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Development of a deer mouse whole-genome radiation hybrid panel and comparative mapping of Mus chromosome 11 loci

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Abstract

A 5000-rad whole-genome radiation hybrid cell panel (BW5000) was developed for mapping the deer mouse (Peromyscus maniculatus bairdii) genome. The panel consists of 103 cell lines and has an estimated marker retention frequency of 63.9% (range, 28%–88%) based on PCR typing of 30 Type I (coding gene) and 25 Type II (microsatellite) markers. Using the composite Mus map, Type I markers were selected from six Mus chromosomes, 22 of which are on Mus Chr 11. Fifteen of the Mus Chr 11 markers were simultaneously mapped on an interspecific (P. maniculatus × P. polionotus) backcross panel to test the utility of the radiation hybrid panel, create a framework map, and help establish gene order. The radiation hybrids have effectively detected linkage in the deer mouse genome between markers as far apart as 6.7 cM and resolved markers that are, in the Mus genome, as close as 0.2 Mb. Combined results from both panels have indicated a high degree of gene order conservation of the telomeric 64 cM of Mus Chr 11 in the deer mouse genome. The remaining centromeric portion also shows gene order conservation with the deer mouse but as a separate linkage group. This indicates a translocation of that portion of Mus Chr 11 in P. maniculatus and is consistent with rearrangement breakpoints observed between Mus and other mammalian genomes, including rat and human. Furthermore, this separate linkage group is likely to reside in a chromosomal region of inversion polymorphism between P. maniculatus and P. polionotus.

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References

  • Adkins RM, Gelke EL, Rowe D, Honeycutt RL (2001) Molecular phylogeny and divergence time estimates for major rodent groups: Evidence from multiple genes. Mol Biol Evol 18(5): 777–791

    CAS  PubMed  Google Scholar 

  • Anderson JF, Magnarelli LA (1984) Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. Yale J Biol Med 57: 627–641

    CAS  PubMed  Google Scholar 

  • Bosler EM, Ormiston BG, Coleman JL, Hanrahan JP, Benach JL (1984). Prevalence of the Lyme disease spirochete in populations of white-tailed deer and white-footed mice. Yale J Biol Med 57: 651–659

    CAS  PubMed  Google Scholar 

  • Bowen WW, Dawson WD (1977) Genetic analysis of coat pattern variation in oldfield mice (Peromyscus polionotus) of western Florida. J Mammal 58: 521–530

    Google Scholar 

  • Chowdhary BP, Raudsepp T, Honeycutt D, Owens EK, Piumi F, et al. (2002) Construction of a 5000(rad) whole-genome radiation hybrid panel in the horse and generation of a comprehensive and comparative map for ECA11. Mamm Genome 13: 89–94

    Article  CAS  PubMed  Google Scholar 

  • Cox DR, Burmeister M, Price ER, Kim S, Myers RM (1990) Radiation hybrid mapping: a somatic cell genetic method for constructing high-resolution maps of mammalian chromosomes. Science 250: 245–250

    CAS  PubMed  Google Scholar 

  • Dawson WD (1965) Fertility and size inheritance in a Peromyscus species cross. Evolution 19: 44–55

    Google Scholar 

  • Dawson WD (1982) Protein polymorphisms in American deermice (Peromyscus) and genetic linkage homology. Acta Theriol 16, 213–230

    Google Scholar 

  • Dawson WD, Rogers DS (1993) The genetic linkage map of the deer mouse (Peromyscus maniculatus). In Genetic Maps, O’Brien SJ (ed.) (Cold Spring Harbor, NY: Cold Spring Harbor laboratory press), pp 232–234, 235.

  • Dawson WD, Huang LL, Felder MR, Shaffer JB (1983) Linkage relationships among eleven biochemical loci in Peromyscus. Biochem Genet 21: 1101–1114

    CAS  PubMed  Google Scholar 

  • Dawson WD, Young SR, Wang Z, Liu LW, Greenbaum IF, et al. (1999) Mus and Peromyscus chromosome homology established by FISH with three mouse paint probes. Mamm Genome 10: 730–733

    Article  CAS  PubMed  Google Scholar 

  • DeBry RW, Seldin MF (1996) Human/mouse homology relationships. Genomics 33(3): 337–351

    Article  CAS  PubMed  Google Scholar 

  • Dewey MJ, Dawson WD. (2001) Deer mice: “The Drosophila of North American mammalogy.” Genesis 29: 105–109

