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Nuclear receptor complement of the cnidarian Nematostella vectensis: phylogenetic relationships and developmental expression patterns.

Reitzel AM, Tarrant AM - BMC Evol. Biol. (2009)

Bottom Line: N. vectensis contains a diverse complement of nuclear receptors including orthologs of several bilaterian nuclear receptors.Nuclear receptors exhibited distinct developmental expression patterns, which are consistent with diverse regulatory roles for these genes.Understanding the evolutionary relationships and developmental expression of the N. vectensis nuclear receptor complement provides insight into the evolution of the nuclear receptor superfamily and a foundation for mechanistic characterization of cnidarian nuclear receptor function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA. areitzel@whoi.edu

ABSTRACT

Background: Nuclear receptors are a superfamily of metazoan transcription factors that regulate diverse developmental and physiological processes. Sequenced genomes from an increasing number of bilaterians have provided a more complete picture of duplication and loss of nuclear receptors in protostomes and deuterostomes but have left open the question of which nuclear receptors were present in the cnidarian-bilaterian ancestor. In addition, nuclear receptor expression and function are largely uncharacterized within cnidarians, preventing determination of conserved and novel nuclear receptor functions in the context of animal evolution.

Results: Here we report the first complete set of nuclear receptors from a cnidarian, the starlet sea anemone Nematostella vectensis. Genomic searches using conserved DNA- and ligand-binding domains revealed seventeen nuclear receptors in N. vectensis. Phylogenetic analyses support N. vectensis orthologs of bilaterian nuclear receptors in four nuclear receptor subfamilies within nuclear receptor family 2 (COUP-TF, TLL, HNF4, TR2/4) and one putative ortholog of GCNF (nuclear receptor family 6). Other N. vectensis genes grouped well with nuclear receptor family 2 but represented lineage-specific duplications somewhere within the cnidarian lineage and were not clear orthologs of bilaterian genes. Three nuclear receptors were not well-supported within any particular nuclear receptor family. The seventeen nuclear receptors exhibited distinct developmental expression patterns, with expression of several nuclear receptors limited to a subset of developmental stages.

Conclusion: N. vectensis contains a diverse complement of nuclear receptors including orthologs of several bilaterian nuclear receptors. Novel nuclear receptors in N. vectensis may be ancient genes lost from triploblastic lineages or may represent cnidarian-specific radiations. Nuclear receptors exhibited distinct developmental expression patterns, which are consistent with diverse regulatory roles for these genes. Understanding the evolutionary relationships and developmental expression of the N. vectensis nuclear receptor complement provides insight into the evolution of the nuclear receptor superfamily and a foundation for mechanistic characterization of cnidarian nuclear receptor function.

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Phylogenetic relationships of N. vectensis NRs (NvNRs) depicted by a maximum-likelihood tree with percent bootstrap support of 1000 bootstraps for nodes of evolutionary significance. The alignment was constructed using the DBD and a portion of the LBD (additional details in text). Monophyletic relationships for bilaterian sequences in particular families or subfamilies were recovered in all cases but one (NR2E) and are depicted as horizontal triangle. A full tree with all taxa depicted as individual branches is presented in Additional File 2. The tree was rooted with NR family 2 because this family is monophyletic, represents a defined nuclear receptor family, and includes what is likely the original nuclear receptor, represented by an HNF4-like homolog from the sponge Amphimedon queenslandica [1]. Most N. vectensis NRs group within NR family 2 and many (e.g., NvNR11- NvNR14) are supported as independent radiations of subfamilies within this family. N. vectensis also has a NR related to GCNF (NR family 6), but with low support. Three NRs did not group with any previously described family (NvNR1-3). These genes may represent ancestral genes that later diversified into one or more of the NR 1, 3, and 4 families.
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Figure 2: Phylogenetic relationships of N. vectensis NRs (NvNRs) depicted by a maximum-likelihood tree with percent bootstrap support of 1000 bootstraps for nodes of evolutionary significance. The alignment was constructed using the DBD and a portion of the LBD (additional details in text). Monophyletic relationships for bilaterian sequences in particular families or subfamilies were recovered in all cases but one (NR2E) and are depicted as horizontal triangle. A full tree with all taxa depicted as individual branches is presented in Additional File 2. The tree was rooted with NR family 2 because this family is monophyletic, represents a defined nuclear receptor family, and includes what is likely the original nuclear receptor, represented by an HNF4-like homolog from the sponge Amphimedon queenslandica [1]. Most N. vectensis NRs group within NR family 2 and many (e.g., NvNR11- NvNR14) are supported as independent radiations of subfamilies within this family. N. vectensis also has a NR related to GCNF (NR family 6), but with low support. Three NRs did not group with any previously described family (NvNR1-3). These genes may represent ancestral genes that later diversified into one or more of the NR 1, 3, and 4 families.

