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Adoption of conserved developmental genes in development and origin of the medusa body plan.

Kraus JE, Fredman D, Wang W, Khalturin K, Technau U - Evodevo (2015)

Bottom Line: It is therefore unclear whether medusa formation has evolved independently in different medusozoans.Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa.We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, Wien, Vienna 1090 Austria.

ABSTRACT

Background: The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required.

Results: We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen.

Conclusions: Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

No MeSH data available.


Related in: MedlinePlus

Oral marker gene expression is mostly restricted to developing oral regions in polyps and medusae of Clytia hemisphaerica and Aurelia aurita. (a) Expression of Ch-bra1 in the mouth endoderm. (b–d) During medusa formation, it is expressed from the earliest budding stages onwards, initially in the entire entocodon, then restricted to the oral ectoderm. In late medusa buds and the medusa, Ch-bra1 is restricted to the mouth endoderm. (e) Ch-foxA expression in the entire head endoderm in polyps but absent from the tentacles. (f–h). During medusa formation, the onset of Ch-foxA expression coincides with the appearance of the mouth tube. In later medusa buds and in the free medusa, the entire mouth tube apart from the mouth tip region is foxA-positive. (i) Ch-otp expression in the polyp ectodermal mouth region and in single cells in the tentacles. In early medusa budding stages (k), Ch-otp is expressed in cell clusters in the developing oral ectoderm and in single cells in the outer bud ectoderm. In late medusa budding stages and medusa the oral expression of otp becomes more prominent and numerous otp-positive cells and cell clusters appear at the bell rim and at the aboral side of the tentacle bulbs and single cells at the bell rim. (n–q) Schematics illustrate oral marker gene expression in the representative stages of Clytia. (r) Aurelia ephyra show Aa-bra1 expression in the mouth tip. s Aaotp expression in single cells of the rhopalar arm ectoderm and the mouth tip. (t) AafoxA expression in the entire mouth tube of the ephyra but not in the lips (u) Schematic shows summary of mouth marker expression in the Aurelia ephyra
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Fig3: Oral marker gene expression is mostly restricted to developing oral regions in polyps and medusae of Clytia hemisphaerica and Aurelia aurita. (a) Expression of Ch-bra1 in the mouth endoderm. (b–d) During medusa formation, it is expressed from the earliest budding stages onwards, initially in the entire entocodon, then restricted to the oral ectoderm. In late medusa buds and the medusa, Ch-bra1 is restricted to the mouth endoderm. (e) Ch-foxA expression in the entire head endoderm in polyps but absent from the tentacles. (f–h). During medusa formation, the onset of Ch-foxA expression coincides with the appearance of the mouth tube. In later medusa buds and in the free medusa, the entire mouth tube apart from the mouth tip region is foxA-positive. (i) Ch-otp expression in the polyp ectodermal mouth region and in single cells in the tentacles. In early medusa budding stages (k), Ch-otp is expressed in cell clusters in the developing oral ectoderm and in single cells in the outer bud ectoderm. In late medusa budding stages and medusa the oral expression of otp becomes more prominent and numerous otp-positive cells and cell clusters appear at the bell rim and at the aboral side of the tentacle bulbs and single cells at the bell rim. (n–q) Schematics illustrate oral marker gene expression in the representative stages of Clytia. (r) Aurelia ephyra show Aa-bra1 expression in the mouth tip. s Aaotp expression in single cells of the rhopalar arm ectoderm and the mouth tip. (t) AafoxA expression in the entire mouth tube of the ephyra but not in the lips (u) Schematic shows summary of mouth marker expression in the Aurelia ephyra

Mentions: The current model of polyp-medusa body plan homology assumes that the polyp mouth region corresponds to the entire subumbrella of medusae [7, 22, 36]. If correct, this model implies that the expression of conserved polyp mouth marker genes should expand to future subumbrellar regions during medusa formation (Fig. 1d). We tested this hypothesis by comparing the expression of Clytia and Aurelia orthologs of the T-box gene brachyury (bra), the winged helix gene forkhead-box transcription factor A (foxA) and the homeobox gene orthopedia (otp) between developing polyps and medusae. These transcription factors were chosen for their conserved oral (or blastoporal) expression domains in the anthozoan Nematostella vectensis [37–39] and in bilaterians [40–42]. Accordingly, these genes were all expressed specifically in an oral domain of the Clytia polyp (Fig. 3a, e, i, n). In contrast to the prediction, however, we found that brachyury and foxA orthologs were never expanded to developing bell regions during the development of Clytia medusae or Aurelia ephyrae but were restricted to oral regions in both species (Fig. 3a–u). Both Ch-otp and Aa-otp were expressed not only in the oral ectoderm but also in single ectodermal cells in the tentacles of the Clytia polyp, in the developing bell rim and tentacles of Clytia medusae and in the rhopalar arms of the Aurelia ephyra. It is possible that these cells belong to the neuronal lineage, given that otp marks neurons in many bilaterians [43]. Together, these findings indicate that the polyp mouth region and the medusa bell do not share a common profile of hallmark transcription factor expression during their development and might thus not share a common evolutionary and developmental origin.Fig. 3


Adoption of conserved developmental genes in development and origin of the medusa body plan.

