Advertisement

Mammalian Genome

, Volume 21, Issue 1–2, pp 77–87 | Cite as

Divergent patterns of breakpoint reuse in Muroid rodents

  • E. E. Mlynarski
  • C. J. Obergfell
  • M. J. O’Neill
  • R. J. O’Neill
Article

Abstract

Multiple Genome Rearrangement (MGR) analysis was used to define the trajectory and pattern of chromosome rearrangement within muroid rodents. MGR was applied using 107 chromosome homologies between Mus, Rattus, Peromyscus, the muroid sister taxon Cricetulus griseus, and Sciurus carolinensis as a non-Muroidea outgroup, with specific attention paid to breakpoint reuse and centromere evolution. This analysis revealed a high level of chromosome breakpoint conservation between Rattus and Peromyscus and indicated that the chromosomes of Mus are highly derived. This analysis identified several conserved evolutionary breakpoints that have been reused multiple times during karyotypic evolution in rodents. Our data demonstrate a high level of reuse of breakpoints among muroid rodents, further supporting the “Fragile Breakage Model” of chromosome evolution. We provide the first analysis of rodent centromeres with respect to evolutionary breakpoints. By analyzing closely related rodent species we were able to clarify muroid rodent karyotypic evolution. We were also able to derive several high-resolution ancestral karyotypes and identify rearrangements specific to various stages of Muroidea evolution. These data were useful in further characterizing lineage-specific modes of chromosome evolution.

Keywords

Chromosome Evolution Acrocentric Chromosome Pericentric Inversion Karyotypic Evolution Metacentric Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

EEM, CO, MJO, and RJO were supported by NIH grant P40-RR14279 and the UCONN Research Foundation. Thanks to Glenn Tesler for supplying the MGR program and Gianni Ferreri for running our analyses.

Supplementary material

335_2009_9242_MOESM1_ESM.pdf (351 kb)
Supplementary material 1 (PDF 352 kb)

