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Long noncoding RNA repertoire in chicken liver and adipose tissue

BACKGROUND: Improving functional annotation of the chicken genome is a key challenge in bridging the gap between genotype and phenotype. Among all transcribed regions, long noncoding RNAs (lncRNAs) are a major component of the transcriptome and its regulation, and whole-transcriptome sequencing (RNA...

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Autores principales: Muret, Kévin, Klopp, Christophe, Wucher, Valentin, Esquerré, Diane, Legeai, Fabrice, Lecerf, Frédéric, Désert, Colette, Boutin, Morgane, Jehl, Frédéric, Acloque, Hervé, Giuffra, Elisabetta, Djebali, Sarah, Foissac, Sylvain, Derrien, Thomas, Lagarrigue, Sandrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5225574/
https://www.ncbi.nlm.nih.gov/pubmed/28073357
http://dx.doi.org/10.1186/s12711-016-0275-0
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author Muret, Kévin
Klopp, Christophe
Wucher, Valentin
Esquerré, Diane
Legeai, Fabrice
Lecerf, Frédéric
Désert, Colette
Boutin, Morgane
Jehl, Frédéric
Acloque, Hervé
Giuffra, Elisabetta
Djebali, Sarah
Foissac, Sylvain
Derrien, Thomas
Lagarrigue, Sandrine
author_facet Muret, Kévin
Klopp, Christophe
Wucher, Valentin
Esquerré, Diane
Legeai, Fabrice
Lecerf, Frédéric
Désert, Colette
Boutin, Morgane
Jehl, Frédéric
Acloque, Hervé
Giuffra, Elisabetta
Djebali, Sarah
Foissac, Sylvain
Derrien, Thomas
Lagarrigue, Sandrine
author_sort Muret, Kévin
collection PubMed
description BACKGROUND: Improving functional annotation of the chicken genome is a key challenge in bridging the gap between genotype and phenotype. Among all transcribed regions, long noncoding RNAs (lncRNAs) are a major component of the transcriptome and its regulation, and whole-transcriptome sequencing (RNA-Seq) has greatly improved their identification and characterization. We performed an extensive profiling of the lncRNA transcriptome in the chicken liver and adipose tissue by RNA-Seq. We focused on these two tissues because of their importance in various economical traits for which energy storage and mobilization play key roles and also because of their high cell homogeneity. To predict lncRNAs, we used a recently developed tool called FEELnc, which also classifies them with respect to their distance and strand orientation to the closest protein-coding genes. Moreover, to confidently identify the genes/transcripts expressed in each tissue (a complex task for weakly expressed molecules such as lncRNAs), we probed a particularly large number of biological replicates (16 per tissue) compared to common multi-tissue studies with a larger set of tissues but less sampling. RESULTS: We predicted 2193 lncRNA genes, among which 1670 were robustly expressed across replicates in the liver and/or adipose tissue and which were classified into 1493 intergenic and 177 intragenic lncRNAs located between and within protein-coding genes, respectively. We observed similar structural features between chickens and mammals, with strong synteny conservation but without sequence conservation. As previously reported, we confirm that lncRNAs have a lower and more tissue-specific expression than mRNAs. Finally, we showed that adjacent lncRNA-mRNA genes in divergent orientation have a higher co-expression level when separated by less than 1 kb compared to more distant divergent pairs. Among these, we highlighted for the first time a novel lncRNA candidate involved in lipid metabolism, lnc_DHCR24, which is highly correlated with the DHCR24 gene that encodes a key enzyme of cholesterol biosynthesis. CONCLUSIONS: We provide a comprehensive lncRNA repertoire in the chicken liver and adipose tissue, which shows interesting patterns of co-expression between mRNAs and lncRNAs. It contributes to improving the structural and functional annotation of the chicken genome and provides a basis for further studies on energy storage and mobilization traits in the chicken. