Seminars

CRISPR targeting of H3K4me3 Reprograms Transcription, Immunity, and Meiotic
Recombination in Plants
Plants can develop a form of molecular memory through repeated exposure to specific stresses,
allowing them to respond more effectively upon subsequent challenges, a process known as
priming. Primed genes have an enhanced transcriptional responsiveness upon repeated exposure
to stress, while returning to baseline levels of expression in the absence of stimuli. These genes
are thought to remain in ‘primed’ or ‘poised’ state, with an altered chromatin landscape that
facilitates hyper-induction upon a recurrent stress event. We aim to synthetically recreate the
pathogen-primed state in Arabidopsis thaliana by targeted deposition of H3K4me3. To achieve
this, we employ the CRISPR-based SunTag system to recruit the catalytic domain of SDG2, a key
histone methyltransferase responsible for H3K4me3 deposition in plants, to targeted promoters.
Our work shows that H3K4me3 deposition by SunTag-SDG2 is sufficient to transcriptionally
activate the epigenetically silenced gene FWA, establishing that H3K4me3 itself can act as a causal
regulatory mark. Next we demonstrate that SunTag-SDG2 can be employed to increase pathogen
resistance by targeting the H3K4me3-regulated disease resistance gene, SNC1. Extending this
approach to pathogen memory, we show that SunTag-directed H3K4me3 deposition can
successfully prime a WRKY-family transcription factor, further enhancing pathogen resistance.
Beyond transcriptional regulation, targeting SunTag-SDG2 to low recombining centromeric
regions significantly increases proximal crossover formation. Together, these findings establish
that locus-specific H3K4me3 deposition is able to modulate transcription, immunity, stress
memory and recombination, highlighting the potential of chromatin engineering as a tool for
precise modulation of important agricultural traits