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Title: The developmental transcriptome of Drosophila melanogaster

Abstract

Drosophila melanogaster is one of the most well studied genetic model organisms; nonetheless, its genome still contains unannotated coding and non-coding genes, transcripts, exons and RNA editing sites. Full discovery and annotation are pre-requisites for understanding how the regulation of transcription, splicing and RNA editing directs the development of this complex organism. Here we used RNA-Seq, tiling microarrays and cDNA sequencing to explore the transcriptome in 30 distinct developmental stages. We identified 111,195 new elements, including thousands of genes, coding and non-coding transcripts, exons, splicing and editing events, and inferred protein isoforms that previously eluded discovery using established experimental, prediction and conservation-based approaches. These data substantially expand the number of known transcribed elements in the Drosophila genome and provide a high-resolution view of transcriptome dynamics throughout development. Drosophila melanogaster is an important non-mammalian model system that has had a critical role in basic biological discoveries, such as identifying chromosomes as the carriers of genetic information and uncovering the role of genes in development. Because it shares a substantial genic content with humans, Drosophila is increasingly used as a translational model for human development, homeostasis and disease. High-quality maps are needed for all functional genomic elements. Previous studies demonstrated that amore » rich collection of genes is deployed during the life cycle of the fly. Although expression profiling using microarrays has revealed the expression of, 13,000 annotated genes, it is difficult to map splice junctions and individual base modifications generated by RNA editing using such approaches. Single-base resolution is essential to define precisely the elements that comprise the Drosophila transcriptome. Estimates of the number of transcript isoforms are less accurate than estimates of the number of genes. Whereas, 20% of Drosophila genes are annotated as encoding alternatively spliced premRNAs, splice-junction microarray experiments indicate that this number is at least 40% (ref. 7). Determining the diversity of mRNAs generated by alternative promoters, alternative splicing and RNA editing will substantially increase the inferred protein repertoire. Non-coding RNA genes (ncRNAs) including short interfering RNAs (siRNAs) and microRNAS (miRNAs) (reviewed in ref. 10), and longer ncRNAs such as bxd (ref. 11) and rox (ref. 12), have important roles in gene regulation, whereas others such as small nucleolar RNAs (snoRNAs)and small nuclear RNAs (snRNAs) are important components of macromolecular machines such as the ribosome and spliceosome. The transcription and processing of these ncRNAs must also be fully documented and mapped. As part of the modENCODE project to annotate the functional elements of the D. melanogaster and Caenorhabditis elegans genomes, we used RNA-Seq and tiling microarrays to sample the Drosophila transcriptome at unprecedented depth throughout development from early embryo to ageing male and female adults. We report on a high-resolution view of the discovery, structure and dynamic expression of the D. melanogaster transcriptome.« less

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
Life Sciences Division
OSTI Identifier:
1011108
Report Number(s):
LBNL-4402E
Journal ID: 0028-0836; TRN: US201109%%211
DOE Contract Number:  
DE-AC02-05CH11231; U01HB004271
Resource Type:
Journal Article
Journal Name:
Nature
Additional Journal Information:
Journal Name: Nature
Country of Publication:
United States
Language:
English
Subject:
60; ADULTS; CHROMOSOMES; DROSOPHILA; EMBRYOS; EXONS; FEMALES; FUNCTIONALS; GENE REGULATION; GENES; GENETICS; HOMEOSTASIS; LIFE CYCLE; MALES; PROMOTERS; PROTEINS; RESOLUTION; RIBOSOMES; RNA; SPLICING; TRANSCRIPTION

