DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm

DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm
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DOI:
10.1073/pnas.1821435116
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发表时间:
2019-05-07
影响因子:
11.1
通讯作者:
Fischer, Robert L.
Fischer, Robert L.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Kim, M. Yvonne;Ono, Akemi;Fischer, Robert L.

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在真核生物中,表观遗传重新编程是正确调控基因表达所必需的。在拟南芥中,活跃的DNA去甲基化对种子活力、花粉功能和成功繁殖至关重要。Demeter(DME)DNA糖基酶在营养细胞和中央细胞启动DNA去甲基化,营养细胞和中央细胞分别与精子和卵配子相邻的所谓伴生细胞。在水稻中,中央细胞基因组显示出局部的DNA低甲基化,这表明水稻中也存在活跃的DNA去甲基化;然而,负责这一过程的酶尚不清楚。一个候选基因是水稻沉默1a(ROS1a)基因,该基因与DME相关,对水稻种子活力和花粉功能是必需的。在这里,我们报告了对野生型和ros1a突变精子和营养细胞中DNA甲基化的全基因组分析。我们发现,与精子相比,水稻营养细胞基因组的局部低甲基化是通过需要ROS1a活性的过程进行的。我们发现,营养细胞中的许多ROS1a靶序列在水稻中央细胞中处于低甲基化状态,这表明ROS1a也使中央细胞基因组去甲基化。与拟南芥相似,我们发现在营养细胞中精子的非CG甲基化是通过DNA去甲基化间接促进的。这些结果表明,DNA糖基酶介导的DNA去甲基化过程在拟南芥和水稻中是保守的,这两个物种在1.5亿年前就出现了分歧。最后,尽管精子和卵子的全球非CG甲基化水平不同,但母体和父本胚胎基因组显示出相似的非CG甲基化水平,这表明水稻配子基因组在细胞融合后经历了动态DNA甲基化重编程。
Epigenetic reprogramming is required for proper regulation of gene expression in eukaryotic organisms. In Arabidopsis, active DNA demethylation is crucial for seed viability, pollen function, and successful reproduction. The DEMETER (DME) DNA glycosylase initiates localized DNA demethylation in vegetative and central cells, so-called companion cells that are adjacent to sperm and egg gametes, respectively. In rice, the central cell genome displays local DNA hypomethylation, suggesting that active DNA demethylation also occurs in rice; however, the enzyme responsible for this process is unknown. One candidate is the rice REPRESSOR OF SILENCING 1a (ROS1a) gene, which is related to DME and is essential for rice seed viability and pollen function. Here, we report genome-wide analyses of DNA methylation in wild-type and ros1a mutant sperm and vegetative cells. We find that the rice vegetative cell genome is locally hypomethylated compared with sperm by a process that requires ROS1a activity. We show that many ROS1a target sequences in the vegetative cell are hypomethylated in the rice central cell, suggesting that ROS1a also demethylates the central cell genome. Similar to Arabidopsis, we show that sperm non-CG methylation is indirectly promoted by DNA demethylation in the vegetative cell. These results reveal that DNA glycosylase-mediated DNA demethylation processes are conserved in Arabidopsis and rice, plant species that diverged 150 million years ago. Finally, although global non-CG methylation levels of sperm and egg differ, the maternal and paternal embryo genomes show similar non-CG methylation levels, suggesting that rice gamete genomes undergo dynamic DNA methylation reprogramming after cell fusion.