Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions

Abstract Recent research has uncovered extensive variability in the boundaries of transcript isoforms, yet the functional consequences of this variation remain largely unexplored. Here, we systematically discriminate between the molecular phenotypes of overlapping coding and non‐coding transcription...

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Main Authors: Ishaan Gupta, Sandra Clauder‐Münster, Bernd Klaus, Aino I Järvelin, Raeka S Aiyar, Vladimir Benes, Stefan Wilkening, Wolfgang Huber, Vicent Pelechano, Lars M Steinmetz
Format: Article
Language:English
Published: Springer Nature 2014-02-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1002/msb.135068
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author Ishaan Gupta
Sandra Clauder‐Münster
Bernd Klaus
Aino I Järvelin
Raeka S Aiyar
Vladimir Benes
Stefan Wilkening
Wolfgang Huber
Vicent Pelechano
Lars M Steinmetz
author_facet Ishaan Gupta
Sandra Clauder‐Münster
Bernd Klaus
Aino I Järvelin
Raeka S Aiyar
Vladimir Benes
Stefan Wilkening
Wolfgang Huber
Vicent Pelechano
Lars M Steinmetz
author_sort Ishaan Gupta
collection DOAJ
description Abstract Recent research has uncovered extensive variability in the boundaries of transcript isoforms, yet the functional consequences of this variation remain largely unexplored. Here, we systematically discriminate between the molecular phenotypes of overlapping coding and non‐coding transcriptional events from each genic locus using a novel genome‐wide, nucleotide‐resolution technique to quantify the half‐lives of 3′ transcript isoforms in yeast. Our results reveal widespread differences in stability among isoforms for hundreds of genes in a single condition, and that variation of even a single nucleotide in the 3′ untranslated region (UTR) can affect transcript stability. While previous instances of negative associations between 3′ UTR length and transcript stability have been reported, here, we find that shorter isoforms are not necessarily more stable. We demonstrate the role of RNA‐protein interactions in conditioning isoform‐specific stability, showing that PUF3 binds and destabilizes specific polyadenylation isoforms. Our findings indicate that although the functional elements of a gene are encoded in DNA sequence, the selective incorporation of these elements into RNA through transcript boundary variation allows a single gene to have diverse functional consequences.
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issn 1744-4292
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publishDate 2014-02-01
publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj-art-e00bdb37c6df4a8c847ef2bdd79020622025-08-20T04:03:12ZengSpringer NatureMolecular Systems Biology1744-42922014-02-0110211110.1002/msb.135068Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactionsIshaan Gupta0Sandra Clauder‐Münster1Bernd Klaus2Aino I Järvelin3Raeka S Aiyar4Vladimir Benes5Stefan Wilkening6Wolfgang Huber7Vicent Pelechano8Lars M Steinmetz9European Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Centre for Statistical Data AnalysisEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genomics Core FacilityEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitEuropean Molecular Biology Laboratory (EMBL), Genome Biology UnitAbstract Recent research has uncovered extensive variability in the boundaries of transcript isoforms, yet the functional consequences of this variation remain largely unexplored. Here, we systematically discriminate between the molecular phenotypes of overlapping coding and non‐coding transcriptional events from each genic locus using a novel genome‐wide, nucleotide‐resolution technique to quantify the half‐lives of 3′ transcript isoforms in yeast. Our results reveal widespread differences in stability among isoforms for hundreds of genes in a single condition, and that variation of even a single nucleotide in the 3′ untranslated region (UTR) can affect transcript stability. While previous instances of negative associations between 3′ UTR length and transcript stability have been reported, here, we find that shorter isoforms are not necessarily more stable. We demonstrate the role of RNA‐protein interactions in conditioning isoform‐specific stability, showing that PUF3 binds and destabilizes specific polyadenylation isoforms. Our findings indicate that although the functional elements of a gene are encoded in DNA sequence, the selective incorporation of these elements into RNA through transcript boundary variation allows a single gene to have diverse functional consequences.https://doi.org/10.1002/msb.135068alternative polyadenylationRNA stabilityRNA‐binding proteintranscript isoforms3′UTR
spellingShingle Ishaan Gupta
Sandra Clauder‐Münster
Bernd Klaus
Aino I Järvelin
Raeka S Aiyar
Vladimir Benes
Stefan Wilkening
Wolfgang Huber
Vicent Pelechano
Lars M Steinmetz
Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
Molecular Systems Biology
alternative polyadenylation
RNA stability
RNA‐binding protein
transcript isoforms
3′UTR
title Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
title_full Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
title_fullStr Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
title_full_unstemmed Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
title_short Alternative polyadenylation diversifies post‐transcriptional regulation by selective RNA–protein interactions
title_sort alternative polyadenylation diversifies post transcriptional regulation by selective rna protein interactions
topic alternative polyadenylation
RNA stability
RNA‐binding protein
transcript isoforms
3′UTR
url https://doi.org/10.1002/msb.135068
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