Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects

Adenosine-to-inosine (A-to-I) RNA editing leads to a similar effect to A-to-G mutations. RNA editing provides a temporo-spatial flexibility for organisms. Nonsynonymous (Nonsyn) RNA editing in insects is over-represented compared with synonymous (Syn) editing, suggesting adaptive signals of positive...

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Main Authors: Yuchen Zhang, Yuange Duan
Format: Article
Language:English
Published: MDPI AG 2023-10-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/14/10/1951
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author Yuchen Zhang
Yuange Duan
author_facet Yuchen Zhang
Yuange Duan
author_sort Yuchen Zhang
collection DOAJ
description Adenosine-to-inosine (A-to-I) RNA editing leads to a similar effect to A-to-G mutations. RNA editing provides a temporo-spatial flexibility for organisms. Nonsynonymous (Nonsyn) RNA editing in insects is over-represented compared with synonymous (Syn) editing, suggesting adaptive signals of positive selection on Nonsyn editing during evolution. We utilized the brain RNA editome of <i>Drosophila melanogaster</i> to systematically study the LD (<i>r</i><sup>2</sup>) between editing sites and infer its impact on the adaptive signals of RNA editing. Pairs of editing sites (PESs) were identified from the transcriptome. For CDS PESs of two consecutive editing sites, their occurrence was significantly biased to type-3 PES (Syn-Nonsyn). The haplotype frequency of type-3 PES exhibited a significantly higher abundance of AG than GA, indicating that the rear Nonsyn site is the driver that promotes the editing of the front Syn site (passenger). The exclusion of passenger Syn sites dramatically amplifies the adaptive signal of Nonsyn RNA editing. Our study for the first time quantitatively demonstrates that the linkage between RNA editing events comes from hitchhiking effects and leads to the underestimation of adaptive signals for Nonsyn editing. Our work provides novel insights for studying the evolutionary significance of RNA editing events.
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spelling doaj.art-bc3d75122f074925a9e640488bbc66922023-11-16T10:29:54ZengMDPI AGGenes2073-44252023-10-011410195110.3390/genes14101951Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in InsectsYuchen Zhang0Yuange Duan1MOA Key Lab of Pest Monitoring and Green Management, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, ChinaMOA Key Lab of Pest Monitoring and Green Management, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, ChinaAdenosine-to-inosine (A-to-I) RNA editing leads to a similar effect to A-to-G mutations. RNA editing provides a temporo-spatial flexibility for organisms. Nonsynonymous (Nonsyn) RNA editing in insects is over-represented compared with synonymous (Syn) editing, suggesting adaptive signals of positive selection on Nonsyn editing during evolution. We utilized the brain RNA editome of <i>Drosophila melanogaster</i> to systematically study the LD (<i>r</i><sup>2</sup>) between editing sites and infer its impact on the adaptive signals of RNA editing. Pairs of editing sites (PESs) were identified from the transcriptome. For CDS PESs of two consecutive editing sites, their occurrence was significantly biased to type-3 PES (Syn-Nonsyn). The haplotype frequency of type-3 PES exhibited a significantly higher abundance of AG than GA, indicating that the rear Nonsyn site is the driver that promotes the editing of the front Syn site (passenger). The exclusion of passenger Syn sites dramatically amplifies the adaptive signal of Nonsyn RNA editing. Our study for the first time quantitatively demonstrates that the linkage between RNA editing events comes from hitchhiking effects and leads to the underestimation of adaptive signals for Nonsyn editing. Our work provides novel insights for studying the evolutionary significance of RNA editing events.https://www.mdpi.com/2073-4425/14/10/1951adaptive signalA-to-I RNA editing<i>Drosophila</i>linkagenonsynonymous
spellingShingle Yuchen Zhang
Yuange Duan
Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
Genes
adaptive signal
A-to-I RNA editing
<i>Drosophila</i>
linkage
nonsynonymous
title Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
title_full Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
title_fullStr Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
title_full_unstemmed Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
title_short Genome-Wide Analysis on Driver and Passenger RNA Editing Sites Suggests an Underestimation of Adaptive Signals in Insects
title_sort genome wide analysis on driver and passenger rna editing sites suggests an underestimation of adaptive signals in insects
topic adaptive signal
A-to-I RNA editing
<i>Drosophila</i>
linkage
nonsynonymous
url https://www.mdpi.com/2073-4425/14/10/1951
work_keys_str_mv AT yuchenzhang genomewideanalysisondriverandpassengerrnaeditingsitessuggestsanunderestimationofadaptivesignalsininsects
AT yuangeduan genomewideanalysisondriverandpassengerrnaeditingsitessuggestsanunderestimationofadaptivesignalsininsects