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Selection against Robertsonian fusions involving housekeeping genes in the house mouse: integrating data from gene expression arrays and chromosome evolution

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Abstract

Monobrachial homology resulting from Robertsonian (Rb) fusions is thought to contribute to chromosomal speciation through underdominance. Given the karyotypic diversity characterizing wild house mouse populations [Mus musculus domesticus, (MMU)], variation that results almost exclusively from Rb fusions (diploid numbers range from 22 to 40) and possibly whole arm reciprocal translocations (WARTs), this organism represents an excellent model for testing hypotheses of chromosomal evolution. Previous studies of chromosome size and recombination rates have failed to explain the bias for certain chromosomes to be involved more frequently than others in these rearrangements. Here, we show that the pericentromeric region of one such chromosome, MMU19, which is infrequently encountered as a fusion partner in wild populations, is significantly enriched for housekeeping genes when compared to other chromosomes in the genome. These data suggest that there is selection against breakpoints in the pericentromeric region and provide new insights into factors that constrain chromosomal reorganizations in house mice. Given the anticipated increase in vertebrate whole genome sequences, the examination of gene content and expression profiles of the pericentromeric regions of other mammalian lineages characterized by Rb fusions (i.e., other rodents, bats, and bovids, among others) is both achievable and crucial to developing broadly applicable models of chromosome evolution.

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Abbreviations

MMU:

Mus musculus domesticus

Rb:

Robertsonian

HSKP:

Housekeeping

DSBs:

Double strand breaks

PEV:

Position effect variegation

References

  • Baker RJ, Bickham JW (1986) Speciation by monobranchial centric fusions. Proc Natl Acad Sci USA 83:8245–8248

    Article  CAS  PubMed  Google Scholar 

  • Bourque G, Pevzner PA, Tesler G (2004) Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res 14:507–516

    Article  CAS  PubMed  Google Scholar 

  • Britton-Davidian J, Nadeau JH, Croset H, Thaler L (1989) Genetic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus). Genet Res 53:29–44

    Article  CAS  PubMed  Google Scholar 

  • Britton-Davidian J, Catalan J, Ramalhinho MD et al (2000) Rapid chromosomal evolution in island mice. Nature 403:158

    Article  CAS  PubMed  Google Scholar 

  • Britton-Davidian J, Catalan J, Ramalhinho MDG et al (2005) Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational processes. Genet Res Camb 86:171–183

    Article  CAS  Google Scholar 

  • Butte AJ, Dzau VJ, Glueck SB (2001) Further defining housekeeping, or “maintenance”, genes. Focus on “a compendium of gene expression in normal human tissues”. Physiol Genomics 7:95–96

    CAS  PubMed  Google Scholar 

  • Cattanach BM (1974) Position effect variegation in the mouse. Genet Res 23:291–306

    Article  CAS  PubMed  Google Scholar 

  • Cattanach BM (1975) Control of chromosome inactivation. Annu Rev Genet 9:1–18

    Article  CAS  PubMed  Google Scholar 

  • Dobie KW, Leet M, Fantest JA et al (1996) Variegated transgene expression in mouse mammary gland is determined by the transgene integration locus. Proc Natl Acad Sci USA 93:6659–6664

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg E, Levanon EY (2003) Human housekeeping genes are compact. Trends Genet 19:362–365

    Article  CAS  PubMed  Google Scholar 

  • Evans EP, Lyon MF, Daglish M (1967) A mouse translocation giving a metacentric marker chromosome. Cytogenet Cell Genet 6:105–119

    Article  CAS  Google Scholar 

  • Freilich S, Massingham T, Bhattacharyya S et al (2005) Relationship between the tissue-specificity of mouse gene expression and the evolutionary origin and function of the proteins. Genome Biol 6:R56

    Article  PubMed  Google Scholar 

  • Garagna S, Broccoli D, Redi CA, Searle JB, Cooke HJ, Cappana E (1995) Robertsonian metacentrics of the house mouse lose telomeric sequences but retain some minor satellite sequences DNA in the pericentromeric area. Chromosoma 103:685–692

    Article  CAS  PubMed  Google Scholar 

  • Garagna S, Marziliano N, Zuccotti M, Searle JB, Capanna E, Redi CA (2001) Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci U S A 98:171–175

    Article  CAS  PubMed  Google Scholar 

  • Garagna S, Zuccotti M, Capanna E, Redi CA (2002) High resolution organization of mouse telomeric and pericentromeric DNA. Cytogenet Genome Res 96:125–129

    Article  CAS  PubMed  Google Scholar 

  • Gazave E, Catalan J, Ramalhinho MD et al (2003) The non-random occurrence of Robertsonian fusion in the house mouse. Genet Res 81:33–42

    Article  CAS  PubMed  Google Scholar 

  • Kalitsis P, Griffiths B, Choo KH (2006) Mouse telomeric sequences reveal a high rate of homogenization and possible role in Robertsonian translocation. Proc Natl Acad Sci U S A 103:8786–8791

    Article  CAS  PubMed  Google Scholar 

  • King M (1993) Species evolution: the role of chromosome change. Cambridge University Press

  • Larkin DM, Pape G, Donthu R, Auvil L, Welge M, Lewin HA (2009) Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Res 19:770–777

