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Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi.

Pang K, Ryan JF, NISC Comparative Sequencing ProgramMullikin JC, Baxevanis AD, Martindale MQ - Evodevo (2010)

Bottom Line: In situ hybridization of the four Wnt ligands showed that they are expressed in discrete regions associated with the aboral pole, tentacle apparati and apical organ.Furthermore, it is difficult to compare the Mnemiopsis Wnt expression patterns with those of other metazoans. mRNA expression of Wnt pathway components appears later in development than expected, and zygotic gene expression does not appear to play a role in early axis specification.Notably absent in the Mnemiopsis genome are most major secreted antagonists, which suggests that complex regulation of this secreted signaling pathway probably evolved later in animal evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI, USA. mqmartin@hawaii.edu.

ABSTRACT

Background: Intercellular signaling pathways are a fundamental component of the integrating cellular behavior required for the evolution of multicellularity. The genomes of three of the four early branching animal phyla (Cnidaria, Placozoa and Porifera) have been surveyed for key components, but not the fourth (Ctenophora). Genomic data from ctenophores could be particularly relevant, as ctenophores have been proposed to be one of the earliest branching metazoan phyla.

Results: A preliminary assembly of the lobate ctenophore Mnemiopsis leidyi genome generated using next-generation sequencing technologies were searched for components of a developmentally important signaling pathway, the Wnt/β-catenin pathway. Molecular phylogenetic analysis shows four distinct Wnt ligands (MlWnt6, MlWnt9, MlWntA and MlWntX), and most, but not all components of the receptor and intracellular signaling pathway were detected. In situ hybridization of the four Wnt ligands showed that they are expressed in discrete regions associated with the aboral pole, tentacle apparati and apical organ.

Conclusions: Ctenophores show a minimal (but not obviously simple) complement of Wnt signaling components. Furthermore, it is difficult to compare the Mnemiopsis Wnt expression patterns with those of other metazoans. mRNA expression of Wnt pathway components appears later in development than expected, and zygotic gene expression does not appear to play a role in early axis specification. Notably absent in the Mnemiopsis genome are most major secreted antagonists, which suggests that complex regulation of this secreted signaling pathway probably evolved later in animal evolution.

No MeSH data available.


Ctenophore development and body plan. (A) Early cleavage from egg to 60-cell stage, based on Martindale and Henry [20] and others. The top row shows the view from the aboral (or vegetal) pole and the bottom row shows the lateral view, with the oral pole at the bottom. The first two divisions are equal and meridional, and the third cleavage is unequal and oblique, giving rise to middle (M) and end (E) macromeres. Subsequent divisions are unequal, with micromeres given off at the aboral pole. (B) Basic ctenophore body plan, as shown during the cydippid stage. The oral pole is the location of the mouth, which opens to the pharynx. The pharynx leads internally to the gut and endodermal canals (yellow). Also shown are paired tentacle bulbs (from which the tentacles grow), the eight comb rows, and the apical sensory organ located at the aboral pole.
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Figure 2: Ctenophore development and body plan. (A) Early cleavage from egg to 60-cell stage, based on Martindale and Henry [20] and others. The top row shows the view from the aboral (or vegetal) pole and the bottom row shows the lateral view, with the oral pole at the bottom. The first two divisions are equal and meridional, and the third cleavage is unequal and oblique, giving rise to middle (M) and end (E) macromeres. Subsequent divisions are unequal, with micromeres given off at the aboral pole. (B) Basic ctenophore body plan, as shown during the cydippid stage. The oral pole is the location of the mouth, which opens to the pharynx. The pharynx leads internally to the gut and endodermal canals (yellow). Also shown are paired tentacle bulbs (from which the tentacles grow), the eight comb rows, and the apical sensory organ located at the aboral pole.

Mentions: Unlike the other non-bilaterians, ctenophores display a stereotypical developmental program (Figure 2A), with a well-studied cell lineage [19,20]. The first two cleavages are equal and meridional, whereas the third cleavage is unequal and oblique. At this stage, the eight macromeres divide unequally to give off micromeres at the future aboral pole. Many of the early blastomeres in ctenophore embryos display a precocious determination of cell fate that is consistent with segregation of cytoplasmic determinants, although some inductive interactions are known to occur [21]. Unfortunately, no good molecular candidates for cell fate specification determinants have been identified in ctenophores. The primary adult body axis, the oral--aboral axis, is established at the time of the first cleavage [22] and early cleavages are important for localizing developmental potential [23]. The oral-aboral axis of larval (or cydippid) and adult ctenophores is demarcated by the mouth at the oral pole and the apical sensory organ at the aboral pole (Figure 2B). Additionally, there are two planes of rotational symmetry: the tentacular plane, which passes through the two tentacles, and the oesophageal or sagittal plane, which is perpendicular to the tentacular plane. Ctenophores also possess complex features, such as a well-developed muscular system composed of non-epithelial muscle cells and a nervous system that comprises sensory cells and a subepidermal nerve net [reviewed in [24]].


Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi.

