Modeling early germline immunization after horizontal transfer of transposable elements reveals internal piRNA cluster heterogeneity

BMC Biology

Research Article

Laure Teysset¹  Elise Viodé¹  Amna Asif-Laidin¹  Zoheir Ziriat¹  Valérie Delmarre¹  Antoine Boivin¹  Stéphane Ronsseray¹  Clément Carré¹  Karine Casier² 

[1] Sorbonne Université, CNRS, Institut de Biologie Paris-Seine, Laboratoire Biologie du Développement, UMR7622, “Transgenerational Epigenetics & Small RNA Biology”, F-75005, Paris, France;Sorbonne Université, CNRS, Institut de Biologie Paris-Seine, Laboratoire Biologie du Développement, UMR7622, “Transgenerational Epigenetics & Small RNA Biology”, F-75005, Paris, France;Present Address: CNRS, Institut de Biologie Physico-Chimique, Laboratoire de Biologie Moléculaire et Cellulaire des Eucaryotes, UMR8226, Telomere Biology, F-75005, Paris, France;

关键词: Transposable elements;    piRNA clusters;    PIWI-interacting RNA;    Subtelomeres;    Drosophila;    Horizontal transfer;    Transgenerational inheritance;   

DOI  :  10.1186/s12915-023-01616-z

 received in 2022-11-17, accepted in 2023-05-05,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundA fraction of all genomes is composed of transposable elements (TEs) whose mobility needs to be carefully controlled. In gonads, TE activity is repressed by PIWI-interacting RNAs (piRNAs), a class of small RNAs synthesized by heterochromatic loci enriched in TE fragments, called piRNA clusters. Maintenance of active piRNA clusters across generations is secured by maternal piRNA inheritance providing the memory for TE repression. On rare occasions, genomes encounter horizontal transfer (HT) of new TEs with no piRNA targeting them, threatening the host genome integrity. Naïve genomes can eventually start to produce new piRNAs against these genomic invaders, but the timing of their emergence remains elusive.ResultsUsing a set of TE-derived transgenes inserted in different germline piRNA clusters and functional assays, we have modeled a TE HT in Drosophila melanogaster. We have found that the complete co-option of these transgenes by a germline piRNA cluster can occur within four generations associated with the production of new piRNAs all along the transgenes and the germline silencing of piRNA sensors. Synthesis of new transgenic TE piRNAs is linked to piRNA cluster transcription dependent on Moonshiner and heterochromatin mark deposition that propagates more efficiently on short sequences. Moreover, we found that sequences located within piRNA clusters can have different piRNA profiles and can influence transcript accumulation of nearby sequences.ConclusionsOur study reveals that genetic and epigenetic properties, such as transcription, piRNA profiles, heterochromatin, and conversion efficiency along piRNA clusters, could be heterogeneous depending on the sequences that compose them. These findings suggest that the capacity of transcriptional signal erasure induced by the chromatin complex specific of the piRNA cluster can be incomplete through the piRNA cluster loci. Finally, these results have revealed an unexpected level of complexity that highlights a new magnitude of piRNA cluster plasticity fundamental for the maintenance of genome integrity.

【 授权许可】

CC BY   
© The Author(s) 2023

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