Telomerase lost?

Abstract

Telomerase and telomerase-generated telomeric DNA sequences are widespread throughout eukaryotes, yet they are not universal. Neither telomerase nor the simple DNA repeats associated with telomerase have been found in some plant and animal species. Telomerase was likely lost from Diptera before the divergence of Diptera and Siphonaptera, some 260 million years ago. Even so, Diptera is one of the most successful animal orders, making up 11% of known animal species. In addition, many species of Coleoptera and Hemiptera seem to lack canonical telomeric repeats at their chromosome ends. These and other insects that appear to lack canonical terminal repeat sequences account for another 10-15% of animal species. Conversely, the silk moth Bombyx mori maintains canonical telomeric sequences at its chromosome ends but seems to lack a functional telomerase. We speculate that a telomere-specific capping complex that recognizes the telomeric repeats and protects chromosome ends is the determining factor in maintaining canonical telomeric sequences and that telomerase is an early and efficacious mechanism for satisfying the needs of capping complex. There are alternate mechanisms for maintaining chromosome ends that do not depend on telomerase, such as recombination found in some human cancer cells and yeast mutants. These mechanisms may maintain the canonical telomeric repeats or allow the terminal sequence to evolve when specificity of the capping complex for terminal repeat sequences is weak.

The Deadbeat Paternal Effect of Uncapped Sperm Telomeres on Cell Cycle Progression and Chromosome Behavior in Drosophila melanogaster

“…Rapid evolution of reproductive proteins has been attributed to a variety of selective forces, including sperm competition and fertilization competency (Swanson and Vacquier 2002). Rapid evolution of TCC restricted proteins has been attributed to relaxed constraints on telomere sequences in the Dipteran lineage, after the loss of telomerase (estimated 260 MYA) and with adoption of retrotransposon-based telomere elongation mechanisms (estimated 65-230 MYA) (Mason et al 2015). We propose that Ddbt may be coevolving with TCCs to enable its telomere recruitment.…”

“…Multiple proteins are enriched predominantly, if not exclusively, at telomeres and form a capping complex that protects telomeric DNA from engaging in aberrant DNA repair activities. Protein components of the telomere-capping complex (TCC) vary among organisms, in part because species differ in telomeric sequences and whether telomeres are maintained by telomerase or alternative mechanisms (Raffa et al 2011;Mason et al 2015). Nonetheless, the TCC's essential functions are well conserved.…”

Cytogenetic Characterization of Eight Odonata Species Originating from the Curonian Spit (the Baltic Sea, Russia) Using C-Banding and FISH with 18S rDNA and Telomeric (TTAGG)_n Probes

“…More recent findings include, e.g., those on Coleoptera [Mravinac et al, 2011], Hymenoptera [Gokhman et al, 2014], Mantophasmatodea [Lachowska-Cierlik et al, 2015], Neuroptera , and many Hemiptera including Aphidoidea [Mandrioli et al, 2014], Coleorrhyncha [Kuznetsova et al, 2015b], and Heteroptera Kuznetsova et al, 2012;Chirino and Bressa, 2014;Pita et al, 2016;Angus et al, 2017;Chirino et al, 2017]. One of the most notable findings was the unexpected discovery of the (TTAGG) n motif in the true bug family Reduviidae which ruled out the hypothesis of absence (loss) of this motif in the whole evolutionarily advanced infraorder Cimicomorpha [Frydrychová et al, 2004;Grozeva et al, 2011;Mason et al, 2016].…”

Evolutionary perspectives of telomerase RNA structure and function

“…Repeated insertions of retrotransposons into chromosome terminal regions is employed for telomere length maintenance in a small group of insect species that lacks discernable telomerase enzyme components or detectable telomerase activity 16,17 . The lack of telomerase within only a small and closely related group of species, yet retained in neighboring species, indicates that telomerase was recently lost within the dipteran fly insect lineage 18 . Telomerase-independent maintenance has been most extensively studied in Drosophila , whose telomeres are composed of tandem arrays of the HeT-A and TART retrotransposons—parasitic genetic elements capable of self-replication through an RNA intermediate 19 .…”