References

  1. Bourque G, Pevzner PA, Tesler G (2004) Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res 14:507–516CrossRefPubMedGoogle Scholar
  2. Bourque G, Zdobnov EM, Bork P, Pevzner PA, Tesler G (2005) Comparative architectures of mammalian and chicken genomes reveal highly variable rates of genomic rearrangements across different lineages. Genome Res 15:98–110CrossRefPubMedGoogle Scholar
  3. Bourque G, Tesler G, Pevzner PA (2006) The convergence of cytogenetics and rearrangement-based models for ancestral genome reconstruction. Genome Res 16:311–313CrossRefPubMedGoogle Scholar
  4. Bulazel K, Ferreri GC, Eldridge MD, O’Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8(8):R170CrossRefPubMedGoogle Scholar
  5. Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53:470–484CrossRefPubMedGoogle Scholar
  6. Eichler EE, Sankoff D (2003) Structural dynamics of eukaryotic chromosome evolution. Science 301:793–797CrossRefPubMedGoogle Scholar
  7. 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 112:126–130CrossRefPubMedGoogle Scholar
  8. Ferguson-Smith MA, Trifonov V (2007) Mammalian karyotype evolution. Nat Rev 8:950–962CrossRefGoogle Scholar
  9. Ferreri GC, Liscinsky DM, Mack JA, Eldridge MD, O’Neill RJ (2005) Retention of latent centromeres in the mammalian genome. J Hered 96:217–224CrossRefPubMedGoogle Scholar
  10. Froenicke L, Caldes MG, Graphodatsky A, Muller S, Lyons LA et al (2006) Are molecular cytogenetics and bioinformatics suggesting diverging models of ancestral mammalian genomes? Genome Res 16:306–310CrossRefPubMedGoogle Scholar
  11. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493–521CrossRefPubMedGoogle Scholar
  12. Glover TW (2006) Common fragile sites. Cancer Lett 232:4–12CrossRefPubMedGoogle Scholar
  13. Greenbaum IF, Gunn SJ, Smith SA, McAllister BF, Hale DW et al (1994) Cytogenetic nomenclature of deer mice, Peromyscus (Rodentia): revision and review of the standardized karyotype. Report of the Committee for the Standardization of Chromosomes of Peromyscus. Cytogenet Cell Genet 66:181–195Google Scholar
  14. Grutzner F, Himmelbauer H, Paulsen M, Ropers HH, Haaf T (1999) Comparative mapping of mouse and rat chromosomes by fluorescence in situ hybridization. Genomics 55:306–313CrossRefPubMedGoogle Scholar
  15. Helou K, Walentinsson A, Levan G, Stahl F (2001) Between rat and mouse zoo-FISH reveals 49 chromosomal segments that have been conserved in evolution. Mamm Genome 12:765–771PubMedGoogle Scholar
  16. Hsu TC, Arrighi FE (1968) Chromosomes of Peromyscus (Rodentia, Cricetidae). I. Evolutionary trends in 20 species. Cytogenetics 7:417–446CrossRefPubMedGoogle Scholar
  17. Jansa SA, Weksler M (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phylogenet Evol 31:256–276CrossRefPubMedGoogle Scholar
  18. Kuroiwa A, Tsuchiya K, Matsubara K, Namikawa T, Matsuda Y (2001) Construction of comparative cytogenetic maps of the Chinese hamster to mouse, rat and human. Chromosome Res 9:641–648CrossRefPubMedGoogle Scholar
  19. Li T, O’Brien PC, Biltueva L, Fu B, Wang J et al (2004) Evolution of genome organizations of squirrels (Sciuridae) revealed by cross-species chromosome painting. Chromosome Res 12:317–335CrossRefPubMedGoogle Scholar
  20. Lichter P, Tang CJ, Call K, Hermanson G, Evans GA et al (1990) High-resolution mapping of human chromosome 11 by in situ hybridization with cosmid clones. Science 247:64–69CrossRefPubMedGoogle Scholar
  21. Louzada S, Paco A, Kubickova S, Adega F, Guedes-Pinto H et al (2008) Different evolutionary trails in the related genomes Cricetus cricetus and Peromyscus eremicus (Rodentia, Cricetidae) uncovered by orthologous satellite DNA repositioning. Micron 39:1149–1155CrossRefPubMedGoogle Scholar
  22. Ma J, Zhang L, Suh BB, Raney BJ, Burhans RC et al (2006) Reconstructing contiguous regions of an ancestral genome. Genome Res 16:1557–1565CrossRefPubMedGoogle Scholar
  23. Mlynarski EE, Obergfell CJ, Rens W, O’Brien PC, Ramsdell CM et al (2008) Peromyscus maniculatus–Mus musculus chromosome homology map derived from reciprocal cross species chromosome painting. Cytogenet Genome Res 121:288–292CrossRefPubMedGoogle Scholar
  24. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA et al (2001a) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618CrossRefPubMedGoogle Scholar
  25. Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M et al (2001b) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351CrossRefPubMedGoogle Scholar
