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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.


Wnt gene structure and domains of Wnt pathway members. (A) Intron-exon structure of the four Mnemiopsis Wnt transcripts that were cloned. Turquoise shading indicates the coding region and the diagonal lines show the 5' and 3' untranslated regions. The start (ATG) is indicated, and the vertical lines represent intron positions. The conserved intron positions are marked with arrows. (B) Predicted protein domains present in the other Wnt components that were cloned out. Specific domains and other regions of interest are colored and named.
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Figure 5: Wnt gene structure and domains of Wnt pathway members. (A) Intron-exon structure of the four Mnemiopsis Wnt transcripts that were cloned. Turquoise shading indicates the coding region and the diagonal lines show the 5' and 3' untranslated regions. The start (ATG) is indicated, and the vertical lines represent intron positions. The conserved intron positions are marked with arrows. (B) Predicted protein domains present in the other Wnt components that were cloned out. Specific domains and other regions of interest are colored and named.

Mentions: Each Mnemiopsis Wnt gene has a predicted signal peptide at the 5' end. MlWntA, MlWnt9 and MlWntX have the 24 conserved cysteine residues, whereas MlWnt6 has only 22. Comparison of the coding regions with that of genomic data reveals two important intron positions (Figure 5A) that are well conserved across all metazoan Wnt genes analyzed to date [43]. These correspond to introns 3 and 5 in MlWntA, MlWnt6 and MlWnt9, and to introns 2 and 4 in MlWntX. In the current assembly, none of the Wnt genes are on the same scaffold, so there is no evidence of genomic linkage. MlWntA is currently on a 182 kb scaffold, spanning positions 64,343 to 70,583, with predicted genes 4 kb upstream (highest BLAST hit was XP_001624925.1) and 10 kb downstream (XP_002018102). MlWnt9 is on a 283 kb scaffold, spanning 131,863 to 139,362, with adjacent genes located 4 kb upstream (XP_001620894.1) and 12 kb downstream (XP_002755989.1). MlWntX is on a 285 kb scaffold, region 26,134 to 12,946, with no genes detected downstream and the closest hit 12 kb upstream (ZP_03967055). MlWnt6 is currently on a 48 kb contig with no other genes predicted, spanning the region 35,863 to 8,886. Extrapolating, the closest possible distance between any two genes is 20 kb.


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)

Wnt gene structure and domains of Wnt pathway members. (A) Intron-exon structure of the four Mnemiopsis Wnt transcripts that were cloned. Turquoise shading indicates the coding region and the diagonal lines show the 5' and 3' untranslated regions. The start (ATG) is indicated, and the vertical lines represent intron positions. The conserved intron positions are marked with arrows. (B) Predicted protein domains present in the other Wnt components that were cloned out. Specific domains and other regions of interest are colored and named.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Wnt gene structure and domains of Wnt pathway members. (A) Intron-exon structure of the four Mnemiopsis Wnt transcripts that were cloned. Turquoise shading indicates the coding region and the diagonal lines show the 5' and 3' untranslated regions. The start (ATG) is indicated, and the vertical lines represent intron positions. The conserved intron positions are marked with arrows. (B) Predicted protein domains present in the other Wnt components that were cloned out. Specific domains and other regions of interest are colored and named.
Mentions: Each Mnemiopsis Wnt gene has a predicted signal peptide at the 5' end. MlWntA, MlWnt9 and MlWntX have the 24 conserved cysteine residues, whereas MlWnt6 has only 22. Comparison of the coding regions with that of genomic data reveals two important intron positions (Figure 5A) that are well conserved across all metazoan Wnt genes analyzed to date [43]. These correspond to introns 3 and 5 in MlWntA, MlWnt6 and MlWnt9, and to introns 2 and 4 in MlWntX. In the current assembly, none of the Wnt genes are on the same scaffold, so there is no evidence of genomic linkage. MlWntA is currently on a 182 kb scaffold, spanning positions 64,343 to 70,583, with predicted genes 4 kb upstream (highest BLAST hit was XP_001624925.1) and 10 kb downstream (XP_002018102). MlWnt9 is on a 283 kb scaffold, spanning 131,863 to 139,362, with adjacent genes located 4 kb upstream (XP_001620894.1) and 12 kb downstream (XP_002755989.1). MlWntX is on a 285 kb scaffold, region 26,134 to 12,946, with no genes detected downstream and the closest hit 12 kb upstream (ZP_03967055). MlWnt6 is currently on a 48 kb contig with no other genes predicted, spanning the region 35,863 to 8,886. Extrapolating, the closest possible distance between any two genes is 20 kb.

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.