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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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Expression of ParaHox and Mox genes in Clytia hemisphaerica.A–C: CheGsx expression; A: general view of the medusa; B: higher magnification of the distal part of the tentacle bulb; C: distal part of the tentacle bulb after double in situ hybridisation with CheGsx (in blue) and CheMcol3-4 (in red) riboprobes. D–H: CheCdx expression; D: unfertilised egg with animal pole on the top; E: gastrula with ingression pole ( = animal and future oral pole) on the top (arrow); F: expression in one-day-old planula with oral/posterior pole on the top; G: general view of the medusa; H: higher magnification of the tentacle bulb. I–K: CheMox expression; I: general view of the medusa; J: higher magnification of the radial canal (delineated by dotted lines) crossing the gonad; K: higher magnification of the tentacle bulb showing the ectodermal and endodermal layers separated by a dotted line. Scale bars: A, G, I: 100 µm; B, C, H, J, K: 20 µm; D–F: 50 µm. Legends: ec: ectoderm; en: endoderm; g: gonad; m: manubrium; t: tentacle; tb: tentacle bulb.
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pone-0004231-g003: Expression of ParaHox and Mox genes in Clytia hemisphaerica.A–C: CheGsx expression; A: general view of the medusa; B: higher magnification of the distal part of the tentacle bulb; C: distal part of the tentacle bulb after double in situ hybridisation with CheGsx (in blue) and CheMcol3-4 (in red) riboprobes. D–H: CheCdx expression; D: unfertilised egg with animal pole on the top; E: gastrula with ingression pole ( = animal and future oral pole) on the top (arrow); F: expression in one-day-old planula with oral/posterior pole on the top; G: general view of the medusa; H: higher magnification of the tentacle bulb. I–K: CheMox expression; I: general view of the medusa; J: higher magnification of the radial canal (delineated by dotted lines) crossing the gonad; K: higher magnification of the tentacle bulb showing the ectodermal and endodermal layers separated by a dotted line. Scale bars: A, G, I: 100 µm; B, C, H, J, K: 20 µm; D–F: 50 µm. Legends: ec: ectoderm; en: endoderm; g: gonad; m: manubrium; t: tentacle; tb: tentacle bulb.

Mentions: The ParaHox gene CheGsx is expressed specifically at the medusa stage (figure 3A) and no expression has been detected at other stage during the life cycle (not shown). CheGsx transcripts are localised in scattered cells in the tentacles and in the tentacle bulbs (figure 3A), spherical enlargements on the bell margin that bear tentacles. The tentacle bulb is a specialised region devoted to the continuous production of tentacle cells, the latter being permanently used and destroyed because of prey capture. This structure has been recently shown to be a site of intensive nematogenesis characterised by an ordered progression of cell stages along its proximo-distal axis [44]. Nematocyte progenitors are localised in the proximal region of the bulb, near the bell margin, and the nematoblasts move during their differentiation towards the tentacle, where they maturate. The CheGsx-expressing cells are not homogeneously distributed along the proximo-distal axis of the tentacle bulb. They form, in the ectodermal layer, isolated basi-epithelial spots concentrated in the more distal part of the bulb and in the tentacle base, and also more concentrated on the abaxial side of the bulb (figure 3B). This position does not correspond to the crescent-shaped distribution of nematocyte precursors, but rather to the neuron and sensory cell-rich area of the bulb ectoderm. Furthermore, CheHox1 is not co-expressed with the minicollagen CheMcol3-4 (figure 3C), a nematocyte capsule structural component expressed during differentiation of the tentacle main nematocyte type [44]. In addition, we have failed to identify nematocyte capsules (easily distinguishable using DIC optics) inside the CheGsx expressing cells (figure 3B–C). Thus, CheGsx is probably expressed in neural cells or precursors rather than in nematoblasts.


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)

Expression of ParaHox and Mox genes in Clytia hemisphaerica.A–C: CheGsx expression; A: general view of the medusa; B: higher magnification of the distal part of the tentacle bulb; C: distal part of the tentacle bulb after double in situ hybridisation with CheGsx (in blue) and CheMcol3-4 (in red) riboprobes. D–H: CheCdx expression; D: unfertilised egg with animal pole on the top; E: gastrula with ingression pole ( = animal and future oral pole) on the top (arrow); F: expression in one-day-old planula with oral/posterior pole on the top; G: general view of the medusa; H: higher magnification of the tentacle bulb. I–K: CheMox expression; I: general view of the medusa; J: higher magnification of the radial canal (delineated by dotted lines) crossing the gonad; K: higher magnification of the tentacle bulb showing the ectodermal and endodermal layers separated by a dotted line. Scale bars: A, G, I: 100 µm; B, C, H, J, K: 20 µm; D–F: 50 µm. Legends: ec: ectoderm; en: endoderm; g: gonad; m: manubrium; t: tentacle; tb: tentacle bulb.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2626245&req=5

pone-0004231-g003: Expression of ParaHox and Mox genes in Clytia hemisphaerica.A–C: CheGsx expression; A: general view of the medusa; B: higher magnification of the distal part of the tentacle bulb; C: distal part of the tentacle bulb after double in situ hybridisation with CheGsx (in blue) and CheMcol3-4 (in red) riboprobes. D–H: CheCdx expression; D: unfertilised egg with animal pole on the top; E: gastrula with ingression pole ( = animal and future oral pole) on the top (arrow); F: expression in one-day-old planula with oral/posterior pole on the top; G: general view of the medusa; H: higher magnification of the tentacle bulb. I–K: CheMox expression; I: general view of the medusa; J: higher magnification of the radial canal (delineated by dotted lines) crossing the gonad; K: higher magnification of the tentacle bulb showing the ectodermal and endodermal layers separated by a dotted line. Scale bars: A, G, I: 100 µm; B, C, H, J, K: 20 µm; D–F: 50 µm. Legends: ec: ectoderm; en: endoderm; g: gonad; m: manubrium; t: tentacle; tb: tentacle bulb.
Mentions: The ParaHox gene CheGsx is expressed specifically at the medusa stage (figure 3A) and no expression has been detected at other stage during the life cycle (not shown). CheGsx transcripts are localised in scattered cells in the tentacles and in the tentacle bulbs (figure 3A), spherical enlargements on the bell margin that bear tentacles. The tentacle bulb is a specialised region devoted to the continuous production of tentacle cells, the latter being permanently used and destroyed because of prey capture. This structure has been recently shown to be a site of intensive nematogenesis characterised by an ordered progression of cell stages along its proximo-distal axis [44]. Nematocyte progenitors are localised in the proximal region of the bulb, near the bell margin, and the nematoblasts move during their differentiation towards the tentacle, where they maturate. The CheGsx-expressing cells are not homogeneously distributed along the proximo-distal axis of the tentacle bulb. They form, in the ectodermal layer, isolated basi-epithelial spots concentrated in the more distal part of the bulb and in the tentacle base, and also more concentrated on the abaxial side of the bulb (figure 3B). This position does not correspond to the crescent-shaped distribution of nematocyte precursors, but rather to the neuron and sensory cell-rich area of the bulb ectoderm. Furthermore, CheHox1 is not co-expressed with the minicollagen CheMcol3-4 (figure 3C), a nematocyte capsule structural component expressed during differentiation of the tentacle main nematocyte type [44]. In addition, we have failed to identify nematocyte capsules (easily distinguishable using DIC optics) inside the CheGsx expressing cells (figure 3B–C). Thus, CheGsx is probably expressed in neural cells or precursors rather than in nematoblasts.

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