Compartmentalized oskar degradation in the germ plasm safeguards germline development

Partitioning of mRNAs into ribonucleoprotein (RNP) granules supports diverse regulatory programs within the crowded cytoplasm. At least two types of RNP granules populate the germ plasm, a cytoplasmic domain at the posterior of the Drosophila oocyte and embryo. Germ granules deliver mRNAs required f...

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Main Authors: Catherine E Eichler, Anna C Hakes, Brooke Hull, Elizabeth R Gavis
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49988
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author Catherine E Eichler
Anna C Hakes
Brooke Hull
Elizabeth R Gavis
author_facet Catherine E Eichler
Anna C Hakes
Brooke Hull
Elizabeth R Gavis
author_sort Catherine E Eichler
collection DOAJ
description Partitioning of mRNAs into ribonucleoprotein (RNP) granules supports diverse regulatory programs within the crowded cytoplasm. At least two types of RNP granules populate the germ plasm, a cytoplasmic domain at the posterior of the Drosophila oocyte and embryo. Germ granules deliver mRNAs required for germline development to pole cells, the germ cell progenitors. A second type of RNP granule, here named founder granules, contains oskar mRNA, which encodes the germ plasm organizer. Whereas oskar mRNA is essential for germ plasm assembly during oogenesis, we show that it is toxic to pole cells. Founder granules mediate compartmentalized degradation of oskar during embryogenesis to minimize its inheritance by pole cells. Degradation of oskar in founder granules is temporally and mechanistically distinct from degradation of oskar and other mRNAs during the maternal-to-zygotic transition. Our results show how compartmentalization in RNP granules differentially controls fates of mRNAs localized within the same cytoplasmic domain.
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spelling doaj.art-9346a855510b40a3bafb4c082ecebbe02022-12-22T03:52:57ZengeLife Sciences Publications LtdeLife2050-084X2020-01-01910.7554/eLife.49988Compartmentalized oskar degradation in the germ plasm safeguards germline developmentCatherine E Eichler0Anna C Hakes1Brooke Hull2Elizabeth R Gavis3https://orcid.org/0000-0003-0251-0760Department of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesPartitioning of mRNAs into ribonucleoprotein (RNP) granules supports diverse regulatory programs within the crowded cytoplasm. At least two types of RNP granules populate the germ plasm, a cytoplasmic domain at the posterior of the Drosophila oocyte and embryo. Germ granules deliver mRNAs required for germline development to pole cells, the germ cell progenitors. A second type of RNP granule, here named founder granules, contains oskar mRNA, which encodes the germ plasm organizer. Whereas oskar mRNA is essential for germ plasm assembly during oogenesis, we show that it is toxic to pole cells. Founder granules mediate compartmentalized degradation of oskar during embryogenesis to minimize its inheritance by pole cells. Degradation of oskar in founder granules is temporally and mechanistically distinct from degradation of oskar and other mRNAs during the maternal-to-zygotic transition. Our results show how compartmentalization in RNP granules differentially controls fates of mRNAs localized within the same cytoplasmic domain.https://elifesciences.org/articles/49988oskargerm plasmmRNA degradationribonucleoproteinRNA granulefounder granule
spellingShingle Catherine E Eichler
Anna C Hakes
Brooke Hull
Elizabeth R Gavis
Compartmentalized oskar degradation in the germ plasm safeguards germline development
eLife
oskar
germ plasm
mRNA degradation
ribonucleoprotein
RNA granule
founder granule
title Compartmentalized oskar degradation in the germ plasm safeguards germline development
title_full Compartmentalized oskar degradation in the germ plasm safeguards germline development
title_fullStr Compartmentalized oskar degradation in the germ plasm safeguards germline development
title_full_unstemmed Compartmentalized oskar degradation in the germ plasm safeguards germline development
title_short Compartmentalized oskar degradation in the germ plasm safeguards germline development
title_sort compartmentalized oskar degradation in the germ plasm safeguards germline development
topic oskar
germ plasm
mRNA degradation
ribonucleoprotein
RNA granule
founder granule
url https://elifesciences.org/articles/49988
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AT annachakes compartmentalizedoskardegradationinthegermplasmsafeguardsgermlinedevelopment
AT brookehull compartmentalizedoskardegradationinthegermplasmsafeguardsgermlinedevelopment
AT elizabethrgavis compartmentalizedoskardegradationinthegermplasmsafeguardsgermlinedevelopment