Expression of Subtelomeric lncRNAs Links Telomeres Dynamics to RNA Decay in S. cerevisiae

Abstract

Long non-coding RNAs (lncRNAs) have been shown to regulate gene expression, chromatin domains and chromosome stability in eukaryotic cells. Recent observations have reported the existence of telomeric repeats containing long ncRNAs ⁻ <i>TERRA</i> in mammalian and yeast cells. However, their functions remain poorly characterized. Here, we report the existence in <i>S. cerevisiae</i> of several lncRNAs within Y' subtelomeric regions. We have called them <i>subTERRA.</i> These belong to Cryptic Unstable Transcripts (CUTs) and Xrn1p-sensitive Unstable Transcripts (XUTs) family. <i>subTERRA</i> transcription, carried out mainly by RNAPII, is initiated within the subtelomeric Y' element and occurs in both directions, towards telomeres as well as centromeres. We show that <i>subTERRA</i> are distinct from <i>TERRA</i> and are mainly degraded by the general cytoplasmic and nuclear 5'- and 3'- RNA decay pathways in a transcription-dependent manner. <i>subTERRA</i> accumulates preferentially during the G1/S transition and in C-terminal <i>rap1</i> mutant but independently of Rap1p function in silencing. The accumulation of <i>subTERRA</i> in RNA decay mutants coincides with telomere misregulation: shortening of telomeres, loss of telomeric clustering in mitotic cells and changes in silencing of subtelomeric regions. Our data suggest that subtelomeric RNAs expression links telomere maintenance to RNA degradation pathways.