Reproductive Long Intergenic Noncoding RNAs Exhibit Male Gamete Specificity and Polycomb Repressive Complex 2-Mediated Repression

Reproductive Long Intergenic Noncoding RNAs Exhibit Male Gamete Specificity and Polycomb Repressive Complex 2-Mediated Repression
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DOI:
10.1104/pp.17.01269
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发表时间:
2018-07-01
期刊:
影响因子:
7.4
通讯作者:
Sundaresan, Venkatesan
Sundaresan, Venkatesan
中科院分区:
生物学1区
文献类型:
--
作者:
Johnson, Cameron;Conrad, Liza J.;Sundaresan, Venkatesan

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长链非编码RNA(lncRNA)在动物中广泛存在,并参与多种过程,包括同源异型盒基因表达和X染色体失活。相比之下,植物lncRNA的详细表征要少得多,并且植物基因组中编码的不同lncRNA的数量及其通过发育和表观遗传机制的调节在很大程度上仍然未知。在这里,我们分析了来自亚洲水稻(Oryza sativa)的转录组数据,并确定了6,309个长基因间非编码RNA(lincRNA),重点是它们在生殖组织和器官中的表达。大多数O.苜蓿lincRNA以高度组织特异性的方式表达,在雄性配子中特异性表达的比例出乎意料地高。Polycomb抑制复合物2(PRC2)的组分的突变导致另一大类lincRNA的去抑制,其表达与发育中的圆锥花序中的H3K27三甲基化相关。与精细胞特异性lincRNA的重叠表明,圆锥花序中lincRNA的表观遗传抑制在雄性生殖系中部分缓解。lincRNA的一个子集的表达也显示出在生殖组织中受干旱的调节。与其他谷物基因组的比较表明,lincRNA通常在序列和结构水平上具有低水平的保守性。新奇检测支持向量机模型的使用使得能够分别检测紫色假雀麦(Brachypodium distachyon)和玉米(Zea mays)基因组中类似于10%和类似于4%的lincRNA的核苷酸序列和结构同源性。这是第一项报告大量lncRNA的研究,这些lncRNA是PRC2抑制的靶点,而不是通过PRC2介导调控。这里报道的绝大多数lincRNA与其他水稻研究的lincRNA不重叠,这表明这些是对水稻中已知lincRNA的重要补充。
Long noncoding RNAs (lncRNAs) have been characterized extensively in animals and are involved in several processes, including homeobox gene expression and X-chromosome inactivation. In comparison, there has been much less detailed characterization of plant lncRNAs, and the number of distinct lncRNAs encoded in plant genomes and their regulation by developmental and epigenetic mechanisms remain largely unknown. Here, we analyzed transcriptome data from Asian rice (Oryza sativa) and identified 6,309 long intergenic noncoding RNAs (lincRNAs), focusing on their expression in reproductive tissues and organs. Most O. sativa lincRNAs were expressed in a highly tissue-specific manner, with an unexpectedly high fraction specifically expressed in male gametes. Mutation of a component of the Polycomb Repressive Complex2 (PRC2) resulted in derepression of another large class of lincRNAs, whose expression is correlated with H3K27 trimethylation in developing panicles. Overlap with the sperm cell-specific lincRNAs suggests that epigenetic repression of lincRNAs in the panicles was partially relieved in the male germline. Expression of a subset of lincRNAs also showed modulation by drought in reproductive tissues. Comparison with other cereal genomes showed that the lincRNAs generally have low levels of conservation at both the sequence and structural levels. Use of a novelty detection support vector machine model enabled the detection of nucleotide sequence and structural homology in similar to 10% and similar to 4% of the lincRNAs in genomes of purple false brome (Brachypodium distachyon) and maize (Zea mays), respectively. This is the first study to report on a large number of lncRNAs that are targets of repression by PRC2 rather than mediating regulation via PRC2. That the vast majority of the lincRNAs reported here do not overlap with those of other rice studies indicates that these are a significant addition to the known lincRNAs in rice.