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A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila

In animals, PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In Drosophila and other species with a maternally specified germline, piRNAs deposited in the egg initiate piRNA biogenesis in the progeny. However, Y chromosome loci cannot particip...

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Autores principales: Venkei, Zsolt G., Gainetdinov, Ildar, Bagci, Ayca, Starostik, Margaret R., Choi, Charlotte P., Fingerhut, Jaclyn M., Chen, Peiwei, Balsara, Chiraag, Whitfield, Troy W., Bell, George W., Feng, Suhua, Jacobsen, Steven E., Aravin, Alexei A., Kim, John K., Zamore, Phillip D., Yamashita, Yukiko M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10567549/
https://www.ncbi.nlm.nih.gov/pubmed/37723298
http://dx.doi.org/10.1038/s41556-023-01227-4
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author Venkei, Zsolt G.
Gainetdinov, Ildar
Bagci, Ayca
Starostik, Margaret R.
Choi, Charlotte P.
Fingerhut, Jaclyn M.
Chen, Peiwei
Balsara, Chiraag
Whitfield, Troy W.
Bell, George W.
Feng, Suhua
Jacobsen, Steven E.
Aravin, Alexei A.
Kim, John K.
Zamore, Phillip D.
Yamashita, Yukiko M.
author_facet Venkei, Zsolt G.
Gainetdinov, Ildar
Bagci, Ayca
Starostik, Margaret R.
Choi, Charlotte P.
Fingerhut, Jaclyn M.
Chen, Peiwei
Balsara, Chiraag
Whitfield, Troy W.
Bell, George W.
Feng, Suhua
Jacobsen, Steven E.
Aravin, Alexei A.
Kim, John K.
Zamore, Phillip D.
Yamashita, Yukiko M.
author_sort Venkei, Zsolt G.
collection PubMed
description In animals, PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In Drosophila and other species with a maternally specified germline, piRNAs deposited in the egg initiate piRNA biogenesis in the progeny. However, Y chromosome loci cannot participate in such a chain of intergenerational inheritance. How then can the biogenesis of Y-linked piRNAs be initiated? Here, using Suppressor of Stellate (Su(Ste)), a Y-linked Drosophila melanogaster piRNA locus as a model, we show that Su(Ste) piRNAs are made in the early male germline via 5′-to-3′ phased piRNA biogenesis initiated by maternally deposited 1360/Hoppel transposon piRNAs. Notably, deposition of Su(Ste) piRNAs from XXY mothers obviates the need for phased piRNA biogenesis in sons. Together, our study uncovers a developmentally programmed, intergenerational mechanism that allows fly mothers to protect their sons using a Y-linked piRNA locus.
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spelling pubmed-105675492023-10-13 A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila Venkei, Zsolt G. Gainetdinov, Ildar Bagci, Ayca Starostik, Margaret R. Choi, Charlotte P. Fingerhut, Jaclyn M. Chen, Peiwei Balsara, Chiraag Whitfield, Troy W. Bell, George W. Feng, Suhua Jacobsen, Steven E. Aravin, Alexei A. Kim, John K. Zamore, Phillip D. Yamashita, Yukiko M. Nat Cell Biol Article In animals, PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In Drosophila and other species with a maternally specified germline, piRNAs deposited in the egg initiate piRNA biogenesis in the progeny. However, Y chromosome loci cannot participate in such a chain of intergenerational inheritance. How then can the biogenesis of Y-linked piRNAs be initiated? Here, using Suppressor of Stellate (Su(Ste)), a Y-linked Drosophila melanogaster piRNA locus as a model, we show that Su(Ste) piRNAs are made in the early male germline via 5′-to-3′ phased piRNA biogenesis initiated by maternally deposited 1360/Hoppel transposon piRNAs. Notably, deposition of Su(Ste) piRNAs from XXY mothers obviates the need for phased piRNA biogenesis in sons. Together, our study uncovers a developmentally programmed, intergenerational mechanism that allows fly mothers to protect their sons using a Y-linked piRNA locus. Nature Publishing Group UK 2023-09-18 2023 /pmc/articles/PMC10567549/ /pubmed/37723298 http://dx.doi.org/10.1038/s41556-023-01227-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Venkei, Zsolt G.
Gainetdinov, Ildar
Bagci, Ayca
Starostik, Margaret R.
Choi, Charlotte P.
Fingerhut, Jaclyn M.
Chen, Peiwei
Balsara, Chiraag
Whitfield, Troy W.
Bell, George W.
Feng, Suhua
Jacobsen, Steven E.
Aravin, Alexei A.
Kim, John K.
Zamore, Phillip D.
Yamashita, Yukiko M.
A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title_full A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title_fullStr A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title_full_unstemmed A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title_short A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila
title_sort maternally programmed intergenerational mechanism enables male offspring to make pirnas from y-linked precursor rnas in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10567549/
https://www.ncbi.nlm.nih.gov/pubmed/37723298
http://dx.doi.org/10.1038/s41556-023-01227-4
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