Skip to main content

Advertisement

Log in

Recombination within mouse t haplotypes has replaced significant segments of t-specific DNA

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

Previous studies on the fourth inversion of the t complex, In17(4), suggest that loci near the center of this inversion have been subjected to segmental recombination during the past 1–2 million years. We have used a combination of PCR-based restriction site (PBR) analysis and DNA sequencing to perform a high-resolution analysis of a 2-million base pair (Mbp) segment in the middle of In17(4). We examined 21 restriction sites that are polymorphic between t haplotypes and their wild-type homologs, over nine distinct loci. In addition, we examined several other polymorphic sites through DNA sequence analysis of two of these nine loci. We analyzed several haplotypes in this way, including the “complete” t haplotypes t w2, t 0, t w32, t w71, and t w75. We show that only t w32 is a true “complete” t haplotype; the remaining four t haplotypes have segments of wild-type DNA ranging from less than 100 bp to 2 Mbp. The sizes of these wild-type DNA segments are consistent with their being generated by gene-conversion events. The 2-Mbp segment is located in a region that may contain the t-complex distorter gene Tcd2. One of the nine loci examined in this study is Fgd2, a gene that has been proposed to encode Tcd2. Sequencing and PBR data show that at least a portion of the Fgd2 gene has been converted to the wild-type within t w71 and t w75mice.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Artzt K, Barlow D, Dove WF, Fischer-Lindahl K, Klein J et al (1991) Mouse chromosome 17. Mamm Genome 1 Spec No:S280–S300

  • Bauer H, Veron N, Willert J, Koschorz B, Herrmann BG (2007) The t-complex-encoded guanine nucleotide exchange factor Fgd2 reveals that two opposing signaling pathways promote transmission ratio distortion in the mouse. Genes Dev 21(2):143–147

    Article  PubMed  CAS  Google Scholar 

  • Bennett D (1975) The T-locus of the mouse. Cell 6:441–454

    Article  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580. Available at http://c3.biomath.mssm.edu/trf.submit.options.html

  • Bucan M, Herrmann BG, Frischauf AM, Bautch VL, Bode V et al (1987) Deletion and duplication of DNA sequences is associated with the embryonic lethal phenotype of the t9 complementation group of the mouse t complex. Genes Dev 1:376–385

    Article  PubMed  CAS  Google Scholar 

  • Chovnick A (1973) Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics 75:123–131

    PubMed  CAS  Google Scholar 

  • Curtis D, Clark SH, Chovnick A, Bender W (1989) Molecular analysis of recombination events in Drosophila. Genetics 122:653–661

    PubMed  CAS  Google Scholar 

  • Dembic Z, Singer PA, Klein J (1984) E0: a history of a mutation. EMBO J 3:1647–1654

    PubMed  CAS  Google Scholar 

  • Ebersole T, Lai F, Artzt K (1992) New molecular markers for the distal end of the t-complex and their relationships to mutations affecting mouse development. Genetics 131:175–182

    PubMed  CAS  Google Scholar 

  • Eppig JT, Bult CJ, Kadin JA, Richardson JE, Blake JA, members of the Mouse Genome Database Group (2005) The Mouse Genome Database (MGD): from genes to mice—a community resource for mouse biology. Nucleic Acids Res 33:D471–D475. Available at http://www.infomatics.jax.org/

  • Erhart MA, Phillips SJ, Bonhomme F, Boursout P, Wakeland EK et al (1989) Haplotypes that are mosaic for wild-type and t complex-specific alleles in wild mice. Genetics 12:405–415

    Google Scholar 

  • Erhart MA, Lekgothoane S, Grenier J, Nadeau JH (2002) Pattern of segmental recombination in the distal inversion of mouse t haplotypes. Mamm Genome 13:438–444

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1997) BioEdit version 7.0.0. Available at http://www.mbio.ncsu.edu/BioEdit/bioedit.html. Accessed 15 Aug 2007

  • Hammer MF, Silver LM (1993) Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes. Mol Biol Evol 10:971–1001

    PubMed  CAS  Google Scholar 

  • Hammer MF, Bliss S, Silver LM (1991) Genetic exchange across a paracentric inversion of the mouse t complex. Genetics 128:799–812

