Article

Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA. .
EvoDevo (Impact Factor: 3.1). 02/2011; 2(1):3. DOI: 10.1186/2041-9139-2-3
Source: PubMed

ABSTRACT Nuclear receptors (NRs) are an ancient superfamily of metazoan transcription factors that play critical roles in regulation of reproduction, development, and energetic homeostasis. Although the evolutionary relationships among NRs are well-described in two prominent clades of animals (deuterostomes and protostomes), comparatively little information has been reported on the diversity of NRs in early diverging metazoans. Here, we identified NRs from the phylum Ctenophora and used a phylogenomic approach to explore the emergence of the NR superfamily in the animal kingdom. In addition, to gain insight into conserved or novel functions, we examined NR expression during ctenophore development.
We report the first described NRs from the phylum Ctenophora: two from Mnemiopsis leidyi and one from Pleurobrachia pileus. All ctenophore NRs contained a ligand-binding domain and grouped with NRs from the subfamily NR2A (HNF4). Surprisingly, all the ctenophore NRs lacked the highly conserved DNA-binding domain (DBD). NRs from Mnemiopsis were expressed in different regions of developing ctenophores. One was broadly expressed in the endoderm during gastrulation. The second was initially expressed in the ectoderm during gastrulation, in regions corresponding to the future tentacles; subsequent expression was restricted to the apical organ. Phylogenetic analyses of NRs from ctenophores, sponges, cnidarians, and a placozoan support the hypothesis that expansion of the superfamily occurred in a step-wise fashion, with initial radiations in NR family 2, followed by representatives of NR families 3, 6, and 1/4 originating prior to the appearance of the bilaterian ancestor.
Our study provides the first description of NRs from ctenophores, including the full complement from Mnemiopsis. Ctenophores have the least diverse NR complement of any animal phylum with representatives that cluster with only one subfamily (NR2A). Ctenophores and sponges have a similarly restricted NR complement supporting the hypothesis that the original NR was HNF4-like and that these lineages are the first two branches from the animal tree. The absence of a zinc-finger DNA-binding domain in the two ctenophore species suggests two hypotheses: this domain may have been secondarily lost within the ctenophore lineage or, if ctenophores are the first branch off the animal tree, the original NR may have lacked the canonical DBD. Phylogenomic analyses and categorization of NRs from all four early diverging animal phyla compared with the complement from bilaterians suggest the rate of NR diversification prior to the cnidarian-bilaterian split was relatively modest, with independent radiations of several NR subfamilies within the cnidarian lineage.

