Diversity and evolution of telomere and subtelomere DNA sequences in insects

Abstract

In insects, two types of telomere length maintenance are known: telomerase-dependent, resulting in chromosome ends consisting of short nucleotide repeats (typically TTAGG), and telomerase-independent, resulting in chromosome ends consisting of long nucleotide repeats or transposon-like elements. However, only a few species have been previously studied with regard to their telomere DNA sequences. Here, based on analysis of chromosome-level genome assemblies, I present the data on telomere and subtelomere organization for 180 species from 148 genera, 53 families and 8 orders of insects. Analysis of these taxa reveals that in fact chromosome ends of most insect species have an intermediate structure and consist of numerous arrays of short telomeric repeats interspersed with telomere-specific non-LTR retrotransposons. An unexpectedly high level of diversity of short telomeric motifs (22 variants ranging in length from 1 to 17 nucleotides) is documented. Telomeres consisting of long repeats (from 173 to 374 bp) are confirmed for flies (the order Diptera) and also found in the orders Odonata and Hymenoptera. The most unusual telomere structure is found in the bee Lasioglossum lativentre, in which the chromosomes possess the short telomeric repeat TTAGGTCTGGG at only one end, whereas opposing ends terminate with medium and long repeats. I conclude that different types of telomere organization and numerous variants of long and short T-containing motifs, including the (T)n mononucleotide sequence, are compatible with the performance of telomere functions. I argue that both telomerase-dependent and telomerase-independent mechanisms for maintaining telomere length operate simultaneously in many insects. The balance between them and the exchange of sequences between telomeres and subtelomeres are most likely the key factors that determine the structure and evolution of telomeres. SignificanceMultilayer telomeres, resulted from numerous, site-specific insertions of retrotransposons into the region of short telomeric repeats, are not an aberrant type of organization, as previously thought. They are widely distributed among insects and can represent up to 30-40 % of eukaryotic species diversity. Accordingly, the telomere maintenance mechanism based on the joint work of telomerase-dependent and telomerase-independent mechanisms can also be extremely widespread in nature.