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The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development

Dictyostelium discoideum live in the soil as single cells, engulfing bacteria and growing vegetatively. Upon starvation, tens of thousands of amoebae enter a developmental program that includes aggregation, multicellular differentiation, and sporulation. Major shifts across the protein-coding transc...

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Autores principales: Rosengarten, Rafael D., Santhanam, Balaji, Kokosar, Janez, Shaulsky, Gad
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5295588/
https://www.ncbi.nlm.nih.gov/pubmed/27932387
http://dx.doi.org/10.1534/g3.116.037150
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author Rosengarten, Rafael D.
Santhanam, Balaji
Kokosar, Janez
Shaulsky, Gad
author_facet Rosengarten, Rafael D.
Santhanam, Balaji
Kokosar, Janez
Shaulsky, Gad
author_sort Rosengarten, Rafael D.
collection PubMed
description Dictyostelium discoideum live in the soil as single cells, engulfing bacteria and growing vegetatively. Upon starvation, tens of thousands of amoebae enter a developmental program that includes aggregation, multicellular differentiation, and sporulation. Major shifts across the protein-coding transcriptome accompany these developmental changes. However, no study has presented a global survey of long noncoding RNAs (ncRNAs) in D. discoideum. To characterize the antisense and long intergenic noncoding RNA (lncRNA) transcriptome, we analyzed previously published developmental time course samples using an RNA-sequencing (RNA-seq) library preparation method that selectively depletes ribosomal RNAs (rRNAs). We detected the accumulation of transcripts for 9833 protein-coding messenger RNAs (mRNAs), 621 lncRNAs, and 162 putative antisense RNAs (asRNAs). The noncoding RNAs were interspersed throughout the genome, and were distinct in expression level, length, and nucleotide composition. The noncoding transcriptome displayed a temporal profile similar to the coding transcriptome, with stages of gradual change interspersed with larger leaps. The transcription profiles of some noncoding RNAs were strongly correlated with known differentially expressed coding RNAs, hinting at a functional role for these molecules during development. Examining the mitochondrial transcriptome, we modeled two novel antisense transcripts. We applied yet another ribosomal depletion method to a subset of the samples to better retain transfer RNA (tRNA) transcripts. We observed polymorphisms in tRNA anticodons that suggested a post-transcriptional means by which D. discoideum compensates for codons missing in the genomic complement of tRNAs. We concluded that the prevalence and characteristics of long ncRNAs indicate that these molecules are relevant to the progression of molecular and cellular phenotypes during development.
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spelling pubmed-52955882017-02-09 The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development Rosengarten, Rafael D. Santhanam, Balaji Kokosar, Janez Shaulsky, Gad G3 (Bethesda) Investigations Dictyostelium discoideum live in the soil as single cells, engulfing bacteria and growing vegetatively. Upon starvation, tens of thousands of amoebae enter a developmental program that includes aggregation, multicellular differentiation, and sporulation. Major shifts across the protein-coding transcriptome accompany these developmental changes. However, no study has presented a global survey of long noncoding RNAs (ncRNAs) in D. discoideum. To characterize the antisense and long intergenic noncoding RNA (lncRNA) transcriptome, we analyzed previously published developmental time course samples using an RNA-sequencing (RNA-seq) library preparation method that selectively depletes ribosomal RNAs (rRNAs). We detected the accumulation of transcripts for 9833 protein-coding messenger RNAs (mRNAs), 621 lncRNAs, and 162 putative antisense RNAs (asRNAs). The noncoding RNAs were interspersed throughout the genome, and were distinct in expression level, length, and nucleotide composition. The noncoding transcriptome displayed a temporal profile similar to the coding transcriptome, with stages of gradual change interspersed with larger leaps. The transcription profiles of some noncoding RNAs were strongly correlated with known differentially expressed coding RNAs, hinting at a functional role for these molecules during development. Examining the mitochondrial transcriptome, we modeled two novel antisense transcripts. We applied yet another ribosomal depletion method to a subset of the samples to better retain transfer RNA (tRNA) transcripts. We observed polymorphisms in tRNA anticodons that suggested a post-transcriptional means by which D. discoideum compensates for codons missing in the genomic complement of tRNAs. We concluded that the prevalence and characteristics of long ncRNAs indicate that these molecules are relevant to the progression of molecular and cellular phenotypes during development. Genetics Society of America 2016-12-06 /pmc/articles/PMC5295588/ /pubmed/27932387 http://dx.doi.org/10.1534/g3.116.037150 Text en Copyright © 2017 Rosengarten et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article 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 the original work is properly cited.
spellingShingle Investigations
Rosengarten, Rafael D.
Santhanam, Balaji
Kokosar, Janez
Shaulsky, Gad
The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title_full The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title_fullStr The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title_full_unstemmed The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title_short The Long Noncoding RNA Transcriptome of Dictyostelium discoideum Development
title_sort long noncoding rna transcriptome of dictyostelium discoideum development
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5295588/
https://www.ncbi.nlm.nih.gov/pubmed/27932387
http://dx.doi.org/10.1534/g3.116.037150
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