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Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). I. The genome homology of tundra vole, field vole, mouse and golden hamster revealed by comparative chromosome painting

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Abstract

Cross-species chromosome painting has become the mainstay of comparative cytogenetic and chromosome evolution studies. Here we have made a set of chromosomal painting probes for the field vole (Microtus agrestis) by DOP-PCR amplification of flow-sorted chromosomes. Together with painting probes of golden hamster (Mesocricetus auratus) and mouse (Mus musculus), the field vole probes have been hybridized onto the metaphases of the tundra vole (Microtus oeconomus). A comparative chromosome map between these two voles, golden hamster and mouse has been established based on the results of cross-species chromosome painting and G-banding comparisons. The sets of paints from the field vole, golden hamster and mouse identified a total of 27, 40 and 47 homologous autosomal regions, respectively, in the genome of tundra vole; 16, 41 and 51 fusion/fission rearrangements differentiate the karyotype of the tundra vole from the karyotypes of the field vole, golden hamster and mouse, respectively.

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References

  • Aniskin VM (2006) Selected karyotypes. In O’Brien SJ, Nash WG, Menninger JC, eds., Atlas of Mammalian Karyotypes. Chichester: Wiley, pp. 231–233, 235–236, 263.

    Google Scholar 

  • Avise JC, Walker D, Johns GC (1998) Speciation durations and Pleistocene effects on vertebrate and phylogeography. Proc R Soc Lond B 265: 1707-712.

    Article  CAS  Google Scholar 

  • Chaline J, Brunet-Lecomte P, Motuire S, Viriot L, Courant F (1999) Anatomy of the arvicoline radiation (Rodentia): paleaogeographical, paleaoecological history and evolutionary data. Ann Zool Fennici 36: 239-67.

    Google Scholar 

  • Chernjavsky FB, Kozlovsky AI (1980) Species status and history of the Arctic lemmings (Dicrostonyx, Rodentia) of Wrangel Island. Zool J (Moscow) 59: 266–273 (Russian).

    Google Scholar 

  • Conroy CJ, Cook JA (1999) MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. J Mamm Evol 6: 221-45.

    Article  Google Scholar 

  • Conroy CJ, Cook JA (2000) Molecular systematics of a holarctic rodent (Microtus: Muridae). J Mammal 81: 344-59.

    Article  Google Scholar 

  • DeWoody JA, Chesser RK, Baker RJ (1999) A translocated mitochondrial cytochrome b pseudogene in voles (Rodentia: Microtus). J Mol Evol 48: 380-82.

    Article  CAS  PubMed  Google Scholar 

  • Elisaphenko EA, Nesterova TB, Duthie SM et al. (1998) Repetitive DNA sequences in the common vole: cloning, characterization and chromosome localization of two novel complex repeats MS3 and MS4 from the genome of the East European vole Microtus rossiaemeridionalis. Chromosome Res 6: 351-60.

    Article  CAS  PubMed  Google Scholar 

  • Engelbrecht A, Dobigny G, Robinson TJ (2006) Further insights into the ancestral murine karyotype: the contribution of the Otomys–Mus comparison using chromosome painting. Cytogenet Genome Res 112: 126-30.

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1988) Aberrant chromosomal sex-determining mechanisms in mammals, with special reference to species with XY females. Phil Trans R Soc Lond B 322: 83-5.

    Article  CAS  Google Scholar 

  • Fredga K, Lyapunova E (1991) Fertile males with two X chromosomes in Ellobius tancrei (Rodentia, Mammalia). Hereditas 115: 86-7.

    Google Scholar 

  • Golenishchev FN, Malikov VG (2006) The ‘developmental conduit’ of the tribe Microtini (Rodentia, Arvicolinae): systematic and evolutionary aspects. Russ J Theriol 5: 17-4.

    Google Scholar 

  • Graphodatsky AS (1989) Conserved and variable elements of mammalian chromosomes. In Halnan C, ed., Cytogenetics of Animals. Oxford: CAB International Press, pp. 95–123.

    Google Scholar 

  • Graphodatsky AS, Sablina OV, Meyer MN et al. (2000) Comparative cytogenetics of hamsters of the genus Calomyscus. Cytogenet Cell Genet 88: 296-04.

    Article  CAS  PubMed  Google Scholar 

  • Graphodatsky AS, Yang F, O’Brien PCM et al. (2001) Phylogenetic implications of the 38 putative ancestral chromosome segments for four canid species. Cytogenet Cell Genet 92:243-47.

    Article  CAS  PubMed  Google Scholar 

  • Guilly M-N, Fouchet P, de Chamisso P, Schmitz A, Dutrillaux B (1999) Comparative karyotype of rat and mouse using bidirectional chromosome painting. Chromosome Res 7: 213-21.

