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

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 and Steven E. Jacobsen ()
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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
Tyler J. Buckley: University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
Brandon A. Boone: University of California Los Angeles, Department of Molecular, Cell and Developmental Biology
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

Nature Communications, 2025, vol. 16, issue 1, 1-19

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-65686-z

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