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Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila

The co-packaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to post-transcriptionally regulate mRNAs that function in germline development and maintenance. In D. melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates that co...

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Autores principales: Doyle, Dominique A., Burian, Florencia N., Aharoni, Benjamin, Klinder, Annabelle J., Menzel, Melissa M., Nifras, Gerard Carlo C., Shabazz-Henry, Ahad L., Palma, Bianca Ulrich, Hidalgo, Gisselle A., Sottolano, Christopher J., Ortega, Bianca M., Niepielko, Matthew G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9980053/
https://www.ncbi.nlm.nih.gov/pubmed/36865184
http://dx.doi.org/10.1101/2023.02.21.529147
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author Doyle, Dominique A.
Burian, Florencia N.
Aharoni, Benjamin
Klinder, Annabelle J.
Menzel, Melissa M.
Nifras, Gerard Carlo C.
Shabazz-Henry, Ahad L.
Palma, Bianca Ulrich
Hidalgo, Gisselle A.
Sottolano, Christopher J.
Ortega, Bianca M.
Niepielko, Matthew G.
author_facet Doyle, Dominique A.
Burian, Florencia N.
Aharoni, Benjamin
Klinder, Annabelle J.
Menzel, Melissa M.
Nifras, Gerard Carlo C.
Shabazz-Henry, Ahad L.
Palma, Bianca Ulrich
Hidalgo, Gisselle A.
Sottolano, Christopher J.
Ortega, Bianca M.
Niepielko, Matthew G.
author_sort Doyle, Dominique A.
collection PubMed
description The co-packaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to post-transcriptionally regulate mRNAs that function in germline development and maintenance. In D. melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates that contain multiple transcripts from a specific gene. Nucleated by Oskar (Osk), homotypic clusters in D. melanogaster are generated through a stochastic seeding and self-recruitment process that requires the 3′ UTR of germ granule mRNAs. Interestingly, the 3′ UTR belonging to germ granule mRNAs, such as nanos (nos), have considerable sequence variations among Drosophila species. Thus, we hypothesized that evolutionary changes in the 3′ UTR influences germ granule development. To test our hypothesis, we investigated the homotypic clustering of nos and polar granule component (pgc) in four Drosophila species and concluded that homotypic clustering is a conserved developmental process used to enrich germ granule mRNAs. Additionally, we discovered that the number of transcripts found in nos and/or pgc clusters could vary significantly among species. By integrating biological data with computational modeling, we determined that multiple mechanisms underlie naturally occurring germ granule diversity, including changes in nos, pgc, osk levels, and/or homotypic clustering efficacy. Finally, we found that the nos 3′ UTR from different species can alter the efficacy of nos homotypic clustering, resulting in germ granules with reduced nos accumulation. Our findings highlight the impact that evolution has on the development of germ granules and may provide insight into processes that modify the content of other classes of biomolecular condensates.
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spelling pubmed-99800532023-03-03 Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila Doyle, Dominique A. Burian, Florencia N. Aharoni, Benjamin Klinder, Annabelle J. Menzel, Melissa M. Nifras, Gerard Carlo C. Shabazz-Henry, Ahad L. Palma, Bianca Ulrich Hidalgo, Gisselle A. Sottolano, Christopher J. Ortega, Bianca M. Niepielko, Matthew G. bioRxiv Article The co-packaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to post-transcriptionally regulate mRNAs that function in germline development and maintenance. In D. melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates that contain multiple transcripts from a specific gene. Nucleated by Oskar (Osk), homotypic clusters in D. melanogaster are generated through a stochastic seeding and self-recruitment process that requires the 3′ UTR of germ granule mRNAs. Interestingly, the 3′ UTR belonging to germ granule mRNAs, such as nanos (nos), have considerable sequence variations among Drosophila species. Thus, we hypothesized that evolutionary changes in the 3′ UTR influences germ granule development. To test our hypothesis, we investigated the homotypic clustering of nos and polar granule component (pgc) in four Drosophila species and concluded that homotypic clustering is a conserved developmental process used to enrich germ granule mRNAs. Additionally, we discovered that the number of transcripts found in nos and/or pgc clusters could vary significantly among species. By integrating biological data with computational modeling, we determined that multiple mechanisms underlie naturally occurring germ granule diversity, including changes in nos, pgc, osk levels, and/or homotypic clustering efficacy. Finally, we found that the nos 3′ UTR from different species can alter the efficacy of nos homotypic clustering, resulting in germ granules with reduced nos accumulation. Our findings highlight the impact that evolution has on the development of germ granules and may provide insight into processes that modify the content of other classes of biomolecular condensates. Cold Spring Harbor Laboratory 2023-02-21 /pmc/articles/PMC9980053/ /pubmed/36865184 http://dx.doi.org/10.1101/2023.02.21.529147 Text en https://creativecommons.org/licenses/by-nd/4.0/This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Doyle, Dominique A.
Burian, Florencia N.
Aharoni, Benjamin
Klinder, Annabelle J.
Menzel, Melissa M.
Nifras, Gerard Carlo C.
Shabazz-Henry, Ahad L.
Palma, Bianca Ulrich
Hidalgo, Gisselle A.
Sottolano, Christopher J.
Ortega, Bianca M.
Niepielko, Matthew G.
Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title_full Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title_fullStr Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title_full_unstemmed Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title_short Evolutionary changes in germ granule mRNA content are driven by multiple mechanisms in Drosophila
title_sort evolutionary changes in germ granule mrna content are driven by multiple mechanisms in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9980053/
https://www.ncbi.nlm.nih.gov/pubmed/36865184
http://dx.doi.org/10.1101/2023.02.21.529147
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