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Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals

Long intergenic noncoding RNAs (lincRNAs) play diverse regulatory roles in human development and disease, but little is known about their evolutionary history and constraint. Here, we characterize human lincRNA expression patterns in nine tissues across six mammalian species and multiple individuals...

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Detalles Bibliográficos
Autores principales: Washietl, Stefan, Kellis, Manolis, Garber, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975061/
https://www.ncbi.nlm.nih.gov/pubmed/24429298
http://dx.doi.org/10.1101/gr.165035.113
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author Washietl, Stefan
Kellis, Manolis
Garber, Manuel
author_facet Washietl, Stefan
Kellis, Manolis
Garber, Manuel
author_sort Washietl, Stefan
collection PubMed
description Long intergenic noncoding RNAs (lincRNAs) play diverse regulatory roles in human development and disease, but little is known about their evolutionary history and constraint. Here, we characterize human lincRNA expression patterns in nine tissues across six mammalian species and multiple individuals. Of the 1898 human lincRNAs expressed in these tissues, we find orthologous transcripts for 80% in chimpanzee, 63% in rhesus, 39% in cow, 38% in mouse, and 35% in rat. Mammalian-expressed lincRNAs show remarkably strong conservation of tissue specificity, suggesting that it is selectively maintained. In contrast, abundant splice-site turnover suggests that exact splice sites are not critical. Relative to evolutionarily young lincRNAs, mammalian-expressed lincRNAs show higher primary sequence conservation in their promoters and exons, increased proximity to protein-coding genes enriched for tissue-specific functions, fewer repeat elements, and more frequent single-exon transcripts. Remarkably, we find that ∼20% of human lincRNAs are not expressed beyond chimpanzee and are undetectable even in rhesus. These hominid-specific lincRNAs are more tissue specific, enriched for testis, and faster evolving within the human lineage.
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spelling pubmed-39750612014-10-01 Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals Washietl, Stefan Kellis, Manolis Garber, Manuel Genome Res Research Long intergenic noncoding RNAs (lincRNAs) play diverse regulatory roles in human development and disease, but little is known about their evolutionary history and constraint. Here, we characterize human lincRNA expression patterns in nine tissues across six mammalian species and multiple individuals. Of the 1898 human lincRNAs expressed in these tissues, we find orthologous transcripts for 80% in chimpanzee, 63% in rhesus, 39% in cow, 38% in mouse, and 35% in rat. Mammalian-expressed lincRNAs show remarkably strong conservation of tissue specificity, suggesting that it is selectively maintained. In contrast, abundant splice-site turnover suggests that exact splice sites are not critical. Relative to evolutionarily young lincRNAs, mammalian-expressed lincRNAs show higher primary sequence conservation in their promoters and exons, increased proximity to protein-coding genes enriched for tissue-specific functions, fewer repeat elements, and more frequent single-exon transcripts. Remarkably, we find that ∼20% of human lincRNAs are not expressed beyond chimpanzee and are undetectable even in rhesus. These hominid-specific lincRNAs are more tissue specific, enriched for testis, and faster evolving within the human lineage. Cold Spring Harbor Laboratory Press 2014-04 /pmc/articles/PMC3975061/ /pubmed/24429298 http://dx.doi.org/10.1101/gr.165035.113 Text en © 2014 Washietl et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/3.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.
spellingShingle Research
Washietl, Stefan
Kellis, Manolis
Garber, Manuel
Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title_full Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title_fullStr Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title_full_unstemmed Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title_short Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals
title_sort evolutionary dynamics and tissue specificity of human long noncoding rnas in six mammals
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975061/
https://www.ncbi.nlm.nih.gov/pubmed/24429298
http://dx.doi.org/10.1101/gr.165035.113
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