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12711-016-0275-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-52255742017-01-17 Long noncoding RNA repertoire in chicken liver and adipose tissue Muret, Kévin Klopp, Christophe Wucher, Valentin Esquerré, Diane Legeai, Fabrice Lecerf, Frédéric Désert, Colette Boutin, Morgane Jehl, Frédéric Acloque, Hervé Giuffra, Elisabetta Djebali, Sarah Foissac, Sylvain Derrien, Thomas Lagarrigue, Sandrine Genet Sel Evol Research Article BACKGROUND: Improving functional annotation of the chicken genome is a key challenge in bridging the gap between genotype and phenotype. Among all transcribed regions, long noncoding RNAs (lncRNAs) are a major component of the transcriptome and its regulation, and whole-transcriptome sequencing (RNA-Seq) has greatly improved their identification and characterization. We performed an extensive profiling of the lncRNA transcriptome in the chicken liver and adipose tissue by RNA-Seq. We focused on these two tissues because of their importance in various economical traits for which energy storage and mobilization play key roles and also because of their high cell homogeneity. To predict lncRNAs, we used a recently developed tool called FEELnc, which also classifies them with respect to their distance and strand orientation to the closest protein-coding genes. Moreover, to confidently identify the genes/transcripts expressed in each tissue (a complex task for weakly expressed molecules such as lncRNAs), we probed a particularly large number of biological replicates (16 per tissue) compared to common multi-tissue studies with a larger set of tissues but less sampling. RESULTS: We predicted 2193 lncRNA genes, among which 1670 were robustly expressed across replicates in the liver and/or adipose tissue and which were classified into 1493 intergenic and 177 intragenic lncRNAs located between and within protein-coding genes, respectively. We observed similar structural features between chickens and mammals, with strong synteny conservation but without sequence conservation. As previously reported, we confirm that lncRNAs have a lower and more tissue-specific expression than mRNAs. Finally, we showed that adjacent lncRNA-mRNA genes in divergent orientation have a higher co-expression level when separated by less than 1 kb compared to more distant divergent pairs. Among these, we highlighted for the first time a novel lncRNA candidate involved in lipid metabolism, lnc_DHCR24, which is highly correlated with the DHCR24 gene that encodes a key enzyme of cholesterol biosynthesis. CONCLUSIONS: We provide a comprehensive lncRNA repertoire in the chicken liver and adipose tissue, which shows interesting patterns of co-expression between mRNAs and lncRNAs. It contributes to improving the structural and functional annotation of the chicken genome and provides a basis for further studies on energy storage and mobilization traits in the chicken. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12711-016-0275-0) contains supplementary material, which is available to authorized users. BioMed Central 2017-01-10 /pmc/articles/PMC5225574/ /pubmed/28073357 http://dx.doi.org/10.1186/s12711-016-0275-0 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Muret, Kévin
Klopp, Christophe
Wucher, Valentin
Esquerré, Diane
Legeai, Fabrice
Lecerf, Frédéric
Désert, Colette
Boutin, Morgane
Jehl, Frédéric
Acloque, Hervé
Giuffra, Elisabetta
Djebali, Sarah
Foissac, Sylvain
Derrien, Thomas
Lagarrigue, Sandrine
Long noncoding RNA repertoire in chicken liver and adipose tissue
title Long noncoding RNA repertoire in chicken liver and adipose tissue
title_full Long noncoding RNA repertoire in chicken liver and adipose tissue
title_fullStr Long noncoding RNA repertoire in chicken liver and adipose tissue
title_full_unstemmed Long noncoding RNA repertoire in chicken liver and adipose tissue
title_short Long noncoding RNA repertoire in chicken liver and adipose tissue
title_sort long noncoding rna repertoire in chicken liver and adipose tissue
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5225574/
https://www.ncbi.nlm.nih.gov/pubmed/28073357
http://dx.doi.org/10.1186/s12711-016-0275-0
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