Chromosome Research

, Volume 18, Issue 2, pp 265–275

New insights into the karyotypic evolution in muroid rodents revealed by multicolor banding applying murine probes

  • Vladimir A. Trifonov
  • Nadezda Kosyakova
  • Svetlana A. Romanenko
  • Roscoe Stanyon
  • Alexander S. Graphodatsky
  • Thomas Liehr
Article

Abstract

Muroid rodents are composed of a wide range of species characterized by extensive karyotypic evolution. Even if this group includes such important laboratory animal models as domestic mouse (Mus musculus), Norway rat (Rattus norvegicus), Chinese hamster (Cricetulus griseus), and golden hamster (Mesocricetus auratus), comparative cytogenetic studies between rodents are difficult due to the characteristic rapid karyotypic evolution. Molecular cytogenetic methods can help resolve problems of comparing muroid chromosomes. Here, we used cross-species comparative multicolour banding with probes obtained from mouse chromosomes 3, 6, 18, and 19 to study the karyotypes of nine muroid species from the three subfamilies Murinae, Cricetinae, and Arvicolinae. Results from multicolour banding with these murine probes (mcb) allowed us to improve the comparative homology maps between these species and to obtain new insights into their karyotypic evolution. We identified evolutionary conserved chromosomal breakpoints and revealed four previously unrecognized homologous segments, four inversions, and 14 evolutionary new centromeres in the nine muroid species studied. We found Mus apomorphic rearrangements, not seen in other muroids, and defined several subfamily specific chromosome breaks, characteristic for Arvicolinae and Cricetinae. We show that mcb libraries are an effective tool both for the cytogenetic characterisation of important laboratory models such as the rat and hamster as well as elucidating the complex phylogenomics relationships of muroids.

