CRISPR targeting of H3K4me3 activates gene expression and unlocks centromere-proximal crossover recombination in Arabidopsis

Jenia Binenbaum, Vanda Adamkova, Hannah Fryer, Linhao Xu, Nicola Gorringe, Piotr Włodzimierz, Robin Burns, Ashot Papikian, Steven E. Jacobsen, Ian R. Henderson and C. Jake Harris ()
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Jenia Binenbaum: University of Cambridge
Vanda Adamkova: University of Cambridge
Hannah Fryer: University of Cambridge
Linhao Xu: University of Cambridge
Nicola Gorringe: University of Cambridge
Piotr Włodzimierz: University of Cambridge
Robin Burns: University of Cambridge
Ashot Papikian: University of California
Steven E. Jacobsen: University of California
Ian R. Henderson: University of Cambridge
C. Jake Harris: University of Cambridge

Nature Communications, 2025, vol. 16, issue 1, 1-13

Abstract: Abstract H3K4me3 is a fundamental and highly conserved chromatin mark across eukaryotes, playing a central role in many genome-related processes, including transcription, maintenance of cell identity, DNA damage repair, and meiotic recombination. However, identifying the causal function of H3K4me3 in these diverse pathways remains a challenge, and we lack the tools to manipulate it for agricultural benefit. Here we use the CRISPR-based SunTag system to direct H3K4me3 methyltransferases in the model plant, Arabidopsis thaliana. Targeting of SunTag-SDG2 activates the expression of the endogenous reporter gene, FWA. We show that SunTag-SDG2 can be employed to increase pathogen resistance by targeting the H3K4me3-dependent disease resistance gene, SNC1. Meiotic crossover recombination rates impose a limit on the speed with which new traits can be transferred to elite crop varieties. We demonstrate that targeting of SunTag-SDG2 to low recombining centromeric regions can significantly stimulate proximal crossover formation. Finally, we reveal that the effect is not specific to SDG2 and is likely dependent on the H3K4me3 mark itself, as the orthogonal mammalian-derived H3K4me3 methyltransferase, PRDM9, produces a similar effect on gene expression with reduced off-target potential. Overall, our study supports an instructive role for H3K4me3 in transcription and meiotic recombination and opens the door to precise modulation of important agricultural traits.

Date: 2025
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DOI: 10.1038/s41467-025-65167-3

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