Kraus JE, Fredman D, Wang W, Khalturin K, Technau U - Evodevo (2015)

Oral marker gene expression is mostly restricted to developing oral regions in polyps and medusae of Clytia hemisphaerica and Aurelia aurita. (a) Expression of Ch-bra1 in the mouth endoderm. (b–d) During medusa formation, it is expressed from the earliest budding stages onwards, initially in the entire entocodon, then restricted to the oral ectoderm. In late medusa buds and the medusa, Ch-bra1 is restricted to the mouth endoderm. (e) Ch-foxA expression in the entire head endoderm in polyps but absent from the tentacles. (f–h). During medusa formation, the onset of Ch-foxA expression coincides with the appearance of the mouth tube. In later medusa buds and in the free medusa, the entire mouth tube apart from the mouth tip region is foxA-positive. (i) Ch-otp expression in the polyp ectodermal mouth region and in single cells in the tentacles. In early medusa budding stages (k), Ch-otp is expressed in cell clusters in the developing oral ectoderm and in single cells in the outer bud ectoderm. In late medusa budding stages and medusa the oral expression of otp becomes more prominent and numerous otp-positive cells and cell clusters appear at the bell rim and at the aboral side of the tentacle bulbs and single cells at the bell rim. (n–q) Schematics illustrate oral marker gene expression in the representative stages of Clytia. (r) Aurelia ephyra show Aa-bra1 expression in the mouth tip. s Aaotp expression in single cells of the rhopalar arm ectoderm and the mouth tip. (t) AafoxA expression in the entire mouth tube of the ephyra but not in the lips (u) Schematic shows summary of mouth marker expression in the Aurelia ephyra
© Copyright Policy - open-access
Related In: Results  -  Collection

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Fig3: Oral marker gene expression is mostly restricted to developing oral regions in polyps and medusae of Clytia hemisphaerica and Aurelia aurita. (a) Expression of Ch-bra1 in the mouth endoderm. (b–d) During medusa formation, it is expressed from the earliest budding stages onwards, initially in the entire entocodon, then restricted to the oral ectoderm. In late medusa buds and the medusa, Ch-bra1 is restricted to the mouth endoderm. (e) Ch-foxA expression in the entire head endoderm in polyps but absent from the tentacles. (f–h). During medusa formation, the onset of Ch-foxA expression coincides with the appearance of the mouth tube. In later medusa buds and in the free medusa, the entire mouth tube apart from the mouth tip region is foxA-positive. (i) Ch-otp expression in the polyp ectodermal mouth region and in single cells in the tentacles. In early medusa budding stages (k), Ch-otp is expressed in cell clusters in the developing oral ectoderm and in single cells in the outer bud ectoderm. In late medusa budding stages and medusa the oral expression of otp becomes more prominent and numerous otp-positive cells and cell clusters appear at the bell rim and at the aboral side of the tentacle bulbs and single cells at the bell rim. (n–q) Schematics illustrate oral marker gene expression in the representative stages of Clytia. (r) Aurelia ephyra show Aa-bra1 expression in the mouth tip. s Aaotp expression in single cells of the rhopalar arm ectoderm and the mouth tip. (t) AafoxA expression in the entire mouth tube of the ephyra but not in the lips (u) Schematic shows summary of mouth marker expression in the Aurelia ephyra
Mentions: The current model of polyp-medusa body plan homology assumes that the polyp mouth region corresponds to the entire subumbrella of medusae [7, 22, 36]. If correct, this model implies that the expression of conserved polyp mouth marker genes should expand to future subumbrellar regions during medusa formation (Fig. 1d). We tested this hypothesis by comparing the expression of Clytia and Aurelia orthologs of the T-box gene brachyury (bra), the winged helix gene forkhead-box transcription factor A (foxA) and the homeobox gene orthopedia (otp) between developing polyps and medusae. These transcription factors were chosen for their conserved oral (or blastoporal) expression domains in the anthozoan Nematostella vectensis [37–39] and in bilaterians [40–42]. Accordingly, these genes were all expressed specifically in an oral domain of the Clytia polyp (Fig. 3a, e, i, n). In contrast to the prediction, however, we found that brachyury and foxA orthologs were never expanded to developing bell regions during the development of Clytia medusae or Aurelia ephyrae but were restricted to oral regions in both species (Fig. 3a–u). Both Ch-otp and Aa-otp were expressed not only in the oral ectoderm but also in single ectodermal cells in the tentacles of the Clytia polyp, in the developing bell rim and tentacles of Clytia medusae and in the rhopalar arms of the Aurelia ephyra. It is possible that these cells belong to the neuronal lineage, given that otp marks neurons in many bilaterians [43]. Together, these findings indicate that the polyp mouth region and the medusa bell do not share a common profile of hallmark transcription factor expression during their development and might thus not share a common evolutionary and developmental origin.Fig. 3

Bottom Line: It is therefore unclear whether medusa formation has evolved independently in different medusozoans.Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa.We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, Wien, Vienna 1090 Austria.

ABSTRACT

Background: The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required.

Results: We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen.

Conclusions: Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

No MeSH data available.


Related in: MedlinePlus