Pre-Bilaterian Origins of the Hox Cluster and the Hox Code: Evidence from the Sea Anemone, Nematostella vectensis

Abstract

BackgroundHox genes were critical to many morphological innovations of bilaterian animals. However, early Hox evolution remains obscure. Phylogenetic, developmental, and genomic analyses on the cnidarian sea anemone Nematostella vectensis challenge recent claims that the Hox code is a bilaterian invention and that no “true” Hox genes exist in the phylum Cnidaria.Methodology/Principal FindingsPhylogenetic analyses of 18 Hox-related genes from Nematostella identify putative Hox1, Hox2, and Hox9+ genes. Statistical comparisons among competing hypotheses bolster these findings, including an explicit consideration of the gene losses implied by alternate topologies. In situ hybridization studies of 20 Hox-related genes reveal that multiple Hox genes are expressed in distinct regions along the primary body axis, supporting the existence of a pre-bilaterian Hox code. Additionally, several Hox genes are expressed in nested domains along the secondary body axis, suggesting a role in “dorsoventral” patterning.Conclusions/SignificanceA cluster of anterior and posterior Hox genes, as well as ParaHox cluster of genes evolved prior to the cnidarian-bilaterian split. There is evidence to suggest that these clusters were formed from a series of tandem gene duplication events and played a role in patterning both the primary and secondary body axes in a bilaterally symmetrical common ancestor. Cnidarians and bilaterians shared a common ancestor some 570 to 700 million years ago, and as such, are derived from a common body plan. Our work reveals several conserved genetic components that are found in both of these diverse lineages. This finding is consistent with the hypothesis that a set of developmental rules established in the common ancestor of cnidarians and bilaterians is still at work today.

Acoel development supports a simple planula-like urbilaterian

“…We show (figure 4a-d ) that ClEvx expression in the acoel is more similar to the pattern found in cnidarians and, at least in the hatchling, is expressed exclusively in distinct neurons of the brain anterior and posterior to the statocyst (figure 4b). ClEvx expression at earlier stages appears to play a role in sensory cell specification in both cnidarians and acoels (Ryan et al 2007). A similar pattern of evx expression in the brain is found in Branchiostoma ( Ferrier et al 2001) and thus suggests a neural function of evx in the urbilaterian and not a role in posterior patterning.…”

“…Although our molecular understanding of acoelomorphs is in its infancy, it appears that they might display features expected for their position between cnidarians and eubilaterians. For example, the search for HOX genes in four acoelomorph species (Cook et al 2004;Jiménez-Guri et al 2006; own results) yielded a small number of HOX class genes: 1-2 anterior class, a single posterior class, and 1-2 central class (central class HOX genes appear to be absent in cnidarians; Chourrout et al 2006;Ryan et al 2006Ryan et al , 2007. In addition, a Cdx and Xlox orthologue has been found in acoels and nemertodermatids (Cook et al 2004;Jiménez-Guri et al 2006).…”

Early origin of the bilaterian developmental toolkit

“…There are many cnidarian model systems, but the development of the sea anemone N. vectensis has received considerable attention and the entire genome sequence was recently released (Ryan et al 2007b). Other cnidarians have also been studied, including the coral Acropora and Hydra, a hydrozoan.…”

Back in time: a new systematic proposal for the Bilateria

“…Suggested synapomorphies for the Planulozoa are the presence of endodermal myoepithelial musculature, septate junctions in epithelial cells, symmetrically arranged spermatozoon heads with a mid-piece and a set of several clustered HOX genes (Wallberg et al 2004). Such features, however, are plesiomorphic or have not been tested in other phyla, and, when referring to HOX clustering in cnidarians, seem at odds with most recent genomic data (Chourrout et al 2006;Ryan et al 2007). Moreover, the name Planulozoa stems from the presumed similarities between the planula larva and acoel worms, both being vermiform and having an apparent polar development of the nervous system (for specific references, see Wallberg et al 2004).…”