Citation Formats

University of Connecticut, Graveley, Brenton R, Brooks, Angela N, Carlson, Joseph W, Duff, Michael O, Landolin, Jane M, Yang, Li, Artieri, Carlo G, van Baren, Marijke J, Boley, Nathan, Booth, Benjamin W, Brown, James B, Cherbas, Lucy, Davis, Carrie A, Dobin, Alex, Li, Renhua, Lin, Wei, Malone, John H, Mattiuzzo, Nicolas R, Miller, David, Sturgill, David, Tuch, Brian B, Zaleski, Chris, Zhang, Dayu, Blanchette, Marco, Dudoit, Sandrine, Eads, Brian, Green, Richard E, Hammonds, Ann, Jiang, Lichun, Kapranov, Phil, Langton, Laura, Perrimon, Norbert, Sandler, Jeremy E, Wan, Kenneth H, Willingham, Aarron, Zhang, Yu, Zou, Yi, Andrews, Justen, Bicke, Peter J, Brenner, Steven E, Brent, Michael R, Cherbas, Peter, Gingeras, Thomas R, Hoskins, Roger A, Kaufman, Thomas C, Oliver, Brian, and Celniker, Susan E. The developmental transcriptome of Drosophila melanogaster. United States: N. p., 2010. Web.
University of Connecticut, Graveley, Brenton R, Brooks, Angela N, Carlson, Joseph W, Duff, Michael O, Landolin, Jane M, Yang, Li, Artieri, Carlo G, van Baren, Marijke J, Boley, Nathan, Booth, Benjamin W, Brown, James B, Cherbas, Lucy, Davis, Carrie A, Dobin, Alex, Li, Renhua, Lin, Wei, Malone, John H, Mattiuzzo, Nicolas R, Miller, David, Sturgill, David, Tuch, Brian B, Zaleski, Chris, Zhang, Dayu, Blanchette, Marco, Dudoit, Sandrine, Eads, Brian, Green, Richard E, Hammonds, Ann, Jiang, Lichun, Kapranov, Phil, Langton, Laura, Perrimon, Norbert, Sandler, Jeremy E, Wan, Kenneth H, Willingham, Aarron, Zhang, Yu, Zou, Yi, Andrews, Justen, Bicke, Peter J, Brenner, Steven E, Brent, Michael R, Cherbas, Peter, Gingeras, Thomas R, Hoskins, Roger A, Kaufman, Thomas C, Oliver, Brian, & Celniker, Susan E. The developmental transcriptome of Drosophila melanogaster. United States.
University of Connecticut, Graveley, Brenton R, Brooks, Angela N, Carlson, Joseph W, Duff, Michael O, Landolin, Jane M, Yang, Li, Artieri, Carlo G, van Baren, Marijke J, Boley, Nathan, Booth, Benjamin W, Brown, James B, Cherbas, Lucy, Davis, Carrie A, Dobin, Alex, Li, Renhua, Lin, Wei, Malone, John H, Mattiuzzo, Nicolas R, Miller, David, Sturgill, David, Tuch, Brian B, Zaleski, Chris, Zhang, Dayu, Blanchette, Marco, Dudoit, Sandrine, Eads, Brian, Green, Richard E, Hammonds, Ann, Jiang, Lichun, Kapranov, Phil, Langton, Laura, Perrimon, Norbert, Sandler, Jeremy E, Wan, Kenneth H, Willingham, Aarron, Zhang, Yu, Zou, Yi, Andrews, Justen, Bicke, Peter J, Brenner, Steven E, Brent, Michael R, Cherbas, Peter, Gingeras, Thomas R, Hoskins, Roger A, Kaufman, Thomas C, Oliver, Brian, and Celniker, Susan E. Thu . "The developmental transcriptome of Drosophila melanogaster". United States. https://www.osti.gov/servlets/purl/1011108.
@article{osti_1011108,
title = {The developmental transcriptome of Drosophila melanogaster},
author = {University of Connecticut and Graveley, Brenton R and Brooks, Angela N and Carlson, Joseph W and Duff, Michael O and Landolin, Jane M and Yang, Li and Artieri, Carlo G and van Baren, Marijke J and Boley, Nathan and Booth, Benjamin W and Brown, James B and Cherbas, Lucy and Davis, Carrie A and Dobin, Alex and Li, Renhua and Lin, Wei and Malone, John H and Mattiuzzo, Nicolas R and Miller, David and Sturgill, David and Tuch, Brian B and Zaleski, Chris and Zhang, Dayu and Blanchette, Marco and Dudoit, Sandrine and Eads, Brian and Green, Richard E and Hammonds, Ann and Jiang, Lichun and Kapranov, Phil and Langton, Laura and Perrimon, Norbert and Sandler, Jeremy E and Wan, Kenneth H and Willingham, Aarron and Zhang, Yu and Zou, Yi and Andrews, Justen and Bicke, Peter J and Brenner, Steven E and Brent, Michael R and Cherbas, Peter and Gingeras, Thomas R and Hoskins, Roger A and Kaufman, Thomas C and Oliver, Brian and Celniker, Susan E},
abstractNote = {Drosophila melanogaster is one of the most well studied genetic model organisms; nonetheless, its genome still contains unannotated coding and non-coding genes, transcripts, exons and RNA editing sites. Full discovery and annotation are pre-requisites for understanding how the regulation of transcription, splicing and RNA editing directs the development of this complex organism. Here we used RNA-Seq, tiling microarrays and cDNA sequencing to explore the transcriptome in 30 distinct developmental stages. We identified 111,195 new elements, including thousands of genes, coding and non-coding transcripts, exons, splicing and editing events, and inferred protein isoforms that previously eluded discovery using established experimental, prediction and conservation-based approaches. These data substantially expand the number of known transcribed elements in the Drosophila genome and provide a high-resolution view of transcriptome dynamics throughout development. Drosophila melanogaster is an important non-mammalian model system that has had a critical role in basic biological discoveries, such as identifying chromosomes as the carriers of genetic information and uncovering the role of genes in development. Because it shares a substantial genic content with humans, Drosophila is increasingly used as a translational model for human development, homeostasis and disease. High-quality maps are needed for all functional genomic elements. Previous studies demonstrated that a rich collection of genes is deployed during the life cycle of the fly. Although expression profiling using microarrays has revealed the expression of, 13,000 annotated genes, it is difficult to map splice junctions and individual base modifications generated by RNA editing using such approaches. Single-base resolution is essential to define precisely the elements that comprise the Drosophila transcriptome. Estimates of the number of transcript isoforms are less accurate than estimates of the number of genes. Whereas, 20% of Drosophila genes are annotated as encoding alternatively spliced premRNAs, splice-junction microarray experiments indicate that this number is at least 40% (ref. 7). Determining the diversity of mRNAs generated by alternative promoters, alternative splicing and RNA editing will substantially increase the inferred protein repertoire. Non-coding RNA genes (ncRNAs) including short interfering RNAs (siRNAs) and microRNAS (miRNAs) (reviewed in ref. 10), and longer ncRNAs such as bxd (ref. 11) and rox (ref. 12), have important roles in gene regulation, whereas others such as small nucleolar RNAs (snoRNAs)and small nuclear RNAs (snRNAs) are important components of macromolecular machines such as the ribosome and spliceosome. The transcription and processing of these ncRNAs must also be fully documented and mapped. As part of the modENCODE project to annotate the functional elements of the D. melanogaster and Caenorhabditis elegans genomes, we used RNA-Seq and tiling microarrays to sample the Drosophila transcriptome at unprecedented depth throughout development from early embryo to ageing male and female adults. We report on a high-resolution view of the discovery, structure and dynamic expression of the D. melanogaster transcriptome.},
doi = {},
url = {https://www.osti.gov/biblio/1011108}, journal = {Nature},
number = ,
volume = ,
place = {United States},
year = {2010},
month = {12}
}