Canonical TTAGG-repeat telomeres and telomerase in the honey bee, Apis mellifera

Abstract

The draft assembly of the honey bee Apis mellifera genome sequence reveals that the 17 centromeric-distal telomeres are of a simple, shared, and canonical structure, with 3-4 kb of a unique subtelomeric sequence, followed by several kilobases of TTAGG or variant telomeric repeats. This simple subtelomeric structure differs from the centromericproximal telomeres on the short arms of the 15 acrocentric chromosomes, which are apparently composed primarily of the 176-bp AluI tandem repeat. This dichotomy between the distal and proximal telomeres may involve differential participation of the telomeres of the 15 acrocentric chromosomes in the Rabl configuration after mitosis and the chromosome bouquet in meiotic prophase I. As expected from the presence of canonical TTAGG telomeric repeats, we identified a candidate telomerase gene in the bee, as well as the silkmoth Bombyx mori and the flour beetle Tribolium castaneum.

Drosophila telomeric retrotransposons derived from an ancestral element that was recruited to replace telomerase

“…The recent discoveries of the telomerase reverse transcriptase (TERT) of Bombyx mori (Lepidoptera), Tribolium castaneum (Coleoptera), and Apis mellifera (Hymenoptera) has confirmed the absence of telomerase orthologs in the available Drosophila and Anopheles genomes (Osanai et al 2006;Robertson and Gordon 2006). This is consistent with the absence of TTAGG telomeric repeats in flies and mosquitoes.…”

“…This is consistent with the absence of TTAGG telomeric repeats in flies and mosquitoes. The phylogenetic relationships using the core RT domain of the three insect TERTs showed, as expected, that the insect telomerases cluster together, and that A. mellifera appears basal to T. castaneum (Robertson and Gordon 2006) in the same way that the Hymenoptera is basal to the Coleoptera in the Holometabola (Honey Bee Genome Sequencing Consortium 2006). These insect TERTs lack the N-terminal domain implicated in processivity in others telomerases, and this feature could explain why telomerase activity is low in the bee and virtually undetectable in the silkworm.…”

The genome of the model beetle and pest Tribolium castaneum

“…Manual assembly of the proximal regions of multiple telomeres beyond the ends of the assembled scaffolds (Supplementary Information) reveals TCAGG repeats interrupted by full-length and 59-truncated non-LTR retrotransposons belonging to the R1 clade, best known for insertions in the rDNA locus 14 . Tribolium telomeres range in length from 15 kilobases (kb) upwards and probably represent a stage intermediate to the loss of telomeres and telomerase in Diptera compared with the simple canonical structure of the honeybee 15 or the more regular insertion of non-LTR retrotransposons into the simple repeats of the silkmoth 16 .…”

Simple Telomeres in a Simple Animal: Absence of Subtelomeric Repeat Regions in the PlacozoanTrichoplax adhaerens

“…Not all subtelomeric regions are as uniformly repeated at each telomere as those of the honeybee (Robertson and Gordon 2006); for example, human subtelomeric regions, while commonly sharing subtelomeric repeats or Srpts, are quite distinctive overall (e.g., Riethman et al 2005), and there are some eukaryotes known to have no shared subtelomeric repeats, such as Tetrahymena (e.g., Jacob et al 2004). Nevertheless, the absence of subtelomeric repeats in T. adhaerens suggests that if these have important roles in other organisms, they are either dispensed with in placozoans or substituted for by other means.…”

“…In some species this subtelomeric repetitive nature extends to suites of genes with similar copies at each telomere. For example, the draft genome sequence of the honeybee Apis mellifera provided a first view of an insect with simple TTAGG telomeric repeats and revealed a simple 3.5-kb subtelomeric repeat region with 70% DNA identity between all 17 telomeres on the long euchromatic arms (Robertson and Gordon 2006). These subtelomeric regions could serve several roles, including binding sites for proteins that locate the telomeres within the nucleus or orchestrate the bouquet formation during meiosis, as a barrier against chromatin silencing of neighboring genes, as backup for maintenance of telomere length through recombination in the absence of telomerase, or as transcription initiation sites for TERRA/TelRNA transcripts of the TTAGGG repeats (e.g., Pryde et al 1997;Jacob et al 2004;Riethman et al 2005;Siderakis and Tarsounas 2007;Horard and Gilson 2008;Mason et al 2008).…”