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Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria).

Chiori R, Jager M, Denker E, Wincker P, Da Silva C, Le Guyader H, Manuel M, Quéinnec E - PLoS ONE (2009)

Bottom Line: 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.Cross 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.

View Article: PubMed Central - PubMed

Affiliation: UPMC Univ Paris 06, UMR 7138 CNRS UPMC MNHN IRD, Paris, France.

ABSTRACT

Background: 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 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 findings: Hox, 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/significance: Cross 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.

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Comparison of Hox expression patterns among cnidarian species.Each expression pattern is represented by a red shading on the planula, polyp or medusa diagrams. The diagrams illustrate a schematic view of each stage after theoretical longitudinal section to expose the ectodermal layer (dark gray) and the endodermal layer (light gray) separated by the mesoglea (black line). All published expression data for cnidarian species were mapped on the ML phylogenetic tree. Branches for bilaterian sequences were compressed to simplify the figure. Black disks indicate statistically supported nodes.
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pone-0004231-g005: Comparison of Hox expression patterns among cnidarian species.Each expression pattern is represented by a red shading on the planula, polyp or medusa diagrams. The diagrams illustrate a schematic view of each stage after theoretical longitudinal section to expose the ectodermal layer (dark gray) and the endodermal layer (light gray) separated by the mesoglea (black line). All published expression data for cnidarian species were mapped on the ML phylogenetic tree. Branches for bilaterian sequences were compressed to simplify the figure. Black disks indicate statistically supported nodes.

Mentions: Collinearity has been initially defined for non-fragmented Hox clusters as a correlation between the physical order of Hox genes in the genome and their expression domains along the antero-posterior axis of bilaterian animals [52], “cis-collinearity” according to Duboule [53]. However, in the case of a partially or totally dispersed cluster or when no genomic data are available, Hox expression domains along the antero-posterior axis can be correlated with the phylogenetic position of the genes with respect to paralogous groups in species with an intact cluster (“trans-collinearity” according to Duboule [53]). The only reported instance of a genomic linkage between several Hox genes in Cnidaria concerns the Nematostella genome, which contains a 50 kb cluster of five genes arranged in the following order: the HOX1 gene NveAnthox6, the EVE gene NveEve and the three HOX2 genes NveAnthox8b, NveAnthox8a and NveAnthox7 [38]. However, the expression of these four Hox genes along the oral-aboral axis shows no evidence of cis-collinearity, Anthox6 being expressed in the pharyngeal endoderm and NveAnthox8a-8b-7 being expressed all along the axis in the body wall endoderm (figure 5; [37]). For the remaining cnidarian species (and for the remaining Nematostella genes), lack of physical linkage or of information about it leaves trans-collinearity (with the order of orthologous Hox gene expression in bilaterians taken as a reference) as the only potential form of collinearity to be considered.


Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria).

Chiori R, Jager M, Denker E, Wincker P, Da Silva C, Le Guyader H, Manuel M, Quéinnec E - PLoS ONE (2009)

Comparison of Hox expression patterns among cnidarian species.Each expression pattern is represented by a red shading on the planula, polyp or medusa diagrams. The diagrams illustrate a schematic view of each stage after theoretical longitudinal section to expose the ectodermal layer (dark gray) and the endodermal layer (light gray) separated by the mesoglea (black line). All published expression data for cnidarian species were mapped on the ML phylogenetic tree. Branches for bilaterian sequences were compressed to simplify the figure. Black disks indicate statistically supported nodes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2626245&req=5

pone-0004231-g005: Comparison of Hox expression patterns among cnidarian species.Each expression pattern is represented by a red shading on the planula, polyp or medusa diagrams. The diagrams illustrate a schematic view of each stage after theoretical longitudinal section to expose the ectodermal layer (dark gray) and the endodermal layer (light gray) separated by the mesoglea (black line). All published expression data for cnidarian species were mapped on the ML phylogenetic tree. Branches for bilaterian sequences were compressed to simplify the figure. Black disks indicate statistically supported nodes.
Mentions: Collinearity has been initially defined for non-fragmented Hox clusters as a correlation between the physical order of Hox genes in the genome and their expression domains along the antero-posterior axis of bilaterian animals [52], “cis-collinearity” according to Duboule [53]. However, in the case of a partially or totally dispersed cluster or when no genomic data are available, Hox expression domains along the antero-posterior axis can be correlated with the phylogenetic position of the genes with respect to paralogous groups in species with an intact cluster (“trans-collinearity” according to Duboule [53]). The only reported instance of a genomic linkage between several Hox genes in Cnidaria concerns the Nematostella genome, which contains a 50 kb cluster of five genes arranged in the following order: the HOX1 gene NveAnthox6, the EVE gene NveEve and the three HOX2 genes NveAnthox8b, NveAnthox8a and NveAnthox7 [38]. However, the expression of these four Hox genes along the oral-aboral axis shows no evidence of cis-collinearity, Anthox6 being expressed in the pharyngeal endoderm and NveAnthox8a-8b-7 being expressed all along the axis in the body wall endoderm (figure 5; [37]). For the remaining cnidarian species (and for the remaining Nematostella genes), lack of physical linkage or of information about it leaves trans-collinearity (with the order of orthologous Hox gene expression in bilaterians taken as a reference) as the only potential form of collinearity to be considered.

Bottom Line: 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.Cross 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.

View Article: PubMed Central - PubMed

Affiliation: UPMC Univ Paris 06, UMR 7138 CNRS UPMC MNHN IRD, Paris, France.

ABSTRACT

Background: 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 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 findings: Hox, 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/significance: Cross 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.

Show MeSH
Related in: MedlinePlus