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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.

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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.

Accession codes

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.).

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Authors

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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