Diversity and evolution of telomeric motifs and telomere DNA organization in insects

The telomerase mechanism and telomeric motifs are vital for maintaining chromosome integrity. Their functions are conserved in eukaryotic organisms; therefore, it is not surprising that the structure of telomeric motifs is stable. For example, the TTAGG motif persists for hundreds of millions of years in most insects and other arthropods. Here we describe bursts of high diversity of telomeric motifs that have evolved independently in pentatomomorphic bugs (Hemiptera, Pentatomomorpha) and several lineages of parasitic and stinging wasps and bees (Hymenoptera, Apocrita). We show that in most insects, the telomeric DNA sequence is not just a collection of short repeats, but a very long array consisting of (TTAGG)(n) (or other motifs such as TTGGG, TCAGG, TCTGGG, TTAGGGATGG, TTAGGGGTGG, TTAGGGTGGT, TTAGGTCTGGG, TTAGGTTGGGG, TTAGGTTTGGG and TTGGGTCTGGG), regularly and specifically interrupted by the insertion of non-long terminal repeat (non-LTR) retrotransposons of the TRAS and SART families. Long (173-381 bp) repeats were found at chromosome ends in flies of the families Syrphidae and Tachinidae (Diptera). We hypothesize that the balance of telomerase-dependent machinery and telomerase-independent mechanisms (such as SART and TRAS transpositions) maintains telomeres in many insects. We also discuss how shifting this balance can lead to an increased variability of telomeric motifs and to their complete disappearance.

Automated summary

The telomerase mechanism and telomeric motifs are important for maintaining chromosome integrity and are conserved in eukaryotic organisms. Telomeric motifs, such as TTAGG, have persisted for hundreds of millions of years in most insects and other arthropods. However, bursts of high diversity in telomeric motifs have been observed in certain bugs and bees, which is hypothesized to be maintained by a balance between telomerase-dependent machinery and telomerase-independent mechanisms like retrotransposon insertions.