Transgenerational function of Tetrahymena Piwi protein Twi8p at distinctive noncoding RNA loci
Transgenerational function of Tetrahymena Piwi protein Twi8p at distinctive noncoding RNA loci
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DOI：
10.1261/rna.060012.116
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发表时间：
2017-04-01
期刊：
影响因子：
4.5
通讯作者：
Collins, Kathleen
中科院分区：
文献类型：
--
作者：
Farley, Brian M.;Collins, Kathleen
基因组调控表观遗传信息的跨代传递可以决定有性繁殖后代的表型。跨代调控的序列特异性来自组装成Piwi-蛋白质复合体的小RNA。已知的跨代调控的目标主要是转座子和转座子衍生的序列。在这里，我们扩大了Piwi介导的跨代调节的范围，包括独特的非编码RNA基因座。纤毛虫如四膜虫具有典型的沉默的种系微核和表达的体细胞大核，这在有性繁殖中与种系的基因组拷贝有新的区别。我们发现核定位的四膜虫蛋白Twi8p从亲本穿梭到合子大核。Twi8p的基因消除对处于无性生长状态的细胞没有表型。另一方面，缺乏Twi8p的细胞在有性繁殖中被阻止，合子核保留了生殖系基因组结构，没有产生功能大核所需的DNA消除和碎裂。Twi8p结合的小RNA来自具有末端发夹的长非编码RNA，在没有Twi8p的情况下可以检测到。奇怪的是，产生Twi8p结合的小RNA的基因座对于无性细胞的生长是必不可少的，尽管Twi8RNP只在有性繁殖中是必不可少的。我们的发现表明，Twi8RNPs作用于沉默的生殖系染色体，允许它们转化为表达的大核染色体的模型。总体而言，这项工作揭示了携带来自长非编码RNA基因座的小RNA的Piwi蛋白在建立合子核基因表达能力方面具有跨代功能。
Transgenerational transmission of genome-regulatory epigenetic information can determine phenotypes in the progeny of sexual reproduction. Sequence specificity of transgenerational regulation derives from small RNAs assembled into Piwi-protein complexes. Known targets of transgenerational regulation are primarily transposons and transposon-derived sequences. Here, we extend the scope of Piwi-mediated transgenerational regulation to include unique noncoding RNA loci. Ciliates such as Tetrahymena have a phenotypically silent germline micronucleus and an expressed somatic macronucleus, which is differentiated anew from a germline genome copy in sexual reproduction. We show that the nuclear-localized Tetrahymena Piwi protein Twi8p shuttles from parental to zygotic macronuclei. Genetic elimination of Twi8p has no phenotype for cells in asexual growth. On the other hand, cells lacking Twi8p arrest in sexual reproduction with zygotic nuclei that retain the germline genome structure, without the DNA elimination and fragmentation required to generate a functional macronucleus. Twi8p-bound small RNAs originate from long-noncoding RNAs with a terminal hairpin, which become detectable in the absence of Twi8p. Curiously, the loci that generate Twi8p-bound small RNAs are essential for asexual cell growth, even though Twi8 RNPs are essential only in sexual reproduction. Our findings suggest the model that Twi8 RNPs act on silent germline chromosomes to permit their conversion to expressed macronuclear chromosomes. Overall this work reveals that a Piwi protein carrying small RNAs from long-noncoding RNA loci has transgenerational function in establishing zygotic nucleus competence for gene expression.