Diversity and dynamics of the Drosophila transcriptome

Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A) + RNA sequencing from Drosophila melanogaster in cultured c...

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Published inNature (London) Vol. 512; no. 7515; pp. 393 - 399
Main Authors Brown, James B., Boley, Nathan, Eisman, Robert, May, Gemma E., Stoiber, Marcus H., Duff, Michael O., Booth, Ben W., Wen, Jiayu, Park, Soo, Suzuki, Ana Maria, Wan, Kenneth H., Yu, Charles, Zhang, Dayu, Carlson, Joseph W., Cherbas, Lucy, Eads, Brian D., Miller, David, Mockaitis, Keithanne, Roberts, Johnny, Davis, Carrie A., Frise, Erwin, Hammonds, Ann S., Olson, Sara, Shenker, Sol, Sturgill, David, Samsonova, Anastasia A., Weiszmann, Richard, Robinson, Garret, Hernandez, Juan, Andrews, Justen, Bickel, Peter J., Carninci, Piero, Cherbas, Peter, Gingeras, Thomas R., Hoskins, Roger A., Kaufman, Thomas C., Lai, Eric C., Oliver, Brian, Perrimon, Norbert, Graveley, Brenton R., Celniker, Susan E.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 28.08.2014
Nature Publishing Group
Subjects
14
38
38/39
45/91
631/114/2401
631/208/191/2018
631/208/212
631/208/212/2019
64/24
Alternative Splicing - genetics
Analysis
Animals
Developmental stages
Drosophila
Drosophila melanogaster - anatomy & histology
Drosophila melanogaster - cytology
Drosophila melanogaster - genetics
Female
Gene Expression Profiling
Genes
Genetic aspects
Genetic research
Genetic transcription
Genomes
Genomics
Gonads
Humanities and Social Sciences
Insects
Male
Methods
Molecular Sequence Annotation
multidisciplinary
Nerve Tissue - metabolism
Organ Specificity
Poly A - genetics
Polyadenylation
Promoter Regions, Genetic - genetics
Proteins
RNA
RNA, Long Noncoding - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
Science
Sex Characteristics
Stress, Physiological - genetics
Transcriptome - genetics
Online AccessGet full text

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Abstract Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A) + RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites. A large-scale transcriptome analysis in Drosophila melanogaster , across tissues, cell types and conditions, provides insights into global patterns and diversity of transcription initiation, splicing, polyadenylation and non-coding RNA expression.
AbstractList Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A)^sup +^ RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites.
Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A)+ RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites.
Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A)+ RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites.Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A)+ RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites.
Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. Here we have identified new genes, transcripts and proteins using poly(A) + RNA sequencing from Drosophila melanogaster in cultured cell lines, dissected organ systems and under environmental perturbations. We found that a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long non-coding RNAs (lncRNAs), some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized, with this complexity arising from combinatorial usage of promoters, splice sites and polyadenylation sites. A large-scale transcriptome analysis in Drosophila melanogaster , across tissues, cell types and conditions, provides insights into global patterns and diversity of transcription initiation, splicing, polyadenylation and non-coding RNA expression.
Animal transcriptomes are dynamic, each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. We identified new genes, transcripts, and proteins using poly(A)+ RNA sequence from Drosophila melanogaster cultured cell lines, dissected organ systems, and environmental perturbations. We found a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long noncoding RNAs (lncRNAs) some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized arising from combinatorial usage of promoters, splice sites, and polyadenylation sites.
Audience Academic
Author Eisman, Robert
Frise, Erwin
Lai, Eric C.
Boley, Nathan
Bickel, Peter J.
Carninci, Piero
Celniker, Susan E.
May, Gemma E.
Miller, David
Perrimon, Norbert
Suzuki, Ana Maria
Hammonds, Ann S.
Shenker, Sol
Duff, Michael O.
Olson, Sara
Sturgill, David
Wan, Kenneth H.
Graveley, Brenton R.
Gingeras, Thomas R.
Carlson, Joseph W.
Robinson, Garret
Kaufman, Thomas C.
Eads, Brian D.
Cherbas, Lucy
Roberts, Johnny
Oliver, Brian
Mockaitis, Keithanne
Stoiber, Marcus H.
Wen, Jiayu
Brown, James B.
Yu, Charles
Park, Soo
Davis, Carrie A.
Samsonova, Anastasia A.
Weiszmann, Richard
Hoskins, Roger A.
Cherbas, Peter
Booth, Ben W.
Andrews, Justen
Zhang, Dayu
Hernandez, Juan
AuthorAffiliation h Section of Developmental Genomics, Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes or Health, Bethesda MD
e Center for Genomics and Bioinformatics, Indiana University, 1001 E. 3rd Street, Bloomington, IN
g Sloan-Kettering Institute, 1017C Rockefeller Research Labs 1275 York Avenue, Box 252 New York, NY 10065
d Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, CT
c Department of Biology, Indiana University, 1001 E. 3rd Street, Bloomington, IN
i Omics Science Center, RIKEN Yokohama Institute, Yokohama, 230-0045 Kanagawa, Japan
a Department of Statistics, University of California Berkeley, Berkeley, CA
b Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA
f Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
j Department of Genetics, Harvard Medical School, 77 Avenue Lou
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– name: a Department of Statistics, University of California Berkeley, Berkeley, CA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24670639$$D View this record in MEDLINE/PubMed
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Copyright Nature Publishing Group Aug 28, 2014
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Snippet Animal transcriptomes are dynamic, with each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial...
Animal transcriptomes are dynamic, each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial...
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Alternative Splicing - genetics
Analysis
Animals
Developmental stages
Drosophila
Drosophila melanogaster - anatomy & histology
Drosophila melanogaster - cytology
Drosophila melanogaster - genetics
Female
Gene Expression Profiling
Genes
Genetic aspects
Genetic research
Genetic transcription
Genomes
Genomics
Gonads
Humanities and Social Sciences
Insects
Male
Methods
Molecular Sequence Annotation
multidisciplinary
Nerve Tissue - metabolism
Organ Specificity
Poly A - genetics
Polyadenylation
Promoter Regions, Genetic - genetics
Proteins
RNA
RNA, Long Noncoding - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
Science
Sex Characteristics
Stress, Physiological - genetics
Transcriptome - genetics
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Title Diversity and dynamics of the Drosophila transcriptome
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