Pang K, Ryan JF, NISC Comparative Sequencing ProgramMullikin JC, Baxevanis AD, Martindale MQ - Evodevo (2010)

Ctenophore development and body plan. (A) Early cleavage from egg to 60-cell stage, based on Martindale and Henry [20] and others. The top row shows the view from the aboral (or vegetal) pole and the bottom row shows the lateral view, with the oral pole at the bottom. The first two divisions are equal and meridional, and the third cleavage is unequal and oblique, giving rise to middle (M) and end (E) macromeres. Subsequent divisions are unequal, with micromeres given off at the aboral pole. (B) Basic ctenophore body plan, as shown during the cydippid stage. The oral pole is the location of the mouth, which opens to the pharynx. The pharynx leads internally to the gut and endodermal canals (yellow). Also shown are paired tentacle bulbs (from which the tentacles grow), the eight comb rows, and the apical sensory organ located at the aboral pole.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2959043&req=5

Figure 2: Ctenophore development and body plan. (A) Early cleavage from egg to 60-cell stage, based on Martindale and Henry [20] and others. The top row shows the view from the aboral (or vegetal) pole and the bottom row shows the lateral view, with the oral pole at the bottom. The first two divisions are equal and meridional, and the third cleavage is unequal and oblique, giving rise to middle (M) and end (E) macromeres. Subsequent divisions are unequal, with micromeres given off at the aboral pole. (B) Basic ctenophore body plan, as shown during the cydippid stage. The oral pole is the location of the mouth, which opens to the pharynx. The pharynx leads internally to the gut and endodermal canals (yellow). Also shown are paired tentacle bulbs (from which the tentacles grow), the eight comb rows, and the apical sensory organ located at the aboral pole.
Mentions: Unlike the other non-bilaterians, ctenophores display a stereotypical developmental program (Figure 2A), with a well-studied cell lineage [19,20]. The first two cleavages are equal and meridional, whereas the third cleavage is unequal and oblique. At this stage, the eight macromeres divide unequally to give off micromeres at the future aboral pole. Many of the early blastomeres in ctenophore embryos display a precocious determination of cell fate that is consistent with segregation of cytoplasmic determinants, although some inductive interactions are known to occur [21]. Unfortunately, no good molecular candidates for cell fate specification determinants have been identified in ctenophores. The primary adult body axis, the oral--aboral axis, is established at the time of the first cleavage [22] and early cleavages are important for localizing developmental potential [23]. The oral-aboral axis of larval (or cydippid) and adult ctenophores is demarcated by the mouth at the oral pole and the apical sensory organ at the aboral pole (Figure 2B). Additionally, there are two planes of rotational symmetry: the tentacular plane, which passes through the two tentacles, and the oesophageal or sagittal plane, which is perpendicular to the tentacular plane. Ctenophores also possess complex features, such as a well-developed muscular system composed of non-epithelial muscle cells and a nervous system that comprises sensory cells and a subepidermal nerve net [reviewed in [24]].

Bottom Line: In situ hybridization of the four Wnt ligands showed that they are expressed in discrete regions associated with the aboral pole, tentacle apparati and apical organ.Furthermore, it is difficult to compare the Mnemiopsis Wnt expression patterns with those of other metazoans. mRNA expression of Wnt pathway components appears later in development than expected, and zygotic gene expression does not appear to play a role in early axis specification.Notably absent in the Mnemiopsis genome are most major secreted antagonists, which suggests that complex regulation of this secreted signaling pathway probably evolved later in animal evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI, USA. mqmartin@hawaii.edu.

ABSTRACT

Background: Intercellular signaling pathways are a fundamental component of the integrating cellular behavior required for the evolution of multicellularity. The genomes of three of the four early branching animal phyla (Cnidaria, Placozoa and Porifera) have been surveyed for key components, but not the fourth (Ctenophora). Genomic data from ctenophores could be particularly relevant, as ctenophores have been proposed to be one of the earliest branching metazoan phyla.

Results: A preliminary assembly of the lobate ctenophore Mnemiopsis leidyi genome generated using next-generation sequencing technologies were searched for components of a developmentally important signaling pathway, the Wnt/β-catenin pathway. Molecular phylogenetic analysis shows four distinct Wnt ligands (MlWnt6, MlWnt9, MlWntA and MlWntX), and most, but not all components of the receptor and intracellular signaling pathway were detected. In situ hybridization of the four Wnt ligands showed that they are expressed in discrete regions associated with the aboral pole, tentacle apparati and apical organ.

Conclusions: Ctenophores show a minimal (but not obviously simple) complement of Wnt signaling components. Furthermore, it is difficult to compare the Mnemiopsis Wnt expression patterns with those of other metazoans. mRNA expression of Wnt pathway components appears later in development than expected, and zygotic gene expression does not appear to play a role in early axis specification. Notably absent in the Mnemiopsis genome are most major secreted antagonists, which suggests that complex regulation of this secreted signaling pathway probably evolved later in animal evolution.

No MeSH data available.