Primordial Germ Cell Specification in Vertebrate Embryos: Phylogenetic Distribution and Conserved Molecular Features of Preformation and Induction

Abstract

The differentiation of primordial germ cells (PGCs) occurs during early embryonic development and is critical for the survival and fitness of sexually reproducing species. Here, we review the two main mechanisms of PGC specification, induction, and preformation, in the context of four model vertebrate species: mouse, axolotl, Xenopus frogs, and zebrafish. We additionally discuss some notable molecular characteristics shared across PGC specification pathways, including the shared expression of products from three conserved germline gene families, DAZ (Deleted in Azoospermia) genes, nanos-related genes, and DEAD-box RNA helicases. Then, we summarize the current state of knowledge of the distribution of germ cell determination systems across kingdom Animalia, with particular attention to vertebrate species, but include several categories of invertebrates – ranging from the “proto-vertebrate” cephalochordates to arthropods, cnidarians, and ctenophores. We also briefly highlight ongoing investigations and potential lines of inquiry that aim to understand the evolutionary relationships between these modes of specification.

Germ Granules in Animal Oogenesis

“…Zebrafish ( Danio rerio ) is one of the most common model organisms with an inherited (preformative) type of PGC determination [ 18 ]. The germline cells are determined by maternal factors transmitted to the embryo.…”

“…This is the mitochondrial cloud or the Balbiani body (Bb), a phase-separated structure that is conserved among vertebrate oocytes. It is a large aggregate of organelles found in the oocytes of many species that translocates from a location near the nucleus to the vegetal pole during oogenesis (see also Section 7 and Section 9 ) [ 18 , 43 ]. The vertebrate animal-vegetal axis is established during oogenesis, whereas the anteroposterior and dorsoventral embryonic axes arise after fertilization.…”

Nanos Is Expressed in Somatic and Germline Tissue during Larval and Post-Larval Development of the Annelid Alitta virens

“…Expression of this factor is associated with the germline across the Metazoa, and in some cases, Nanos function has been shown to be required for germline development [ 3 , 4 , 5 , 6 , 7 , 8 ]. However, based on expression patterns, this gene appears to have multiple roles during embryonic and larval development.…”

Primordial Germ Cell Development in the Poeciliid, Gambusia holbrooki, Reveals Shared Features Between Lecithotrophs and Matrotrophs

“…Despite earlier thoughts, the germ plasm acquisition is not confined to primitive animals, but repeatedly shared in higher taxa ( Ewen-Campen et al, 2010 ; Whittle and Extavour, 2017 ) particularly in those that exhibit lecithotrophy. With high species diversity, fish taxa have evolved both modes of PGC specification ( Walvig, 1963 ; Extavour and Akam, 2003 ; Hansen and Pelegri, 2021 ). With majority of oviparous teleost including research models ( Raz, 2002 ; Herpin et al, 2007 ) and commercial species ( Nagasawa et al, 2013 ; Su et al, 2014 ) following the preformation mode, while most chondrichthyans ( i.e., cartilaginous fishes) following induction mode ( Extavour and Akam, 2003 ) that also typically exhibit a degree of matrotrophy.…”