Abstract
We have shown previously that the progeny of crosses between heterozygous females and C57BL/6 males show transmission ratio distortion at the Om locus on mouse chromosome 11. This result has been replicated in several independent experiments. Here we show that the distortion maps to a single locus on chromosome 11, closely linked to Om, and that gene conversion is not implicated in the origin of this phenomenon. To further investigate the origin of the transmission ratio distortion we generated a test using the well-known effect of recombination on maternal meiotic drive. The genetic test presented here discriminates between unequal segregation of alleles during meiosis and lethality, based on the analysis of genotype at both the distorted locus and the centromere of the same chromosome. We used this test to determine the cause of the transmission ratio distortion observed at the Om locus. Our results indicate that transmission ratio distortion at Om is due to unequal segregation of alleles to the polar body at the second meiotic division. Because the presence of segregation distortion at Om also depends on the genotype of the sire, our results confirm that the sperm can influence segregation of maternal chromosomes to the second polar body.
Full Text
The Full Text of this article is available as a PDF (129.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Agulnik S. I., Agulnik A. I., Ruvinsky A. O. Meiotic drive in female mice heterozygous for the HSR inserts on chromosome 1. Genet Res. 1990 Apr;55(2):97–100. doi: 10.1017/s0016672300025325. [DOI] [PubMed] [Google Scholar]
- Agulnik S. I., Sabantsev I. D., Ruvinsky A. O. Effect of sperm genotype on chromatid segregation in female mice heterozygous for aberrant chromosome 1. Genet Res. 1993 Apr;61(2):97–100. doi: 10.1017/s0016672300031190. [DOI] [PubMed] [Google Scholar]
- Babinet C., Richoux V., Guénet J. L., Renard J. P. The DDK inbred strain as a model for the study of interactions between parental genomes and egg cytoplasm in mouse preimplantation development. Dev Suppl. 1990:81–87. [PubMed] [Google Scholar]
- Baldacci P. A., Cohen-Tannoudji M., Kress C., Pournin S., Babinet C. A high-resolution map around the locus Om on mouse Chromosome 11. Mamm Genome. 1996 Feb;7(2):114–116. doi: 10.1007/s003359900030. [DOI] [PubMed] [Google Scholar]
- Baldacci P. A., Richoux V., Renard J. P., Guénet J. L., Babinet C. The locus Om, responsible for the DDK syndrome, maps close to Sigje on mouse chromosome 11. Mamm Genome. 1992;2(2):100–105. doi: 10.1007/BF00353857. [DOI] [PubMed] [Google Scholar]
- Biddle F. G. Segregation distortion of X-linked marker genes in interspecific crosses between Mus musculus and M. spretus. Genome. 1987 Apr;29(2):389–392. doi: 10.1139/g87-067. [DOI] [PubMed] [Google Scholar]
- Canham R. P., Birdsall D. A., Cameron D. G. Disturbed segregation at the transferrin locus of the deer mouse. Genet Res. 1970 Dec;16(3):355–357. doi: 10.1017/s0016672300002639. [DOI] [PubMed] [Google Scholar]
- Ceci J. D., Siracusa L. D., Jenkins N. A., Copeland N. G. A molecular genetic linkage map of mouse chromosome 4 including the localization of several proto-oncogenes. Genomics. 1989 Nov;5(4):699–709. doi: 10.1016/0888-7543(89)90111-0. [DOI] [PubMed] [Google Scholar]
- Chakraborty R., Stivers D. N., Deka R., Yu L. M., Shriver M. D., Ferrell R. E. Segregation distortion of the CTG repeats at the myotonic dystrophy locus. Am J Hum Genet. 1996 Jul;59(1):109–118. [PMC free article] [PubMed] [Google Scholar]
- Crow J. F. Unmasking a cheating gene. Science. 1999 Mar 12;283(5408):1651–1652. doi: 10.1126/science.283.5408.1651. [DOI] [PubMed] [Google Scholar]
- Dawe R. K., Cande W. Z. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8512–8517. doi: 10.1073/pnas.93.16.8512. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dietrich W. F., Miller J. C., Steen R. G., Merchant M., Damron D., Nahf R., Gross A., Joyce D. C., Wessel M., Dredge R. D. A genetic map of the mouse with 4,006 simple sequence length polymorphisms. Nat Genet. 1994 Jun;7(2 Spec No):220–245. doi: 10.1038/ng0694supp-220. [DOI] [PubMed] [Google Scholar]
- Eaves I. A., Bennett S. T., Forster P., Ferber K. M., Ehrmann D., Wilson A. J., Bhattacharyya S., Ziegler A. G., Brinkmann B., Todd J. A. Transmission ratio distortion at the INS-IGF2 VNTR. Nat Genet. 1999 Aug;22(4):324–325. doi: 10.1038/11890. [DOI] [PubMed] [Google Scholar]
