ABSTRACT: Unraveling the Intricate Pathways of Telomere Evolution
Telomerase, telomeric DNA and associated proteins together represent a complex, finely tuned, and functionally conserved mechanism that ensures genome integrity by protecting and maintaining chromosome ends. Its central component is telomerase RNA (TR) as it templates telomere DNA synthesis, its mutation can change telomere DNA and disrupt its recognition by telomere proteins, thereby leading to collapse of their end-protective and telomerase recruitment functions. TR subunit, in contrast to the catalytic subunit of telomerase, is highly divergent in size, sequence and biogenesis pathways across eukaryotes. Current views on TR evolution assume a common origin of TRs transcribed with RNA polymerase II in Opisthokonta (the supergroup including Animalia and Fungi) and Trypanosomida on one hand, and TRs transcribed with RNA polymerase III under the control of type 3 promoter, found in TSAR and Archaeplastida supergroups (including e.g., ciliates and Viridiplantae taxa, respectively).
Our story began with the discovery of unusual telomeres in Allium plants (Fajkus et al., 2016), and led to the identification of TRs across the land plant phylogeny (Fajkus et al., 2019), and within Diaphoretickes megagroup (Fajkus et al., 2021). Surprisingly, the same type of TR was recently discovered also in Hymenoptera and Lepidoptera insects (Animalia) (Fajkus et al., 2023). Using a combination of bioinformatic and experimental approaches, we examined the enigma of evolution of unusual telomeres: on one hand, any change in telomere/telomerase interplay can threaten an organism’s viability; on the other hand, molecular innovation in telomere maintenance has occurred multiple times during eukaryote evolution, giving rise to species/taxa with unusual telomeric DNA sequences, telomerase components, or telomerase-independent telomere maintenance. We examined a plausible scenario of evolutionary changes in TR underlying telomere transitions. We identified plants harbouring multiple TR paralogs whose template regions could support the synthesis of diverse telomeres. In our hypothesis, formation of unusual telomeres is associated with the emergence and occurrence of TR paralogs that can accumulate mutations, and through their functional redundancy, allow for the adaptive evolution of the other telomere components. Experimental analyses of telomeres and telomerase in the examined plants demonstrate evolutionary telomere transitions corresponding to TR paralogs with diverse template regions.
Funding: Czech Science Foundation, project 20-01331X.
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