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich J, Sankoff D, Nadeau JH (1997) Synteny conservation and chromosomal rearrangments during mammalian evolution. Genetics 147: 289–296

    CAS  PubMed  Google Scholar 

  • Eklund AC, Ober C (2000) Polymorphic microsatellite markers within the MHC of Peromyscus polionotus. Hereditas 133: 179–181

    Article  CAS  PubMed  Google Scholar 

  • Eppig JT, Nadeau JH (1995) Comparative maps: the mammalian jigsaw puzzle. Curr Opin Genet Dev 5: 709–716

    Article  CAS  PubMed  Google Scholar 

  • Flaherty L, Herron B (1998) The new kid on the block—a whole genome mouse radiation hybrid panel. Mamm Genome 9: 417–418

    Article  CAS  PubMed  Google Scholar 

  • Goss SJ, Harris H (1975) New method for mapping genes in human chromosomes. Nature 255: 680–684

    Article  CAS  PubMed  Google Scholar 

  • Greenbaum IF, Reed MJ (1984) Evidence for heterosynaptic pairing of the inverted segment in pericentric inversion heterozygotes of the deer mouse (Peromyscus maniculatus). Cytogenet Cell Genet 38: 106–111

    CAS  PubMed  Google Scholar 

  • Greenbaum IF, Baker RJ, Ramsey PR (1978) Chromosomal evolution and the mode of speciation in three species of Peromyscus. Evolution 32: 646–654

    Google Scholar 

  • Gyapay G, Schmitt K, Fizames C, Jones H, Vega-Czarny N, et al. (1996) A radiation hybrid map of the human genome. Hum Mol Genet 5: 339–346

    Article  CAS  PubMed  Google Scholar 

  • Hale DW (1986) Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse. Chromosoma 94: 425–432

    CAS  PubMed  Google Scholar 

  • Hale DW, Greenbaum IF (1988) Synapsis of a chromosomal pair heterozygous for a pericentric inversion and the presence of a heterochromatic short arm. Cytogenet Cell Genet 48: 55–57

    CAS  PubMed  Google Scholar 

  • Hammer MF, Schimenti J, Silver LM (1989) Evolution of mouse chromosome 17 and the origin of inversions associated with the t haplotypes. Proc Natl Acad Sci U S A 86: 3261–3265

    CAS  PubMed  Google Scholar 

  • Hjelle B, Jenison S, Torrez-Martinez N, Yamada T, Nolte K, et al. (1994) A novel hantavirus associated with an outbreak of fatal respiratory disease in the southwestern United States: Evolutionary relationships to known hantaviruses. J Virol 68: 592–596

    CAS  PubMed  Google Scholar 

  • Jansa SA, Weksler M (2004) Phylogeny of muroid rodent: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phylogenet Evol 31: 256–276

    CAS  PubMed  Google Scholar 

  • Jiang Z, Priat C, Galibert F (1998) Traced orthologous amplified sequence tags (TOASTS) and mammalian comparative maps. Mamm Genome 9: 577–578

    Article  CAS  PubMed  Google Scholar 

  • King JA (1968) Biology of Peromyscus. (Lawrence, KS: American Society of Mammalogy), 593 pp

    Google Scholar 

  • Kirkland GL Jr, Layne JN (1989) Advances in the Study of Peromyscus (Rodentia). (Lubbock, TX: Texas Tech University Press), 366 pp

    Google Scholar 

  • Lunetta KL, Boehnke M, Lange K, Cox DR (1995) Experimental design and error detection for polyploid radiation hybrid mapping. Genome Res 5: 151–163

    CAS  PubMed  Google Scholar 

  • Lyons LA, Laughlin TF, Copeland NG, Jenkins NA, Womack JE, et al. (1997) Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes. Nat Genet 15: 47–56

    Article  CAS  PubMed  Google Scholar 

  • Manly KF, Olson JM (1999) Overview of QTL mapping software and introduction to Map Manager QT. Mamm Genome 10: 327–334

    Article  CAS  PubMed  Google Scholar 

  • Manly KF, Cudmore RH, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12: 930–932

    Article  CAS  PubMed  Google Scholar 

  • McCarthy LC (1996) Whole genome radiation hybrid mapping. Trends Genet 12: 491–493

    Article  CAS  PubMed  Google Scholar 

  • McCarthy LC, Terrett J, Davis ME, Knights CJ, Smith AL, et al. (1997) A first-generation whole genome-radiation hybrid map spanning the mouse genome. Genome Res 7: 1153–1161