- Evans K., Fryer A., Inglehearn C., Duvall-Young J., Whittaker J. L., Gregory C. Y., Butler R., Ebenezer N., Hunt D. M., Bhattacharya S. Genetic linkage of cone-rod retinal dystrophy to chromosome 19q and evidence for segregation distortion. Nat Genet. 1994 Feb;6(2):210–213. doi: 10.1038/ng0294-210. [DOI] [PubMed] [Google Scholar]
- Johnson K. R., Cook S. A., Davisson M. T. Identification and genetic mapping of 151 dispersed members of 16 ribosomal protein multigene families in the mouse. Mamm Genome. 1994 Nov;5(11):670–687. doi: 10.1007/BF00426073. [DOI] [PubMed] [Google Scholar]
- Justice M. J., Siracusa L. D., Gilbert D. J., Heisterkamp N., Groffen J., Chada K., Silan C. M., Copeland N. G., Jenkins N. A. A genetic linkage map of mouse chromosome 10: localization of eighteen molecular markers using a single interspecific backcross. Genetics. 1990 Aug;125(4):855–866. doi: 10.1093/genetics/125.4.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaszás E., Birchler J. A. Meiotic transmission rates correlate with physical features of rearranged centromeres in maize. Genetics. 1998 Dec;150(4):1683–1692. doi: 10.1093/genetics/150.4.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magee A. C., Hughes A. E. Segregation distortion in myotonic dystrophy. J Med Genet. 1998 Dec;35(12):1045–1046. doi: 10.1136/jmg.35.12.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mann J. R. DDK egg-foreign sperm incompatibility in mice is not between the pronuclei. J Reprod Fertil. 1986 Mar;76(2):779–781. doi: 10.1530/jrf.0.0760779. [DOI] [PubMed] [Google Scholar]
- Merrill C., Bayraktaroglu L., Kusano A., Ganetzky B. Truncated RanGAP encoded by the Segregation Distorter locus of Drosophila. Science. 1999 Mar 12;283(5408):1742–1745. doi: 10.1126/science.283.5408.1742. [DOI] [PubMed] [Google Scholar]
- Montagutelli X., Turner R., Nadeau J. H. Epistatic control of non-Mendelian inheritance in mouse interspecific crosses. Genetics. 1996 Aug;143(4):1739–1752. doi: 10.1093/genetics/143.4.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Montgomery J. C., Silverman K. A., Buchberg A. M. Encyclopedia of the mouse genome VII. Mouse chromosome 11. Mamm Genome. 1998;8(Spec No):S215–S240. doi: 10.1007/s003359900656. [DOI] [PubMed] [Google Scholar]
- Naumova A. K., Leppert M., Barker D. F., Morgan K., Sapienza C. Parental origin-dependent, male offspring-specific transmission-ratio distortion at loci on the human X chromosome. Am J Hum Genet. 1998 Jun;62(6):1493–1499. doi: 10.1086/301860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nur U. Maintenance of a "Parasitic" B Chromosome in the Grasshopper MELANOPLUS FEMUR-RUBRUM. Genetics. 1977 Nov;87(3):499–512. doi: 10.1093/genetics/87.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pardo-Manual de Villena F., Slamka C., Fonseca M., Naumova A. K., Paquette J., Pannunzio P., Smith M., Verner A., Morgan K., Sapienza C. Transmission-ratio distortion through F1 females at chromosome 11 loci linked to Om in the mouse DDK syndrome. Genetics. 1996 Apr;142(4):1299–1304. doi: 10.1093/genetics/142.4.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pardo-Manuel de Villena F., Naumova A. K., Verner A. E., Jin W. H., Sapienza C. Confirmation of maternal transmission ratio distortion at Om and direct evidence that the maternal and paternal "DDK syndrome" genes are linked. Mamm Genome. 1997 Sep;8(9):642–646. doi: 10.1007/s003359900529. [DOI] [PubMed] [Google Scholar]
- Pardo-Manuel de Villena F., de la Casa-Esperón E., Verner A., Morgan K., Sapienza C. The maternal DDK syndrome phenotype is determined by modifier genes that are not linked to Om. Mamm Genome. 1999 May;10(5):492–497. doi: 10.1007/s003359901029. [DOI] [PubMed] [Google Scholar]
