Are Hox Genes Ancestrally Involved in Axial Patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria)

Abstract

BackgroundThe early evolution and diversification of Hox-related genes in eumetazoans has been the subject of conflicting hypotheses concerning the evolutionary conservation of their role in axial patterning and the pre-bilaterian origin of the Hox and ParaHox clusters. The diversification of Hox/ParaHox genes clearly predates the origin of bilaterians. However, the existence of a “Hox code” predating the cnidarian-bilaterian ancestor and supporting the deep homology of axes is more controversial. This assumption was mainly based on the interpretation of Hox expression data from the sea anemone, but growing evidence from other cnidarian taxa puts into question this hypothesis.Methodology/Principal FindingsHox, ParaHox and Hox-related genes have been investigated here by phylogenetic analysis and in situ hybridisation in Clytia hemisphaerica, an hydrozoan species with medusa and polyp stages alternating in the life cycle. Our phylogenetic analyses do not support an origin of ParaHox and Hox genes by duplication of an ancestral ProtoHox cluster, and reveal a diversification of the cnidarian HOX9-14 genes into three groups called A, B, C. Among the 7 examined genes, only those belonging to the HOX9-14 and the CDX groups exhibit a restricted expression along the oral-aboral axis during development and in the planula larva, while the others are expressed in very specialised areas at the medusa stage.Conclusions/SignificanceCross species comparison reveals a strong variability of gene expression along the oral-aboral axis and during the life cycle among cnidarian lineages. The most parsimonious interpretation is that the Hox code, collinearity and conservative role along the antero-posterior axis are bilaterian innovations.

Indirect development, transdifferentiation and the macroregulatory evolution of metazoans

“…In addition, the sequence of mesentery formation and their involvement in gametogenesis also correlates with the spatial expression of Hox genes along the directive axis (Extavour et al 2005;Ryan et al 2007). Interestingly, Cdx and posterior group Hox genes are also coexpressed in the gonads of the hydrozoan Clytia hemisphaerica (Chiori et al 2009). Perhaps the main Hox vector of bilaterians corresponds with the Hox vector of the directive axis of N. vectensis and relates in both groups primarily to gonad formation.…”

Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals

“…In addition, Hox genes regulate other developmental processes, such as limb patterning in vertebrates and segment identity in insects (reviewed by (Pearson et al, 2005)). While roles of Hox genes in bilaterian axial patterning are highly conserved, their function in Cnidarians remains disputable, and it is therefore unclear when the strong connection between Hox genes and anteroposterior patterning arose during evolution (Chourrout et al, 2006;Kamm et al, 2006;Ryan et al, 2007;Chiori et al, 2009). On the other hand, germ layer patterning, and especially determination of endomesoderm (which is intimately linked with the event of gastrulation), utilizes the same set of DTFs, including Twist, Snail, Forkhead, Brachury and Tcf in bilaterians and cnidarians (Davidson et al, 2002;Röttinger et al, 2012).…”

How Hox genes can shed light on the place of echinoderms among the deuterostomes

“…In basal animals, such as the cnidarian Clytia , the cluster seems to be fragmented and displays no colinearity [13]. Other exceptions of importance occur within the superphylum Deuterostomia, in which fully organized clusters are most often found.…”