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      First evidence for (TTAGG)n telomeric sequence and sex chromosome post-reduction in Coleorrhyncha (Insecta, Hemiptera)

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          Abstract

          Abstract

          Telomeric repeats are general and significant structures of eukaryotic chromosomes. However, nothing is known about the molecular structure of telomeres in the enigmatic hemiptera n suborder Coleorrhyncha (moss bugs) commonly considered as the sister group to the suborder Heteroptera (true bugs). The true bugs are known to differ from the rest of the Hemiptera in that they display an inverted sequence of sex chromosome divisions in male meiosis, the so-called sex chromosome post-reduction. To date, there has been no information about meiosis in Coleorrhyncha . Here we report a cytogenetic observation of Peloridium pomponorum , a representative of the single extant coleorrhyncha n family Peloridiidae , using the standard chromosome staining and fluorescence in situ hybridization (FISH) with a (TTAGG) n telomeric probe. We show that Peloridium pomponorum displays 2n = 31 (30A + X) in males, the classical insect (TTAGG) n telomere organization and sex chromosome post-reduction during spermatocyte meiosis. The plesiomorphic insect-type (TTAGG) n telomeric sequence is suggested to be preserved in Coleorrhyncha and in a basal heteroptera n infraorder Nepomorpha , but absent (lost) in the advanced heteroptera n lineages Cimicomorpha and Pentatomomorpha . The telomere structure in other true bug infraorders is currently unknown. We consider here the inverted sequence of sex chromosome divisions as a synapomorphy of the group Coleorrhyncha + Heteroptera .

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          Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic?

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            TTAGG telomeric repeats in chromosomes of some insects and other arthropods.

            We studied the occurrence of the TTAGG telomere repeats by fluorescence in-situ hybridization (FISH) and Southern hybridization in ten insect species and two other arthropods. (TTAGG)n-containing telomeres were found in three Lepidoptera species, the silkworm Bombyx mori (in which the telomeric sequence was recently discovered), the flour moth Ephestia kuehniella, and the wax moth Galleria mellonella, in one species of Hymenoptera, the honey bee Apis mellifera, in one species of Coleoptera, the bark beetle Ips typographus, in one species of Orthoptera, the locust Locusta migratoria, and in a crustacean, the amphipod Gammarus pulex. They were absent in another species of Coleoptera, the mealworm Tenebrio molitor, two representatives of Diptera, Drosophila melanogaster and Megaselia scalaris, a species of Heteroptera, the bug Pyrrhocoris apterus and a spider, Tegenaria ferruginea. Our results, which confirm and extend earlier observations, suggest that (TTAGG)n was a phylogenetically ancestral telomere motif in the insect lineage but was lost independently in different groups, being replaced probably by other telomere motifs. In the Coleoptera this must have happened rather recently as even members of the same family, Curculionidae, differ with respect to the telomeric DNA.
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              Phylogenetic distribution of TTAGG telomeric repeats in insects.

              We examined the presence of TTAGG telomeric repeats in 22 species from 20 insect orders with no or inconclusive information on the telomere composition by single-primer polymerase chain reaction with (TTAGG)6 primers, Southern hybridization of genomic DNAs, and fluorescence in situ hybridization of chromosomes with (TTAGG)n probes. The (TTAGG)n sequence was present in 15 species and absent in 7 species. In a compilation of new and published data, we combined the distribution of (TTAGG)n telomere motif with the insect phylogenetic tree. The pattern of phylogenetic distribution of the TTAGG repeats clearly supported a hypothesis that the sequence was an ancestral motif of insect telomeres but was lost repeatedly during insect evolution. The motif was conserved in the "primitive" apterous insect orders, the Archaeognatha and Zygentoma, in the "lower" Neoptera (Plecoptera, Phasmida, Orthoptera, Blattaria, Mantodea, and Isoptera) with the exception of Dermaptera, and in Paraneoptera (Psocoptera, Thysanoptera, Auchenorrhyncha, and Sternorrhyncha) with the exception of Heteroptera. Surprisingly, the (TTAGG)n motif was not found in the "primitive" pterygotes, the Palaeoptera (Ephemeroptera and Odonata). The Endopterygota were heterogeneous for the occurrence of TTAGG repeats. The motif was conserved in Hymenoptera, Lepidoptera, and Trichoptera but was lost in one clade formed by Diptera, Siphonaptera, and Mecoptera. It was also lost in Raphidioptera, whereas it was present in Megaloptera. In contrast with previous authors, we did not find the motif in Neuroptera. Finally, both TTAGG-positive and TTAGG-negative species were reported in Coleoptera. The repeated losses of TTAGG in different branches of the insect phylogenetic tree and, in particular, in the most successful lineage of insect evolution, the Endopterygota, suggest a backup mechanism in the genome of insects that enabled them frequent evolutionary changes in telomere composition.
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                Author and article information

                Journal
                Comp Cytogenet
                Comp Cytogenet
                CompCytogen
                Comparative Cytogenetics
                Pensoft Publishers
                1993-0771
                1993-078X
                2015
                2 September 2015
                : 9
                : 4
                : 523-532
                Affiliations
                [1 ]Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia
                [2 ]Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Blvd Tsar Osvoboditel 1, Sofia 1000, Bulgaria
                [3 ]Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstraße 43, 10115 Berlin, Germany
                [4 ]Staatliches Museum für Naturkunde Karlsruhe, Erbprinzenstraße 13, 76133 Karlsruhe, Germany
                Author notes
                Corresponding author: Valentina Kuznetsova ( valentina_kuznetsova@ 123456yahoo.com )

                Academic editor: I. Gavrilov-Zimin

                Article
                10.3897/CompCytogen.v9i4.5609
                4698568
                26753072
                a144b7a9-2b16-4aef-b2e6-8f7a0d66d338
                Valentina G. Kuznetsova, Snejana M. Grozeva, Viktor Hartung, Boris A. Anokhin

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 July 2015
                : 10 August 2015
                Categories
                Research Articles

                karyotype,sex chromosome post-reduction,(ttagg)n telomeric sequence,hemiptera,coleorrhyncha,peloridiidae,peloridium pomponorum

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