Transposition, duplication, and divergence of the telomerase RNA underlies the evolution ofMimulustelomeres

Abstract

AbstractTelomeres are nucleoprotein complexes with a crucial role of protecting chromosome ends. It consists of simple repeat sequences and dedicated telomere-binding proteins. Because of its vital functions, components of the telomere, for example its sequence, should be under strong evolutionary constraint. But across all plants, telomere sequences display a range of variation and the evolutionary mechanism driving this diversification is largely unknown. Here, we discovered in Monkeyflower (Mimulus) the telomere sequence is even variable between species. We investigated the basis ofMimulustelomere sequence evolution by studying the long noncoding telomerase RNA (TR), which is a core component of the telomere maintenance complex and determines the telomere sequence. We conducted total RNA-basedde novotranscriptomics from 16Mimulusspecies and analyzed reference genomes from 6 species, and discoveredMimulusspecies have evolved at least three different telomere sequences: (AAACCCT)n, (AAACCCG)n, and (AAACCG)n. Unexpectedly, we discovered several species with TR duplications and the paralogs had functional consequences that could influence telomere evolution. For instance,M. lewisiihad two sequence-divergent TR paralogs and synthesized a telomere with sequence heterogeneity, consisting of AAACCG and AAACCCG repeats. Evolutionary analysis of theM. lewisiiTR paralogs indicated it had arisen from a transposition-mediate duplication process. Further analysis of the TR from multipleMimulusspecies showed the gene had frequently transposed and inserted into new chromosomal positions duringMimulusevolution. From our results, we propose the TR transposition, duplication, and divergence model to explain the evolutionary sequence turnovers inMimulusand potentially all plant telomeres.