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The developmental transcriptome of Drosophila melanogaster

Nature volume 471, pages 473–479 (2011)Cite this article

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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.

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Figure 1: Discovery of new RNAs in the Bithorax complex.
Figure 2: Discovery of small non-coding RNAs.
Figure 3: Dynamics of gene expression.
Figure 4: Developmentally regulated splicing events.
Figure 5: Discovery of RNA editing events.

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Data deposits

All sequence data have been deposited in the SRA, cDNA sequences have been deposited in GenBank, and array data deposited in GEO (see Supplementary Table 35 for all accession numbers). All data is also available at http://www.modencode.org.

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Acknowledgements

We thank C. Trapnell and L. Pachter for discussions and assistance with Cufflinks, and E. Clough for comments and feedback. A.N.B. was partially supported by an NSF graduate fellowship. This work was funded by an award from the National Human Genome Research INstitute modENCODE Project (U01 HB004271) to S.E.C. (Principal Investigator) and M.R.B., P.C., T.R.G., B.R.G. and N.P. (co-Principal Investigators) under Department of Energy contract no. DE-AC02-05CH11231, and by the National Institute of Diabetes and Digestive and Kidney Diseases Intramural Research Program (B.O.).

Author information

Author notes

  1. Brenton R. Graveley, Angela N. Brooks, Joseph W. Carlson, Michael O. Duff, Jane M. Landolin and Li Yang: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Genetics and Developmental Biology, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, Connecticut 06030-6403, USA,

    Brenton R. Graveley, Michael O. Duff & Li Yang

  2. Department of Molecular and Cell Biology, University of California, Berkeley, 94720, California, USA

    Angela N. Brooks & Steven E. Brenner

  3. Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, 94720, California, USA

    Joseph W. Carlson, Jane M. Landolin, Benjamin W. Booth, Ann Hammonds, Jeremy E. Sandler, Kenneth H. Wan, Roger A. Hoskins & Susan E. Celniker

  4. Section of Developmental Genomics, Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, 20892, Maryland, USA

    Carlo G. Artieri, Renhua Li, John H. Malone, Nicolas R. Mattiuzzo, David Sturgill, Lichun Jiang, Yu Zhang & Brian Oliver

  5. Center for Genome Sciences and Department of Computer Science, Washington University, St Louis, 63108, Missouri, USA

    Marijke J. van Baren, Laura Langton & Michael R. Brent

  6. Department of Statistics, University of California, Berkeley, 94720, California, USA

    Nathan Boley, James B. Brown & Peter J. Bickel

  7. Center for Genomics and Bioinformatics, Indiana University, 1001 E. 3rd Street, Bloomington, Indiana 47405-7005, USA ,

    Lucy Cherbas, Dayu Zhang, Yi Zou & Peter Cherbas

  8. Cold Spring Harbor Laboratory, Cold Spring Harbor, 11724, New York, USA

    Carrie A. Davis, Alex Dobin, Wei Lin, Chris Zaleski, Phil Kapranov & Thomas R. Gingeras

  9. Department of Biology, Indiana University, 1001 E. 3rd Street, Bloomington, Indiana 47405-7005, USA,

    David Miller, Brian Eads, Justen Andrews, Peter Cherbas & Thomas C. Kaufman

  10. Genetic Systems Division, Research and Development, Life Technologies, Foster City, California 94404, USA,

    Brian B. Tuch

  11. Genome Analysis Unit, Amgen, South San Francisco, 94080, California, USA

    Brian B. Tuch

  12. Stowers Institute for Medical Research, 1000 East 50th street, Kansas City, 64110, Missouri, USA

    Marco Blanchette

  13. Department of Pathology and Laboratory Medicine, Kansas University Medical Center, 3901 Rainbow Boulevard, Kansas City, Kansas 66160, USA,

