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A-MYB and BRDT-dependent RNA Polymerase II pause release orchestrates transcriptional regulation in mammalian meiosis

Author

Listed:
  • Adriana K. Alexander

    (Cornell University
    Cornell University)

  • Edward J. Rice

    (Cornell University)

  • Jelena Lujic

    (Cornell University)

  • Leah E. Simon

    (Cornell University)

  • Stephanie Tanis

    (Cornell University)

  • Gilad Barshad

    (Cornell University)

  • Lina Zhu

    (Cornell University)

  • Jyoti Lama

    (Cornell University)

  • Paula E. Cohen

    (Cornell University
    Cornell University)

  • Charles G. Danko

    (Cornell University
    Cornell University
    Cornell University)

Abstract

During meiotic prophase I, spermatocytes must balance transcriptional activation with homologous recombination and chromosome synapsis, biological processes requiring extensive changes to chromatin state. We explored the interplay between chromatin accessibility and transcription through prophase I of mammalian meiosis by measuring genome-wide patterns of chromatin accessibility, nascent transcription, and processed mRNA. We find that Pol II is loaded on chromatin and maintained in a paused state early during prophase I. In later stages, paused Pol II is released in a coordinated transcriptional burst mediated by the transcription factors A-MYB and BRDT, resulting in ~3-fold increase in transcription. Transcriptional activity is temporally and spatially segregated from key steps of meiotic recombination: double strand breaks show evidence of chromatin accessibility earlier during prophase I and at distinct loci from those undergoing transcriptional activation, despite shared chromatin marks. Our findings reveal mechanisms underlying chromatin specialization in either transcription or recombination in meiotic cells.

Suggested Citation

  • Adriana K. Alexander & Edward J. Rice & Jelena Lujic & Leah E. Simon & Stephanie Tanis & Gilad Barshad & Lina Zhu & Jyoti Lama & Paula E. Cohen & Charles G. Danko, 2023. "A-MYB and BRDT-dependent RNA Polymerase II pause release orchestrates transcriptional regulation in mammalian meiosis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37408-w
    DOI: 10.1038/s41467-023-37408-w
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    References listed on IDEAS

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    1. Alexander Widger & Shantha K. Mahadevaiah & Julian Lange & Elias ElInati & Jasmin Zohren & Takayuki Hirota & Sarai Pacheco & Andros Maldonado-Linares & Marcello Stanzione & Obah Ojarikre & Valdone Mac, 2018. "ATR is a multifunctional regulator of male mouse meiosis," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Kevin Brick & Fatima Smagulova & Pavel Khil & R. Daniel Camerini-Otero & Galina V. Petukhova, 2012. "Genetic recombination is directed away from functional genomic elements in mice," Nature, Nature, vol. 485(7400), pages 642-645, May.
    3. Wu Zuo & Guangming Chen & Zhimei Gao & Shuai Li & Yanyan Chen & Chenhui Huang & Juan Chen & Zhengjun Chen & Ming Lei & Qian Bian, 2021. "Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
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    Cited by:

    1. Emily G. Kaye & Kavyashree Basavaraju & Geoffrey M. Nelson & Helena D. Zomer & Debarun Roy & Irene Infancy Joseph & Reza Rajabi-Toustani & Huanyu Qiao & Karen Adelman & Prabhakara P. Reddi, 2024. "RNA polymerase II pausing is essential during spermatogenesis for appropriate gene expression and completion of meiosis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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