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The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis

Nuclear RNA degradation pathways are highly conserved across eukaryotes and play important roles in RNA quality control. Key substrates for exosomal degradation include aberrant functional RNAs and cryptic unstable transcripts (CUTs). It has recently been reported that the nuclear exosome is inactiv...

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Autores principales: Frenk, Stephen, Oxley, David, Houseley, Jonathan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161446/
https://www.ncbi.nlm.nih.gov/pubmed/25210768
http://dx.doi.org/10.1371/journal.pone.0107648
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author Frenk, Stephen
Oxley, David
Houseley, Jonathan
author_facet Frenk, Stephen
Oxley, David
Houseley, Jonathan
author_sort Frenk, Stephen
collection PubMed
description Nuclear RNA degradation pathways are highly conserved across eukaryotes and play important roles in RNA quality control. Key substrates for exosomal degradation include aberrant functional RNAs and cryptic unstable transcripts (CUTs). It has recently been reported that the nuclear exosome is inactivated during meiosis in budding yeast through degradation of the subunit Rrp6, leading to the stabilisation of a subset of meiotic unannotated transcripts (MUTs) of unknown function. We have analysed the activity of the nuclear exosome during meiosis by deletion of TRF4, which encodes a key component of the exosome targeting complex TRAMP. We find that TRAMP mutants produce high levels of CUTs during meiosis that are undetectable in wild-type cells, showing that the nuclear exosome remains functional for CUT degradation, and we further report that the meiotic exosome complex contains Rrp6. Indeed Rrp6 over-expression is insufficient to suppress MUT transcripts, showing that the reduced amount of Rrp6 in meiotic cells does not directly cause MUT accumulation. Lack of TRAMP activity stabilises ∼1600 CUTs in meiotic cells, which occupy 40% of the binding capacity of the nuclear cap binding complex (CBC). CBC mutants display defects in the formation of meiotic double strand breaks (DSBs), and we see similar defects in TRAMP mutants, suggesting that a key function of the nuclear exosome is to prevent saturation of the CBC complex by CUTs. Together, our results show that the nuclear exosome remains active in meiosis and has an important role in facilitating meiotic recombination.
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spelling pubmed-41614462014-09-17 The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis Frenk, Stephen Oxley, David Houseley, Jonathan PLoS One Research Article Nuclear RNA degradation pathways are highly conserved across eukaryotes and play important roles in RNA quality control. Key substrates for exosomal degradation include aberrant functional RNAs and cryptic unstable transcripts (CUTs). It has recently been reported that the nuclear exosome is inactivated during meiosis in budding yeast through degradation of the subunit Rrp6, leading to the stabilisation of a subset of meiotic unannotated transcripts (MUTs) of unknown function. We have analysed the activity of the nuclear exosome during meiosis by deletion of TRF4, which encodes a key component of the exosome targeting complex TRAMP. We find that TRAMP mutants produce high levels of CUTs during meiosis that are undetectable in wild-type cells, showing that the nuclear exosome remains functional for CUT degradation, and we further report that the meiotic exosome complex contains Rrp6. Indeed Rrp6 over-expression is insufficient to suppress MUT transcripts, showing that the reduced amount of Rrp6 in meiotic cells does not directly cause MUT accumulation. Lack of TRAMP activity stabilises ∼1600 CUTs in meiotic cells, which occupy 40% of the binding capacity of the nuclear cap binding complex (CBC). CBC mutants display defects in the formation of meiotic double strand breaks (DSBs), and we see similar defects in TRAMP mutants, suggesting that a key function of the nuclear exosome is to prevent saturation of the CBC complex by CUTs. Together, our results show that the nuclear exosome remains active in meiosis and has an important role in facilitating meiotic recombination. Public Library of Science 2014-09-11 /pmc/articles/PMC4161446/ /pubmed/25210768 http://dx.doi.org/10.1371/journal.pone.0107648 Text en © 2014 Frenk et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Frenk, Stephen
Oxley, David
Houseley, Jonathan
The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title_full The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title_fullStr The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title_full_unstemmed The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title_short The Nuclear Exosome Is Active and Important during Budding Yeast Meiosis
title_sort nuclear exosome is active and important during budding yeast meiosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161446/
https://www.ncbi.nlm.nih.gov/pubmed/25210768
http://dx.doi.org/10.1371/journal.pone.0107648
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