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

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 such as the loss of stomatal genes, while other functions such as an algal-like cell wall composition were acquired. Beyond these, the genome structure and organization were comparable with those of 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 fluorescence in situ hybridization (FISH), genome skimming by next-generation sequencing (NGS), and analysis of non-coding transcriptome, we have confirmed its telomeric location in the chromosomes of Z. marina. We have also identified its telomerase RNA (TR) subunit, 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 led us to the hypothesis that plants may retain 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.This work was supported by: European Regional Development Fund [project SYMBIT, reg. no. CZ.02.1.01/0.0/0.0/15_003/0000477], The Czech Science Foundation [19-03442S to TM and 20-01331X to JF], Ministry of Education, Youth and Sports of the Czech Republic [project CEITEC 2020 (LQ1601)], and by the Spanish [CGL2016-75694-P (AEI/ FEDER, UE)] and Catalan [grant number 2017SGR1116] governments. VP benefited from an European Molecular Biology organization Short-Term fellowship (grant no. 7368) and SG is the holder of a Ramón y Cajal contract (RYC-2014-16608).Abstract Introduction Materials and methods Results and discussion Supplementary data Acknowledgements Data availability Author contributions Conflict of interest References Author notes Supplementary dat