Skip to main content
×
×
Home

Different patterns of Robertsonian fusion pairing in Bovidae and the house mouse: the relationship between chromosome size and nuclear territories

  • PHILIPP L. WESCHE (a1) and TERENCE J. ROBINSON (a1)
Summary

Using a dataset of karyotypic changes reported for bovids and the house mouse (Mus musculus domesticus) together with information from the cattle (Bos taurus) and mouse genomes, we examined two principal variables that have been proposed to predict chromosomal positioning in the nucleus, chromosome size and GC content. These were expected to influence the distribution of Robertsonian (Rb) fusions, the predominant mode of chromosomal change in both taxa. We found the largest chromosomes to be most frequently involved in fusions in bovids, and confirm earlier reports that chromosomes of intermediate size were the most frequent fusers in mice. We then tested whether chromosomal positioning can explain Rb fusion frequencies. We classified chromosomes into groups by size and considered the frequency of interactions between specific groups. Among the interactions, mouse chromosomes showed a slight tendency to fuse with neighbouring chromosomes, in line with expectations of chromosomal positioning, but also resembling predictions from meiotic spindle-induced bias. Bovids, on the other hand, showed no trend in interactions, with small chromosomes being the least frequent partner for all size classes. We discuss the results in terms of nuclear organization at various cell cycle stages and the proposed mechanisms of Rb fusion formation, and note that the difference can be explained by (i) considering bovid species generally to be characterized by a greater intermingling of chromosomal size classes than the house mouse, or (ii) by the vastly different timescales underpinning their evolutionary histories.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Different patterns of Robertsonian fusion pairing in Bovidae and the house mouse: the relationship between chromosome size and nuclear territories
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Different patterns of Robertsonian fusion pairing in Bovidae and the house mouse: the relationship between chromosome size and nuclear territories
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Different patterns of Robertsonian fusion pairing in Bovidae and the house mouse: the relationship between chromosome size and nuclear territories
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602 South Africa. E-mail: mail@philippwesche.org
tjr@sun.ac.za
References
Hide All
Adega, F., Guedes-Pinto, H. & Chaves, R. (2009). Satellite DNA in the karyotype evolution of domestic animals – clinical considerations. Cytogenetic and Genome Research 126, 1220.
Arndt, P. F., Petrov, D. A. & Hwa, T. (2003). Distinct changes of genomic biases in nucleotide substitution at the time of mammalian radiation. Molecular Biology and Evolution 20, 18871896.
Ashley, T., Gaeth, A. P., Inagaki, H., Seftel, A., Cohen, M. M., Anderson, L. K., Kurahashi, H. & Emanuel, B. S. (2006). Meiotic recombination and spatial proximity in the etiology of the recurrent t(11;22). American Journal of Human Genetics 79, 524538.
Bandyopadhyay, R., Berend, S. A., Page, S. L., Choo, K. H. A. & Shaffer, L. G. (2001). Satellite III sequences on 14p and their relevance to Robertsonian translocation formation. Chromosome Research 9, 235242.
Belle, E. M. S., Duret, L., Galtier, N. & Eyre-Walker, A. (2004). The decline of isochores in mammals: an assessment of the GC content variation along the mammalian phylogeny. Journal of Molecular Evolution 58, 653660.
Berríos, S., Manterola, M., Prieto, Z., López-Fenner, J., Page, J. & Fernández-Donoso, R. (2010). Model of chromosome associations in Mus domesticus spermatocytes. Biological Research 43, 275295.
Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., Müller, S., Eils, R., Cremer, C., Speicher, M. R. & Cremer, T. (2005). Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biology 3, e157.
Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A. & Bickmore, W. A. (2001). The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Chromosome Research 9, 541567.
Branco, M. R. & Pombo, A. (2006). Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biology 4, e138.
