Skip to main content
Log in

Unusual distribution pattern of telomeric repeats in the shrews Sorex araneus and Sorex granarius

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Sorex araneus and Sorex granarius are sibling species within the Sorex araneus group with karyotypes composed of almost identical chromosome arms. S. granarius has a largely acrocentric karyotype, while, in S. araneus, various of these acrocentrics have combined together by Robertsonian (Rb) fusions to form metacentrics, with the numbers and types of metacentrics differing between chromosomal races. Our studies on telomeric sequences in S. araneus and S. granarius revealed differences between chromosomes and between species. In S. araneus (the Novosibirsk race), hybridization signals were present on the telomeres of all the chromosomes after FISH with a PCR-generated telomeric probe. In addition, hybridization signals were observed at high frequencies in the pericentric regions of some but not all metacentrics formed by Rb fusion. There were fewer signals on those metacentrics formed earlier in the evolution of S. araneus. This suggests that S. araneus chromosomes retain at least some telomeric repeats during Rb fusion, but that these repeats are lost or modified over time. These results are critical for the interpretation of the well-studied hybrid zones between chromosomal races of S. araneus, given that Rb fission has been postulated in such hybrid zones and that the likelihood of Rb fission will relate to presence/absence of telomeric sequences at the centromeres of metacentrics. In S. granarius, there were strong signals at the proximal (centromeric) telomeres of the acrocentrics after FISH with a DNA telomeric probe. FISH with a PNA telomeric probe on S. granarius acrocentrics showed that the proximal telomeres were 213 kb on average, while the length of the distal telomeres was 3.8 kb on average. Two-colour FISH, using a telomeric DNA probe and a microdissected probe generated from the pericentric regions of the S. granarius chromosomes a and b, revealed regions on distinct chromatin fibres where telomeric and microdissected probes were colocalized or localized sequentially. The proximal telomeres of S. granarius are highly unusual both in their large size and their heterogeneous structure relative to the telomeres of other mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Azzalin CM, Nergadze SG, Giolotto E (2001) Human intrachromosomal telomeric-like repeats: sequence organization and mechanism of origin. Chromosoma 110: 75–82.

    PubMed  Google Scholar 

  • Brünner H, Lugon-Moulin N, Balloux F, Fumagalli L, Hausser J (2002) A taxonomical re-evaluation of the Valais chromosome race of the common shrew Sorex araneus (Insectivora: Soricidae). Acta Theriol 47: 245–275.

    Google Scholar 

  • Castiglia R, Gornung E, Corti M (2002) Cytogenetic analyses of chromosomal rearrangements in Mus minutoides/musculoides from North–West Zambia through mapping of the telomeric sequence (TTAGGG)n and banding techniques. Chromosome Res 10: 399–406.

    Article  PubMed  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2003) Evolution of rRNA gene clusters and telomeric repeats during explosive genome repatterning in Taterillus X (Rodentia, Gerbillinae). Cytogenet Genome Res 103: 94–103.

    Article  PubMed  Google Scholar 

  • Garagna S, Broccoli D, Redi CA, Searle JB, Cook HJ, Capanna E (1995) Robertsonian metacentrics of the house mouse lose telomeric sequences but retain some minor satellite DNA in the pericentromeric area. Chromosoma 103: 685–692.

    PubMed  Google Scholar 

  • Garagna S, Zuccotti M, Capanna E, Redi CA (2002) High-resolution organization of mouse telomeric and pericentromeric DNA. Cytogenet Genome Res 96: 125–129.

    Article  PubMed  Google Scholar 

  • Hanish JP, Yanowitz JL, de Lange T (1994) Stringent sequence requirements for the formation of human telomeres. Proc Natl Acad Sci USA 91: 8861–8865.

    PubMed  Google Scholar 

  • Hartmann N, Scherthan H (2004) Characterization of ancestral chromosome fusion points in the Indian muntjac deer. Chromosoma 112: 213–220.

    Article  PubMed  Google Scholar 

  • Hausser J, Fumagalli L, Taberlet P (1998) Mitochondrial DNA evolution in shrews. In Wójcik JM, Wolsan M Eds. Evolution of Shrews. Białowieża, Poland: Mammal Research Institute, pp 295–308.

    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.

    PubMed  Google Scholar 

  • Kilburn AE, Shea MJ, Sargent RG, Wilson JH (2001) Insertion of a telomere repeat sequence into a mammalian gene causes chromosome instability. Mol Cell Biol 21: 126–135.

    Article  PubMed  Google Scholar 

  • Lansdorp PM, Verwoerd NP, van de Rijke FM et al. (1996) Heterogeneity in telomere length of human chromosomes. Hum Mol Genet 5: 685–691.

    Article  PubMed  Google Scholar 

  • Manning EL, Crosland J, Dewey MJ, Van Zant G (2002) Influence of inbreeding and genetics on telomere length in mice. Mamm Genome 13: 234–238.

    Article  PubMed  Google Scholar 

  • Martens UM, Zijlmans JM, Poon SS et al. (1998) Short telomeres on human chromosome 17p. Nat Genet 18: 76–80.

    Article  PubMed  Google Scholar 

  • Metcalfe CJ, Eldridge MD, Toder R, Johnston PG (1998) Mapping of the distribution of the telomeric sequence (TTAGGG)n in the Macropoidea (Marsupialia) by fluorescence in-situ hybridization. 1. The swamp wallaby, Wallabia bicolor. Chromosome Res 6: 603–610.

