Maternally inherited siRNAs initiate piRNA cluster formation

Luo, Yicheng; He, Peng; Kanrar, Nivedita; Fejes Toth, Katalin; Aravin, Alexei A.

doi:10.1016/j.molcel.2023.09.033

Cited by 12 publications

(8 citation statements)

References 122 publications

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“…RNAi might contribute to reducing transposon transcripts during oogenesis, although it is unable to completely silence these elements 46 . It was recently shown that maternally provided siRNAs loaded in the developing eggs promote piRNA cluster activation in the Drosophila embryo 52 . Unlike Drosophila, Rhodnius does not produce abundant piRNAs during oogenesis.…”

Section: Discussionmentioning

confidence: 99%

“Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs”

Brito,

Cardoso,

Atinbayeva

et al. 2024

Preprint

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Piwi proteins and the associated Piwi-interacting RNAs (piRNAs) coordinate a surveillance system that protects the animal genome from DNA damage induced by transposable element (TE) mobilization. Here, we investigated the adaptation of the piRNA pathway to horizontally transferred transposons (HTTs) in the assassin bug Rhodnius prolixus, a primary vector of Chagas disease. Rhodnius acquired specific classes of HTTs by feeding on bats, opossums and squirrel monkeys. By analyzing the temporal dynamics of piRNA cluster expression and piRNA production during critical stages of Rhodnius development, we show that peak levels of ~28 nt long piRNAs correlate with reduced HTT and resident TE expression primarily during embryogenesis. Strikingly, while resident TEs piRNAs seem to engage in a typical ping-pong amplification mechanism, sense and antisense HTT piRNAs instead overlap by ~20 nt or do not display ping-pong signatures. These features are explained at least in part by the low number of HTT copies inserted into the piRNA clusters and might point to a non-canonical mechanism of biogenesis. Our data reveal that the piRNA, but not the siRNA pathway, responded to HTTs that were recently transferred from vertebrate tetrapods to a hematophagous insect of medical relevance.

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Section: Discussionmentioning

confidence: 99%

“Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs”

Brito,

Cardoso,

Atinbayeva

et al. 2024

Preprint

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“…Maternally inherited siRNAs initiate piRNA biogenesis from a transgene inserted into the uni-strand piRNA cluster 20A 14 . In this previous report, evidence was presented that siRNAs induce “ de novo” Rhino loading onto this transgene (20A-X) via H3K9me3.…”

Section: Discussionmentioning

confidence: 99%

“…These clusters are occupied with the repressive histone mark H3K9me3 and lack typical promoters, but are transcribed in both directions from the internal sites 6,7 . This unconventional transcription requires special factors, including heterochromatin protein 1 (HP1) homolog HP1d/Rhino (Rhino), and provides piRNA precursors with a variety of sequences, which are then processed to mature piRNAs in the cytoplasm 5,6,7,8,9,10,11,12,13,14 . The mechanism dedicated to this piRNA processing is known as the ping-pong cycle, where Aubergine and Argonaute 3 cleave the precursors in a manner dependent on the sequences of piRNAs already bound to them 1,2,3 .…”

Section: Introductionmentioning

confidence: 99%

“…Like other HP1 family members, Rhino has a chromodomain through which it binds to H3K9me3 scattered on dual-strand piRNA clusters 6,8,9,12,13,14,15,16 . Deadlock and Cutoff then join Rhino, assembling the Rhino−Deadlock−Cutoff (RDC) complex, which further recruits the transcription factor IIA-L (TFIIA-L) paralogue Moonshiner, the transcription factor IIA-S (TFIIA-S), and the animal TATA-box-binding protein (TBP) paralog TRF2, initiating transcription of the clusters 6,7,10 .…”

Section: Introductionmentioning

confidence: 99%

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ADMA-histones define genomic loading of Rhino at the initial step of piRNA cluster formation

Saito,

Ishizu,

Harigai

et al. 2024

Preprint

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In Drosophila germ cells, piRNAs arise from dual-strand piRNA clusters. These clusters are occupied by H3K9me3, but are transcribed from internal sites in a manner dependent on the binding of HP1 homolog Rhino to H3K9me3 on the clusters. However, how initial loading of Rhino onto the clusters occurs remains unknown. Here, we used cultured ovarian somatic cells (OSCs), which lack endogenous Rhino and Rhino stabilizer Kipferl, the absence of which renders the dual-strand clusters inert, and found that exogenous Rhino tends to bind to the ends of dual-strand clusters with asymmetric dimethylarginine histones (ADMA-histones). Depletion of the arginine methyltransferases responsible for ADMA modification affected the genomic localization of Rhino in OSCs and in the ovary. We also identified genomic regions, termed INSECTs, where ADMA-dependent Rhino propagation begins. We propose that ADMA-histones define the initial genomic loading of Rhino and stabilize Rhino-genome association during cluster formation.

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“…Although the Drosophila oocyte is mainly inactive in transcription, it gains massive maternal contribution of proteins and RNAs from the surrounding nurse cells, including the Piwi/piRNA complexes [130][131][132][133][134]. Furthermore, biochemical communication is required between the cytoplasmic AGO3 and AUB and the nuclear PIWI to promote piRNA amplification and facilitating this maternal contribution from nurse cells to oocytes [124,135].…”

Section: Nuclear Versus Cytoplasmic Piwi-pirna Complexes: What Do Mos...mentioning

confidence: 99%

Transposon and Transgene Tribulations in Mosquitoes: A Perspective of piRNA Proportions

Lau,

Macias

2024

DNA

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Mosquitoes, like Drosophila, are dipterans, the order of “true flies” characterized by a single set of two wings. Drosophila are prime model organisms for biomedical research, while mosquito researchers struggle to establish robust molecular biology in these that are arguably the most dangerous vectors of human pathogens. Both insects utilize the RNA interference (RNAi) pathway to generate small RNAs to silence transposons and viruses, yet details are emerging that several RNAi features are unique to each insect family, such as how culicine mosquitoes have evolved extreme genomic feature differences connected to their unique RNAi features. A major technical difference in the molecular genetic studies of these insects is that generating stable transgenic animals are routine in Drosophila but still variable in stability in mosquitoes, despite genomic DNA-editing advances. By comparing and contrasting the differences in the RNAi pathways of Drosophila and mosquitoes, in this review we propose a hypothesis that transgene DNAs are possibly more intensely targeted by mosquito RNAi pathways and chromatin regulatory pathways than in Drosophila. We review the latest findings on mosquito RNAi pathways, which are still much less well understood than in Drosophila, and we speculate that deeper study into how mosquitoes modulate transposons and viruses with Piwi-interacting RNAs (piRNAs) will yield clues to improving transgene DNA expression stability in transgenic mosquitoes.

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Maternally inherited siRNAs initiate piRNA cluster formation

Cited by 12 publications

References 122 publications

“Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs”

“Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs”

ADMA-histones define genomic loading of Rhino at the initial step of piRNA cluster formation

Transposon and Transgene Tribulations in Mosquitoes: A Perspective of piRNA Proportions

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