Download full-text

Full-text

Available from: Adam M Reitzel, Sep 01, 2015
0 Followers
 · 
93 Views
 · 
76 Downloads
  • Source
    • "Animals (i.e., Metazoa) Collagen, oogenesis, spermatogenesis (polar bodies), special sperm structure, mitochondrial genome reduction All animals except Ctenophora Paired domains linked to homeodomains (Ryan et al. 2010), NR2A genes include DNA binding domain (Reitzel et al. 2011), Drosha microRNA processing (Maxwell et al. 2012) Parahoxozoa Hox and ParaHox genes (Ryan et al. 2010) Planulozoa (sensu Wallberg et al. 2004) "
    [Show abstract] [Hide abstract]
    ABSTRACT: In recent years, scientists have made remarkable progress reconstructing the animal phylogeny. There is broad agreement regarding many deep animal relationships, including the monophyly of animals, Bilateria, Protostomia, Ecdysozoa, and Spiralia. This stability now allows researchers to articulate the diminishing number of remaining questions in terms of well-defined alternative hypotheses. These remaining questions include relationships at the base of the animal tree, the position of Xenacoelomorpha, and the internal relationships of Spiralia. Recent progress in the field of animal phylogeny has important implications for our understanding of the evolution of development, morphology, genomes, and other characters. A remarkable pattern emerges—there is far more homoplasy for all these characters than had previously been anticipated, even among many complex characters such as segmentation and nervous systems. The fossil record dates most deep branches of the animal tree to an evolutionary radiation in the early Cambrian with roots in the Late Neoproterozoic.
    Annual Review of Ecology Evolution and Systematics 11/2014; 45:371-395. DOI:10.1146/annurev-ecolsys-120213-091627 · 10.98 Impact Factor
  • Source
    • "Here, we describe an in-depth characterization of both the miRNA biogenesis pathway proteins and genomic regions that may correspond to pri-miRNA loci in the recently sequenced genome of Mnemiopsis leidyi (http://research.nhgri.nih.gov/mnemiopsis/). Recent phylogenomic analyses suggest that Ctenophora may be the earliest branching metazoan lineage [31,32], and genomic studies of a number of gene superclasses [33,34] and signaling pathways [35] in Mnemiopsis are consistent with this theory. If ctenophores are, indeed, the earliest metazoan branch, examining the genome of Mnemiopsis provides us a rare opportunity to better understand the origin of miRNA processing in metazoans. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background MicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined thus far, except for the placozoan Trichoplax. The genomic repertoires of metazoan microRNAs have become increasingly endorsed as phylogenetic characters and drivers of biological complexity. Results In this study, we report the first investigation of microRNAs in a species from the phylum Ctenophora. We use short RNA sequencing and the assembled genome of the lobate ctenophore Mnemiopsis leidyi to show that this species appears to lack any recognizable microRNAs, as well as the nuclear proteins Drosha and Pasha, which are critical to canonical microRNA biogenesis. This finding represents the first reported case of a metazoan lacking a Drosha protein. Conclusions Recent phylogenomic analyses suggest that Mnemiopsis may be the earliest branching metazoan lineage. If this is true, then the origins of canonical microRNA biogenesis and microRNA-mediated gene regulation may postdate the last common metazoan ancestor. Alternatively, canonical microRNA functionality may have been lost independently in the lineages leading to both Mnemiopsis and the placozoan Trichoplax, suggesting that microRNA functionality was not critical until much later in metazoan evolution.
    BMC Genomics 12/2012; 13(1):714. DOI:10.1186/1471-2164-13-714 · 4.04 Impact Factor
  • Source
    • "Recent gene content studies [45-47] give support for Porifera and Ctenophora diverging prior to the ParaHoxozoa (Placozoa, Cnidaria, Bilaterian) during early animal evolution. This is further supported by the present study, in which we have further classified the genomic complement of M. leidyi Lhx genes. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Nervous systems are thought to be important to the evolutionary success and diversification of metazoans, yet little is known about the origin of simple nervous systems at the base of the animal tree. Recent data suggest that ctenophores, a group of macroscopic pelagic marine invertebrates, are the most ancient group of animals that possess a definitive nervous system consisting of a distributed nerve net and an apical statocyst. This study reports on details of the evolution of the neural cell type specifying transcription factor family of LIM homeobox containing genes (Lhx), which have highly conserved functions in neural specification in bilaterian animals. Using next generation sequencing, the first draft of the genome of the ctenophore Mnemiopsis leidyi has been generated. The Lhx genes in all animals are represented by seven subfamilies (Lhx1/5, Lhx3/4, Lmx, Islet, Lhx2/9, Lhx6/8, and LMO) of which four were found to be represented in the ctenophore lineage (Lhx1/5, Lhx3/4, Lmx, and Islet). Interestingly, the ctenophore Lhx gene complement is more similar to the sponge complement (sponges do not possess neurons) than to either the cnidarian-bilaterian or placozoan Lhx complements. Using whole mount in situ hybridization, the Lhx gene expression patterns were examined and found to be expressed around the blastopore and in cells that give rise to the apical organ and putative neural sensory cells. This research gives us a first look at neural cell type specification in the ctenophore M. leidyi. Within M. leidyi, Lhx genes are expressed in overlapping domains within proposed neural cellular and sensory cell territories. These data suggest that Lhx genes likely played a conserved role in the patterning of sensory cells in the ancestor of sponges and ctenophores, and may provide a link to the expression of Lhx orthologs in sponge larval photoreceptive cells. Lhx genes were later co-opted into patterning more diversified complements of neural and non-neural cell types in later evolving animals.
    EvoDevo 01/2012; 3(1):2. DOI:10.1186/2041-9139-3-2 · 3.10 Impact Factor
Show more