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Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development

The copackaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to posttranscriptionally regulate germline mRNAs. In Drosophila melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates containing multiple transcripts from the same...

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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: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414811/
https://www.ncbi.nlm.nih.gov/pubmed/37527522
http://dx.doi.org/10.1093/molbev/msad174
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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 copackaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to posttranscriptionally regulate germline mRNAs. In Drosophila melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates containing multiple transcripts from the same gene. Nucleated by Oskar (Osk), homotypic clusters are generated through a stochastic seeding and self-recruitment process that requires the 3′ untranslated region (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 and we hypothesized that this diversity influences homotypic clustering. To test our hypothesis, we investigated the homotypic clustering of nos and polar granule component (pgc) in four Drosophila species and concluded that clustering is a conserved process used to enrich germ granule mRNAs. However, we discovered germ granule phenotypes that included significant changes in the abundance of transcripts present in species’ homotypic clusters, which also reflected diversity in the number of coalesced primordial germ cells within their embryonic gonads. By integrating biological data with computational modeling, we found that multiple mechanisms underlie naturally occurring germ granule diversity, including changes in nos, pgc, osk levels and/or homotypic clustering efficacy. Furthermore, we demonstrated how the nos 3′ UTR from different species influences nos clustering, causing granules to have ∼70% less nos and increasing the presence of defective primordial germ cells. Our results highlight the impact that evolution has on germ granules, which should provide broader insight into processes that modify compositions and activities of other classes of biomolecular condensate.
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spelling pubmed-104148112023-08-11 Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development 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 Mol Biol Evol Discoveries The copackaging of mRNAs into biomolecular condensates called germ granules is a conserved strategy to posttranscriptionally regulate germline mRNAs. In Drosophila melanogaster, mRNAs accumulate in germ granules by forming homotypic clusters, aggregates containing multiple transcripts from the same gene. Nucleated by Oskar (Osk), homotypic clusters are generated through a stochastic seeding and self-recruitment process that requires the 3′ untranslated region (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 and we hypothesized that this diversity influences homotypic clustering. To test our hypothesis, we investigated the homotypic clustering of nos and polar granule component (pgc) in four Drosophila species and concluded that clustering is a conserved process used to enrich germ granule mRNAs. However, we discovered germ granule phenotypes that included significant changes in the abundance of transcripts present in species’ homotypic clusters, which also reflected diversity in the number of coalesced primordial germ cells within their embryonic gonads. By integrating biological data with computational modeling, we found that multiple mechanisms underlie naturally occurring germ granule diversity, including changes in nos, pgc, osk levels and/or homotypic clustering efficacy. Furthermore, we demonstrated how the nos 3′ UTR from different species influences nos clustering, causing granules to have ∼70% less nos and increasing the presence of defective primordial germ cells. Our results highlight the impact that evolution has on germ granules, which should provide broader insight into processes that modify compositions and activities of other classes of biomolecular condensate. Oxford University Press 2023-08-01 /pmc/articles/PMC10414811/ /pubmed/37527522 http://dx.doi.org/10.1093/molbev/msad174 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
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
Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title_full Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title_fullStr Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title_full_unstemmed Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title_short Germ Granule Evolution Provides Mechanistic Insight into Drosophila Germline Development
title_sort germ granule evolution provides mechanistic insight into drosophila germline development
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414811/
https://www.ncbi.nlm.nih.gov/pubmed/37527522
http://dx.doi.org/10.1093/molbev/msad174
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