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Spatially revealed roles for lncRNAs in Drosophila spermatogenesis, Y chromosome function and evolution

Author

Listed:
  • Zhantao Shao

    (University of Toronto)

  • Jack Hu

    (University of Toronto)

  • Allison Jandura

    (University of Toronto
    University of Toronto
    The Hospital for Sick Children)

  • Ronit Wilk

    (University of Toronto)

  • Matthew Jachimowicz

    (University of Toronto
    University of Toronto
    The Hospital for Sick Children)

  • Lingfeng Ma

    (University of Toronto
    University of Toronto
    The Hospital for Sick Children)

  • Chun Hu

    (University of Toronto)

  • Abby Sundquist

    (University of Toronto)

  • Indrani Das

    (University of Toronto)

  • Phillip Samuel-Larbi

    (University of Toronto)

  • Julie A. Brill

    (University of Toronto
    The Hospital for Sick Children)

  • Henry M. Krause

    (University of Toronto
    University of Toronto)

Abstract

Unlike coding genes, the number of lncRNA genes in organism genomes is relatively proportional to organism complexity. From plants to humans, the tissues with highest numbers and levels of lncRNA gene expression are the male reproductive organs. To learn why, we initiated a genome-wide analysis of Drosophila lncRNA spatial expression patterns in these tissues. The numbers of genes and levels of expression observed greatly exceed those previously reported, due largely to a preponderance of non-polyadenylated transcripts. In stark contrast to coding genes, the highest numbers of lncRNAs expressed are in post-meiotic spermatids. Correlations between expression levels, localization and previously performed genetic analyses indicate high levels of function and requirement. More focused analyses indicate that lncRNAs play major roles in evolution by controlling transposable element activities, Y chromosome gene expression and sperm construction. A new type of lncRNA-based particle found in seminal fluid may also contribute to reproductive outcomes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47346-w
    DOI: 10.1038/s41467-024-47346-w
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    1. Arang Rhie & Sergey Nurk & Monika Cechova & Savannah J. Hoyt & Dylan J. Taylor & Nicolas Altemose & Paul W. Hook & Sergey Koren & Mikko Rautiainen & Ivan A. Alexandrov & Jamie Allen & Mobin Asri & And, 2023. "The complete sequence of a human Y chromosome," Nature, Nature, vol. 621(7978), pages 344-354, September.
    2. Sarah Kimmins & Paolo Sassone-Corsi, 2005. "Chromatin remodelling and epigenetic features of germ cells," Nature, Nature, vol. 434(7033), pages 583-589, March.
    3. 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.
    4. Ankur Jain & Ronald D. Vale, 2017. "RNA phase transitions in repeat expansion disorders," Nature, Nature, vol. 546(7657), pages 243-247, June.
    5. Sarah Djebali & Carrie A. Davis & Angelika Merkel & Alex Dobin & Timo Lassmann & Ali Mortazavi & Andrea Tanzer & Julien Lagarde & Wei Lin & Felix Schlesinger & Chenghai Xue & Georgi K. Marinov & Jaina, 2012. "Landscape of transcription in human cells," Nature, Nature, vol. 489(7414), pages 101-108, September.
    6. Matthew J Hangauer & Ian W Vaughn & Michael T McManus, 2013. "Pervasive Transcription of the Human Genome Produces Thousands of Previously Unidentified Long Intergenic Noncoding RNAs," PLOS Genetics, Public Library of Science, vol. 9(6), pages 1-13, June.
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