Distinct <i>cis</i>-acting elements mediate targeting and clustering of <i>Drosophila</i> polar granule mRNAs

Eagle, Whitby V.I.; Yeboah-Kordieh, Daniel K.; Niepielko, Matthew G.; Gavis, Elizabeth R.

doi:10.1242/dev.164657

Cited by 31 publications

(54 citation statements)

References 51 publications

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“…S6 " type="url"/> ). These observations are echoed by other reports of homotypic mRNA spatial separation within germ granules ( Eagle et al, 2018 ; Trcek et al, 2015 ) and suggest a complex organization to granules and the mRNAs they contain.…”

Section: Resultssupporting

confidence: 49%

mRNA localization is linked to translation regulation in theCaenorhabditis elegansgerm lineage

et al. 2020

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Caenorhabditis elegans early embryos generate cell-specific transcriptomes despite lacking active transcription, thereby presenting an opportunity to study mechanisms of post-transcriptional regulatory control. We observed that some cell-specific mRNAs accumulate nonhomogenously within cells, localizing to membranes, P granules (associated with progenitor germ cells in the P lineage) and P-bodies (associated with RNA processing). The subcellular distribution of transcripts differed in their dependence on 3′UTRs and RNA binding proteins, suggesting diverse regulatory mechanisms. Notably, we found strong but imperfect correlations between low translational status and P granule localization within the progenitor germ lineage. By uncoupling translation from mRNA localization, we untangled a long-standing question: Are mRNAs directed to P granules to be translationally repressed, or do they accumulate there as a consequence of this repression? We found that translational repression preceded P granule localization and could occur independently of it. Further, disruption of translation was sufficient to send homogenously distributed mRNAs to P granules. These results implicate transcriptional repression as a means to deliver essential maternal transcripts to the progenitor germ lineage for later translation.

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Section: Resultssupporting

confidence: 49%

mRNA localization is linked to translation regulation in theCaenorhabditis elegansgerm lineage

et al. 2020

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“…Curiously, we noticed transcripts did not mix homogenously within P granules but occupied discrete regions within granules depending on their type. For example, clu-1 mRNA typically surrounded a chs-1 mRNA core ( 9/38 separation within germ granules [Eagle et al, 2018, Trcek et al, 2015 and suggest a complex organization to granules and the mRNAs they contain.…”

Section: Quantification Strategies To Characterize Mrna Patterningmentioning

confidence: 99%

mRNA localization is linked to translation regulation in the Caenorhabditis elegans germ lineage

Parker¹

2020

Preprint

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Caenorhabditis elegans early embryos generate cell-specific transcriptomes despite lacking active transcription. This presents an opportunity to study mechanisms of post-transcriptional regulatory control. In seeking the mechanisms behind this patterning, we discovered that some cell-specific mRNAs accumulate non-homogenously within cells, localizing to membranes, P granules (associated with progenitor germ cells in the P lineage), and P-bodies (associated with RNA processing). Transcripts differed in their dependence on 3'UTRs and RNA Binding Proteins, suggesting diverse regulatory mechanisms. Notably, we found strong but imperfect correlations between low translational status and P granule localization within the progenitor germ lineage. By uncoupling these, we untangled a long-standing question: Are mRNAs directed to P granules for translational repression or do they accumulate there as a downstream step? We found translational repression preceded P granule localization and could occur independent of it. Further, disruption of translation was sufficient to send homogenously distributed mRNAs to P granules. Overall, we show transcripts important for germline development are directed to P granules by translational repression, and this, in turn, directs their accumulation in the progenitor germ lineage where their repression can ultimately be relieved.

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“…However, it has recently been shown that in Drosophila germ granules, formed at the egg’s posterior cytoplasm (germ plasm) referred to as polar granules, RNA molecules form homotypic clusters which contain multiple molecules of the same RNA species 7,8 . Further studies provided evidence that these homotypic RNA clusters are built up in the granules, starting from single RNA molecules, by a continuous seeding mechanism, which involves these RNAs’ 3’UTR elements responsible for RNA targeting to and clustering within the granules 9,10 . These studies provided important insights into RNA assembly in the polar granules.…”

Section: Introductionmentioning

confidence: 99%

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

Wahiduzzaman

Tindell

et al. 2019

Sci Rep

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The assembly of large RNA-protein granules occurs in germ cells of many animals and these germ granules have provided a paradigm to study structure-functional aspects of similar structures in different cells. Germ granules in Drosophila oocyte’s posterior pole (polar granules) are composed of RNA, in the form of homotypic clusters, and proteins required for germline development. In the granules, Piwi protein Aubergine binds to a scaffold protein Tudor, which contains 11 Tudor domains. Using a super-resolution microscopy, we show that surprisingly, Aubergine and Tudor form distinct clusters within the same polar granules in early Drosophila embryos. These clusters partially overlap and, after germ cells form, they transition into spherical granules with the structural organization unexpected from these interacting proteins: Aubergine shell around the Tudor core. Consistent with the formation of distinct clusters, we show that Aubergine forms homo-oligomers and using all purified Tudor domains, we demonstrate that multiple domains, distributed along the entire Tudor structure, interact with Aubergine. Our data suggest that in polar granules, Aubergine and Tudor are assembled into distinct phases, partially mixed at their “interaction hubs”, and that association of distinct protein clusters may be an evolutionarily conserved mechanism for the assembly of germ granules.

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Distinct cis-acting elements mediate targeting and clustering of Drosophila polar granule mRNAs

Cited by 31 publications

References 51 publications

mRNA localization is linked to translation regulation in theCaenorhabditis elegansgerm lineage

mRNA localization is linked to translation regulation in theCaenorhabditis elegansgerm lineage

mRNA localization is linked to translation regulation in the Caenorhabditis elegans germ lineage

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

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