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“Sex Determination”-Related Genes in the Ctenophore Mnemiopsis Leidyi

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“Sex Determination”-Related Genes in the Ctenophore Mnemiopsis Leidyi Reitzel et al. EvoDevo (2016) 7:17 DOI 10.1186/s13227-016-0051-9 EvoDevo RESEARCH Open Access Developmental expression of “germline”‑ and “sex determination”‑related genes in the ctenophore Mnemiopsis leidyi Adam M. Reitzel1* , Kevin Pang2 and Mark Q. Martindale3 Abstract Background: An essential developmental pathway in sexually reproducing animals is the specification of germ cells and the differentiation of mature gametes, sperm and oocytes. The “germline” genes vasa, nanos and piwi are commonly identified in primordial germ cells, suggesting a molecular signature for the germline throughout ani- mals. However, these genes are also expressed in a diverse set of somatic stem cells throughout the animal kingdom leaving open significant questions for whether they are required for germline specification. Similarly, members of the Dmrt gene family are essential components regulating sex determination and differentiation in bilaterian animals, but the functions of these transcription factors, including potential roles in sex determination, in early diverging animals remain unknown. The phylogenetic position of ctenophores and the genome sequence of the lobate Mnemiopsis leidyi motivated us to determine the compliment of these gene families in this species and determine expression pat- terns during development. Results: Our phylogenetic analyses of the vasa, piwi and nanos gene families show that Mnemiopsis has multiple genes in each family with multiple lineage-specific paralogs. Expression domains of Mnemiopsis nanos, vasa and piwi, during embryogenesis from fertilization to the cydippid stage, were diverse, with little overlapping expression and no or little expression in what we think are the germ cells or gametogenic regions. piwi paralogs in Mnemiopsis had distinct expression domains in the ectoderm during development. We observed overlapping expression domains in the apical organ and tentacle apparatus of the cydippid for a subset of “germline genes,” which are areas of high cell proliferation, suggesting that these genes are involved with “stem cell” specification and maintenance. Similarly, the five Dmrt genes show diverse non-overlapping expression domains, with no clear evidence for expression in future gametogenic regions of the adult. We also report on splice variants for two Mnemiopsis Dmrt genes that impact the presence and composition of the DM DNA binding domain for these transcription factors. Conclusion: Our results are consistent with a potential role for vasa, piwi and nanos genes in the specification or maintenance of somatic stem cell populations during development in Mnemiopsis. These results are similar to previ- ous results in the tentaculate ctenophore Pleurobrachia, with the exception that these genes were also expressed in gonads and developing gametes of adult Pleurobrachia. These differences suggest that the Mnemiopsis germline is either specified later in development than hypothesized, the germline undergoes extensive migration, or the ger- mline does not express these classic molecular markers. Our results highlight the utility of comparing expression of orthologous genes across multiple species. We provide the first description of Dmrt expression in a ctenophore, which indicates that Dmrt genes are expressed in distinct structures and regions during development but not in future gametogenic regions, the only sex-specific structure for this hermaphroditic species. Keywords: Cell proliferation, Dmrt, Germline, Mnemiopsis leidyi, Stem cell *Correspondence: [email protected] 1 Department of Biological Sciences, University of North Carolina at Charlotte, 9201 University City Blvd., Charlotte, NC, USA Full list of author information is available at the end of the article © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Reitzel et al. EvoDevo (2016) 7:17 Page 2 of 16 Background determination in traditional invertebrate models such as Sexual reproduction is critical for nearly all animals as it Drosophila melanogaster and C. elegans as well as many is the means by which individuals pass on their genetic vertebrates. Epigenesis is the alternate mode of germline material to future generations. Thus, the specification specification where there is no maternally deposited and development of gametes in males and females is a germ plasm and germ cells are determined later in devel- central process in animal life cycles. Due to the common- opment via inductive interactions between cells. Here, ality of sexual reproduction, we may expect that deeply a population of cells with the potential to become germ conserved molecular mechanisms may be responsible cells are induced by a signal to differentiate into PGCs. for these developmental events in all animals. However, Epigenesis is particularly common and well studied in despite the presence of sperm and oocytes in all sexu- mammals [5]. Across the metazoa, preformation is more ally reproducing animals, the relative conservation of widely understood due to its commonality in traditional the mechanisms responsible for their specification and model organisms; however, epigenesis is likely more differentiation remains debated. The uncertainty about common and widespread across the animal kingdom and the extent of homologous mechanisms for developmen- likely the ancestral condition of the stem animal [3]. Spe- tal processes related to sexual reproduction results, in cies in early diverging phyla in most all cases have germ part, from the diversity of described processes in vari- cell development consistent with epigenetic mechanisms ous lineages but also from the relative paucity of spe- [but see 6 that suggest preformation may date to cnidar- cies that have been studied. Research with species from ian–bilaterian ancestor], but the mechanisms remain early diverging animal phyla, including Porifera, Cnidaria largely unstudied. and Ctenophora, has proven insightful for comparative While germ cells were originally characterized mor- research describing the origin of gene families central to phologically by a large round nucleus, large nucleolus, particular developmental processes in bilaterians as well relatively clear cytoplasm and granular cytoplasmic as the conservation of function in deep animal evolution. material, often referred to as “nuage” [reviewed in 3], in Two general developmental processes, for which studies recent years, molecular markers for protein and RNA in these lineages could be insightful, are related to sexual expression have provided a useful way of identifying germ reproduction in animals: (1) specification of a set of cells cells [7–9]. Three prominent genes have been character- for the germline and (2) differentiation of the germline ized showing a conserved expression pattern in germ into the sex-specific gametes, sperm and oocytes, as part cells: nanos, vasa and piwi [10]. nanos is a CCHC zinc of the sex determination in the reproductive adult. Study- finger protein that likely functions as a transcriptional ing these two related questions in early diverging phyla is and translational repressor. Originally isolated from important to inform two general research areas in com- Drosophila, nanos is an important regulator involved parative evolutionary developmental biology: What is the with both anterior–posterior patterning as well as germ potential conservation compared with bilaterian species, cell specification [11, 12]. Similarly in zebrafish, uniform and what functions do molecules commonly used in ger- maternal nanos transcripts later become concentrated mline specification and gamete differentiation have in in the PGCs [13]. In the sea urchin, Strongylocentrotus other developmental processes. purpuratus, nanos is involved in oogenesis and then later localized only to the small micromeres [14], which give Germline specification rise to germ cells [15, 16]. In the annelid Capitella teleta, The precursors to the gametes, referred to as the germ it is expressed maternally and through cleavage in a uni- cells and part of the germline, become distinct from form pattern, later becoming segregated to both putative somatic cell lineages during development, but the tim- PGCs and a subset of somatic cells [17]. Similar mater- ing of this transition from somatic to germline appears nal and then segregated expression of nanos in subsets labile over animal evolution [1–3]. The germline in ani- of blastomeres has been reported in molluscs [18]. Work mals is specified via two general processes: preforma- in three cnidarians, Nematostella, Clytia and Hydra, has tion and epigenesis [reviewed in 3]. Preformation occurs shown expression of nanos paralogs in putative germ when maternally synthesized cytoplasmic proteins and cells, stem cells, as well as somatic cells (e.g., base of ten- mRNAs (i.e., germ plasm) are deposited and segregated tacle bulbs in Clytia) [6, 19, 20]. nanos is expressed in the in the oocyte such that the blastomeres that inherit them oocytes and during development of the sponge Sycon cili- become
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