The JIL-1 Kinase Affects Telomere Expression in the Different Telomere Domains of Drosophila

Abstract

In Drosophila, the non-LTR retrotransposons HeT-A, TART and TAHRE build a head-to-tail array of repetitions that constitute the telomere domain by targeted transposition at the end of the chromosome whenever needed. As a consequence, Drosophila telomeres have the peculiarity to harbor the genes in charge of telomere elongation. Understanding telomere expression is important in Drosophila since telomere homeostasis depends in part on the expression of this genomic compartment. We have recently shown that the essential kinase JIL-1 is the first positive regulator of the telomere retrotransposons. JIL-1 mediates chromatin changes at the promoter of the HeT-A retrotransposon that are necessary to obtain wild type levels of expression of these telomere transposons. With the present study, we show how JIL-1 is also needed for the expression of a reporter gene embedded in the telomere domain. Our analysis, using different reporter lines from the telomere and subtelomere domains of different chromosomes, indicates that JIL-1 likely acts protecting the telomere domain from the spreading of repressive chromatin from the adjacent subtelomere domain. Moreover, the analysis of the 4R telomere suggests a slightly different chromatin structure at this telomere. In summary, our results strongly suggest that the action of JIL-1 depends on which telomere domain, which chromosome and which promoter is embedded in the telomere chromatin.

Key role of piRNAs in telomeric chromatin maintenance and telomere nuclear positioning inDrosophilagermline

“…All transgenes were mapped at between 12-23 kb distance from TAS (43). The orange eye colour of EY08176, EY00453 and EY00802 transgenic flies corresponds to the previously reported phenotype and indicates a high level of the mini-white reporter gene expression (43,46). The EY03383 strain carries P{EPgy2} in the 2R TAS (43).…”

“…The Drosophila TAS regions consist of complex satellite-like repeats of 400-1800-bp in length and form heterochromatin domains that are able to induce silencing of transgenic constructs in somatic cells, a phenomenon known as telomeric position effect (58,59). The TAS regions are enriched with H3K27me3 marks and bind Polycomb group proteins (44)(45)(46). In the germline, we observed HP1, Rhi, and H3K9me3 enrichment in the EY03383 subtelomeric transgene (Fig.…”

“…In contrast to the TAS that exert Polycomb group (PcG) protein-mediated silencing of transgenes inserted in these regions (44)(45)(46), the telomeric retrotransposon arrays show euchromatic characteristics and do not silence transgene reporters in somatic tissues, which in fact allowed selection of such transgenic strains (43). Therefore, based on their different ability to silence the integrated transgenes, two telomeric subdomains were defined within the Drosophila telomere in somatic tissues, namely transcriptionally active retrotransposon arrays and heterochromatic TAS (43,44).…”

Site-specific non-LTR retrotransposons

“…All dipteran insects have lost the telomeric repeats; it has been suggested that they use a telomerase-independent telomere maintenance system (41,42,43,44,45). In D. melanogaster, telomeres are composed of three specialized non-LTR retrotransposons, TART, HeT-A, and TAHRE and maintained mainly by retrotransposition of these elements, which have been extensively studied to date (41,42,43,46,47,48,49,50,51,52) (Fig. 3B).…”

Specific Localization of the Drosophila Telomere Transposon Proteins and RNAs, Give Insight in Their Behavior, Control and Telomere Biology in This Organism

“…We have recently described some of the chromatin proteins involved in the epigenetic regulation of Drosophila telomeres [16], [17], [18]. …”