Ectopic enhancer-enhancer interactions as causal forces driving RNA-directed DNA methylation in gene regulatory regions

文献类型： 外文期刊

第一作者： Yang, Yazhou

作者： Yang, Yazhou;Wang, Xiping;Liu, Jia;Singer, Stacy D.;Yan, Guohua;Bennet, Dennis R.;Liu, Zongrang;Liu, Yue;Hily, Jean-Michel;Xu, Weirong;Yang, Yingzhen;Zhong, Gan-Yuan;Liu, Zhongchi;An, Yong-Chiang;Liu, Huawei

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关键词： CRE-CRE interactions; ncRNA transcription; RdDM; de novo methylation; transcriptional silencing; mutant flowers

期刊名称：PLANT BIOTECHNOLOGY JOURNAL （ 影响因子：10.1； 五年影响因子：11.6 ）

ISSN： 1467-7644

年卷期： 2024 年

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收录情况： SCI

摘要： Cis-regulatory elements (CREs) are integral to the spatiotemporal and quantitative expression dynamics of target genes, thus directly influencing phenotypic variation and evolution. However, many of these CREs become highly susceptible to transcriptional silencing when in a transgenic state, particularly when organised as tandem repeats. We investigated the mechanism of this phenomenon and found that three of the six selected flower-specific CREs were prone to transcriptional silencing when in a transgenic context. We determined that this silencing was caused by the ectopic expression of non-coding RNAs (ncRNAs), which were processed into 24-nt small interfering RNAs (siRNAs) that drove RNA-directed DNA methylation (RdDM). Detailed analyses revealed that aberrant ncRNA transcription within the AGAMOUS enhancer (AGe) in a transgenic context was significantly enhanced by an adjacent CaMV35S enhancer (35Se). This particular enhancer is known to mis-activate the regulatory activities of various CREs, including the AGe. Furthermore, an insertion of 35Se approximately 3.5 kb upstream of the AGe in its genomic locus also resulted in the ectopic induction of ncRNA/siRNA production and de novo methylation specifically in the AGe, but not other regions, as well as the production of mutant flowers. This confirmed that interactions between the 35Se and AGe can induce RdDM activity in both genomic and transgenic states. These findings highlight a novel epigenetic role for CRE-CRE interactions in plants, shedding light on the underlying forces driving hypermethylation in transgenes, duplicate genes/enhancers, and repetitive transposons, in which interactions between CREs are inevitable.

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