Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation

PIWI proteins and their guiding Piwi-interacting small RNAs (piRNAs) are crucial for fertility and transposon defense in the animal germline. In most species, the majority of piRNAs are produced from distinct large genomic loci, called piRNA clusters. It is assumed that germline-expressed piRNA clus...

Full description

Bibliographic Details
Main Authors: Gebert, Daniel, Neubert, Lena K, Lloyd, Catrin, Gui, Jinghua, Lehmann, Ruth, Teixeira, Felipe Karam
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:English
Published: Elsevier BV 2022
Online Access:https://hdl.handle.net/1721.1/146884
_version_ 1826214387258490880
author Gebert, Daniel
Neubert, Lena K
Lloyd, Catrin
Gui, Jinghua
Lehmann, Ruth
Teixeira, Felipe Karam
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Gebert, Daniel
Neubert, Lena K
Lloyd, Catrin
Gui, Jinghua
Lehmann, Ruth
Teixeira, Felipe Karam
author_sort Gebert, Daniel
collection MIT
description PIWI proteins and their guiding Piwi-interacting small RNAs (piRNAs) are crucial for fertility and transposon defense in the animal germline. In most species, the majority of piRNAs are produced from distinct large genomic loci, called piRNA clusters. It is assumed that germline-expressed piRNA clusters, particularly in Drosophila, act as principal regulators to control transposons dispersed across the genome. Here, using synteny analysis, we show that large clusters are evolutionarily labile, arise at loci characterized by recurrent chromosomal rearrangements, and are mostly species-specific across the Drosophila genus. By engineering chromosomal deletions in D. melanogaster, we demonstrate that the three largest germline clusters, which account for the accumulation of >40% of all transposon-targeting piRNAs in ovaries, are neither required for fertility nor for transposon regulation in trans. We provide further evidence that dispersed elements, rather than the regulatory action of large Drosophila germline clusters in trans, may be central for transposon defense.
first_indexed 2024-09-23T16:04:15Z
format Article
id mit-1721.1/146884
institution Massachusetts Institute of Technology
language English
last_indexed 2024-09-23T16:04:15Z
publishDate 2022
publisher Elsevier BV
record_format dspace
spelling mit-1721.1/1468842022-12-16T03:03:05Z Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation Gebert, Daniel Neubert, Lena K Lloyd, Catrin Gui, Jinghua Lehmann, Ruth Teixeira, Felipe Karam Massachusetts Institute of Technology. Department of Biology PIWI proteins and their guiding Piwi-interacting small RNAs (piRNAs) are crucial for fertility and transposon defense in the animal germline. In most species, the majority of piRNAs are produced from distinct large genomic loci, called piRNA clusters. It is assumed that germline-expressed piRNA clusters, particularly in Drosophila, act as principal regulators to control transposons dispersed across the genome. Here, using synteny analysis, we show that large clusters are evolutionarily labile, arise at loci characterized by recurrent chromosomal rearrangements, and are mostly species-specific across the Drosophila genus. By engineering chromosomal deletions in D. melanogaster, we demonstrate that the three largest germline clusters, which account for the accumulation of >40% of all transposon-targeting piRNAs in ovaries, are neither required for fertility nor for transposon regulation in trans. We provide further evidence that dispersed elements, rather than the regulatory action of large Drosophila germline clusters in trans, may be central for transposon defense. 2022-12-15T17:19:33Z 2022-12-15T17:19:33Z 2021 2022-12-15T16:59:53Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/146884 Gebert, Daniel, Neubert, Lena K, Lloyd, Catrin, Gui, Jinghua, Lehmann, Ruth et al. 2021. "Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation." Molecular Cell, 81 (19). en 10.1016/J.MOLCEL.2021.07.011 Molecular Cell Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Elsevier BV Elsevier
spellingShingle Gebert, Daniel
Neubert, Lena K
Lloyd, Catrin
Gui, Jinghua
Lehmann, Ruth
Teixeira, Felipe Karam
Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title_full Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title_fullStr Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title_full_unstemmed Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title_short Large Drosophila germline piRNA clusters are evolutionarily labile and dispensable for transposon regulation
title_sort large drosophila germline pirna clusters are evolutionarily labile and dispensable for transposon regulation
url https://hdl.handle.net/1721.1/146884
work_keys_str_mv AT gebertdaniel largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation
AT neubertlenak largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation
AT lloydcatrin largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation
AT guijinghua largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation
AT lehmannruth largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation
AT teixeirafelipekaram largedrosophilagermlinepirnaclustersareevolutionarilylabileanddispensablefortransposonregulation