    Marco Blanchette

  14. Division of Biostatistics, School of Public Health, University of California, Berkeley, 94720, California, USA

    Sandrine Dudoit

  15. Department of Biomolecular Engineering. University of California, Santa Cruz. Santa Cruz, 95064, California, USA

    Richard E. Green

  16. Department of Genetics and Howard Hughes Medical Institute, Harvard Medical School, Boston, 02115, Massachusetts, USA

    Norbert Perrimon

  17. Department of Plant and Microbial Biology, University of California, Berkeley, 94720, California, USA

    Aarron Willingham & Steven E. Brenner

  18. Affymetrix, Santa Clara, 95051, California, USA

    Thomas R. Gingeras

Authors
  1. Brenton R. Graveley
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  2. Angela N. Brooks
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  3. Joseph W. Carlson
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  4. Michael O. Duff
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  6. Li Yang
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  7. Carlo G. Artieri
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  36. Yu Zhang
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Contributions

J.A., M.R.B., P.C., T.R.G., B.R.G., R.A.H., T.C.K., B.O., N.P. and S.E.C. designed the project. J.A., S.E.B., M.R.B., P.C., T.R.G., B.R.G., R.A.H., B.O. and S.E.C. managed the project. D.M. prepared biological samples. T.C.K. oversaw biological sample production. D.Z. and B.E. prepared RNA samples. J.A. oversaw RNA sample production. W.L. and A.W. analysed array data. P.K. managed array data production. L.Y. prepared Illumina RNA-Seq libraries. C.A.D., L.L., J.E.S., K.H.W. and L.Y. performed Illumina sequencing. J.M.L., B.R.G. and S.E.C. managed Illumina sequencing production. M.B. and R.E.G. performed 454 sequencing of adults. R.A.H. managed production of the embryonic SOLiD and 454 sequencing. C.A.D. managed data transfers. C.Z. managed databases and formatted array and sequence data for submission. C.G.A., P.J.B., S.E.B., A.N.B., S.D., M.O.D., B.R.G. and D.S. developed analysis methods. C.G.A., J.B.B., N.B., B.W.B., S.E.B., A.N.B., J.W.C., S.E.C., L.C., P.C., C.A.D., A.D., M.O.D., B.R.G., R.L., J.H.M., N.R.M., D.S. and Yi.Z. analysed data. B.B.T. aligned the SOLiD data. M.J.V. and J.M.L. generated annotations. C.G.A., D.S. and J.H.M. analysed species validation data. L.J., C.G.A., D.S. and N.R.M. performed species RNA-Seq quality control. Yu.Z. and J.H.M. oversaw sequencing and gathered species samples. C.G.A., A.N.B., J.W.C., L.C., P.C., A.H., D.S., J.M.L., R.L. N.R.M., J.H.M. and B.O. contributed to the text. A.H. assisted with manuscript preparation. B.R.G. and S.E.C. wrote the paper with input from all authors. All authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Brenton R. Graveley or Susan E. Celniker.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Text, Supplementary references, Supplementary Figures 1-13 with legends and Supplementary Table legends 1-34. (PDF 3767 kb)

Supplementary Tables

The file contains Supplementary Tables 1-12. The file extension name for Supplementary Table 10 was amended on January 9 2011. (ZIP 11757 kb)

Supplementary Tables

The file contains Supplementary Tables 13-18. The file extension name for Supplementary Table 18 was amended on January 9 2011. (ZIP 22949 kb)

Supplementary Tables

The file contains Supplementary Tables 19-26. The file extension names for Supplementary Tables 19 and 22 were amended on January 9 2011. (ZIP 18901 kb)

Supplementary Tables

The file contains Supplementary Tables 27-34. The file extension names for Supplementary Tables 27 and 28 were amended on January 9 2011. (ZIP 17989 kb)

Supplementary Table 35

This file contains the Accession Numbers for RNA-seq, microarrays and cDNAs.  Supplementary Table 35 was added on 9 January 2011. (PDF 222 kb)

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Graveley, B., Brooks, A., Carlson, J. et al. The developmental transcriptome of Drosophila melanogaster. Nature 471, 473–479 (2011). https://doi.org/10.1038/nature09715

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