HOX genes in the sepiolid squid Euprymna scolopes : Implications for the evolution of complex body plans

Abstract

Molluscs display a rich diversity of body plans ranging from the wormlike appearance of aplacophorans to the complex body plan of the cephalopods with highly developed sensory organs, a complex central nervous system, and cognitive abilities unrivaled among the invertebrates. The aim of the current study is to define molecular parameters relevant to the developmental evolution of cephalopods by using the sepiolid squid Euprymna scolopes as a model system. Using PCR-based approaches, we identified one anterior, one paralog group 3, five central, and two posterior group Hox genes. The deduced homeodomain sequences of the E. scolopes Hox cluster genes are most similar to known annelid, brachiopod, and nemertean Hox gene homeodomain sequences. Our results are consistent with the presence of a single Hox gene cluster in cephalopods. Our data also corroborate the proposed existence of a differentiated Hox gene cluster in the last common ancestor of Bilaterians. Furthermore, our phylogenetic analysis and in particular the identification of Post-1 and Post-2 homologs support the Lophotrochozoan clade.

The rise and fall of Hox gene clusters

“…Callaerts et al, 2002) but also in nemerteans (Kmita-Cunisse et al, 1998) or brachiopods (de Rosa et al, 1999). Yet, so far, the genomic organization of only a flatworm (see above) and the annelid polychaete Platynereis is known, and these probably contain a rather intact cluster (D. Ferrier, personal communication).…”

Evolution of Hox genes in molluscs: a comparison among seven morphologically diverse classes

“…Degnan & Morse (1993) revealed that there were five Hox genes in the abalone Haliotis rufescens, which is considered a relatively basal species in Gastropoda (see also Giusti et al, 2000;Hinman et al, 2003). Callaerts et al (2002) described nine Hox genes in the squid Euprymna scolopes, also inferring that a molluscan genome has only one Hox cluster. de Rosa et al (1999) compared Hox genes among various bilaterian animals, using the limpet Patella vulgata with six Hox genes as the molluscan representative, whereas Balavoine, de Rosa & Adoutte (2002), in a review paper, used the squid E. scolopes with nine Hox genes as the molluscan representative.…”

Presence of Proboscipedia and Caudal Gene Homologues in a Bivalve Mollusc

“…Vox2 shows a higher level of homology with Drosophila, mouse or human Pb homeodomains (they diverge by 0% and 9% respectively). The identification of proboscipedia orthologs from molluscs has proven difficult (Callaerts et al, 2002) although a study of the gastropod Haliotis suggested the presence of a Hox2 paralog (Degnan and Morse, 1993); in fact, Vox1 and Vox2 display significant similarity to the Hrox3 and 5 sequences. Alignment of the Vox4 and Vox5-derived amino acid sequences reveals the greatest similarity to members of the Cad protein family (Fig.…”

“…The Cad function in Drosophila and its expression pattern in vertebrates indicate that this gene family is important in the axial pattern formation (Epstein et al, 1997). Homologues of pb and cad genes have been reported in different taxa including sepiolid squids (Euprymna scolopes) (Callaerts et al, 2002) or abalones (Haliotis rufescens) (Degnan and Morse, 1993), but no cad or pb gene fragments have been reported in bivalve molluscs.…”

“…The genome of molluscs is not as well described as are those of model bilaterian organisms, although in recent years several homologues of developmental genes have been identified (Wray et al, 1995;Lee et al, 2001;Callaerts et al, 2002). In fact, the DNA-binding motif from homeobox genes has been very useful for isolating gene homologues in different animals on the basis of sequence similarity.…”