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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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Phylogenetic relationships between cnidarian, placozoan and bilaterian Hox/ParaHox related homeodomains inferred by ML analysis.Support values higher than 50% for each Hox/ParaHox related group are shown on the branches. Numbers above the branches indicate ML bootstrap values (100 replicates). Numbers below the branches indicate NJ bootstrap values (1000 replicates). Abbreviations: Ami, Acropora millepora; Bfl, Branchiostoma floridae; Che, Clytia hemisphaerica; Csa, Cupiennus salei; Csp, Capitella sp.; Cvi, Chlorohydra viridissima; Cxa, Cassiopeia xamachana; Dme, Drosophila melanogaster; Edi, Eleutheria dichotoma; Esc, Euprymna scolopes; Hma, Hydra magnipapillata; Hru, Haliotis rufescens; Hsy, Hydractinia symbiolongicarpus; Hvu, Hydra vulgaris; Mse, Metridium senile; Ner, Nereis virens; Nve, Nematostella vectensis; Pca, Podocoryne carnea; Tr, Trichoplax adhaerens.
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pone-0004231-g001: Phylogenetic relationships between cnidarian, placozoan and bilaterian Hox/ParaHox related homeodomains inferred by ML analysis.Support values higher than 50% for each Hox/ParaHox related group are shown on the branches. Numbers above the branches indicate ML bootstrap values (100 replicates). Numbers below the branches indicate NJ bootstrap values (1000 replicates). Abbreviations: Ami, Acropora millepora; Bfl, Branchiostoma floridae; Che, Clytia hemisphaerica; Csa, Cupiennus salei; Csp, Capitella sp.; Cvi, Chlorohydra viridissima; Cxa, Cassiopeia xamachana; Dme, Drosophila melanogaster; Edi, Eleutheria dichotoma; Esc, Euprymna scolopes; Hma, Hydra magnipapillata; Hru, Haliotis rufescens; Hsy, Hydractinia symbiolongicarpus; Hvu, Hydra vulgaris; Mse, Metridium senile; Ner, Nereis virens; Nve, Nematostella vectensis; Pca, Podocoryne carnea; Tr, Trichoplax adhaerens.

Mentions: Sixteen ANTP homeodomain sequences have been retrieved by tBLASTn search from our Clytia EST collection (figures S1 and S2). Among them, 8 belong to the Hox-extended family, which includes Hox, ParaHox, Mox, HlxB9, Rough and Eve genes (figure 1). 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].


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)

Phylogenetic relationships between cnidarian, placozoan and bilaterian Hox/ParaHox related homeodomains inferred by ML analysis.Support values higher than 50% for each Hox/ParaHox related group are shown on the branches. Numbers above the branches indicate ML bootstrap values (100 replicates). Numbers below the branches indicate NJ bootstrap values (1000 replicates). Abbreviations: Ami, Acropora millepora; Bfl, Branchiostoma floridae; Che, Clytia hemisphaerica; Csa, Cupiennus salei; Csp, Capitella sp.; Cvi, Chlorohydra viridissima; Cxa, Cassiopeia xamachana; Dme, Drosophila melanogaster; Edi, Eleutheria dichotoma; Esc, Euprymna scolopes; Hma, Hydra magnipapillata; Hru, Haliotis rufescens; Hsy, Hydractinia symbiolongicarpus; Hvu, Hydra vulgaris; Mse, Metridium senile; Ner, Nereis virens; Nve, Nematostella vectensis; Pca, Podocoryne carnea; Tr, Trichoplax adhaerens.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0004231-g001: Phylogenetic relationships between cnidarian, placozoan and bilaterian Hox/ParaHox related homeodomains inferred by ML analysis.Support values higher than 50% for each Hox/ParaHox related group are shown on the branches. Numbers above the branches indicate ML bootstrap values (100 replicates). Numbers below the branches indicate NJ bootstrap values (1000 replicates). Abbreviations: Ami, Acropora millepora; Bfl, Branchiostoma floridae; Che, Clytia hemisphaerica; Csa, Cupiennus salei; Csp, Capitella sp.; Cvi, Chlorohydra viridissima; Cxa, Cassiopeia xamachana; Dme, Drosophila melanogaster; Edi, Eleutheria dichotoma; Esc, Euprymna scolopes; Hma, Hydra magnipapillata; Hru, Haliotis rufescens; Hsy, Hydractinia symbiolongicarpus; Hvu, Hydra vulgaris; Mse, Metridium senile; Ner, Nereis virens; Nve, Nematostella vectensis; Pca, Podocoryne carnea; Tr, Trichoplax adhaerens.
Mentions: Sixteen ANTP homeodomain sequences have been retrieved by tBLASTn search from our Clytia EST collection (figures S1 and S2). Among them, 8 belong to the Hox-extended family, which includes Hox, ParaHox, Mox, HlxB9, Rough and Eve genes (figure 1). 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].

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