P-body-like condensates in the germline

Abstract

P-bodies are cytoplasmic condensates that accumulate low-translation mRNAs for temporary storage before translation or degradation. P-bodies have been best characterized in yeast and mammalian tissue culture cells. We describe here related condensates in the germline of animal models. Germline P-bodies have been reported at all stages of germline development from primordial germ cells to gametes. The activity of the universal germ cell fate regulator, Nanos, is linked to the mRNA decay function of P-bodies, and spatially-regulated condensation of P-body like condensates in embryos is required to localize mRNA regulators to primordial germ cells. In most cases, however, it is not known whether P-bodies represent functional compartments or non-functional condensation by-products that arise when ribonucleoprotein complexes saturate the cytoplasm. We speculate that the ubiquity of P-body-like condensates in germ cells reflects the strong reliance of the germline on cytoplasmic, rather than nuclear, mechanisms of gene regulation.

Keywords: Germ cells; Germ granules; Germline; Nanos; P-body; RNA.

Fig. 1.

P-body like granules in gametes and embryonic germ cells. A) In C. elegans, oogenesis occurs in a syncytium, where germ cells progress through meiosis in an assembly-line like fashion. A large fraction of germ cells function as nurse cells and undergo apoptosis to provide RNA and protein to the surviving developing oocytes [80]. Large, stable grP bodies assemble in C. elegans oocytes that arrest when sperm is absent. These granules contain P granule components (green) and canonical P-body proteins (pink) that occupy distinct subdomains within the granule [46,52]. B) In Drosophila, oogenesis occurs in ovarioles, which consist of progressively developing egg chambers that are produced from the germarium, that contain the germline stem cells. Each egg chamber consists of 16 cells, including one oocyte and 15 nurse cells that provide RNA and protein for the oocyte [6]. In Drosophila egg chambers, sponge bodies/P-bodies (pink) form in the cytoplasm of nurse cells and the oocyte. Polar granules (green) localize to the posterior pole of the oocyte where the embryonic germline will form. C) MARDO (pink) assemble in mouse germinal vesicle (GV) stage oocytes and cluster around mitochondria (green). In round spermatids, the chromatid body (pink) associates with the nuclear membrane. Oocyte and round spermatid are not drawn to scale. D) In C. elegans early germline blastomeres, germline P-bodies (pink) enrich on the surface of P granules (green). E) In early Drosophila embryos, founder granules (pink) degrade oskar mRNA prior to pole cell formation. Polar granules (green) localize mRNAs required for pole cell development, such as Nanos, in the posterior. F) In mouse gonocytes, perinuclear foci termed piP-bodies (green) contain piRNA pathway proteins and canonical P-body components, which localize to the surface of the granule (pink). Pi-bodies (blue) containing MILI are distinct perinuclear granules that frequently localize adjacent to the piP-bodies. P-bodies containing Nanos2 and dead end1 also localize in the cytoplasm.