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Are the TTAGG and TTAGGG telomeric repeats phylogenetically conserved in aculeate Hymenoptera?

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Abstract

Despite the (TTAGG)n telomeric repeat supposed being the ancestral DNA motif of telomeres in insects, it was repeatedly lost within some insect orders. Notably, parasitoid hymenopterans and the social wasp Metapolybia decorata (Gribodo) lack the (TTAGG)n sequence, but in other representatives of Hymenoptera, this motif was noticed, such as different ant species and the honeybee. These findings raise the question of whether the insect telomeric repeat is or not phylogenetically predominant in Hymenoptera. Thus, we evaluated the occurrence of both the (TTAGG)n sequence and the vertebrate telomere sequence (TTAGGG)n using dot-blotting hybridization in 25 aculeate species of Hymenoptera. Our results revealed the absence of (TTAGG)n sequence in all tested species, elevating the number of hymenopteran families lacking this telomeric sequence to 13 out of the 15 tested families so far. The (TTAGGG)n was not observed in any tested species. Based on our data and compiled information, we suggest that the (TTAGG)n sequence was putatively lost in the ancestor of Apocrita with at least two subsequent independent regains (in Formicidae and Apidae).

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References

  • Anjos A, Rocha GC, Paladini A, Mariguela TC, Cabral-de-Mello DC (2016) Karyotypes and repetitive DNA evolution in six species of the genus Mahanarva (Auchenorrhyncha: Cercopidae). Cytogenet Genome Res 149:321–327

    Article  CAS  PubMed  Google Scholar 

  • Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573

    Article  CAS  PubMed  Google Scholar 

  • Branstetter MG, Danforth BN, Pitts JP, Faircloth BC, Ward PS, Buffington ML et al (2017a) Phylogenomic insights into the evolution of stinging wasps and the origins of ants and bees. Curr Biol 27:1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Branstetter MG, Longino JT, Ward PS, Faircloth BC (2017b) Enriching the ant tree of life: enhanced UCE bait set for genome-scale phylogenetics of ants and other Hymenoptera. Methods Ecol Evol 8:768–776

    Article  Google Scholar 

  • Cesare AJ, Reddel RR (2010) Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 11:319–330

    Article  CAS  PubMed  Google Scholar 

  • De Lange T (2009) How telomeres solve the end-protection problem. Science 326:948–952

    Article  PubMed  PubMed Central  Google Scholar 

  • Dlaska M, Schöffski P, Bechter OE (2013) Inter-telomeric recombination is present in telomerase-positive human cells. Cell Cycle 12:2084–2099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes T, Madalena CRG, Gorab E (2012) Cloning and characterisation of a novel chromosome end repeat enriched with homopolymeric (dA)/(dT) DNA in Rhynchosciara americana (Diptera: Sciaridae). Chromosom Res 20:435–445

    Article  CAS  Google Scholar 

  • Frydrychová R, Grossmann P, Trubac P, Vítková M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178

    Article  PubMed  Google Scholar 

  • Frydrychova RC, Biessmann H, Mason JM (2009) Regulation of telomere length in Drosophila. Cytogenet Genome Res 122:356–364

    Article  PubMed Central  Google Scholar 

  • Fulcher N, Derboven E, Valuchova S, Riha K (2014) If the cap fits, wear it: an overview of telomeric structures over evolution. Cell Mol Life Sci 71:847–865

    Article  CAS  PubMed  Google Scholar 

  • Gokhman VE, Anokhin BA, Kuznetsova VG (2014) Distribution of 18S rDNA sites and absence of the canonical TTAGG insect telomeric repeat in parasitoid Hymenoptera. Genetica 142:317–322

    Article  PubMed  Google Scholar 

  • Greider CW, Blackburn EH (1996) Telomeres, telomerase and cancer. Sci Am 274:92–97

    Article  CAS  PubMed  Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klopfstein S, Vilhelmsen L, Heraty JM, Sharkey M, Ronquist F (2013) The hymenopteran tree of life: evidence from protein-coding genes and objectively aligned ribosomal data. PLoS One 8:e69344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krupp G, Klapper W, Parwaresch R (2000) Cell proliferation, carcinogenesis and diverse mechanisms of telomerase regulation. Cell Mol Life Sci 57:464–486

    Article  CAS  PubMed  Google Scholar 

  • Lorite P, Carrillo JA, Palomeque T (2002) Conservation of (TTAGG)n telomeric sequences among ants (Hymenoptera, Formicidae). J Hered 93:282–285

