Step-by-Step Evolution of Telomeres: Lessons from Yeasts

Abstract

In virtually every eukaryotic species, the ends of nuclear chromosomes are protected by telomeres, nucleoprotein structures counteracting the end-replication problem and suppressing recombination and undue DNA repair. Although in most cases, the primary structure of telomeric DNA is conserved, there are several exceptions to this rule. One is represented by the telomeric repeats of ascomycetous yeasts, which encompass a great variety of sequences, whose evolutionary origin has been puzzling for several decades. At present, the key questions concerning the driving force behind their rapid evolution and the means of co-evolution of telomeric repeats and telomere-binding proteins remain largely unanswered. Previously published studies addressed mostly the general concepts of the evolutionary origin of telomeres, key properties of telomeric proteins as well as the molecular mechanisms of telomere maintenance; however, the evolutionary process itself has not been analyzed thoroughly. Here, we aimed to inspect the evolution of telomeres in ascomycetous yeasts from the subphyla Saccharomycotina and Taphrinomycotina, with special focus on the evolutionary origin of species-specific telomeric repeats. We analyzed the sequences of telomeric repeats from 204 yeast species classified into 20 families and as a result, we propose a step-by-step model, which integrates the diversity of telomeric repeats, telomerase RNAs, telomere-binding protein complexes and explains a propensity of certain species to generate the repeat heterogeneity within a single telomeric array.

Extraordinary diversity of telomeres, telomerase RNAs and their template regions in Saccharomycetaceae

“…Here, we report, for the first time, the telomere sequence and the maximum putative template regions in Toluraspora , using the previously predicted TRs from T. delbrueckii and T. microellipsoides and our own TR predictions for other species of Torulaspora . Our results from Saccharomycetaceae also support some of the putative telomere sequences in comprehensive telomere searches across Ascomycota 23 . Torulaspora delbrueckii and T. microellipsoides are examples of the intrageneric variability of the telomere sequence.…”

“…In the genus Tetrapisispora , until now, the TR was known only in T. blattae (with an unspecified template region) and telomere sequences were found only very recently in three other species of the genus 23 ; we also detected the three published telomere candidates, with 25/28, and 25 nt long motifs, respectively, T. fleetii , T. iriomotensis , and T. namnaoensis . Cervenak et al 23 also showed that T. iriomotensis had telomere motifs 28/29 nucleotides long at the ends of genomic scaffolds. This would make these species record holders in the motif length among Saccharomycetaceae.…”

“…Considerable variability in telomere units was described at the level of genome assembly in numerous species of Saccharomycetaceae, e.g., T. iriomotensis , S. cerevisiae , and Kazachstania exigua 23 . We show here that even telomeres with complex sequences have a clear consensus with its maximum putative template counterpart.…”

“…The enormous telomere repeat unit size, in fact one of the longest units reported in Saccharomycetaceae, led us to hypothesize that yeast may compensate for a possible low telomerase processivity by expanding the telomere motif to keep the telomere length stable. The hypothetical ancestral telomere sequence TTAGGG 23 , 55 is here substituted by motifs of multiple sizes, e.g., by a fourfold increase in Tetrapisispora . On the other hand, the genus Lachancea exhibits the opposite trend, a shortening of the telomere motif despite the sequence variability in descendant taxa (Fig.…”

“…Later works showed unprecedented variability in the telomere sequences in yeasts, and made the eukaryotic consensus obsolete. The step-by-step telomere sequence evolution in yeasts was currently proposed 23 . However, any obvious feature of the telomere sequence common for all yeasts is difficult to determine, except the clusters of at least two adjacent guanines in the telomere motifs, although the significance of it has not been yet clarified.…”