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DNA methyltransferase CHROMOMETHYLASE3 prevents ONSEN transposon silencing under heat stress

文献类型： 外文期刊

作者： Nozawa, Kosuke 1 ; Chen, Jiani 2 ; Jiang, Jianjun 2 ; Leichter, Sarah M. 2 ; Yamada, Masataka 1 ; Suzuki, Takamasa; 1 ;

作者机构： 1.Hokkaido Univ, Grad Sch Life Sci, Kita Ku, Kita10 Nishi8, Sapporo, Hokkaido, Japan

2.Univ Wisconsin, Wisconsin Inst Discovery, Madison, WI USA

3.Univ Wisconsin, Lab Genet, Madison, WI USA

4.Inst Plant Protect, Jiangsu Acad Agr Sci, Nanjing, Peoples R China

5.Chubu Univ, Coll Biosci & Biotechnol, 1200 Matsumoto Cho, Kasugai, Aichi, Japan

6.Hokkaido Univ, Fac Sci, Kita Ku, Kita10 Nishi8, Sapporo, Hokkaido, Japan

期刊名称：PLOS GENETICS （ 影响因子：5.917； 五年影响因子：6.284 ）

ISSN： 1553-7404

年卷期： 2021 年 17 卷 8 期

页码：

收录情况： SCI

摘要： 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. Author summary DNA methylation is generally known to silence transposon and maintain genome integrity. Environmental stress has been reported to release the transcriptional silencing of some transposable elements. DNA methylation is involved in the transcriptional restriction of heat-induced Copia-type retrotransposon ONSEN in Arabidopsis when subjected to heat stress. Here, we identified a non-canonical and positive role of the DNA methyltransferase CMT3 in ONSEN reactivation under heat stress. We showed that CMT3 prevents CMT2-mediated CHH methylation and H3K9me2 accumulation under heat at ONSEN chromatin to modulate ONSEN transcription. Our work revealed the molecular mechanism of CMT3 in heat-induced ONSEN activation and sheds new light on the survival mechanism of certain transposons in the host genome under stress conditions.

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