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An antagonistic epigenetic mechanism regulating gene expression in pollen revealed through single-nucleus multiomics

Author

Listed:
  • Colette L. Picard

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology)

  • Lucia Ichino

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
    University of California Los Angeles, Molecular Biology Institute)

  • Tyler J. Buckley

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
    University of California Los Angeles, Molecular Biology Institute)

  • Brandon A. Boone

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
    University of California Los Angeles, Molecular Biology Institute
    Western Carolina University, Department of Chemistry and Physics)

  • Jaewon Yun

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology)

  • Kevin D. Abuhanna

    (University of California Los Angeles, Department of Human Genetics)

  • Yi Zhang

    (University of California Los Angeles, Department of Human Genetics)

  • Noah J. Behrendt

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology)

  • Su May Lei Soe

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology)

  • Chongyuan Luo

    (University of California Los Angeles, Department of Human Genetics)

  • Steven E. Jacobsen

    (University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
    University of California Los Angeles, Molecular Biology Institute
    UCLA, Howard Hughes Medical Institute (HHMI))

Abstract

Arabidopsis MBD5, MBD6, and MBD7 are CG-specific methyl-readers with opposite functions: MBD5 and MBD6 (MBD5/6) repress methylated loci in pollen vegetative nuclei (VN), while MBD7 prevents transgene silencing, possibly by promoting DNA demethylation. Here we show that loss of MBD7 rescues transcriptional defects at a large subset of MBD5/6-bound loci. Using simultaneous profiling of DNA methylation and transcription in single pollen nuclei, we found that MBD5/6-bound loci that are actively demethylated in immature VN lose additional methylation in mbd5/6, prior to transcriptional derepression. A subset of these loci is also bound by MBD7, correlating with demethylation and transcriptional derepression in mbd5/6 that are both reversed by loss of MBD7. Conversely, ectopically recruiting the MBD7 complex to MBD5/6 targets causes partial demethylation and upregulation. We propose that MBD5/6 maintain silencing in VN in part by preventing the MBD7 complex from enhancing the active demethylation that occurs during VN maturation.

Suggested Citation

  • Colette L. Picard & Lucia Ichino & Tyler J. Buckley & Brandon A. Boone & Jaewon Yun & Kevin D. Abuhanna & Yi Zhang & Noah J. Behrendt & Su May Lei Soe & Chongyuan Luo & Steven E. Jacobsen, 2025. "An antagonistic epigenetic mechanism regulating gene expression in pollen revealed through single-nucleus multiomics," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-65686-z
    DOI: 10.1038/s41467-025-65686-z
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