The Chromosomal Proteins JIL-1 and Z4/Putzig Regulate the Telomeric Chromatin in <em>Drosophila melanogaster</em>

<div><p><em>Drosophila</em> telomere maintenance depends on the transposition of the specialized retrotransposons <em>HeT-A</em>, <em>TART</em>, and <em>TAHRE</em>. Controlling the activation and silencing of these elements is crucial for a precise telomere function without compromising genomic integrity. Here we describe two chromosomal proteins, JIL-1 and Z4 (also known as Putzig), which are necessary for establishing a fine-tuned regulation of the transcription of the major component of <em>Drosophila</em> telomeres, the <em>HeT-A</em> retrotransposon, thus guaranteeing genome stability. We found that mutant alleles of <em>JIL-1</em> have decreased <em>HeT-A</em> transcription, putting forward this kinase as the first positive regulator of telomere transcription in <em>Drosophila</em> described to date. We describe how the decrease in <em>HeT-A</em> transcription in <em>JIL-1</em> alleles correlates with an increase in silencing chromatin marks such as H3K9me3 and HP1a at the <em>HeT-A</em> promoter. Moreover, we have detected that <em>Z4</em> mutant alleles show moderate telomere instability, suggesting an important role of the JIL-1-Z4 complex in establishing and maintaining an appropriate chromatin environment at <em>Drosophila</em> telomeres. Interestingly, we have detected a biochemical interaction between Z4 and the HeT-A Gag protein, which could explain how the Z4-JIL-1 complex is targeted to the telomeres. Accordingly, we demonstrate that a phenotype of telomere instability similar to that observed for <em>Z4</em> mutant alleles is found when the gene that encodes the HeT-A Gag protein is knocked down. We propose a model to explain the observed transcriptional and stability changes in relation to other heterochromatin components characteristic of <em>Drosophila</em> telomeres, such as HP1a.</p>