    PubMed  CAS  Google Scholar 

  • Heiman M (1997) Webcutter version 2.0. Available at http://www.rna.lundberg.gu.se/cutter2/

  • Huang SW, Ardlie KG, Yu HT (2001) Frequency and distribution of t-haplotypes in the southeast asian house mouse (Mus musculus castaneus) in Taiwan. Mol Ecol 10:2349–2354

    Article  PubMed  CAS  Google Scholar 

  • Hubbard TJ, Aken BL, Beal K, Ballester B, Caccamo M et al (2007) Ensembl 2007. Nucleic Acids Res 35(database issue):D610–D617. Available at http://www.ensembl.org/Mus_musculus/

    Google Scholar 

  • Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM et al (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14(4):528–538

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Subramanian S (2002) Mutation rates in mammalian genomes. Proc Natl Acad Sci USA 99:803–808

    Article  PubMed  CAS  Google Scholar 

  • Lyon MF (1984) Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell 37:621–628

    Article  PubMed  CAS  Google Scholar 

  • Lyon MF (2003) Transmission ratio distortion in mice. Ann Rev Genet 37:393–408

    Article  PubMed  CAS  Google Scholar 

  • Morita T, Kubota H, Murata K, Nozaki M, Delarbre C et al (1992) Evolution of the mouse t haplotype: recent and worldwide introgression to Mus musculus. Proc Natl Acad Sci USA 89:6851–6855

    Article  PubMed  CAS  Google Scholar 

  • Nadeau JH, Phillips SJ (1987) The putative oncogene Pim-1 in the mouse: its linkage and variation among t haplotypes. Genetics 117:533–541

    PubMed  CAS  Google Scholar 

  • Navarro A, Betran E, Barbadilla A, Ruiz A (1997) Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695–709

    PubMed  CAS  Google Scholar 

  • Neufeld E, Vincek V, Figueroa F, Klein J (1991) Limits of the distal inversion in the t complex of the house mouse: evidence from linkage disequilibria. Mamm Genome 1:242–248

    Article  PubMed  CAS  Google Scholar 

  • Novitski E, Braver G (1954) An analysis of crossing over within a heterozygous inversion in Drosophila melanogaster. Genetics 39:197–209

    PubMed  CAS  Google Scholar 

  • Perkins DD (1962) Crossing-over and interference in a multiply marked chromosome arm of Neurospora. Genetics 47:1253–1274

    PubMed  CAS  Google Scholar 

  • Phillips SJ, Nadeau JH (1984) Personal communication. Mouse Newslett 70:83

    Google Scholar 

  • Rozas J, Aguade M (1994) Gene conversion is involved in the transfer of genetic information between naturally occurring inversions of Drosophila. Proc Natl Acad Sci USA 91:11517–11521

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmer. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386. Available at http://frodo.wi.mit.edu/cgi-bin/primer3/primer3_www.cgi

  • Schaeffer SW, Anderson WW (2005) Mechanisms of genetic exchange within the chromosomal inversions of Drosophila pseudoobscura. Genetics 171:1729–1739

    Article  PubMed  CAS  Google Scholar 

  • Silver LM (1990) Gene dosage effects on transmission ratio distortion and fertility in mice that carry t haplotypes. Genet Res 54:221–225

    Article  Google Scholar 

  • Silver L (1993) The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet 9:250–254

    Article  PubMed  CAS  Google Scholar 

  • Silver LM, Remis D (1987) Five of the nine genetically defined regions of mouse t haplotypes are involved in transmission ratio distortion. Genet Res 49:51–56

    Article  PubMed  CAS  Google Scholar 

  • Skow LC, Nadeau JN, Ahn JC, Shin HS, Artzt K et al (1987) Polymorphism and linkage of the A-crystallin gene in t-haplotypes of the mouse. Genetics 116:107–111

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by NIH MBRS/SCORE grant GM08043 to MAE, and by a Chicago State University Biological Sciences Department assistantship to LTW in 2002 and 2003. The authors gratefully acknowledge the helpful comments on the manuscript by Dr. Joyce Ache Gana.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark A. Erhart.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wallace, L.T., Erhart, M.A. Recombination within mouse t haplotypes has replaced significant segments of t-specific DNA. Mamm Genome 19, 263–271 (2008). https://doi.org/10.1007/s00335-008-9103-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-008-9103-3

Keywords

Navigation