    Article  CAS  PubMed  Google Scholar 

  • Guilly M-N, Dano L, de Chamisso P, Fouchet P, Dutrillaux B et al. (2001) Comparative karyotype using biderectional chromosome painting: how and why? Methods Cell Sci 23: 163-70.

    Article  CAS  PubMed  Google Scholar 

  • Jaarola M, Martinkova N, Gündüz I et al. (2004) Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 33: 647-63.

    Article  CAS  PubMed  Google Scholar 

  • Just W, Rau W, Vogel W et al. (1995) Absence of Sry in species of the vole Ellobius. Nature Genet 11: 117-18.

    Article  CAS  PubMed  Google Scholar 

  • Just W, Baumstark A, Hameister H et al. (2002) The sex determination in Ellobius lutescens remains bizarre. Cytogenet Genome Res 96: 146-53.

    Article  CAS  PubMed  Google Scholar 

  • Li T, Wang J, Su W, Yang F (2006) Chromosomal mechanisms underlying the karyotype evolution of the oriental voles (Muridae, Eothenomys). Cytogenet Genome Res 114: 50-5.

    Article  CAS  PubMed  Google Scholar 

  • Marchal JA, Acosta MJ, Bullejos M, Diaz de la Guardia R, Sanchez A (2004a) A repeat DNA sequence from the Y chromosome in species of the genus Microtus. Chromosome Res 12: 757-65.

    Article  CAS  Google Scholar 

  • Marchal JA, Acosta MJ, Nietzel H et al. (2004b) X chromosome painting in Microtus: origin and evolution of the giant sex chromosomes. Chromosome Res 12: 37-7.

    Google Scholar 

  • Matsubara K, Nishida-Umehara C, Kuriowa A, Tsuchiya K, Matsuda Y (2003) Identification of chromosome rearrangements between the laboratory mouse (Mus musculus) and the Indian spiny mouse (Mus platythrix) by comparative FISH analysis. Chromosome Res 11: 57-4.

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Nishuda-Umehara C, Tsuchiya K, Nukaya D, Matsuda Y (2004) Karyotypic evolution of Apodemus (Muridae, Rodentia) inferred from comparative FISH analyses. Chromosome Res 12: 383-95.

    Article  CAS  PubMed  Google Scholar 

  • Mazurok NA, Rubtsova NV, Isaenko AA et al. (2001) Comparative chromosome and mitochondrial DNA analyses and phylogenetic relationships within common voles (Microtus, Arvicolidae). Chromosome Res 9: 107-20.

    Article  CAS  PubMed  Google Scholar 

  • Meyer MN, Golenishchev FN, Radjabli SI, Sablina OV (1996) Voles (Subgenus Microtus Schrank) of Russia and Ajacent Territories. Russ Acad Sci, Proc Zool Inst 232: 3–320 (Russian).

    Google Scholar 

  • Modi WS (1987) Phylogenetic analyses of chromosomal banding patterns among the Neartcic Arvicolidae (Mammalia: Rodentia). Syst Zool 36: 109-36.

    Article  Google Scholar 

  • Modi WS (1993) Comparative analyses of heterochromatin in Microtus: sequence heterogeneity and localized expansion and contraction of satellite DNA arrays. Cytogenet Cell Genet 62: 142-48.

    Article  CAS  PubMed  Google Scholar 

  • Modi WS (2006) Selected karyotypes. In O’Brien SJ, Nash WG, Menninger JC, eds., Atlas of Mammalian Karyotypes. Chichester: Wiley, pp. 232, 234, 240, 253–254, 262, 269–272, 274–275.

    Google Scholar 

  • Modi WS, Serdyukova NA, Vorobieva NV, Graphodatsky AS (2003) Chromosomal localization of six repeat DNA sequences among species of Microtus (Rodentia). Chromosome Res 11: 705-13.

    Article  CAS  PubMed  Google Scholar 

  • Musser GG, Carleton MD (2005) Order Rodentia. In Wilson DE, Reeder DM, eds., Mammal Species of the World: a Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press, pp. 926–930, 1039–1186.

    Google Scholar 

  • Nanda I, Neitzel H, Sperling K et al. (1988) Simple GATCA repeats characterize the X chromosome heterochromatin in Microtus agrestis, European field vole (Rodentia, Cricetidae). Chromosoma 96: 213-19.

    Article  CAS  PubMed  Google Scholar 

  • Rambau RV, Robinson TJ (2003) Chromosome painting in the African four-striped mouse Rhabdomys pumilio: detection of possible murid specific contiguous segment combination. Chromosome Res 11: 91-8.

