to be less derived from the POU consensus. Initial analyses (not shown) with the POU homeodomain alone showed that the Nematostella POU 1, 3 and 4 class genes (Ryan et al, 2006;Chourrout et al, 2006) also seem to be less derived from the POU consensus. However, the homeodomain of the Nematostella POU class 6 gene (Ryan et al, 2006;Chourrout et al, 2006) as well as a putative POU6 gene from Condylactis (with only partial POU S and partial POU H domain) (Shah et al, 2000) show similar deviations as the Eleutheria POU6 homeodomain.…”

“…Initial analyses (not shown) with the POU homeodomain alone showed that the Nematostella POU 1, 3 and 4 class genes (Ryan et al, 2006;Chourrout et al, 2006) also seem to be less derived from the POU consensus. However, the homeodomain of the Nematostella POU class 6 gene (Ryan et al, 2006;Chourrout et al, 2006) as well as a putative POU6 gene from Condylactis (with only partial POU S and partial POU H domain) (Shah et al, 2000) show similar deviations as the Eleutheria POU6 homeodomain. For example, at homeodomain position 44 all cnidarian class 6 genes show a threonine residue, whereas all other POU genes (including bilaterian class 6) have a valine residue at this position.…”

“…'98;Latchman,'99). To accommodate the alignment for a Nematostella POU class 6 gene, available with a POU S domain of 74aa (Chourrout et al, 2006), a conserved F residue was treated as position 11, whereas an E/D residue at position 74 marked the end of the subdomain (note that POU class 4 proteins contain a conserved insertion of the motif PGV after position 38). The variable linker between POU S and POU H was removed from the alignment for the analysis of both domains.…”