- Renard J. P., Babinet C. Identification of a paternal developmental effect on the cytoplasm of one-cell-stage mouse embryos. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6883–6886. doi: 10.1073/pnas.83.18.6883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhoades M M. Preferential Segregation in Maize. Genetics. 1942 Jul;27(4):395–407. doi: 10.1093/genetics/27.4.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhoades M. M., Dempsey E. The Effect of Abnormal Chromosome 10 on Preferential Segregation and Crossing over in Maize. Genetics. 1966 May;53(5):989–1020. doi: 10.1093/genetics/53.5.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhoades M. M., Vilkomerson H. On the Anaphase Movement of Chromosomes. Proc Natl Acad Sci U S A. 1942 Oct;28(10):433–436. doi: 10.1073/pnas.28.10.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rowe L. B., Nadeau J. H., Turner R., Frankel W. N., Letts V. A., Eppig J. T., Ko M. S., Thurston S. J., Birkenmeier E. H. Maps from two interspecific backcross DNA panels available as a community genetic mapping resource. Mamm Genome. 1994 May;5(5):253–274. doi: 10.1007/BF00389540. [DOI] [PubMed] [Google Scholar]
- Rubinsztein D. C., Leggo J. Non-Mendelian transmission at the Machado-Joseph disease locus in normal females: preferential transmission of alleles with smaller CAG repeats. J Med Genet. 1997 Mar;34(3):234–236. doi: 10.1136/jmg.34.3.234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruvinsky A. O., Agulnik S. I., Agulnik A. I., Belyaev D. K. The influence of mutations on chromosome 17 upon the segregation of homologues in female mice heterozygous for Robertsonian translocations. Genet Res. 1987 Dec;50(3):235–237. doi: 10.1017/s0016672300023752. [DOI] [PubMed] [Google Scholar]
- Ruvinsky A. Meiotic drive in female mice: an essay. Mamm Genome. 1995 May;6(5):315–320. doi: 10.1007/BF00364793. [DOI] [PubMed] [Google Scholar]
- Sapienza C., Paquette J., Pannunzio P., Albrechtson S., Morgan K. The polar-lethal Ovum mutant gene maps to the distal portion of mouse chromosome 11. Genetics. 1992 Sep;132(1):241–246. doi: 10.1093/genetics/132.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shendure J., Melo J. A., Pociask K., Derr R., Silver L. M. Sex-restricted non-Mendelian inheritance of mouse chromosome 11 in the offspring of crosses between C57BL/6J and (C57BL/6J x DBA/2J)F1 mice. Mamm Genome. 1998 Oct;9(10):812–815. doi: 10.1007/s003359900872. [DOI] [PubMed] [Google Scholar]
- Silver L. M. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 1993 Jul;9(7):250–254. doi: 10.1016/0168-9525(93)90090-5. [DOI] [PubMed] [Google Scholar]
- Siracusa L. D., Alvord W. G., Bickmore W. A., Jenkins N. A., Copeland N. G. Interspecific backcross mice show sex-specific differences in allelic inheritance. Genetics. 1991 Aug;128(4):813–821. doi: 10.1093/genetics/128.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vongs A., Kakutani T., Martienssen R. A., Richards E. J. Arabidopsis thaliana DNA methylation mutants. Science. 1993 Jun 25;260(5116):1926–1928. doi: 10.1126/science.8316832. [DOI] [PubMed] [Google Scholar]
- Vorechovský I., Webster A. D., Plebani A., Hammarström L. Genetic linkage of IgA deficiency to the major histocompatibility complex: evidence for allele segregation distortion, parent-of-origin penetrance differences, and the role of anti-IgA antibodies in disease predisposition. Am J Hum Genet. 1999 Apr;64(4):1096–1109. doi: 10.1086/302326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wakasugi N. Studies on fertility of DDK mice: reciprocal crosses between DDK and C57BL/6J strains and experimental transplantation of the ovary. J Reprod Fertil. 1973 May;33(2):283–291. doi: 10.1530/jrf.0.0330283. [DOI] [PubMed] [Google Scholar]
- Wakasugi N., Tomita T., Kondo K. Differences of fertility in reciprocal crosses between inbred strains of mice. DDK, KK and NC. J Reprod Fertil. 1967 Feb;13(1):41–50. doi: 10.1530/jrf.0.0130041. [DOI] [PubMed] [Google Scholar]
- Weinstein A. The Theory of Multiple-Strand Crossing over. Genetics. 1936 May;21(3):155–199. doi: 10.1093/genetics/21.3.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu H. G., Hiatt E. N., Chan A., Sweeney M., Dawe R. K. Neocentromere-mediated chromosome movement in maize. J Cell Biol. 1997 Nov 17;139(4):831–840. doi: 10.1083/jcb.139.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao H., McPeek M. S., Speed T. P. Statistical analysis of chromatid interference. Genetics. 1995 Feb;139(2):1057–1065. doi: 10.1093/genetics/139.2.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de la Casa-Esperon E., Pardo-Manuel de Villena F., Verner A. E., Briscoe T. L., Malette J. M., Rosa M., Jin W. H., Sapienza C. Sex-of-offspring-specific transmission ratio distortion on mouse chromosome X. Genetics. 2000 Jan;154(1):343–350. doi: 10.1093/genetics/154.1.343. [DOI] [PMC free article] [PubMed] [Google Scholar]