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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.

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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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Nuclear receptor gene structure. Nuclear receptors are composed of two well-conserved regions, the DNA binding domain (DBD) and the ligand binding domain (LBD).
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Figure 1: Nuclear receptor gene structure. Nuclear receptors are composed of two well-conserved regions, the DNA binding domain (DBD) and the ligand binding domain (LBD).

Mentions: Nuclear receptors (NRs) are one of the most abundant classes of transcription factors in metazoans and coordinate diverse processes ranging from developmental patterning to physiological regulation. NRs appear to be restricted to animals because extensive work has shown nuclear receptors are present in all metazoan phyla (e.g., sponges [1,2], cnidarians [3,4], and bilaterians [5]) but not in plants, fungi or choanoflagellates [6]. The signature motifs of NRs are the DNA-binding domain (DBD), which includes a Cys-Cys zinc coordinating region, and the ligand-binding domain (LBD), a carboxy-terminal domain that binds ligands and facilitates receptor dimerization and coactivator recruitment (Figure 1). High sequence conservation within these domains, particularly the DBD, has permitted identification of NRs from a number of animals and phylogenetic analysis of the NR superfamily [5].


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

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

Nuclear receptor gene structure. Nuclear receptors are composed of two well-conserved regions, the DNA binding domain (DBD) and the ligand binding domain (LBD).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2749838&req=5

Figure 1: Nuclear receptor gene structure. Nuclear receptors are composed of two well-conserved regions, the DNA binding domain (DBD) and the ligand binding domain (LBD).
Mentions: Nuclear receptors (NRs) are one of the most abundant classes of transcription factors in metazoans and coordinate diverse processes ranging from developmental patterning to physiological regulation. NRs appear to be restricted to animals because extensive work has shown nuclear receptors are present in all metazoan phyla (e.g., sponges [1,2], cnidarians [3,4], and bilaterians [5]) but not in plants, fungi or choanoflagellates [6]. The signature motifs of NRs are the DNA-binding domain (DBD), which includes a Cys-Cys zinc coordinating region, and the ligand-binding domain (LBD), a carboxy-terminal domain that binds ligands and facilitates receptor dimerization and coactivator recruitment (Figure 1). High sequence conservation within these domains, particularly the DBD, has permitted identification of NRs from a number of animals and phylogenetic analysis of the NR superfamily [5].

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