    Article  CAS  PubMed  Google Scholar 

  • Romanenko SA, Perelman PL, Serdukova NA et al. (2006) Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17: 1183-192.

    Article  PubMed  Google Scholar 

  • Romanenko SA, Volobouev VT, Perelman PL et al. (2007) Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison. Chromosome Res doi: 10.1007/s10577-007-1124-3. (Published online).

  • Sablina OV, Radjabli SI, Graphodatsky AS (2006) Selected karyotypes. In O’Brien SJ, Nash WG, Menninger JC, eds., Atlas of Mammalian Karyotypes. Chichester: Wiley, pp. 237–239, 241–252, 255–262, 264–268, 273, 276–279.

    Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2: 971-72.

    Article  CAS  PubMed  Google Scholar 

  • Shenbrot GI, Krasnov BR (2005) An Atlas of the Geographic Distribution of the Arvicoline Rodents of the World (Rodentia, Muridae: Arvicolinae). Sofia-Moscow: Pensoft Publ. 3-50

    Google Scholar 

  • Stanyon R, Yang F, Cavagna P et al. (1999) Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats. Cytogenet Cell Genet 84: 150-55.

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Yang F, Morescalchi AM, Galleni L (2004) Chromosome painting in the long-tailed field mouse provides insights into the ancestral murid karyotype. Cytogenet Genome Res 105: 406-11.

    Article  CAS  PubMed  Google Scholar 

  • Steppan SJ, Adkins RM, Anderson J (2004) Phylogeny and divergence-data estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53: 533-53.

    Article  PubMed  Google Scholar 

  • Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4: 257-63.

    Article  CAS  PubMed  Google Scholar 

  • Triant DA, DeWoody JA (2006) Accelerated molecular evolution in Microtus (Rodentia) as assessed via complete mitochondrial genome sequences. Genetica 128: 95-08.

    Article  CAS  PubMed  Google Scholar 

  • Veyrunes F, Dobigny G, Yang F, O’Brien PCM, Catalan J, Robinson TJ, Britton-Davidian J (2006) Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse. Proc R Soc B 273: 2925-934.

    Article  PubMed  Google Scholar 

  • Volobouev VT, Gallardo MH, Graphodatsky AS (2006) Rodents cytogenetics. In O’Brien SJ, Nash WG, Menninger JC, eds., Atlas of Mammalian Karyotypes. Chichester: Wiley, pp. 173–176.

    Google Scholar 

  • Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642-52.

    Article  CAS  PubMed  Google Scholar 

  • Yang F, O’Brien PC, Milne BS et al. (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62:189-02.

    Article  CAS  PubMed  Google Scholar 

  • Yang E, O'Brien PCM, Ferguson-Smith MA (2000) Comparative chromosome map of the laboratory mouse and Chinese hamster defined by reciprocal chromosome painting. Chromosome Res 8: 219-27.

    Article  CAS  PubMed  Google Scholar 

  • Zheng S-H, Zhang Z-Q (2000) Late Miocene–Early Pleistocene micromammals from Wenwanggou of Lingtai, Gansu, China. Vertebrata PalAsiatica 38: 58-1.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Cytology and Genetics, SB RAS, Novosibirsk, 630090, Russia

    Natalia A. Sitnikova, Svetlana A. Romanenko, Polina L. Perelman, Nadezhda V. Rubtsova, Natalya A. Serdukova, Vladimir A. Trifonov & Alexander S. Graphodatsky

  2. Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge, CB3 OES, UK

    Patricia C. M. O’Brien, Beiyuan Fu, Vladimir A. Trifonov & Malcolm A. Ferguson-Smith

  3. Zoological Institute, RAS, Saint-Petersburg, Russia

    Feodor N. Golenishchev

  4. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

    Fengtang Yang

Authors
  1. Natalia A. Sitnikova
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  2. Svetlana A. Romanenko
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  3. Patricia C. M. O’Brien
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  4. Polina L. Perelman
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  5. Beiyuan Fu
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  6. Nadezhda V. Rubtsova
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  7. Natalya A. Serdukova
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  8. Feodor N. Golenishchev
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  9. Vladimir A. Trifonov
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  10. Malcolm A. Ferguson-Smith
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  11. Fengtang Yang
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  12. Alexander S. Graphodatsky
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Correspondence to Alexander S. Graphodatsky.

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Sitnikova, N.A., Romanenko, S.A., O’Brien, P.C.M. et al. Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). I. The genome homology of tundra vole, field vole, mouse and golden hamster revealed by comparative chromosome painting. Chromosome Res 15, 447–456 (2007). https://doi.org/10.1007/s10577-007-1137-y

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  • DOI: https://doi.org/10.1007/s10577-007-1137-y

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