    Article  PubMed  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH et al. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequences in vertebrate chromosomes Chromosoma 99: 3–10.

    Article  PubMed  Google Scholar 

  • Mondello C, Pirzio L, Azzalin CM, Giulotto E (2000) Instability of interstitial telomeric sequences in the human genome. Genomics 68: 111–117.

    Article  PubMed  Google Scholar 

  • Nanda I, Schneider-Rasp S, Winking H, Schmid M (1995) Loss of telomeric sites in the chromosomes of Mus musculus domesticus (Rodentia: Muridae) during Robertsonian rearrangements. Chromosome Res 3: 399–409.

    Article  PubMed  Google Scholar 

  • Pack SD, Borodin PM, Serov OL, Searle JB (1993) The X-autosome translocation in the common shrew (Sorex araneus L.): late replication in female somatic cells and pairing in male meiosis. Chromosoma 102: 355–360.

    Article  PubMed  Google Scholar 

  • Pagnozzi JM, De Jesus Silva MJ, Yonenaga-Yassuda Y (2000) Intraspecific variation in the distribution of the interstitial telomeric (TTAGGG)n sequences in Micoureus demerarae (Marsupialia: Didelphidae). Chromosome Res 8: 585–591.

    Article  PubMed  Google Scholar 

  • Rivero MT, Mosquera A, Goyanes V, Slijepcevic P, Fernandez JL (2004) Differences in repair profiles of interstitial telomeric sites between normal and DNA double-strand break repair deficient Chinese hamster cells. Exp Cell Res 295: 161–172.

    Article  PubMed  Google Scholar 

  • Rogatcheva MB, Ono T, Sonta S, Oda S, Borodin PM (2000) Robertsonian metacentrics of the house musk shrew (Suncus murinus. Insectivora. Soricidae) lose the telomeric sequences in the centromeric area. Genes Genet Syst 75: 155–158.

    Article  PubMed  Google Scholar 

  • Rubtsov N, Karamysheva T, Babochkina T et al. (2000) A new simple version of chromosome microdissection tested by probe generation for 24-multi-color FISH, Multi-color banding (MCB), ZOO-FISH and in clinical diagnostics. Medgen 12: 65.

    Google Scholar 

  • Ruiz-Herrera A, Garcia F, Azzalin C, Giulotto E, Ponsa M, Garcia M (2002) Distribution of intrachromosomal telomeric sequences (ITS) on Macaca fascicularis (Primates) chromosomes and their implication for chromosome evolution. Hum Genet 110: 578–586.

    Article  PubMed  Google Scholar 

  • Searle JB, (1993) Robertsonian Chromosomal Variation in the Common Shrew Sorex araneus L. PhD thesis, University of Aberdeen.

  • Searle JB (1993) Chromosomal hybrid zones in eutherian mammals. In: Harrison RG (ed) Hybrid Zones and the Evolutionary Process. New York: Oxford University Press, pp. 309–353.

    Google Scholar 

  • Searle JB, Fedyk S, Fredga K, Hausser J, Volobouev VT (1991) Nomenclature for the chromosomes of the common shrew (Sorex araneus). Mem Soc Vaud Sc Nat 19: 13–22.

    Google Scholar 

  • Sharman GB (1991) History of discovery and recognition of XY1Y2 systems and chromosome polymorphism in mammals. Mem Soc Vaud Sc Nat 19: 7–12.

    Google Scholar 

  • Slijepcevic P (1998) Telomeres and mechanisms of Robertsonian fusion. Chromosoma 107: 136–140.

    Article  PubMed  Google Scholar 

  • Volobouev VT, Dutrillaux B (1991) Chromosomal evolution and phylogenetic relationships of the Sorex araneusarcticus species group. Mem Soc Vaud Sc Nat 19: 131–139.

    Google Scholar 

  • Wójcik JM, Searle JB (1988) The chromosome complement of Sorex granarius — the ancestral karyotype of the common shrew (Sorex araneus)? Heredity 61: 225–229.

    PubMed  Google Scholar 

  • Wójcik JM, Borodin PM, Fedyk S et al. (2003) The list of the chromosome races of the common shrew Sorex araneus (updated 2002). Mammalia 67: 169–178.

    Google Scholar 

  • Zhu L, Hathcock KS, Hande P, Lansdorp PM, Seldin MF, Hodes RJ (1998) Telomere length regulation in mice is linked to a novel chromosome locus. Proc Natl Acad Sci USA 95: 8648–8653.

    Article  PubMed  Google Scholar 

  • Zijlmans JM, Martens UM, Poon SS et al. (1997) Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc Natl Acad Sci USA 94: 7423–7438.

    Article  PubMed  Google Scholar 

  • Zima J, Lukáèová L, Macholán M (1998) Chromosomal evolution in shrews. In: Wójcik JM, Wolsan M Eds. Evolution of Shrews. Białowieża, Poland: Mammal Research Institute, pp. 175–218.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeremy B. Searle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhdanova, N.S., Karamisheva, T.V., Minina, J. et al. Unusual distribution pattern of telomeric repeats in the shrews Sorex araneus and Sorex granarius. Chromosome Res 13, 617–625 (2005). https://doi.org/10.1007/s10577-005-0988-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-005-0988-3

Key words

Navigation