Aggregation, segregation, and dispersal of homotypic germ plasm RNPs in the early zebrafish embryo

Abstract

Background In zebrafish and many other organisms, specification of primordial germ cells (PGCs) requires the transmission of maternally‐derived germ plasm. Zebrafish germ plasm ribonucleoparticles (RNPs) aggregate along the cleavage furrows during the first several cell cycles, segregate asymmetrically during the cleavage stages, and undergo cytoplasmic dispersal in the late blastula. Results For all tested germ plasm RNAs [carbonic anhydrase 15b (ca15b), deleted in azoospermia‐like (dazl), dead end (dnd), nanos 3 (nos3), regulator of G‐protein signaling14a (rgs14a), and vasa/DEAD box polypeptide 4 (vasa/ddx4)], RNPs are homotypic (containing a single RNA type), with RNPs packing tightly yet remaining distinct within germ plasm aggregates. Homotypic clustering of RNAs within RNPs is observed before aggregation in the cortex and is maintained through germ plasm recruitment, asymmetric segregation and RNP dispersal. We also identify a step of germ plasm fragmentation during the cleavage stages that precedes RNP dispersal. Conclusions Our findings suggest that germ plasm aggregates act as subcellular compartments that temporarily collect and carry single RNA‐type RNPs from fertilization until their cytoplasmic dispersal in PGCs at the end of the blastula period, and describe a previously unknown fragmentation step that allows for an increase in the pool of germ plasm‐carrying cells, presumably PGCs. Developmental Dynamics 248:306–318, 2019. © 2019 Wiley Periodicals, Inc.

Phase Separation during Germline Development

“…The homotypic clustering of mRNAs seems to be a conserved mechanism because it is also observed in the germplasm of zebrafish [59]. Moreover, RNA self-assembly contributes to stress granule assembly and the formation of abnormal nuclear foci in some neurological diseases [60,61].…”

RNA Granules: A View from the RNA Perspective

“…mRNA assemblies have been observed in diverse RNA condensates, including germ granules in Drosophila [49,125] and zebrafish [143,144], P-bodies in Drosophila oocytes [145], in mammalian stress granules [29], and P-bodies [104]. Thus, homotypic assembly is an inherent property of mRNAs, revealed when they become sufficiently crowded, such as upon their enrichment in RNA condensates.…”

Feed Restriction Modulates Growth, Gut Morphology and Gene Expression in Zebrafish

“…This gene was upregulated 2.25-fold in FR70, but downregulated 2.49-fold in FR85 ( Figure 4 ). Another example includes mid1ip1l gene, which is understood to be involved in the regulation of cytoskeleton organization and regulation of ribonucleoprotein complex localization [ 48 , 49 , 50 ]. This gene was upregulated 1.08-fold in FR85, but downregulated 1.26-fold in FR70 zebrafish.…”