Mentions: When DBD plus LBD were used for phylogenetic analyses of N. vectensis and bilaterian NRs, the topology of the tree with the highest likelihood was consistent with monophyletic relationships of the recognized NR families. Nodes for NR families 1-4 were each supported by high bootstrap scores (Figure 2, for a more detailed tree with nodes expanded see Additional file 2). Although NR families 5 and 6 were each weakly supported (BS = 40 and 37, respectively), a clade grouping these two families was fairly well supported (BS = 79) as previously shown by Thornton [21]. Phylogenetic analyses using just the DBD or portion of the LBD resulted in more poorly supported nodes throughout the tree and in some cases failed to recover monophyletic NR families (see Additional files 3 and 4). In addition, a complementary analysis using neighbor joining with the DBD and LBD also resulted in weakly supported nodes for the NR families (see Additional file 5). Therefore, we inferred the phylogenetic relationships of the N. vectensis NRs from the likelihood analysis based on the DBD plus LBD.


Nuclear receptor complement of the cnidarian Nematostella vectensis: phylogenetic relationships and developmental expression patterns.

Reitzel AM, Tarrant AM - BMC Evol. Biol. (2009)

Phylogenetic relationships of N. vectensis NRs (NvNRs) depicted by a maximum-likelihood tree with percent bootstrap support of 1000 bootstraps for nodes of evolutionary significance. The alignment was constructed using the DBD and a portion of the LBD (additional details in text). Monophyletic relationships for bilaterian sequences in particular families or subfamilies were recovered in all cases but one (NR2E) and are depicted as horizontal triangle. A full tree with all taxa depicted as individual branches is presented in Additional File 2. The tree was rooted with NR family 2 because this family is monophyletic, represents a defined nuclear receptor family, and includes what is likely the original nuclear receptor, represented by an HNF4-like homolog from the sponge Amphimedon queenslandica [1]. Most N. vectensis NRs group within NR family 2 and many (e.g., NvNR11- NvNR14) are supported as independent radiations of subfamilies within this family. N. vectensis also has a NR related to GCNF (NR family 6), but with low support. Three NRs did not group with any previously described family (NvNR1-3). These genes may represent ancestral genes that later diversified into one or more of the NR 1, 3, and 4 families.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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Figure 2: Phylogenetic relationships of N. vectensis NRs (NvNRs) depicted by a maximum-likelihood tree with percent bootstrap support of 1000 bootstraps for nodes of evolutionary significance. The alignment was constructed using the DBD and a portion of the LBD (additional details in text). Monophyletic relationships for bilaterian sequences in particular families or subfamilies were recovered in all cases but one (NR2E) and are depicted as horizontal triangle. A full tree with all taxa depicted as individual branches is presented in Additional File 2. The tree was rooted with NR family 2 because this family is monophyletic, represents a defined nuclear receptor family, and includes what is likely the original nuclear receptor, represented by an HNF4-like homolog from the sponge Amphimedon queenslandica [1]. Most N. vectensis NRs group within NR family 2 and many (e.g., NvNR11- NvNR14) are supported as independent radiations of subfamilies within this family. N. vectensis also has a NR related to GCNF (NR family 6), but with low support. Three NRs did not group with any previously described family (NvNR1-3). These genes may represent ancestral genes that later diversified into one or more of the NR 1, 3, and 4 families.
Mentions: When DBD plus LBD were used for phylogenetic analyses of N. vectensis and bilaterian NRs, the topology of the tree with the highest likelihood was consistent with monophyletic relationships of the recognized NR families. Nodes for NR families 1-4 were each supported by high bootstrap scores (Figure 2, for a more detailed tree with nodes expanded see Additional file 2). Although NR families 5 and 6 were each weakly supported (BS = 40 and 37, respectively), a clade grouping these two families was fairly well supported (BS = 79) as previously shown by Thornton [21]. Phylogenetic analyses using just the DBD or portion of the LBD resulted in more poorly supported nodes throughout the tree and in some cases failed to recover monophyletic NR families (see Additional files 3 and 4). In addition, a complementary analysis using neighbor joining with the DBD and LBD also resulted in weakly supported nodes for the NR families (see Additional file 5). Therefore, we inferred the phylogenetic relationships of the N. vectensis NRs from the likelihood analysis based on the DBD plus LBD.

