An Epigenetic Role for Maternally Inherited piRNAs in Transposon Silencing

Watson School of Biological Sciences, Howard Hughes Medical Institute, Cold Spring Harbor Laboratory (CSHL), 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.
Science (Impact Factor: 33.61). 12/2008; 322(5906):1387-92. DOI: 10.1126/science.1165171
Source: PubMed


In plants and mammals, small RNAs indirectly mediate epigenetic inheritance by specifying cytosine methylation. We found that
small RNAs themselves serve as vectors for epigenetic information. Crosses between Drosophila strains that differ in the presence of a particular transposon can produce sterile progeny, a phenomenon called hybrid dysgenesis.
This phenotype manifests itself only if the transposon is paternally inherited, suggesting maternal transmission of a factor
that maintains fertility. In both P- and I-element–mediated hybrid dysgenesis models, daughters show a markedly different content of Piwi-interacting RNAs (piRNAs)
targeting each element, depending on their parents of origin. Such differences persist from fertilization through adulthood.
This indicates that maternally deposited piRNAs are important for mounting an effective silencing response and that a lack
of maternal piRNA inheritance underlies hybrid dysgenesis.

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    • "The relative levels of putative microRNAs and piRNAs change markedly as development progresses. piRNAs are highly abundant in the earliest stages of development , consistent with their maternal deposition (Brennecke et al. 2008). MicroRNA levels, on the other hand, are initially very low but gradually increase and account for nearly 30% of all small RNA reads in the late embryo. "
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    • "Because these embryos have no fully onset transcription (Vlassova et al. 1991; Pritchard and Schubiger 1996), their small RNAs and Piwi proteins are essentially the same of the maternal germ cells (Harris and Macdonald 2001; Megosh et al. 2006; Brennecke et al. 2008; Le Thomas et al. 2014). A similar scenario was found for D. melanogaster (Brennecke et al. 2008). At early embryogenesis, the maternally inherited piRNAs and piwi proteins could be leading elements in the process of defining heterochromatic domains (Sentmanat et al. 2013). "
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    ABSTRACT: Drosophila INterspersed Elements (DINEs) constitute an abundant but poorly understood group of Helitrons present in several Drosophila species. The general structure of DINEs includes two conserved blocks that may or not contain a region with tandem repeats in between. These central tandem repeats (CTRs) are similar within species but highly divergent between species. It has been assumed that CTRs have independent origins. Herein, we identify a subset of DINEs, termed DINE-TR1, which contain homologous CTRs of approximately 150 bp. We found DINE-TR1 in the sequenced genomes of several Drosophila species and in Bactrocera tryoni (Acalyptratae, Diptera). However, interspecific high sequence identity (∼88 %) is limited to the first ∼30 bp of each tandem repeat, implying that evolutionary constraints operate differently over the monomer length. DINE-TR1 is unevenly distributed across the Drosophila phylogeny. Nevertheless, sequence analysis suggests vertical transmission. We found that CTRs within DINE-DINE-TR1 have independently expanded into satellite DNA-like arrays at least twice within Drosophila. By analyzing the genome of Drosophila virilis and Drosophila americana, we show that DINE-TR1 is highly abundant in pericentromeric heterochromatin boundaries, some telomeric regions and in the Y chromosome. It is also present in the centromeric region of one autosome from D. virilis and dispersed throughout several euchromatic sites in both species. We further found that DINE-TR1 is abundant at piRNA clusters, and small DINE-TR1-derived RNA transcripts (∼25 nt) are predominantly expressed in the testes and the ovaries, suggesting active targeting by the piRNA machinery. These features suggest potential piRNA-mediated regulatory roles for DINEs at local and genomewide scales in Drosophila.
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    • "et al., 2013; Siomi et al., 2011). In this view, Aub-bound, maternally deposited antisense piRNAs must initiate ping-pong amplification, leading to the accumulation of Ago3-bound sense piRNAs (Brennecke et al., 2008; Le Thomas et al., 2014). Pingpong amplification of Ago3-bound piRNAs would then serve to ensure a sufficient supply of guides for Piwi. "
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