Telotrons: spliceosomal introns composed of telomeric repeats

Abstract

Spliceosomal intron numbers vary widely across eukaryotes, but the only established mechanism for large bursts of intron gain is the spread of transposable introner elements. We describe telotrons, spliceosomal introns composed predominantly of telomeric repeats. In a survey of 10,310 eukaryotic genome assemblies, we identified 7,008 introns with >85% telomeric repeat coverage and an additional 44,423 with >50% to [≤]85% coverage, in 25 genomes spanning haptophytes, dinoflagellates, a cryptophyte, stramenopiles, the apicomplexan Eimeria, and the nematode Mesorhabditis. Most telotrons carry GT-AG or GC-AG splice boundaries, and RNA-seq supports their splicing. Their repeat orientations are consistent with telomerase extension of broken DNA ends, and intron absence at corresponding positions in orthologs supports widespread de novo gain. In Eimeria and Mesorhabditis, telotrons instead occupy positions where orthologs carry ordinary introns, suggesting modification of existing introns. Telotrons thus point to telomerase as an endogenous driver of structural innovation through intron creation and remodeling.