Bottom Line: N. vectensis contains a diverse complement of nuclear receptors including orthologs of several bilaterian nuclear receptors.Nuclear receptors exhibited distinct developmental expression patterns, which are consistent with diverse regulatory roles for these genes.Understanding the evolutionary relationships and developmental expression of the N. vectensis nuclear receptor complement provides insight into the evolution of the nuclear receptor superfamily and a foundation for mechanistic characterization of cnidarian nuclear receptor function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA. areitzel@whoi.edu

ABSTRACT

Background: Nuclear receptors are a superfamily of metazoan transcription factors that regulate diverse developmental and physiological processes. Sequenced genomes from an increasing number of bilaterians have provided a more complete picture of duplication and loss of nuclear receptors in protostomes and deuterostomes but have left open the question of which nuclear receptors were present in the cnidarian-bilaterian ancestor. In addition, nuclear receptor expression and function are largely uncharacterized within cnidarians, preventing determination of conserved and novel nuclear receptor functions in the context of animal evolution.

Results: Here we report the first complete set of nuclear receptors from a cnidarian, the starlet sea anemone Nematostella vectensis. Genomic searches using conserved DNA- and ligand-binding domains revealed seventeen nuclear receptors in N. vectensis. Phylogenetic analyses support N. vectensis orthologs of bilaterian nuclear receptors in four nuclear receptor subfamilies within nuclear receptor family 2 (COUP-TF, TLL, HNF4, TR2/4) and one putative ortholog of GCNF (nuclear receptor family 6). Other N. vectensis genes grouped well with nuclear receptor family 2 but represented lineage-specific duplications somewhere within the cnidarian lineage and were not clear orthologs of bilaterian genes. Three nuclear receptors were not well-supported within any particular nuclear receptor family. The seventeen nuclear receptors exhibited distinct developmental expression patterns, with expression of several nuclear receptors limited to a subset of developmental stages.

Conclusion: N. vectensis contains a diverse complement of nuclear receptors including orthologs of several bilaterian nuclear receptors. Novel nuclear receptors in N. vectensis may be ancient genes lost from triploblastic lineages or may represent cnidarian-specific radiations. Nuclear receptors exhibited distinct developmental expression patterns, which are consistent with diverse regulatory roles for these genes. Understanding the evolutionary relationships and developmental expression of the N. vectensis nuclear receptor complement provides insight into the evolution of the nuclear receptor superfamily and a foundation for mechanistic characterization of cnidarian nuclear receptor function.

Show MeSH