Britton-Davidian, J., Catalan, J., da Graça Ramalhinho, M., Auffray, J.-C., Nunes, A. C., Gazave, E., Searle, J. B. & da Luz Mathias, M. (2005). Chromosomal phylogeny of Robertsonian races of the house mouse in the island of Madeira: testing between alternative mutational processes. Genetics Research 86, 171183.
Britton-Davidian, J., Catalan, J., da Graça Ramalhinho, M., Ganem, G., Auffray, J.-C., Capela, R., Biscoito, M., Searle, J. B. & da Luz Mathias, M. (2000). Environmental genetics: rapid chromosomal evolution in island mice. Nature 403, 158.
Choo, K. H., Vissel, B., Brown, R., Filby, R. G. & Earle, E. (1988). Homologous alpha satellite sequences on human acrocentric chromosomes with selectivity for chromosomes 13, 14 and 21: implications for recombination between nonhomologues and Robertsonian translocations. Nucleic Acids Research 16, 12731284.
Cremer, M., von Hase, J., Volm, T., Brero, A., Kreth, G., Walter, J., Fischer, C., Solovei, I., Cremer, C. & Cremer, T. (2001). Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Research 9, 541567.
Cremer, T. & Cremer, M. (2010). Chromosome territories. Cold Spring Harbor Perspectives in Biology 2, a003889.
Dietzel, S., Schiebel, K., Little, G., Edelmann, P., Rappold, G. A., Eils, R., Cremer, C. & Cremer, T. (1999). The 3D positioning of ANT2 and ANT3 genes within female X chromosome territories correlates with gene activity. Experimental Cell Research 252, 363375.
Dumitrache, L. C., Hu, L. & Hasty, P. (2009). TREX2 exonuclease defective cells exhibit double-strand breaks and chromosomal fragments but not Robertsonian translocations. Mutation Research 662, 8487.
Duret, L., Semon, M., Piganeau, G., Mouchiroud, D. & Galtier, N. (2002). Vanishing GC-rich isochores in mammalian genomes. Genetics 162, 18371847.
Eaker, S., Pyle, A., Cobb, J. & Handel, M. A. (2001). Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. Journal of Cell Science 114, 29532965.
Foster, H. A., Abeydeera, L. R., Griffin, D. K. & Bridger, J. M. (2005). Non-random chromosome positioning in mammalian sperm nuclei, with migration of the sex chromosomes during late spermatogenesis. Journal of Cell Science 118, 18111820.
Fraser, P. & Bickmore, W. (2007). Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413417.
Fritsch, C. C. & Langowski, J. (2011). Chromosome dynamics, molecular crowding, and diffusion in the interphase cell nucleus: a Monte Carlo lattice simulation study. Chromosome Research 19, 6381.
Garagna, S., Zuccotti, M., Thornhill, A., Fernandez-Donoso, R., Berrios, S., Capanna, E. & Redi, C. A. (2001). Alteration of nuclear architecture in male germ cells of chromosomally derived subfertile mice. Journal of Cell Science 114, 44294434.
Gauthier, P., Hima, K. & Dobigny, G. (2010). Robertsonian fusions, pericentromeric repeat organization and evolution: a case study within a highly polymorphic rodent species, Gerbillus nigeriae. Chromosome Research 18, 473486.
Gazave, E., Catalan, J., da Graça Ramalhinho, M., da Luz Mathias, M., Nunes, A. C., Dumas, D., Britton-Davidian, J. & Affray, J.-C. (2003). The non-random occurrence of Robertsonian fusion in the house mouse. Genetical Research 81, 3342.
Gilbert, N., Gilchrist, S. & Bickmore, W. A. (2005). Chromatin organization in the mammalian nucleus. International Review of Cytology 242, 283336.
Harper, L., Golubovskaya, I. & Cande, W. Z. (2004). A bouquet of chromosomes. Journal of Cell Science 117, 40254032.
Hecht, F. & Kimberling, W. J. (1971). Patterns of D chromosome involvement in human (DqDq) and (DqGq) Robertsonian rearrangements. American Journal of Human Genetics 23, 361367.
