Human-like telomeres in Zostera marina reveal a mode of transition from the plant to the human telomeric sequences

Abstract

A previous study describing the genome of Zostera marina, the most widespread seagrass in the Northern hemisphere, revealed some genomic signatures of adaptation to the aquatic environment. Important features related to the ‘back-to-the-sea’ reverse evolutionary pathway were found, such as the loss of stomatal genes, while other functions like an algal-like cell wall composition were acquired. Beyond these, the genome structure and organization were comparable to the majority of plant genomes sequenced, except for one striking feature that went unnoticed at that time: the presence of human-like instead of the expected plant-type telomeric sequences. By using different experimental approaches including FISH, NGS and Ba131 analysis, we have confirmed its telomeric location in the chromosomes of Z. marina. We have also identified its telomerase RNA subunit (TR), confirming the presence of the human-type telomeric sequence in the template region. Remarkably, this region was found to be very variable even in clades with a highly conserved telomeric sequence across their species. Based on this observation, we propose that alternative annealing preferences in the template borders can explain the transition between the plant and human telomeric sequences. The further identification of paralogues of TR in several plant genomes brought us to the hypothesis that plants may keep an increased ability to change their telomeric sequence. We discuss the implications of this occurrence in the evolution of telomeres while introducing a mechanistic model for the transition from the plant to the human telomeric sequences.

A high-quality reference genome for the fission yeastSchizosaccharomyces osmophilus

“…To understand why S. osmophilus differs from S. octosporus and S. cryophilus in the telomeric repeat units, we compared the telomerase RNA genes ( ter1 ) of these three species and paid special attention to the template regions of telomerase RNAs (Figures 3F, S8C, and S8D). The template region in a telomerase RNA usually consists of two parts: a “templating sequence” corresponding to a full telomeric repeat unit and serving as the template for reverse transcription, and on its 3′ side an “annealing sequence” that is identical to the 5′ part of the “templating sequence” and base pairs with the 3′ end of a telomeric DNA that has just finished one round of reverse transcription (Peska et al . 2020, 2021; Fajkus et al .…”

“…The template region in a telomerase RNA usually consists of two parts: a "templating sequence" corresponding to a full telomeric repeat unit and serving as the template for reverse transcription, and on its 3′ side an "annealing sequence" that is identical to the 5′ part of the "templating sequence" and base pairs with the 3′ end of a telomeric DNA that has just finished one round of reverse transcription (Peska et al 2020(Peska et al , 2021Fajkus et al 2021). The telomerase RNA genes of S. osmophilus, S. octosporus and S. cryophilus are well conserved (Figures 3F and S8D).…”

Hymenoptera (Insecta) telomerase RNAs switched to plant/ciliate-like biogenesis

“…Here we have expanded and confirmed recently predicted (12,13) telomere motifs in Hymenoptera species ( Figure 2, Supplementary Table S1 and S2 ). This was achieved by using a modified Tandem Repeats Finder tool (TRFi) (14) for identification of telomere repeats in raw genomic data, which we have utilised for this purpose several times in various eukaryotic organisms (27,29,32,33). TRFi results on raw genomic data are limited to species with available genomes and summarized in Supplementary Table S2 (note: The first sheet contains hyperlinks to particular TRFi results sorted according to species taxonomy).…”