    Article  CAS  PubMed  Google Scholar 

  • Madalena CRG, Amabis JM, Gorab E (2010) Unusually short tandem repeats appear to reach chromosome ends of Rhynchosciara americana (Diptera: Sciaridae). Chromosoma 119:613–623

    Article  PubMed  Google Scholar 

  • Mason JM, Biessmann H (1995) The unusual telomeres of Drosophila. Trends Genet 11:58–62

    Article  CAS  PubMed  Google Scholar 

  • Mason JM, Randall TA, Frydrychova RC (2016) Telomerase lost? Chromosoma 125:65–73

    Article  CAS  PubMed  Google Scholar 

  • Mason JM, Reddy HM, Frydrychova RC (2011) Telomere maintenance in organisms without telomerase, DNA replication-current advances. Dr Herve Seligmann (ed) InTech available from: https://www.intechopen.com/books/dna-replication-current-advances/telomere-maintenance-in-organisms-without-telomerase

  • Menezes RST, Silva TM, Carvalho AF, Andrade-Souza V, Silva JG, Costa MA (2013) Numerical and structural chromosome variation in the swarm-founding wasp Metapolybia decorata Gribodo 1896 (Hymenoptera, Vespidae). Genetica 141:273–280

    Article  PubMed  Google Scholar 

  • Meyne J, Hirai H, Imai HT (1995) FISH analysis of the telomere sequences of bulldog ants (Myrmecia: Formicidae). Chromosoma 104:14–18

    CAS  PubMed  Google Scholar 

  • Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci USA 86:7049–7053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mravinac B, Meštrović N, Cavrak VV, Plohl M (2011) TCAGG, an alternative telomeric sequence in insects. Chromosoma 120:367–376

    Article  CAS  PubMed  Google Scholar 

  • Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fujiwara H (1993) Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol Cell Biol 13:1424–1432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters RS, Krogmann L, Mayer C, Donath A, Gunkel S, Meusemann K et al (2017) Evolutionary history of the Hymenoptera. Curr Biol 27:1013–1018

    Article  CAS  PubMed  Google Scholar 

  • Rossato RM, Madalena CR, Gorab E (2007) Unusually short tandem repeats in the chromosome end structure of Rhynchosciara (Diptera: Sciaridae). Genetica 131:109–116

    Article  CAS  PubMed  Google Scholar 

  • Royle NJ, Foxon J, Jeyapalan JN, Mendez-Bermudez A, Novo CL, Williams J et al (2009) Telomere length maintenance—an ALTernative mechanism. Cytogenet Genome Res 122:281–291

    Article  Google Scholar 

  • Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosom Res 7:449–460

    Article  CAS  Google Scholar 

  • Teng SC, Zakian VA (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19:8083–8093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vítková M, Král J, Traut W, Zrzavý J, Marec F (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosom Res 13:145–156

    Article  Google Scholar 

  • Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK et al (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–348

    Article  CAS  PubMed  Google Scholar 

  • Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, Hunt BG et al (2011) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci U S A 108:5679–5684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakian VA (1995) Telomeres: beginning to understand the end. Science 270:1601–1607

    Article  CAS  PubMed  Google Scholar 

  • Zhang YJ, Kamnert I, López CC, Cohn M, Edström JE (1994) A family of complex tandem repeats in the telomeres of Chironomus pallidivittatus. Mol Cell Biol 14:8028–8036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to Alexandre Somavilla, Dayana Cunha, and Marcel Hermes for kindly contributing with specimens used in this study; José Amilcar Tavares Filho for assistance in the field and Rodrigo M. Feitosa for discussion on the phylogeny of ants. We thank the four anonymous reviewers whose comments helped to improve the manuscript.

Funding

RSTM is thankful to São Paulo Research Foundation (FAPESP) by grants 2015/02432-0 and 2016/21098-7; VBB was benefited by PNPD/Capes scholarship; DCCM was benefited by a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process number 304758/2014-0); DAAL is funded by a FAPESP scholarship (no. 2015/12326-3); and EABA is grateful for funding by FAPESP (grant no. 2011/09477-9) and CNPq (grant no. 459826/2014-0) and is funded by a research productivity fellowship by CNPq (no. 304735/2016-7).

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Correspondence to Rodolpho S. T. Menezes.

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Communicated by: Sven Thatje

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Menezes, R.S.T., Bardella, V.B., Cabral-de-Mello, D.C. et al. Are the TTAGG and TTAGGG telomeric repeats phylogenetically conserved in aculeate Hymenoptera?. Sci Nat 104, 85 (2017). https://doi.org/10.1007/s00114-017-1507-z

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  • DOI: https://doi.org/10.1007/s00114-017-1507-z

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