Spatial organization and function of RNA molecules within phase-separated condensates in zebrafish are controlled by Dnd1

Westerich, Kim Joana; Tarbashevich, Katsiaryna; Schick, Jan; Gupta, Antra; Zhu, Mingzhao; Hull, Kenneth G.; Romo, Daniel; Zeuschner, Dagmar; Goudarzi, Mohammad Ali; Groß-Thebing, Theresa; Raz, Erez

doi:10.1016/j.devcel.2023.06.009

Cited by 13 publications

(2 citation statements)

References 75 publications

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“…In C. elegans oocytes, RNA clustering has been proposed to enhance translational repression ( Cardona et al, 2023 ). In zebrafish, nanos3 mRNA accumulates inside germ granules when translationally repressed early in development and on the granule surface coincident with translational activation ( Westerich et al, 2023 ). Similarly, recent studies in Drosophila have reported that translation of nanos occurs at the granule surface ( Chen et al, 2023 preprint; Ramat et al, 2023 preprint) where ribosomes accumulate ( Mahowald, 1968 ).…”

Section: Discussionmentioning

confidence: 99%

Caenorhabditis elegans germ granules accumulate hundreds of low translation mRNAs with no systematic preference for germ cell fate regulators

Scholl,

Liu,

Seydoux

2024

Development

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In animals with germ plasm, embryonic germline precursors inherit germ granules, condensates proposed to regulate mRNAs coding for germ cell fate determinants. In Caenorhabditis elegans, mRNAs are recruited to germ granules by MEG-3, a sequence non-specific RNA-binding protein that forms stabilizing interfacial clusters on germ granules. Using fluorescence in situ hybridization, we confirmed that 441 MEG-3-bound transcripts are distributed in a pattern consistent with enrichment in germ granules. Thirteen are related to transcripts reported in germ granules in Drosophila or Nasonia. The majority, however, are low-translation maternal transcripts required for embryogenesis that are not maintained preferentially in the nascent germline. Granule enrichment raises the concentration of certain transcripts in germ plasm but is not essential to regulate mRNA translation or stability. Our findings suggest that only a minority of germ granule-associated transcripts contribute to germ cell fate in C. elegans and that the vast majority function as non-specific scaffolds for MEG-3.

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Section: Discussionmentioning

confidence: 99%

Caenorhabditis elegans germ granules accumulate hundreds of low translation mRNAs with no systematic preference for germ cell fate regulators

Scholl,

Liu,

Seydoux

2024

Development

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“…In fermenting yeast cells, mRNAs encoding glycolytic enzymes colocalize in specialized RNP granules and likely undergo translation within these granules 19 . In the PGCs of zebrafish embryos, nanos3 mRNA is suggested to be translated at the periphery of germ granules based on the distribution of ribosomes 75 . Pou5f3 mRNA granules in zebrafish embryos also have been shown to colocalize with nascent Pou5f3 peptides, suggesting the granules as translation sites 18 .…”

Section: Discussionmentioning

confidence: 99%

Repressor sequestration activates translation of germ granule localized mRNA

Chen,

Stainier,

Dufourt

et al. 2023

Preprint

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Biomolecular condensates organize and compartmentalize biochemical processes within cells. Among these, ribonucleoprotein (RNP) granules are characterized as storage depots for translationally repressed mRNA. Whether RNP granules can also activate translation and how such translation is achieved remains unclear. This question is particularly relevant for embryonic germ granules, whose activity has been linked to germ cell fate. Here, we use single-molecule imaging to show that embryonic germ cell RNP granules in Drosophila are the sites of active translation for nanos mRNA. Translating nanos mRNA is oriented with the 5'end preferentially at the germ granule surface while the 3'UTR is buried within the granule. Untranslated nanos mRNAs remain internal within the granule. Quantitative analysis of translational kinetics demonstrates that germ granules activate translation by antagonizing translational repression rather than changing the rate or efficiency of translation. We generated separation-of-function mutations in the disordered linker region of the scaffold protein Oskar that specifically impede nanos translation without affecting germ granule morphology or RNA localization. These mutations reveal that nanos translation is dependent on the sequestration of translational repressors within germ granules. Together, our findings show that RNP granules regulate localized protein synthesis through compartmentalized relief of translational repression raising the possibility that similar repressor-activator switches control translation in other condensates.

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Germ plasm dynamics during oogenesis and early embryonic development in Xenopus and zebrafish

Divyanshi,

Yang

2023

Molecular Reproduction Devel

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Specification of the germline and its segregation from the soma mark one of the most crucial events in the lifetime of an organism. In different organisms, this specification can occur through either inheritance or inductive mechanisms. In species such as Xenopus and zebrafish, the specification of primordial germ cells relies on the inheritance of maternal germline determinants that are synthesized and sequestered in the germ plasm during oogenesis. In this review, we discuss the formation of the germ plasm, how germline determinants are recruited into the germ plasm during oogenesis, and the dynamics of the germ plasm during oogenesis and early embryonic development.

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Spatial organization and function of RNA molecules within phase-separated condensates in zebrafish are controlled by Dnd1

Cited by 13 publications

References 75 publications

Caenorhabditis elegans germ granules accumulate hundreds of low translation mRNAs with no systematic preference for germ cell fate regulators

Caenorhabditis elegans germ granules accumulate hundreds of low translation mRNAs with no systematic preference for germ cell fate regulators

Repressor sequestration activates translation of germ granule localized mRNA

Germ plasm dynamics during oogenesis and early embryonic development in Xenopus and zebrafish

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