    CAS  PubMed  Google Scholar 

  • McPherson JD, Marra M, Hillier L, Waterston RH, Chinwalla A, et al. (2001) A physical map of the human genome. Nature 409: 934–941

    Article  CAS  PubMed  Google Scholar 

  • Michaux J, Reyes A, Catzeflis F (2001) Evolutionary history of the most speciose mammals: Molecular phylogeny of muroid rodents. Mol Biol Evol 18(11): 2017–2031

    CAS  PubMed  Google Scholar 

  • Mullen LM, Hirschmann RJ, Prince KL, Glenn TC, Dewey MJ, et al. (2005) Sixty polymorphic microsatellite markers for the oldfield mouse developed in Peromyscus polionotus and P. maniculatus. Mol Ecol Notes (in press, www.blackwellpublishing.com)

  • Murphy WJ, Sun S, Chen Z, Yuhki N, Hirschmann D, et al. (2000) A radiation hybrid map of the cat genome: implications for comparative mapping. Genome Res 10: 691–702

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Page JE, Smith C, Desrosiers RC, O’Brien SJ (2001) A radiation hybrid mapping panel for the rhesus macaque. J Hered 92: 516–519

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Agarwala R, Schaffer AA, Stephens R, Smith C Jr, et al. (2005) A rhesus macaque radiation hybrid map and comparative analysis with the human genome. Genomics 86(4): 383–395

    Article  CAS  PubMed  Google Scholar 

  • Musser GG, Carleton MD (1993) Peromyscus. In: Mammal Species of the World, 2nd ed. Wilson DE, Reeder DM (eds.) (Washington and London: Smithsonian Institution Press), p 728

    Google Scholar 

  • Nadeau JH, Sankoff D (1998) The lengths of undiscovered conserved segments in comparative maps. Mamm Genome 9: 491–495

    Article  CAS  PubMed  Google Scholar 

  • Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Acad Natl Sci U S A 81: 814–818

    CAS  Google Scholar 

  • Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, et al. (1993) Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914–917

    CAS  PubMed  Google Scholar 

  • O’Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, et al. (1999) The promise of comparative genomics in mammals. Science 286: 458–462

    CAS  PubMed  Google Scholar 

  • Paldi A, Gyapay G, Jami J (1995) Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Curr Biol 5(9): 1030–1035

    Article  CAS  PubMed  Google Scholar 

  • Petkov PM, Graber JH, Churchill GA, DiPetrillo K, King BL, et al. (2005) Evidence of a large-scale functional organization of mammalian chromosomes. PLoS Genet 1(3): 1–11

    Article  Google Scholar 

  • Prince KL, Glenn TC, Dewey MJ (2002) Cross-species amplification among peromyscines of new microsatellite DNA loci from the oldfield mouse (Peromyscus polionotus subgriseus). Mol Ecol Notes 2: 133–136

    Article  CAS  Google Scholar 

  • Robinson R, (1964) Linkage in Peromyscus. J Hered 19: 701–709

    CAS  Google Scholar 

  • Rowe LB, Barter ME, Eppig JT (2000) Cross-referencing radiation hybrid data to the recombination map: lessons from mouse chromosome 18. Genomics 69: 27–36

    Article  CAS  PubMed  Google Scholar 

  • Rowe LB, Barter ME, Kelmenson JA, Eppig JT (2003) The comprehensive mouse radiation hybrid map densely cross-referenced to the recombination map: a tool to support the sequence assemblies. Genome Res 13: 122–133

    Article  CAS  PubMed  Google Scholar 

  • Sankoff D, Nadeau JH (1996) Conserved synteny as a measure of genomic distance. Discrete Applied Math 71: 247–257

    Article  Google Scholar 

  • Scheetz TE, Raymond MR, Nishimura DY, McClain A, Roberts C, et al. (2001) Generation of a high-density rat EST map. Genome Res 11: 497–502

    Article  CAS  PubMed  Google Scholar 

  • Schountz T, Green R, Davenport B, Buniger A, Richens T, et al. (2004) Cloning and characterization of deer mouse (Peromyscus maniculatus) cytokine and chemokine cDNAs. BMC Immunol 5: 1

    Article  PubMed  Google Scholar 

  • Snyder LR, (1980) Evolutionary conservation of linkage groups: additional evidence from murid and cricetid rodents. Biochem Genet 18: 209–220

