Despite the known critical regulatory functions of microRNAs, histone modifications, and DNA methylation in reprograming plant epigenomes in response to pathogen infection, the molecular mechanisms underlying the tight coordination of these components remain poorly understood. Here, we show how Arabidopsis (Arabidopsis thaliana) miR778 coordinately modulates the root transcriptome, histone methylation, and DNA methylation via post-transcriptional regulation of the H3K9 methyltransferases SU(var)3-9 homolog 5 (SUVH5) and SUVH6 upon infection by the beet cyst nematode Heterodera schachtii. miR778 post-transcriptionally silences SUVH5 and SUVH6 upon nematode infection. Manipulation of the expression of miR778 and its two target genes significantly altered plant susceptibility to H. schachtii. RNA-seq analysis revealed a key role of SUVH5 and SUVH6 in reprograming the transcriptome of Arabidopsis roots upon H. schachtii infection. In addition, chromatin immunoprecipitation (ChIP)-seq analysis established SUVH5 and SUVH6 as the main enzymes mediating H3K9me2 deposition in Arabidopsis roots in response to nematode infection. ChIP-seq analysis also showed that these methyltransferases possess distinct DNA binding preferences in that they are targeting transposable elements under noninfected conditions and protein-coding genes in infected plants. Further analyses indicated that H3K9me2 deposition directed by SUVH5 and SUVH6 contributes to gene expression changes both in roots and in nematode feeding sites and preferentially associates with CG DNA methylation. Together, our results uncovered multi-layered epigenetic regulatory mechanisms coordinated by miR778 during Arabidopsis-H. schachtii interactions.

中文翻译：

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miR778 在胞囊线虫寄生过程中介导基因表达、组蛋白修饰和 DNA 甲基化。

尽管 microRNA、组蛋白修饰和 DNA 甲基化在重编程植物表观基因组以响应病原体感染方面具有已知的关键调节功能，但这些成分紧密协调的分子机制仍然知之甚少。在这里，我们展示了拟南芥 (Arabidopsis thaliana) miR778 如何通过 H3K9 甲基转移酶 SU(var)3-9 同系物 5 (SUVH5) 和 SUVH6 的转录后调节在被甜菜胞囊线虫 Heterodera schachtii。线虫感染后，miR778 转录后沉默 SUVH5 和 SUVH6。操纵 miR778 及其两个靶基因的表达可显着改变植物对 H. schachtii 的易感性。RNA-seq 分析揭示了 SUVH5 和 SUVH6 在 H. schachtii 感染后重编程拟南芥根转录组中的关键作用。此外，染色质免疫沉淀 (ChIP)-seq 分析确定 SUVH5 和 SUVH6 是介导拟南芥根中 H3K9me2 沉积以响应线虫感染的主要酶。ChIP-seq 分析还表明，这些甲基转移酶具有不同的 DNA 结合偏好，因为它们在非感染条件下靶向转座因子和感染植物中的蛋白质编码基因。进一步分析表明，由 SUVH5 和 SUVH6 引导的 H3K9me2 沉积有助于根部和线虫摄食部位的基因表达变化，并优先与 CG DNA 甲基化相关。一起，我们的结果揭示了在拟南芥-H 期间由 miR778 协调的多层表观遗传调控机制。schachtii 相互作用。