The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila

Organisms require mechanisms to distinguish self and non-self-RNA. This distinction is crucial to initiate the biogenesis of Piwi-interacting RNAs (piRNAs). In Drosophila ovaries, PIWI-guided slicing and the recognition of piRNA precursor transcripts by the DEAD-box RNA helicase Yb are the 2 known m...

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Main Authors: Shashank Chary, Rippei Hayashi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-06-01
Series:PLoS Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10243637/?tool=EBI
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author Shashank Chary
Rippei Hayashi
author_facet Shashank Chary
Rippei Hayashi
author_sort Shashank Chary
collection DOAJ
description Organisms require mechanisms to distinguish self and non-self-RNA. This distinction is crucial to initiate the biogenesis of Piwi-interacting RNAs (piRNAs). In Drosophila ovaries, PIWI-guided slicing and the recognition of piRNA precursor transcripts by the DEAD-box RNA helicase Yb are the 2 known mechanisms to licence an RNA for piRNA biogenesis in the germline and the soma, respectively. Both the PIWI proteins and Yb are highly conserved across most Drosophila species and are thought to be essential to the piRNA pathway and for silencing transposons. However, we find that species closely related to Drosophila melanogaster have lost the yb gene, as well as the PIWI gene Ago3. We show that the precursor RNA is still selected in the absence of Yb to abundantly generate transposon antisense piRNAs in the soma. We further demonstrate that Drosophila eugracilis, which lacks Ago3, is completely devoid of ping-pong piRNAs and exclusively produces phased piRNAs in the absence of slicing. Thus, core piRNA pathway genes can be lost in evolution while still maintaining efficient transposon silencing. Organisms need to distinguish self and non-self RNA when initiating the biogenesis of piRNAs to target transposons. This study reveals that some Drosophila species have lost the PIWI gene Ago3 and/or the helicase RNA Yb - highly conserved components of the piRNA biogenesis pathway - yet still retain piRNA abundance and specificity.
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spelling doaj.art-0879a29e182147409311157972b61d1d2023-06-08T05:31:10ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-06-01216The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in DrosophilaShashank CharyRippei HayashiOrganisms require mechanisms to distinguish self and non-self-RNA. This distinction is crucial to initiate the biogenesis of Piwi-interacting RNAs (piRNAs). In Drosophila ovaries, PIWI-guided slicing and the recognition of piRNA precursor transcripts by the DEAD-box RNA helicase Yb are the 2 known mechanisms to licence an RNA for piRNA biogenesis in the germline and the soma, respectively. Both the PIWI proteins and Yb are highly conserved across most Drosophila species and are thought to be essential to the piRNA pathway and for silencing transposons. However, we find that species closely related to Drosophila melanogaster have lost the yb gene, as well as the PIWI gene Ago3. We show that the precursor RNA is still selected in the absence of Yb to abundantly generate transposon antisense piRNAs in the soma. We further demonstrate that Drosophila eugracilis, which lacks Ago3, is completely devoid of ping-pong piRNAs and exclusively produces phased piRNAs in the absence of slicing. Thus, core piRNA pathway genes can be lost in evolution while still maintaining efficient transposon silencing. Organisms need to distinguish self and non-self RNA when initiating the biogenesis of piRNAs to target transposons. This study reveals that some Drosophila species have lost the PIWI gene Ago3 and/or the helicase RNA Yb - highly conserved components of the piRNA biogenesis pathway - yet still retain piRNA abundance and specificity.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10243637/?tool=EBI
spellingShingle Shashank Chary
Rippei Hayashi
The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
PLoS Biology
title The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
title_full The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
title_fullStr The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
title_full_unstemmed The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
title_short The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila
title_sort absence of core pirna biogenesis factors does not impact efficient transposon silencing in drosophila
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10243637/?tool=EBI
work_keys_str_mv AT shashankchary theabsenceofcorepirnabiogenesisfactorsdoesnotimpactefficienttransposonsilencingindrosophila
AT rippeihayashi theabsenceofcorepirnabiogenesisfactorsdoesnotimpactefficienttransposonsilencingindrosophila
AT shashankchary absenceofcorepirnabiogenesisfactorsdoesnotimpactefficienttransposonsilencingindrosophila
AT rippeihayashi absenceofcorepirnabiogenesisfactorsdoesnotimpactefficienttransposonsilencingindrosophila