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Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation
Eukaryotic transcriptomes contain a major non–protein-coding component that includes precursors of small RNAs as well as long noncoding RNA (lncRNAs). Here, we utilized the mapping of ribosome footprints on RNAs to explore translational regulation of coding and noncoding RNAs in roots of Arabidopsis...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5699049/ https://www.ncbi.nlm.nih.gov/pubmed/29087317 http://dx.doi.org/10.1073/pnas.1708433114 |
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author | Bazin, Jérémie Baerenfaller, Katja Gosai, Sager J. Gregory, Brian D. Crespi, Martin Bailey-Serres, Julia |
author_facet | Bazin, Jérémie Baerenfaller, Katja Gosai, Sager J. Gregory, Brian D. Crespi, Martin Bailey-Serres, Julia |
author_sort | Bazin, Jérémie |
collection | PubMed |
description | Eukaryotic transcriptomes contain a major non–protein-coding component that includes precursors of small RNAs as well as long noncoding RNA (lncRNAs). Here, we utilized the mapping of ribosome footprints on RNAs to explore translational regulation of coding and noncoding RNAs in roots of Arabidopsis thaliana shifted from replete to deficient phosphorous (Pi) nutrition. Homodirectional changes in steady-state mRNA abundance and translation were observed for all but 265 annotated protein-coding genes. Of the translationally regulated mRNAs, 30% had one or more upstream ORF (uORF) that influenced the number of ribosomes on the principal protein-coding region. Nearly one-half of the 2,382 lncRNAs detected had ribosome footprints, including 56 with significantly altered translation under Pi-limited nutrition. The prediction of translated small ORFs (sORFs) by quantitation of translation termination and peptidic analysis identified lncRNAs that produce peptides, including several deeply evolutionarily conserved and significantly Pi-regulated lncRNAs. Furthermore, we discovered that natural antisense transcripts (NATs) frequently have actively translated sORFs, including five with low-Pi up-regulation that correlated with enhanced translation of the sense protein-coding mRNA. The data also confirmed translation of miRNA target mimics and lncRNAs that produce trans-acting or phased small-interfering RNA (tasiRNA/phasiRNAs). Mutational analyses of the positionally conserved sORF of TAS3a linked its translation with tasiRNA biogenesis. Altogether, this systematic analysis of ribosome-associated mRNAs and lncRNAs demonstrates that nutrient availability and translational regulation controls protein and small peptide-encoding mRNAs as well as a diverse cadre of regulatory RNAs. |
format | Online Article Text |
id | pubmed-5699049 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-56990492017-11-27 Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation Bazin, Jérémie Baerenfaller, Katja Gosai, Sager J. Gregory, Brian D. Crespi, Martin Bailey-Serres, Julia Proc Natl Acad Sci U S A PNAS Plus Eukaryotic transcriptomes contain a major non–protein-coding component that includes precursors of small RNAs as well as long noncoding RNA (lncRNAs). Here, we utilized the mapping of ribosome footprints on RNAs to explore translational regulation of coding and noncoding RNAs in roots of Arabidopsis thaliana shifted from replete to deficient phosphorous (Pi) nutrition. Homodirectional changes in steady-state mRNA abundance and translation were observed for all but 265 annotated protein-coding genes. Of the translationally regulated mRNAs, 30% had one or more upstream ORF (uORF) that influenced the number of ribosomes on the principal protein-coding region. Nearly one-half of the 2,382 lncRNAs detected had ribosome footprints, including 56 with significantly altered translation under Pi-limited nutrition. The prediction of translated small ORFs (sORFs) by quantitation of translation termination and peptidic analysis identified lncRNAs that produce peptides, including several deeply evolutionarily conserved and significantly Pi-regulated lncRNAs. Furthermore, we discovered that natural antisense transcripts (NATs) frequently have actively translated sORFs, including five with low-Pi up-regulation that correlated with enhanced translation of the sense protein-coding mRNA. The data also confirmed translation of miRNA target mimics and lncRNAs that produce trans-acting or phased small-interfering RNA (tasiRNA/phasiRNAs). Mutational analyses of the positionally conserved sORF of TAS3a linked its translation with tasiRNA biogenesis. Altogether, this systematic analysis of ribosome-associated mRNAs and lncRNAs demonstrates that nutrient availability and translational regulation controls protein and small peptide-encoding mRNAs as well as a diverse cadre of regulatory RNAs. National Academy of Sciences 2017-11-14 2017-10-30 /pmc/articles/PMC5699049/ /pubmed/29087317 http://dx.doi.org/10.1073/pnas.1708433114 Text en Copyright © 2017 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | PNAS Plus Bazin, Jérémie Baerenfaller, Katja Gosai, Sager J. Gregory, Brian D. Crespi, Martin Bailey-Serres, Julia Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title | Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title_full | Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title_fullStr | Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title_full_unstemmed | Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title_short | Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation |
title_sort | global analysis of ribosome-associated noncoding rnas unveils new modes of translational regulation |
topic | PNAS Plus |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5699049/ https://www.ncbi.nlm.nih.gov/pubmed/29087317 http://dx.doi.org/10.1073/pnas.1708433114 |
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