Abstract
BackgroundGermline determination is believed to occur by either preformation or epigenesis. Animals that undergo germ cell specification by preformation have a continuous germline. However, animals with germline determination by epigenesis have a discontinuous germline, with somatic cells intercalated. This vision is contrary to August Weismann’s Germ Plasm Theory and has led to several controversies. Recent data from metazoans as diverse as planarians, annelids and sea urchins reveal the presence of pluripotent stem cell populations that express germ plasm components, despite being considered to be somatic. These data also show that germ plasm is continuous in some of these animals, despite their discontinuous germline.Presentation of the hypothesisHere, based on recent molecular data on germ plasm components, I revise the germline concept. I introduce the concept of primordial stem cells, which are evolutionarily conserved stem cells that carry germ plasm components from the zygote to the germ cells. These cells, delineated by the classic concept of the Weismann barrier, can contribute to different extents to somatic tissues or be present in a rudimentary state. The primordial stem cells are a part of the germline that can drive asexual reproduction.Testing the hypothesisMolecular information on the expression of germ plasm components is needed during early development of non-classic model organisms, with special attention to those capable of undergoing asexual reproduction and regeneration. The cell lineage of germ plasm component-containing cells will also shed light on their position with respect to the Weismann barrier. This information will help in understanding the germline and its associated stem cells across metazoan phylogeny.Implications of the hypothesisThis revision of the germline concept explains the extensive similarities observed among stem cells and germline cells in a wide variety of animals, and predicts the expression of germ plasm components in many others. The life history of these animals can be simply explained by changes in the extent of self-renewal, proliferation and developmental potential of the primordial stem cells. The inclusion of the primordial stem cells as a part of the germline, therefore, solves many controversies and provides a continuous germline, just as originally envisaged by August Weismann.
Highlights
Germline determination is believed to occur by either preformation or epigenesis
I define primordial stem cells (PriSCs) as highly conserved stem cells that are predicted to be intercalated between the zygote and the germline during embryonic development and that are delineated by the classical concept of the Weismann barrier
The comparison of different animal embryonic developmental data reveals that proliferative, self-renewing, somatic precursor PriSCs are likely related to the more restricted precursors of the Primordial germ cell (PGC) in more classic developmental organisms
Summary
The concept that the germline is distinct from the soma was introduced in the late 19th century by August Weismann [1]. The small micromere lineage is a distinct population of cells that gives rise only to adult tissues, most likely including the germ cells [23,75] These cells, which express GMP components and have mixed germ/soma potential would constitute the PriSCs in sea urchin, likely following a restricted model similar to the evolutionarily distant P. dumerilii. Such could be the case, for instance, of the colonial barnacle Polyascus polygenea, in which vasa-related mRNAs are expressed in somatic stem cells during the asexual reproduction process, in addition to GCs [83] It would be important, to elucidate if these cells are derived from germ plasm component-containing cells during embryonic development and are, consistent with the PriSC hypothesis, or if the GMP component expression occurs de novo in somatic cells. It would be interesting to know if neoblasts from these species can still regenerate GCs if these are lost
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