Bucky Ball Organizes Germ Plasm Assembly in Zebrafish

Bontems, Franck; Stein, Amandine; Marlow, Florence; Lyautey, Jacqueline; Gupta, Tripti; Mullins, Mary C.; Dosch, Roland

doi:10.1016/j.cub.2009.01.038

Cited by 216 publications

(403 citation statements)

References 45 publications

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“…In almost all of these respects, zebrafish oocytes resemble those of Xenopus (though Xenopus vasa RNA is not localized; Komiya et al 1994). Bucky ball expression is necessary and sufficient for the organization of zebrafish germ plasm (Bontems et al 2009). Homologs of Bucky ball have been identified in other vertebrates, but it is unknown whether these also participate in germ plasm organization.…”

Section: Preformationmentioning

confidence: 99%

Evolution of the germ line–soma relationship in vertebrate embryos

Johnson¹,

Richardson²,

Bachvarova³

et al. 2011

Reproduction

111

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The germ line and soma together maintain genetic lineages from generation to generation: the germ line passes genetic information between generations; the soma is the vehicle for germ line transmission, and is shaped by natural selection. The germ line and somatic lineages arise simultaneously in early embryos, but how their development is related depends on how primordial germ cells (PGC) are specified. PGCs are specified by one of two means. Epigenesis describes the induction of PGCs from pluripotent cells by signals from surrounding somatic tissues. In contrast, PGCs in many species are specified cell-autonomously by maternally derived molecules, known as germ plasm, and this is called preformation. Germ plasm inhibits signaling to PGCs; thus, they are specified cell-autonomously. Germ plasm evolved independently in many animal lineages, suggesting convergent evolution, and therefore it would be expected to convey a selective advantage. But, what this is remains unknown. We propose that the selective advantage that drives the emergence of germ plasm in vertebrates is the disengagement of germ line specification from somatic influences. This liberates the evolution of gene regulatory networks (GRNs) that govern somatic development, and thereby enhances species evolvability, a well-recognized selective advantage. We cite recent evidence showing that frog embryos, which contain germ plasm, have modified GRNs that are not conserved in axolotls, which represent more basal amphibians and employ epigenesis. We also present the correlation of preformation with enhanced species radiations, and we discuss the mutually exclusive trajectories influenced by germ plasm or pluripotency, which shaped chordate evolution.

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Section: Preformationmentioning

confidence: 99%

Evolution of the germ line–soma relationship in vertebrate embryos

Johnson¹,

Richardson²,

Bachvarova³

et al. 2011

Reproduction

111

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“…These granules possess common components across phyla (5) but use unique scaffold proteins, such as Drosophila Oskar (6), zebrafish Bucky Ball (7), and Caenorhabditis elegans paralogs PGL-1 and PGL-3 (8,9), called PGL collectively. Germ granule scaffold proteins from different phyla have distinct amino acid sequences with no conserved domains.…”

mentioning

confidence: 99%

PGL germ granule assembly protein is a base-specific, single-stranded RNase

Aoki

Kershner

Bingman

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Cellular RNA-protein (RNP) granules are ubiquitous and have fundamental roles in biology and RNA metabolism, but the molecular basis of their structure, assembly, and function is poorly understood. Using nematode "P-granules" as a paradigm, we focus on the PGL granule scaffold protein to gain molecular insights into RNP granule structure and assembly. We first identify a PGL dimerization domain (DD) and determine its crystal structure. PGL-1 DD has a novel 13 α-helix fold that creates a positively charged channel as a homodimer. We investigate its capacity to bind RNA and discover unexpectedly that PGL-1 DD is a guanosine-specific, singlestranded endonuclease. Discovery of the PGL homodimer, together with previous results, suggests a model in which the PGL DD dimer forms a fundamental building block for P-granule assembly. Discovery of the PGL RNase activity expands the role of RNP granule assembly proteins to include enzymatic activity in addition to their job as structural scaffolds.C ytoplasmic RNA-protein (RNP) granules are found in virtually all cells and are thought to be central to RNA metabolism (1, 2). These diverse organelles include P-bodies, stress granules, neuronal granules, and germ granules (2). RNP granules are not membrane-bound and display liquid-liquid phase-separation properties (3, 4). Many of their molecular components have been identified, including scaffold proteins: proteins that recruit other key granule components and are sufficient to induce RNP granule assembly. Major challenges now are to understand how RNP granules are assembled and how they control RNAs.Germ granules are exemplary RNP granules with a profound yet largely mysterious role in metazoan germ-line development. These granules possess common components across phyla (5) but use unique scaffold proteins, such as Drosophila Oskar (6), zebrafish Bucky Ball (7), and Caenorhabditis elegans paralogs PGL-1 and PGL-3 (8, 9), called PGL collectively. Germ granule scaffold proteins from different phyla have distinct amino acid sequences with no conserved domains. The importance of these scaffolds has been attributed to their function in germ granule assembly (for examples, see refs. 10-12). However, the molecular basis of that assembly and how it impacts RNA regulation remain unknown.Here we focus on the Caenorhabditid PGL scaffold proteins and their role in assembly of nematode germ granules, called P-granules (13). P-granules are required for germ-line survival (8, 9) and germline totipotency (14). A recent model proposes that P-granules capture selected mRNAs exiting the nucleus (15), an idea based on the finding that untranslated mRNAs are enriched in P-granules, but translated mRNAs are absent (15, 16). The consequences of that capture are unclear but may include mRNA repression.The PGL family comprises the closely related PGL-1 and PGL-3 proteins plus divergent PGL-2. PGL-1 and PGL-3 are required for adult germ cell development but the function of PGL-2 is unknown (8). All three PGL proteins interact with each other in vitro ...