Koehler, D., Zakhartchenko, V., Froenicke, L., Stone, G., Stanyon, R., Wolf, E., Cremer, T. & Brero, A. (2009). Changes of higher order chromatin arrangements during major genome activation in bovine preimplantation embryos. Experimental Cell Research 315, 20532063.
Kosak, S. T. & Groudine, M. (2004). Form follows function: the genomic organization of cellular differentiation. Genes and Development 18, 13711384.
Kuraku, S., Ishijima, J., Nishida-Umehara, C., Agata, K., Kuratani, S. & Matsuda, Y. (2006). cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids. Chromosome Research 14, 187202.
Küpper, K., Kölbl, A., Biener, D., Dittrich, S., von Hase, J., Thormeyer, T., Fiegler, H., Carter, N. P., Speicher, M. R., Cremer, T. & Cremer, M. (2007). Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116, 285306.
Lercher, M. J., Urrutia, A. O. & Hurst, L. D. (2002). Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nature Genetics 31, 180183.
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., Sandstrom, R., Bernstein, B., Bender, M. A., Groudine, M., Gnirke, A., Stamatoyannopoulos, J., Mirny, L. A., Lander, E. S. & Dekker, J. (2009). Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289293.
Manterola, M., Page, J., Vasco, C., Berríos, S., Parra, M. T., Viera, A., Rufas, J. S., Zuccotti, M., Garagna, S. & Fernández-Donoso, R. (2009). A high incidence of meiotic silencing of unsynapsed chromatin is not associated with substantial pachytene loss in heterozygous male mice carrying multiple simple Robertsonian translocations. PLoS Genetics 5, e1000625.
Manuelidis, L. (1985). Individual interphase chromosome domains revealed by in situ hybridization. Human Genetics 71, 288293.
Mayer, R., Brero, A., von Hase, J., Schroeder, T., Cremer, T. & Dietzel, S. (2005). Common themes and cell type specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biology 6, 44.
Merico, V., Pigozzi, M. I., Esposito, A., Merani, M. S. & Garagna, S. (2003). Meiotic recombination and spermatogenic impairment in Mus musculus domesticus carrying multiple simple Robertsonian translocations. Cytogenetic and Genome Research 103, 321329.
Merico, V., de Barboza, G. D., Vasco, C., Ponce, R., Rodriguez, V., Garagna, S. & de Talamoni, N. T. (2008). A mitochondrial mechanism is involved in apoptosis of Robertsonian mouse male germ cells. Reproduction 135, 797804.
Mouse Genome Sequencing Consortium (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520562.
Nanda, I., Schneider-Rasp, S., Winking, H. & Schmid, M. (1995). Loss of telomeric sites in the chromosomes of Mus musculus domesticus (Rodentia: Muridae) during Robertsonian rearrangements. Chromosome Research 3, 399409.
Noordermeer, D., Branco, M. R., Splinter, E., Klous, P., van IJcken, W., Swagemakers, S., Koutsourakis, M., van der Spek, P., Pombo, A. & de Laat, W. (2008). Transcription and chromatin organization of a housekeeping gene cluster containing an integrated β-globin locus control region. PLoS Genetics 4, e1000016.
Nunes, A. C., Catalan, J., Lopez, J., da Graça Ramalhinho, M., da Luz Mathias, M. & Britton-Davidian, J. (2010). Fertility assessment in hybrids between monobrachially homologous Rb races of the house mouse from the island of Madeira: implications for modes of chromosomal evolution. Heredity 106, 348356.
Page, S. L., Shin, J.-C., Han, J.-Y., Choo, K. H. A. & Shaffer, L. G. (1996). Breakpoint diversity illustrates distinct mechanisms for Robertsonian translocation formation. Human Molecular Genetics 5, 12791288.
