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Diversity and dynamics of the Drosophila transcriptome

Author

Listed:
  • James B. Brown

    (University of California Berkeley
    Lawrence Berkeley National Laboratory)

  • Nathan Boley

    (University of California Berkeley)

  • Robert Eisman

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Gemma E. May

    (Institute for Systems Genomics, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, Connecticut 06030, USA)

  • Marcus H. Stoiber

    (University of California Berkeley)

  • Michael O. Duff

    (Institute for Systems Genomics, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, Connecticut 06030, USA)

  • Ben W. Booth

    (Lawrence Berkeley National Laboratory)

  • Jiayu Wen

    (Sloan-Kettering Institute, 1017C Rockefeller Research Labs, 1275 York Avenue, Box 252, New York, New York 10065, USA)

  • Soo Park

    (Lawrence Berkeley National Laboratory)

  • Ana Maria Suzuki

    (RIKEN Omics Science Center, Yokohama, Kanagawa 230-0045, Japan
    RIKEN Center for Life Science Technologies, Yokohama, Kanagawa, 230-0045, Japan)

  • Kenneth H. Wan

    (Lawrence Berkeley National Laboratory)

  • Charles Yu

    (Lawrence Berkeley National Laboratory)

  • Dayu Zhang

    (Center for Genomics and Bioinformatics, Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Joseph W. Carlson

    (Lawrence Berkeley National Laboratory)

  • Lucy Cherbas

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Brian D. Eads

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • David Miller

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Keithanne Mockaitis

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Johnny Roberts

    (Center for Genomics and Bioinformatics, Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Carrie A. Davis

    (Cold Spring Harbor Laboratory)

  • Erwin Frise

    (Lawrence Berkeley National Laboratory)

  • Ann S. Hammonds

    (Lawrence Berkeley National Laboratory)

  • Sara Olson

    (Institute for Systems Genomics, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, Connecticut 06030, USA)

  • Sol Shenker

    (Sloan-Kettering Institute, 1017C Rockefeller Research Labs, 1275 York Avenue, Box 252, New York, New York 10065, USA)

  • David Sturgill

    (Section of Developmental Genomics, Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health)

  • Anastasia A. Samsonova

    (Harvard Medical School, 77 Avenue Louis Pasteur, Boston, Massachusetts 02115, USA
    Howard Hughes Medical Institute, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, Massachusetts 02115, USA)

  • Richard Weiszmann

    (Lawrence Berkeley National Laboratory)

  • Garret Robinson

    (University of California Berkeley)

  • Juan Hernandez

    (University of California Berkeley)

  • Justen Andrews

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Peter J. Bickel

    (University of California Berkeley)

  • Piero Carninci

    (RIKEN Omics Science Center, Yokohama, Kanagawa 230-0045, Japan
    RIKEN Center for Life Science Technologies, Yokohama, Kanagawa, 230-0045, Japan)

  • Peter Cherbas

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA
    Center for Genomics and Bioinformatics, Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Thomas R. Gingeras

    (Cold Spring Harbor Laboratory)

  • Roger A. Hoskins

    (Lawrence Berkeley National Laboratory)

  • Thomas C. Kaufman

    (Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA)

  • Eric C. Lai

    (Sloan-Kettering Institute, 1017C Rockefeller Research Labs, 1275 York Avenue, Box 252, New York, New York 10065, USA)

  • Brian Oliver

    (Section of Developmental Genomics, Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health)

  • Norbert Perrimon

    (Harvard Medical School, 77 Avenue Louis Pasteur, Boston, Massachusetts 02115, USA
    Howard Hughes Medical Institute, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, Massachusetts 02115, USA)

  • Brenton R. Graveley

    (Institute for Systems Genomics, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, Connecticut 06030, USA)

  • Susan E. Celniker

    (Lawrence Berkeley National Laboratory)

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.

