Abstract
DNA methylation plays crucial roles in transposon silencing and genome integrity. CHROMOMETHYLASE3 (CMT3) is a plant-specific DNA methyltransferase responsible for catalyzing DNA methylation at the CHG (H = A, T, C) context. Here, we identified a positive role of CMT3 in heat-induced activation of retrotransposon ONSEN. We found that the full transcription of ONSEN under heat stress requires CMT3. Interestingly, loss-of-function CMT3 mutation led to increased CHH methylation at ONSEN. The CHH methylation is mediated by CMT2, as evidenced by greatly reduced CHH methylation in cmt2 and cmt2 cmt3 mutants coupled with increased ONSEN transcription. Furthermore, we found more CMT2 binding at ONSEN chromatin in cmt3 compared to wild-type accompanied with an ectopic accumulation of H3K9me2 under heat stress, suggesting a collaborative role of H3K9me2 and CHH methylation in preventing heat-induced ONSEN activation. In summary, this study identifies a non-canonical role of CMT3 in preventing transposon silencing and provides new insights into how DNA methyltransferases regulate transcription under stress conditions.
Highlights
DNA methylation is vital for silencing of repetitive sequences and transposable elements (TEs) to ensure genome stability and integrity [1]
DNA methylation is involved in the transcriptional restriction of heat-induced Copia-type retrotransposon ONSEN in Arabidopsis when subjected to heat stress
We have previously shown that heat stress activates ONSEN transcription, and the heat– induced ONSEN transcripts are further accumulated in mutants impaired in the small interfering RNA (siRNA) biogenesis pathway [12]
Summary
DNA methylation is vital for silencing of repetitive sequences and transposable elements (TEs) to ensure genome stability and integrity [1]. In Arabidopsis thaliana, the de novo DNA methylation is mediated by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) through the RNA-directed DNA methylation (RdDM) pathway. This process involves the biogenesis of small interfering RNA (siRNA) and the recruitment of DRM2 to target DNA sequences for methylation [2]. CMT3 tends to methylate CHG at large TEs and leads to the transcriptional repression of these TEs [4,6]. DRM2 maintains CHH methylation at short TEs, the border of large TEs, and other repeat sequences in euchromatic regions [2,7]
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