  26. Murphy WJ, Bourque G, Tesler G, Pevzner P, O’Brien SJ (2003) Reconstructing the genomic architecture of mammalian ancestors using multispecies comparative maps. Hum Genomics 1:30–40PubMedGoogle Scholar
  27. Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G et al (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617CrossRefPubMedGoogle Scholar
  28. Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci U S A 81:814–818CrossRefPubMedGoogle Scholar
  29. Nilsson S, Helou K, Walentinsson A, Szpirer C, Nerman O et al (2001) Rat-mouse and rat-human comparative maps based on gene homology and high-resolution zoo-FISH. Genomics 74:287–298CrossRefPubMedGoogle Scholar
  30. O’Neill RJ, Eldridge MD, Metcalfe CJ (2004) Centromere dynamics and chromosome evolution in marsupials. J Hered 95:375–381CrossRefPubMedGoogle Scholar
  31. Ohno S (1973) Ancient linkage groups and frozen accidents. Nature 244:259–262CrossRefGoogle Scholar
  32. Peng Q, Pevzner PA, Tesler G (2006) The fragile breakage versus random breakage models of chromosome evolution. PLoS Comput Biol 2:e14CrossRefPubMedGoogle Scholar
  33. Pevzner P, Tesler G (2003a) Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Res 13:37–45CrossRefPubMedGoogle Scholar
  34. Pevzner P, Tesler G (2003b) Human and mouse genomic sequences reveal extensive breakpoint reuse in mammalian evolution. Proc Natl Acad Sci U S A 100:7672–7677CrossRefPubMedGoogle Scholar
  35. Richard F, Lombard M, Dutrillaux B (2003) Reconstruction of the ancestral karyotype of eutherian mammals. Chromosome Res 11:605–618CrossRefPubMedGoogle Scholar
  36. Robbins LW, Baker RJ (1981) An assessment of the nature of chromosomal rearrangements in 18 species of Peromyscus (Rodentia: Cricetidae). Cytogenet Cell Genet 31:194–202CrossRefPubMedGoogle Scholar
  37. Robinson TJ, Ruiz-Herrera A, Froenicke L (2006) Dissecting the mammalian genome—new insights into chromosomal evolution. Trends Genet 22:297–301CrossRefPubMedGoogle Scholar
  38. Romanenko SA, Perelman PL, Serdukova NA, Trifonov VA, Biltueva LS et al (2006) Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17:1183–1192CrossRefPubMedGoogle Scholar
  39. Romanenko SA, Volobouev VT, Perelman PL, Lebedev VS, Serdukova NA et al (2007) Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison. Chromosome Res 15:283–297CrossRefPubMedGoogle Scholar
  40. Sarich V (1985) Evolutionary relationships among rodents: a multi-disciplinary analysis. Plenum, New YorkGoogle Scholar
  41. Serov O, Chowdhary BP, Womack JE, Graves JAM (2005) Comparative gene mapping, chromosome painting and the reconstruction of the ancestral karyotype. In: Ruvinsky A, Graves JAM (eds) Mammalian genomics. CABI Publishing, Cambridge, MA, pp 349–392CrossRefGoogle Scholar
  42. Stanyon R, Yang F, Cavagna P, O’Brien PC, Bagga M 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 84:150–155CrossRefPubMedGoogle Scholar
  43. Stanyon R, Stone G, Garcia M, Froenicke L (2003) Reciprocal chromosome painting shows that squirrels, unlike murid rodents, have a highly conserved genome organization. Genomics 82:245–249CrossRefPubMedGoogle Scholar
  44. 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 105:406–411CrossRefPubMedGoogle Scholar
  45. Steppan S, Adkins R, 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
  46. Tesler G (2002) GRIMM: genome rearrangements web server. Bioinformatics 18:492–493CrossRefPubMedGoogle Scholar
  47. Veyrunes F, Dobigny G, Yang F, O’Brien PC, Catalan J et al (2006) Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse. Proc Biol Sci 273:2925–2934CrossRefPubMedGoogle Scholar
  48. Yang F, Graphodatsky AS, Li T, Fu B, Dobigny G et al (2006) Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: further insight into the ancestral karyotype and genome evolution of eutherian mammals. Chromosome Res 14:283–296CrossRefPubMedGoogle Scholar
  49. Zhao S, Shetty J, Hou L, Delcher A, Zhu B et al (2004) Human, mouse, and rat genome large-scale rearrangements: stability versus speciation. Genome Res 14:1851–1860CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • E. E. Mlynarski
    • 1
  • C. J. Obergfell
    • 1
  • M. J. O’Neill
    • 1
  • R. J. O’Neill
    • 2
  1. 1.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA
  2. 2.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA

Personalised recommendations