Division of Biology and Biological Engineering, California Institute of Technology, 1200 E California Blvd, Pasadena, CA, 91125, USA.
Faculty of Biology, Medicine and Health, University of Manchester, Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK.
Genome Biol. 2017 Sep 26;18(1):184. doi: 10.1186/s13059-017-1304-1.
Piwi-interacting RNAs (piRNAs) are a class of short (~26-31-nucleotide) non-protein-coding RNAs expressed in the metazoan germline. The piRNA pathway in arthropods is best understood in the ovary of Drosophila melanogaster, where it acts to silence active transposable elements (TEs). Maternal loading of piRNAs in oocytes is further required for the inheritance of piRNA-mediated transposon defence. However, our understanding of the diversity, evolution and function of the piRNA complement beyond drosophilids is limited. The red flour beetle, Tribolium castaneum, is an emerging model organism separated from Drosophila by ~ 350 million years of evolution that displays a number of features ancestral to arthropods, including short germ embryogenesis. Here, we characterize the maternally deposited and zygotically expressed small RNA and mRNA complements throughout T. castaneum embryogenesis.
We find that beetle oocytes and embryos of all stages are abundant in heterogeneous ~ 28-nucleotide RNAs. These small RNAs originate from discrete genomic loci enriched in TE sequences and display the molecular signatures of transposon-derived piRNAs. In addition to the maternally loaded primary piRNAs, Tribolium embryos produce secondary piRNAs by the cleavage of zygotically activated TE transcripts via the ping-pong mechanism. The two Tribolium piRNA pathway effector proteins, Tc-Piwi/Aub and Tc-Ago3, are also expressed throughout the soma of early embryos.
Our results show that the piRNA pathway in Tribolium is not restricted to the germline, but also operates in the embryo and may act to antagonize zygotically activated transposons. Taken together, these data highlight a functional divergence of the piRNA pathway between insects.
Piwi 相互作用 RNA（piRNA）是一类在后生动物生殖系中表达的短（26-31 个核苷酸）非蛋白编码 RNA。在节肢动物中，piRNA 途径在黑腹果蝇的卵巢中得到了最好的理解，在那里它作用于沉默活跃的转座元件（TE）。piRNA 介导的转座子防御的遗传还需要卵母细胞中 piRNA 的母体加载。然而，我们对果蝇以外的 piRNA 补充的多样性、进化和功能的理解是有限的。红面粉甲虫，Tribolium castaneum，是一种新兴的模式生物，与果蝇分离了3.5 亿年的进化，显示了一些节肢动物祖先的特征，包括短的胚胎发生。在这里，我们描述了 T. castaneum 胚胎发生过程中母体沉积和合子表达的小 RNA 和 mRNA 补充。
我们发现，甲虫卵母细胞和所有阶段的胚胎都富含异质的~28 个核苷酸的 RNA。这些小 RNA 来源于富含 TE 序列的离散基因组位点，并显示出转座子衍生的 piRNA 的分子特征。除了母体加载的初级 piRNA 外，Tribolium 胚胎还通过 ping-pong 机制切割合子激活的 TE 转录物产生次级 piRNA。两种 Tribolium piRNA 途径效应蛋白，Tc-Piwi/Aub 和 Tc-Ago3，也在早期胚胎的体节中表达。
我们的结果表明，Tribolium 的 piRNA 途径不仅限于生殖系，而且也在胚胎中运作，并可能作用于拮抗合子激活的转座子。总的来说，这些数据突出了昆虫之间 piRNA 途径的功能分歧。