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“…The novelty of oskar to insects is one indication that germ plasm arose independently via different genetic mechanisms across the metazoans, at least between the insects and noninsect animal systems. Consistent with the notion of independent genetic regulators of germ plasm across animals, the bucky ball gene in the zebrafish D. rerio has been shown to be critical for germplasm assembly in that taxon (83)(84)(85), whereas this process is believed to be modulated by the nematode-specific MEG (maternal-effect germ-cell defective) and PGL (P-granule abnormality) genes in the model nematode C. elegans (86,87). It is worth noting that oskar (Drosophila), bucky ball (Dario), and MEG/PGL (Caenorhabditis) differ in their pleiotropic roles.…”

Section: Is the Transition To Inheritance Mode Irreversible And Convementioning

confidence: 63%

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Whittle

Extavour

2017

Proc. Natl. Acad. Sci. U.S.A.

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In animals, primordial germ cells (PGCs) give rise to the germ lines, the cell lineages that produce sperm and eggs. PGCs form in embryogenesis, typically by one of two modes: a likely ancestral mode wherein germ cells are induced during embryogenesis by cell-cell signaling (induction) or a derived mechanism whereby germ cells are specified by using germ plasm-that is, maternally specified germ-line determinants (inheritance). The causes of the shift to germ plasm for PGC specification in some animal clades remain largely unknown, but its repeated convergent evolution raises the question of whether it may result from or confer an innate selective advantage. It has been hypothesized that the acquisition of germ plasm confers enhanced evolvability, resulting from the release of selective constraint on somatic gene networks in embryogenesis, thus leading to acceleration of an organism's protein-sequence evolution, particularly for genes expressed at early developmental stages, and resulting in high speciation rates in germ plasm-containing lineages (denoted herein as the "PGCspecification hypothesis"). Although that hypothesis, if supported, could have major implications for animal evolution, our recent large-scale coding-sequence analyses from vertebrates and invertebrates provided important examples of genera that do not support the hypothesis of liberated constraint under germ plasm. Here, we consider reasons why germ plasm might be neither a direct target of selection nor causally linked to accelerated animal evolution. We explore alternate scenarios that could explain the repeated evolution of germ plasm and propose potential consequences of the inheritance and induction modes to animal evolutionary biology.germ line | preformation | epigenesis | primordial germ cell | spandrel P rimordial germ cells (PGCs) are specialized cells located in sexual organs of animals. These cells are central to reproduction because they give rise to the germ lines and, ultimately, the sperm and eggs. The PGCs typically arise during early embryogenesis by one of two distinct modes: (i) induction, wherein germ cells are induced by cell-cell signaling pathways (also known as epigenesis); or (ii) inheritance, wherein germ cells are formed by using germ plasm (a specialized cytoplasm containing proteins and RNAs needed for PGC formation), that is, maternally generated germ-line determinants that are "preformed" before embryogenesis begins (also known as preformation) (1-3). The induction mode appears to be the more prevalent mode in animals and occurs in basally branching lineages, and thus is the hypothesized ancestral mechanism of PGC specification, whereas inheritance comprises the likely derived state (1) (Fig. 1) (see SI Appendix, section 1 on the less parsimonious scenario that induction is the derived mode). Induction has been inferred based on microscopic data from most animal clades studied to date and has been experimentally shown to occur in a diverse range of organisms, including mammals (Mus musculus) (4-8), salamanders (...

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Bucky Ball Organizes Germ Plasm Assembly in Zebrafish

Cited by 216 publications

References 45 publications

Evolution of the germ line–soma relationship in vertebrate embryos

Evolution of the germ line–soma relationship in vertebrate embryos

PGL germ granule assembly protein is a base-specific, single-stranded RNase

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

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