Parada, L. A., McQueen, P. G., Munson, P. J. & Misteli, T. (2002). Conservation of relative chromosome positioning in normal and cancer cells. Current Biology 12, 16921697.
Parada, L. A., Roix, J. J. & Misteli, T. (2003). An uncertainty principle in chromosome positioning. Trends in Cell Biology 13, 393396.
Pardo-Manuel de Vi llena, F. & Sapienza, C. (2001). Female meiosis drives karyotypic evolution in mammals. Genetics 159, 11791189.
Piálek, J., Hauffe, H. C. & Searle, J. B. (2005). Chromosomal variation in the house mouse. Biological Journal of the Linnean Society 84, 535563.
Robinson, T. J. & Ropiquet, A. (2011). Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Systematic Biology 60, 439450.
Romiguier, J., Ranwez, V., Douzery, E. J. P. & Galtier, N. (2010). Contrasting GC-content dynamics across 33 mammalian genomes: relationship with life-history traits and chromosome sizes. Genome Research 20, 10011009.
Rowley, J. D. & Pergament, E. (1969). Possible non random selection of D group chromosomes involved in centric-fusion translocations. Annals of Genetics 12, 177183.
Ruiz-Herrera, A., Farré, M., Ponsà, M. & Robinson, T. J. (2010). Selection against Robertsonian fusions involving housekeeping genes in the house mouse: integrating data from gene expression arrays and chromosome evolution. Chromosome Research 18, 801808.
Schardin, M., Cremer, T., Hager, H. D. & Lang, M. (1985). Specific staining of human chromosomes in Chinese hamster×man hybrid cell lines demonstrates interphase chromosome territories. Human Genetics 71, 281287.
Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Härle, M. & Cremer, T. (1996). Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. Journal of Cell Biology 134, 11091125.
Scheuermann, M. O., Tajbakhsh, J., Kurz, A., Saracoglu, K., Eils, R. & Lichter, P. (2004). Topology of genes and nontranscribed sequences in human interphase nuclei. Experimental Cell Research 301, 266279.
Skinner, B. M., Völker, M., Ellis, M. & Griffin, D. K. (2009). An appraisal of nuclear organization in interphase embryonic fibroblasts of chicken, turkey, and duck. Cytogenetic and Genome Research 126, 156164.
Slijepcevic, P., Hande, M. P., Bouffler, S. D.Lansdorp, P. & Bryant, P. E. (1997). Telomere length, chromatin structure and chromosome fusigenic potential. Chromosoma 106, 413421.
Su, A. I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K. A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., Cooke, M. P., Walker, J. R. & Hogenesch, J. B. (2004). A gene atlas of the mouse and human protein-encoding transcriptomes. Proceedings of the National Academy of Sciences USA 101, 60626067.
Sun, H. B., Shen, J. & Yokota, H. (2000). Size-dependent positioning of human chromosomes in interphase nuclei. Biophysical Journal 79, 184190.
Treff, N. R., Su, J., Taylor, D. & Scott, R. T. Jr. (2011). Telomere DNA deficiency is associated with development of human embryonic aneuploidy. PLoS Genetics 7, e1002161.
Vavouri, T. & Lehner, B. (2011). Chromatin organization in sperm may be the major functional consequence of base composition variation in the human genome. PLoS Genetics 7, e1002036.
Wise, J. L., Crout, R. J., McNeil, D. W., Weyant, R. J., Marazita, M. L. & Wenger, S. L. (2009). Human telomere length correlates to the size of the associated chromosome arm. PLoS One 4, e6013.
Zirbel, R. M., Mathieu, U. R., Kurz, A., Cremer, T. & Lichter, P. (1993). Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Research 1, 93–106.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Genetics Research
  • ISSN: 0016-6723
  • EISSN: 1469-5073
  • URL: /core/journals/genetics-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×
Type Description Title
PDF
Supplementary materials

Wesche supplementary material
Wesche supplementary material

 PDF (460 KB)
460 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed