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.
Highlights
Since the discovery of mice and Drosophila Hox clusters [1,2,3] the evolutionary conservation of the Hox axial patterning system has been the starting point of a conceptual framework in evolutionary developmental biology
The Hox/ParaHox-extended complement retrieved here from Clytia equates in gene number the complement present in the full genomic sequence of Hydra (8 genes) but is less rich than the repertoire present in the sea anemone genome (15 genes) [38]. This Clytia Hox/ParaHox complement well represents the diversity generally encountered in this gene family in cnidarian species
Among the 8 Hox/ ParaHox clades identified in our tree, the ‘‘anterior’’ (HOX1 and HOX2 / GSX) and ‘‘posterior’’ (HOX9-14 / collinearity since EdiCnox4 (CDX)) groups contain cnidarian sequences, but sequences from Clytia or other cnidarian species are absent from the ‘‘median’’ Hox and ParaHox groups (HOX3, HOX4-8, XLOX), as previously noticed (e.g. [29])
Summary
Since the discovery of mice and Drosophila Hox clusters [1,2,3] the evolutionary conservation of the Hox axial patterning system has been the starting point of a conceptual framework in evolutionary developmental biology (evo-devo). Each phylum could be characterised by a particular Hox pattern responsible for the establishment of its specific body plan This particular pattern establishes a ‘‘Hox code’’ consisting in a combinatorial information of position along the antero-posterior axis [9]. The 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 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
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