Suggested Citation

  • James B. Brown & Nathan Boley & Robert Eisman & Gemma E. May & Marcus H. Stoiber & Michael O. Duff & Ben W. Booth & Jiayu Wen & Soo Park & Ana Maria Suzuki & Kenneth H. Wan & Charles Yu & Dayu Zhang &, 2014. "Diversity and dynamics of the Drosophila transcriptome," Nature, Nature, vol. 512(7515), pages 393-399, August.
    • Handle: RePEc:nat:nature:v:512:y:2014:i:7515:d:10.1038_nature12962
    DOI: 10.1038/nature12962
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    Citations

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    Cited by:

    1. Matthew A. Lawlor & Weihuan Cao & Christopher E. Ellison, 2021. "A transposon expression burst accompanies the activation of Y-chromosome fertility genes during Drosophila spermatogenesis," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Marieke R. Wensveen & Aditya A. Dixit & Robin Schendel & Apfrida Kendek & Jan-Paul Lambooij & Marcel Tijsterman & Serafin U. Colmenares & Aniek Janssen, 2024. "Double-strand breaks in facultative heterochromatin require specific movements and chromatin changes for efficient repair," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Xuedi Zhang & Ju Peng & Menghua Wu & Angyang Sun & Xiangyu Wu & Jie Zheng & Wangfei Shi & Guanjun Gao, 2023. "Broad phosphorylation mediated by testis-specific serine/threonine kinases contributes to spermiogenesis and male fertility," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Harpreet Kaur Salgania & Jutta Metz & Mandy Jeske, 2024. "ReLo is a simple and rapid colocalization assay to identify and characterize direct protein–protein interactions," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Zhantao Shao & Jack Hu & Allison Jandura & Ronit Wilk & Matthew Jachimowicz & Lingfeng Ma & Chun Hu & Abby Sundquist & Indrani Das & Phillip Samuel-Larbi & Julie A. Brill & Henry M. Krause, 2024. "Spatially revealed roles for lncRNAs in Drosophila spermatogenesis, Y chromosome function and evolution," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Jie Du & Weizhe Chen & Xihua Jia & Xuejiao Xu & Emily Yang & Ruizhi Zhou & Yuqi Zhang & Matt Metzloff & Philipp W. Messer & Jackson Champer, 2024. "Germline Cas9 promoters with improved performance for homing gene drive," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Seungjae Lee & Yen-Chung Chen & Austin E. Gillen & J. Matthew Taliaferro & Bart Deplancke & Hongjie Li & Eric C. Lai, 2022. "Diverse cell-specific patterns of alternative polyadenylation in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Jianping Quan & Ming Yang & Xingwang Wang & Gengyuan Cai & Rongrong Ding & Zhanwei Zhuang & Shenping Zhou & Suxu Tan & Donglin Ruan & Jiajin Wu & Enqin Zheng & Zebin Zhang & Langqing Liu & Fanming Men, 2024. "Multi-omic characterization of allele-specific regulatory variation in hybrid pigs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Irmgard U. Haussmann & Yanying Wu & Mohanakarthik P. Nallasivan & Nathan Archer & Zsuzsanna Bodi & Daniel Hebenstreit & Scott Waddell & Rupert Fray & Matthias Soller, 2022. "CMTr cap-adjacent 2′-O-ribose mRNA methyltransferases are required for reward learning and mRNA localization to synapses," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. Zhiping Zhang & Bongmin Bae & Winston H. Cuddleston & Pedro Miura, 2023. "Coordination of alternative splicing and alternative polyadenylation revealed by targeted long read sequencing," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Hong-Wen Tang & Kerstin Spirohn & Yanhui Hu & Tong Hao & István A. Kovács & Yue Gao & Richard Binari & Donghui Yang-Zhou & Kenneth H. Wan & Joel S. Bader & Dawit Balcha & Wenting Bian & Benjamin W. Bo, 2023. "Next-generation large-scale binary protein interaction network for Drosophila melanogaster," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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