Key words

muroid rodents mcb chromosome painting evolutionary new centromeres 

Abbreviations

APE

Apodemus peninsulae

BAC

Bacterial artificial chromosomes

CGR

Cricetulus griseus

DTO

Dicrostonyx torquatus

ENC

Evolutionary new centromeres

ETA

Ellobius talpinus

GTG-banding

G-banding by trypsin using Giesma

MAU

Mesocricetus auratus

MCB

Multicolor banding with human probes

mcb

Multicolor banding with murine probes

MMU

Mus musculus

MOE

Microtus oeconomus

MRO

Microtus rossiaemeridionalis

RNO

Rattus norvegicus

TTR

Tscherskia triton

References

  1. Benedek K, Chudoba I, Klein G, Wiener F, Mai S (2004) Rearrangements of the telomeric region of mouse chromosome 11 in pre-B ABL/MYC cells revealed by mBANDing, spectral karyotyping, and fluorescence in-situ hybridization with a subtelomeric probe. Chromosome Res 12:777–785CrossRefPubMedGoogle Scholar
  2. Carbone L, Nergadze SG, Magnani E et al (2006) Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87:777–782CrossRefPubMedGoogle Scholar
  3. Carleton MD, Musser GG (2005) Order Rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference. The John Hopkins University PressGoogle Scholar
  4. Ferguson-Smith MA, Trifonov V (2007) Mammalian karyotype evolution. Nat Rev Genet 8:950–962CrossRefPubMedGoogle Scholar
  5. Gibbs RA, Weinstock GM, Metzker ML et al (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493–521CrossRefPubMedGoogle Scholar
  6. Gross M, Starke H, Trifonov V, Claussen U, Liehr T, Weise A (2006) A molecular cytogenetic study of chromosome evolution in chimpanzee. Cytogenet Genome Res 112:67–75CrossRefPubMedGoogle Scholar
  7. Guilly M, Fouchet P, de Chamisso P, Schmitz A, Dutrillaux B (1999) Comparative karyotype of rat and mouse using bidirectional chromosome painting. Chromosome Res 7:213–221CrossRefPubMedGoogle Scholar
  8. Helou K, Walentinsson A, Levan G, Ståhl F (2001) Between rat and mouse zoo-FISH reveals 49 chromosomal segments that have been conserved in evolution. Mamm Genome 12:765–771PubMedGoogle Scholar
  9. Karst C, Trifonov V, Romanenko SA et al (2006) Molecular cytogenetic characterization of the mouse cell line WMP2 by spectral karyotyping and multicolor banding applying murine probes. Int J Mol Med 17:209–213PubMedGoogle Scholar
  10. Lewin HA, Larkin DM, Pontius J, O'Brien SJ (2009) Every genome sequence needs a good map. Genome Res 19:1925–1928CrossRefPubMedGoogle Scholar
  11. Liehr T, Heller A, Starke H et al (2002) Microdissection-based high resolution multicolor banding for all 24 human chromosomes. Int J Mol Med 9:335–339PubMedGoogle Scholar
  12. Liehr T, Starke H, Heller A et al (2006) Multicolor fluorescence in situ hybridization (FISH) applied to FISH banding. Cytogenet Genome Res 114:240–244CrossRefPubMedGoogle Scholar
  13. Matsubara K, Nishida-Umehara C, Tsuchiya K, Nukaya D, Matsuda Y (2004) Karyotypic evolution of Apodemus (Muridae, Rodentia) inferred from comparative FISH analyses. Chromosome Res 12:383–395CrossRefPubMedGoogle Scholar
  14. Mouse Genome Sequencing Consortium, Waterston RH, Lindblad-Toh K et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562CrossRefPubMedGoogle Scholar
  15. Mrasek K, Heller A, Rubtsov N et al (2001) Reconstruction of the female Gorilla gorilla karyotype by ZOO-FISH using 25-color FISH and multicolor banding (MCB). Cytogenet Cell Genet 93:242–248CrossRefPubMedGoogle Scholar
  16. Mrasek K, Heller A, Rubtsov N, Trifonov V, Starke H, Claussen U, Liehr T (2003) Detailed Hylobates lar karyotype defined by 25-color FISH and multicolor banding. Int J Mol Med 12:139–146PubMedGoogle Scholar
  17. Romanenko SA, Perelman PL, Serdukova NA et al (2006) Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17:1183–1192CrossRefPubMedGoogle Scholar
  18. Romanenko SA, Sitnikova NA, Serdukova NA et al (2007a) Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). II. The genome homology of two mole voles (genus Ellobius), the field vole and golden hamster revealed by comparative chromosome painting. Chromosome Res 15:891–897CrossRefPubMedGoogle Scholar
  19. Romanenko SA, Volobouev VT, Perelman PL et al (2007b) Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison. Chromosome Res 15:293–298CrossRefGoogle Scholar
  20. Satoh H, Yoshida MC, Sasaki M (1989) High-resolution chromosome banding in the Norway rat, Rattus norvegicus. Cytogenet Cell Genet 50:151–154CrossRefPubMedGoogle Scholar
  21. Sitnikova NA, Romanenko SA, O’Brien PCM et al (2007) 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 15:447–456CrossRefPubMedGoogle Scholar
  22. Stanyon R, Yang F, Cavagna P, O'Brien PCM, Bagga M, Ferguson-Smith MA, Wienberg J (1999) Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats. Cytogenet Genome Res 84:150–155CrossRefGoogle Scholar
  23. Stanyon R, Rocchi M, Capozzi O et al (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16:17–39CrossRefPubMedGoogle Scholar
  24. Steppan SJ, Adkins RM, Anderson J (2004) Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53:533–553CrossRefPubMedGoogle Scholar
  25. Trifonov V, Karst C, Claussen U, Mrasek K, Michel S, Avner P, Liehr T (2005) Microdissection-derived murine mcb probes from somatic cell hybrids. J Histochem Cytochem 53:791–792CrossRefPubMedGoogle Scholar
  26. 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 273:2925–2934CrossRefPubMedGoogle Scholar
  27. Weise A, Gross M, Schmidt S, Reichelt F, Claussen U, Liehr T (2007) New aspects of chromosomal evolution in the gorilla and the orangutan. Int J Mol Med 19:437–443PubMedGoogle Scholar
  28. Yang F, O’Brien PC, Ferguson-Smith MA (2000) Comparative chromosome map of the laboratory mouse and Chinese hamster defined by reciprocal chromosome painting. Chromosome Res 8:219–227CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Vladimir A. Trifonov
    • 1
    • 2
  • Nadezda Kosyakova
    • 2
  • Svetlana A. Romanenko
    • 1
  • Roscoe Stanyon
    • 3
  • Alexander S. Graphodatsky
    • 1
  • Thomas Liehr
    • 2
  1. 1.Molecular and Cellular Biology DepartmentInstitute of Chemical Biology and Fundamental Medicine, SВ RASNovosibirskRussia
  2. 2.Institute of Human Genetics and AnthropologyJena University HospitalJenaGermany
  3. 3.Department of Evolutionary BiologyUniversity of FlorenceFlorenceItaly

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