The Conservation of the Germline Multipotency Program, from Sponges to Vertebrates: A Stepping Stone to Understanding the Somatic and Germline Origins

Abstract

The germline definition in metazoans was first based on few bilaterian models. As a result, gene function interpretations were often based on phenotypes observed in those models and led to the definition of a set of genes, considered as specific of the germline, named the “germline core”. However, some of these genes were shown to also be involved in somatic stem cells, thus leading to the notion of germline multipotency program (GMP). Because Porifera and Ctenophora are currently the best candidates to be the sister-group to all other animals, the comparative analysis of gene contents and functions between these phyla, Cnidaria and Bilateria is expected to provide clues on early animal evolution and on the links between somatic and germ lineages. Our present bioinformatic analyses at the metazoan scale show that a set of 18 GMP genes was already present in the last common ancestor of metazoans and indicate more precisely the evolution of some of them in the animal lineage. The expression patterns and levels of 11 of these genes in the homoscleromorph sponge Oscarella lobularis show that they are expressed throughout their life cycle, in pluri/multipotent progenitors, during gametogenesis, embryogenesis and during wound healing. This new study in a nonbilaterian species reinforces the hypothesis of an ancestral multipotency program.

Transdifferentiation and mesenchymal‐to‐epithelial transition during regeneration in Demospongiae (Porifera)

“…According to last investigations in Porifera there are not only two types of adult stem cells (ASCs): Archaeocytes and choanocytes (Funayama, ), but at least four, including pinacocytes and particular ameboid vacuolar cells (Ereskovsky et al, ; Fierro‐Constaín et al, ; Lavrov et al, ).…”

“…In Calcarea, archaeocytes absent and pluripotent ASCs in these sponges are choanocytes and pinacocytes (Korotkova, a, 1962b; Korotkova & Gelihovskaia, ; Lavrov et al, ). In Homoscleromorpha, the pluripotent ASCs are as in Calcarea the choanocytes and pinacocytes, but also mesohyl ameboid vacuolar cells (Gaino et al, ; Ereskovsky, ; Ereskovsky et al, ; Fierro‐Constaín et al, ).…”

Characterization of the piRNA pathway during development of the sea anemone Nematostella vectensis

“…9,10 Therefore, these piRNA pathway components have been suggested to be part of an ancestral gene repertoire conserved from sponges to vertebrates responsible for maintenance of "stemness" in germline stem cells as well as somatic stem cells, referred to as germline mulitpotency program (GMP). 11,12 The phylum Cnidaria, which includes corals, sea anemones, jellyfish and hydroids, is the sister group to Bilateria 13 and thus provides a unique opportunity to study the evolution of shared mechanisms and pathways. Recently, piRNAs and PIWI proteins were identified in the cnidarian Hydra.…”

PL10 DEAD‐Box Protein is Expressed during Germ Cell Differentiation in the Reptile Podarcis sicula (Family Lacertidae)

“…In recent years, a number of “germ line factors” driving germ cell differentiation in both sexes have been identified in several species. Among these factors, the genes of DDX4/Vasa and Ded1/DDX3 subfamilies have been investigated in several invertebrates and vertebrates (Raz, ; Leclère et al., ; Sharma and Jankowsky, ; Kozin and Kostyuchenko, ; Siebert et al., ; Fierro‐Constaín et al., ). These genes encode for DEAD‐box ATP‐dependent RNA helicases (Linder et al., ) and proteins found in all eukaryotes and most prokaryotes (e.g., Schmid and Linder, ; Fujiwara et al., ; Komiya et al., ; Fabioux et al., ; Zhou et al., ).…”

“…DDX4/Vasa proteins are expressed in both male and female germ cells (Lasko and Ashburner, ) and are essential in gametogenesis and germ cell specification during embryogenesis (Raz, ). Nonetheless, in some animals, DDX4/Vasa proteins are also expressed in stem cells of diverse origin, in which they contribute to cell cycle and developmental regulation (Leclère et al., ; Kozin and Kostyuchenko, ; Siebert et al., ; Yajima and Wessel, ; Fierro‐Constaín et al., ). In other animals, their expression appears to be restricted to the germ cell lineage (Zhou et al., ).…”