    Article  CAS  PubMed  Google Scholar 

  • 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: 533–553

    Article  PubMed  Google Scholar 

  • Stewart EA, Cox DR (1997) Radiation hybrid mapping. Dear PH (ed.) In Genome Mapping, (New York: Oxford University Press), pp 73–94

    Google Scholar 

  • Stewart EA, McKusick KB, Aggarwal A, Bajorek E, Brady S, et al. (1997) An STS-based radiation hybrid map of the human genome. Genome Res 7: 422–433

    CAS  PubMed  Google Scholar 

  • Van Etten WJ, Steen RG, Nguyen H, Castle AB, Slonim DK, et al. (1999) Radiation hybrid map of the mouse genome. Nat Genet 22: 384–387

    PubMed  Google Scholar 

  • Venta PJ, Brouillette JA, Yuzbasiyan-Gurkan V, Brewer GJ (1996) Gene-specific universal mammalian sequence-tagged sites: application to the canine genome. Biochem Genet 34: 321–341

    CAS  PubMed  Google Scholar 

  • Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, et al. (2001) The Sequence of the Human Genome. Science 291: 1304–1351

    Article  CAS  PubMed  Google Scholar 

  • Vrana PB, Guan XJ, Ingram RS, Tilghman SM (1998) Genomic imprinting is disrupted in interspecific Peromyscus hybrids. Nat Genet 20, 362–365; erratum (1999) 21, 241

    Google Scholar 

  • Vrana PB, Fossella JA, Matteson P, del Rio T, O’Neill MJ, et al. (2000) Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus. Nat Genet 25: 120–124

    CAS  PubMed  Google Scholar 

  • Walter MA, Goodfellow PN (1993) Radiation hybrids: irradiation and fusion gene transfer. Trends Genet 9: 352–356

    Article  CAS  PubMed  Google Scholar 

  • Walter MA, Spillett DJ, Thomas P, Weissenbach J, Goodfellow PN (1994) A method for constructing radiation hybrid maps of whole genomes. Nat Genet 7: 22–28

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Young SR, Liu L, Dawson WD (1995) Assignment of Tp53 and Tk1 to chromosome 13 in Peromyscus by fluorescence in situ hybridization. Cytogenet Cell Genet 69: 97–100

    CAS  PubMed  Google Scholar 

  • Watanabe I, Tsukamoto K, Shiba T, Emi M (1998) Isolation and radiation hybrid mapping of dinucleotide repeat polymorphism at the human matrix Gla protein (MGP) locus. J Hum Genet 43: 75–76

    Article  CAS  PubMed  Google Scholar 

  • Waterston RH, Lander ES, Lindblah-Toh K, Birney E, Rogers J, Abril JF, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562

    CAS  PubMed  Google Scholar 

  • Willard HF, Goss SJ, Holmes MT, Munroe DL (1985) Regional localization of the phosphoglycerate kinase gene and pseudogene on the human X chromosome and assignment of a related DNA sequence to chromosome 19. Hum Genet 71: 138–143

    Article  CAS  PubMed  Google Scholar 

  • Wilson AC, Sarich VM, Maxson LR (1974) The importance of gene rearrangement in evolution: Evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc Natl Acad Sci U S A 71(8): 3028–3030

    CAS  PubMed  Google Scholar 

  • Womack JE, Johnson JS, Owens EK, Rexroad CE, Schlapfer J, et al. (1997) A whole-genome radiation hybrid panel for bovine gene mapping. Mamm Genome 8: 854–856

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful for the considerable advice and critique generously provided by Lucy Rowe of the Jackson Laboratory and for partial support provided by grants from NSF (DEB-0344710) and NIH (P40-RR14279 and RO1-M069601).

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  1. Peromyscus Genetic Stock Center, Department of Biological Sciences, University of South Carolina, 700 Sumter Street, Columbia, South Carolina, 29208, USA

    Clifton M. Ramsdell, Elizabeth L. Thames, Julie L. Weston & Michael J. Dewey

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  1. Clifton M. Ramsdell
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  2. Elizabeth L. Thames
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Correspondence to Clifton M. Ramsdell.

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Ramsdell, C.M., Thames, E.L., Weston, J.L. et al. Development of a deer mouse whole-genome radiation hybrid panel and comparative mapping of Mus chromosome 11 loci. Mamm Genome 17, 37–48 (2006). https://doi.org/10.1007/s00335-005-0051-x

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