Telomerase RNA in Hymenoptera (Insecta) switched to plant/ciliate-like biogenesis

In contrast to the catalytic subunit of telomerase, its RNA subunit (TR) 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). Here, we focus on unknown TRs in one of the largest Animalia order - Hymenoptera (Arthropoda) with more than 300 available representative genomes. Using a combination of bioinformatic and experimental approaches, we identify their TRs. In contrast to the presumed type of TRs (H/ACA box snoRNAs transcribed with RNA Polymerase II) corresponding to their phylogenetic position, we find here short TRs of the snRNA type, likely transcribed with RNA polymerase III under the control of the type 3 promoter. The newly described insect TRs thus question the hitherto assumed monophyletic origin of TRs across Animalia and point to an evolutionary switch in TR type and biogenesis that was associated with the divergence of Arthropods.

Automated summary

Unlike the catalytic subunit of telomerase, the RNA subunit (TR) shows significant differences in size, sequence and biogenesis across eukaryotes. Previous views assumed a common origin of TRs transcribed with RNA polymerase II in Opisthokonta and Trypanosomida, and TRs transcribed with RNA polymerase III in TSAR and Archaeplastida. However, new findings from studying Hymenoptera TRs challenge this assumption and suggest an evolutionary switch in TR type and biogenesis that is associated with the divergence of Arthropods.