Coordination of transposon expression with DNA replication in the targeting of telomeric retrotransposons in Drosophila

• Published in: The EMBO journal 2014-05, Vol.33 (10), p.1148-1158
• Main Authors: Zhang, Liang, Beaucher, Michelle, Cheng, Yan, Rong, Yikang S
• Format: Article
• Language: English
• Subjects: Animals; Cell cycle; CST complex; Deoxyribonucleic acid; DNA; DNA Replication - genetics; DNA Replication - physiology; DNA Transposable Elements - genetics; Drosophila - genetics; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Drosophila telomere; EMBO13; Gene Expression Regulation; Gene Products, gag - genetics; Gene Products, gag - metabolism; Insects; Proteins; Retroelements - genetics; Telomerase; Telomere - genetics; telomere replication; telomeric transposon
• ISSN: 0261-4189; 1460-2075
• DOI: 10.1002/embj.201386940

In Drosophila , a group of retrotransposons is mobilized exclusively to telomeres in a sequence‐independent manner. How they target chromosome ends is not understood. Here, we focused on the telomeric element HeT‐A and characterized the cell cycle expression and cytological distribution of its protein and RNA products. We determined the timing of telomere replication by creating a single lacO ‐marked telomere and provide evidence suggesting that transposon expression and recruitment to telomeres is linked to telomere replication. The HeT‐A ‐encoded ORF1p protein is expressed predominantly in S phase, particularly in early S phase. Orf1p binds HeT‐A transcripts and forms spherical structures at telomeres undergoing DNA replication. HeT‐A sphere formation requires Verrocchio, a putative homolog of the conserved Stn1 telomeric protein. Our results suggest that coupling of telomere elongation and telomere replication is a universal feature, and raise the possibility that transposon recruitment to Drosophila telomeres is mechanistically related to telomerase recruitment in other organisms. Our study also supports a co‐adaptive relationship between the Drosophila host and HeT‐A mobile elements. Synopsis Telomerase‐independent maintenance of Drosophila telomeres via retrotransposon elements is here shown to involve telomere targeting of ribonucleoprotein structures, in a process that coincides with telomere replication and requires the homolog of a key telomeric protein from telomerase‐dependent species. HeT‐A retrotransposon‐encoded Orf1p protein is produced predominantly in (early) S‐phase cells. Orf1p assembles large, spherical ribonucleoprotein structures (“ HeT‐A spheres”) at telomeres. HeT‐A sphere telomere recruitment and telomere replication happen in a similar time window. HeT‐A sphere attachment to telomeres depends on the putative Stn1 homolog Verrocchio. Graphical Abstract Telomerase‐independent maintenance of Drosophila telomeres via retrotransposon elements involves telomere targeting of ribonucleoprotein structures and coincides with telomere replication, revealing parallels with telomerase‐mediated mechanisms in other species.