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre C, Zaghloul L, Sagot MF et al (2009) Analysis of fine-scale mammalian evolutionary breakpoints provides new insight into their relation to genome organisation. BMC Genomics 10:335

    Article  PubMed  Google Scholar 

  • Nachman MW, Searle JB (1995) Why is the house mouse karyotype so variable? Trends Ecol Evol 10:397–402

    Article  Google Scholar 

  • Muller HJ (1930) Types of visible variations induced by X-rays in Drosophila. J Genet 22:299–334

    Article  Google Scholar 

  • Opsahl ML, McClenaghan M, Springbett A et al (2002) Multiple effects of genetic background on variegated transgene expression in mice. Genetics 160:1107–1112

    CAS  PubMed  Google Scholar 

  • Pedram M, Sprung CN, Gao Q, Lo AWI, Reynolds GE, Murnane JP (2006) Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol Cell Biol 26:1865–1878

    Article  CAS  PubMed  Google Scholar 

  • Pialek J, Hauffe HC, Searle JB (2005) Chromosomal variation in the house mouse. Biol J Linn Soc 84:535–563

    Article  Google Scholar 

  • Qumsiyeh MB (1994) Evolution of number and morphology of mammalian chromosomes. J Hered 85:455–465

    CAS  PubMed  Google Scholar 

  • Redi CA, Capanna E (1988) Robertsonian heterozygotes in the house mouse and the fate of their germ cells. In: Liss AR (ed) The cytogenetics of mammalian autosomal rearrangements. pp 315–359

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    Article  PubMed  Google Scholar 

  • Ruiz-Herrera A, Castresana J, Robinson TJ (2006) Is mammalian chromosomal evolution driven by regions of genome fragility? Genome Biol 7:R115

    Article  PubMed  Google Scholar 

  • Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E (2008) Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res 122:219–228

    Article  CAS  PubMed  Google Scholar 

  • Singer GAC, Lloyd AT, Huminiecki LB, Wolfe KH (2005) Clusters of co-expressed genes in mammalian genomes are conserved by natural selection. Mol Biol Evol 22:767–775

    Article  CAS  PubMed  Google Scholar 

  • Slijepcevic P (1998) Telomeres and mechanisms of Robertsonian fusion. Chromosoma 107:136–140

    Article  CAS  PubMed  Google Scholar 

  • Su AI, Wiltshire T, Batalov S et al (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101:6062–6067

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE, Anatskaya OV (2007) Organismal complexity, cell differentiation and gene expression: human over mouse. Nucleic Acids Res 35:6350–6356

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Rekaya R (2009) Comprehensive analysis of gene expression evolution between humans and mice. Evol Bioinform Online 5:81–90

    CAS  PubMed  Google Scholar 

  • White MJD (1978) Modes of speciation. Freeman, San Francisco

    Google Scholar 

  • White BJ, Tjio JH (1968) A mouse translocation with 38 and 39 chromosomes but normal NF. Hereditas 58:284

    Article  Google Scholar 

  • Williams EJB, Hurst LD (2002) Clustering of tissue-specific genes underlies much of the similarity in rates of protein evolution of linked genes. J Mol Evol 54:511–518

    Article  CAS  PubMed  Google Scholar 

  • Wu C, Orozco C, Boyer J et al (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:R130

    Article  PubMed  Google Scholar 

  • Zhao S, Shetty J, Hou L et al (2004) Human, mouse, and rat genome large-scale rearrangements: stability versus speciation. Genome Res 14:1851–1860

    Article  CAS  PubMed  Google Scholar 

  • Zhimulev IF (1988) Polytene chromosomes, heterochromatin, and position effect variegation. Adv Genet 37:1–555

    Article  Google Scholar 

  • Zhu J, He F, Song S, Wang J, Yu J (2008) How many human genes can be defined as housekeeping with current expression data? BMC Genomics 9:172

    Article  PubMed  Google Scholar 

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Acknowledgements

Financial support from Ministerio de Ciencia y Tecnologia and the Universitat Autònoma de Barcelona (Ph.D. fellowship to M.F.) are gratefully acknowledged. T.J.R. is funded by a grant from the South African National Research Foundation.

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Authors and Affiliations

  1. Departament de Biologia Cel.lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Campus UAB, 08193, Cerdanyola del Vallès, Barcelona, Spain

    Aurora Ruiz-Herrera, Marta Farré & Montserrat Ponsà

  2. Institut de Biotecnologia i Biomedicina, Campus UAB, 08193, Cerdanyola del Vallès, Barcelona, Spain

    Aurora Ruiz-Herrera

  3. Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa

    Terence J. Robinson

Authors
  1. Aurora Ruiz-Herrera
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  2. Marta Farré
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  3. Montserrat Ponsà
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  4. Terence J. Robinson
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Correspondence to Aurora Ruiz-Herrera.

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Responsible Editor: Herbert Macgregor.

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Ruiz-Herrera, A., Farré, M., Ponsà, M. et al. Selection against Robertsonian fusions involving housekeeping genes in the house mouse: integrating data from gene expression arrays and chromosome evolution. Chromosome Res 18, 801–808 (2010). https://doi.org/10.1007/s10577-010-9153-8

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  • DOI: https://doi.org/10.1007/s10577-010-9153-8

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