Chromosoma

, Volume 113, Issue 1, pp 34–41

Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study

  • G. Dobigny
  • C. Ozouf-Costaz
  • C. Bonillo
  • V. Volobouev
Research Article

Abstract

X-autosome translocations are highly deleterious chromosomal rearrangements due to meiotic disruption, the effects of X-inactivation on the autosome, and the necessity of maintaining different replication timing patterns between the two segments. In spite of this, X-autosome translocations are not uncommon. We here focus on the genus Taterillus (Rodentia, Gerbillinae) which provides two sister lineages differing by two autosome–gonosome translocations. Despite the recent and dramatic chromosomal repatterning characterising these lineages, the X-autosome translocated species all display intercalary heterochromatic blocks (IHBs) between the autosomal and the ancestral sexual segments. These blocks, composed of highly amplified telomeric repeats and rDNA clusters, are not observed on the chromosomes of the non-translocated species, nor the Y1 and Y2 of the translocated species. Such IHBs are found in all mammals documented for X-autosome translocation. We propose an epigenomic hypothesis which explains the viability of X-autosome translocations in mammals. This posits that constitutive heterochromatin is probably selected for in X-autosome translocations since it may (1) prevent facultative heterochromatinization of the inactivated X from spreading to the autosomal part, and (2) allow for the independent regulation of replication timing of the sex and autosomal segments.

References

  1. Aagaard L, Schmid M, Warburton P, Jenuwein T (2000) Mitotic phosphorylation of Suv39H1, a novel component of active centromere, coincides with transient accumulation at mammalian centromeres. J Cell Sci 113:817–829PubMedGoogle Scholar
  2. Ashley T (2002) X-autosome translocations, meiotic synapsis, chromosome evolution and speciation. Cytogenet Genome Res 96:33–39CrossRefPubMedGoogle Scholar
  3. Avner D, Heard E (2001) X-chromosome inactivation: counting, choice and initiation. Nat Genet 2:59–67CrossRefGoogle Scholar
  4. Bailey JA, Carrel L, Chakravarti A, Eichler EE (2000) Molecular evidence for a relationship between LINE-1 elements and chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci USA 97:6634–6639CrossRefPubMedGoogle Scholar
  5. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo-domain. Nature 410:120–124CrossRefPubMedGoogle Scholar
  6. Bell AC, West AG, Felsenfeld G (2001) Insulators and boundaries: versatile elements in the eukaryotic genome. Science 291:447–450CrossRefPubMedGoogle Scholar
  7. Benazzou T (1984) Contribution à l’étude chromosomique et de la diversification biochimique des Gerbillidés (Rongeurs). PhD thesis. Université de Paris XI, OrsayGoogle Scholar
  8. Boggs BA, Chinault AC (1994) Analysis of replication timing properties of human X-chromosomal loci by fluorescence in situ hybridization. Proc Natl Acad Sci USA 91:6083–6087PubMedGoogle Scholar
  9. Boissinot S, Entezam A, Furano AV (2001) Selection against deleterious LINE-1 containing loci in the human lineage. Mol Biol Evol 18:926–935PubMedGoogle Scholar
  10. Boumil RM, Lee JT (2000) Forty years of decoding the silence in X-chromosome inactivation. Hum Mol Genet 10:2225–2232Google Scholar
  11. Boyle L, Ballard SG, Ward DC (1990) Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc Natl Acad Sci USA 87:7757–7761PubMedGoogle Scholar
  12. Brockdorff N (1998) The role of Xist in X-inactivation. Curr Opin Genet Dev 8:328–333CrossRefPubMedGoogle Scholar
  13. Carrel L, Cottle AA, Goglin KC, Willard HF (1999) A first-generation X-inactivation profile of the human X chromosome. Proc Natl Acad Sci USA 96:14440–14444CrossRefPubMedGoogle Scholar
  14. Claudio PP, Tonini T, Giordano A (2002) The retinoblastoma family: twins or distant cousins? Genome Biol 3:3012.1–3012.9CrossRefGoogle Scholar
  15. Cost GJ, Golding A, Schlissel MS, Boeke JD (2001) Target DNA chromatinization modulates nicking by L1 endonuclease. Nucl Acid Res 29:573–577CrossRefGoogle Scholar
  16. Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ, Oliver SG (2003) Engineering evolution to study speciation in yeasts. Nature 422:68–72CrossRefPubMedGoogle Scholar
  17. Disteche CM (1999) Escapees on the X chromosome. Proc Natl Acad Sci USA 96:14180–14182CrossRefPubMedGoogle Scholar
  18. Dobigny G (2002) Spéciation chromosomique chez les espèces jumelles ouest-africaines du genre Taterillus (Rodentia, Gerbillinae): implications systématiques et biogéographiques, hypothèses génomiques. PhD thesis. Museum National d’Histoire Naturelle, ParisGoogle Scholar
  19. Dobigny G, Aniskin V, Volobouev V (2002a) Explosive chromosomal evolution and speciation in the gerbil genus Taterillus (Rodentia, Gerbillinae): a case of two new cryptic species. Cytogenet Genome Res 96:117–124CrossRefPubMedGoogle Scholar
  20. Dobigny G, Baylac M, Denys C (2002b) Geometric morphometrics, neural networks and diagnosis of sibling Taterillus species (Rodentia, Gerbillinae). Biol J Linnean Soc 77:319–327CrossRefGoogle Scholar
  21. Dobigny G, Granjon L, Aniskin V, Bâ K, Volobouev V (2003a) A new sibling species of Taterillus (Rodentia, Gerbillinae) from West Africa. Mamm Biol 68:299–316Google Scholar
  22. Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2003b) Evolution of rRNA genes clusters and telomeric evolution during explosive genome repatterning in Taterillus (Rodentia, Gerbillinae). Cytogenet Genome Res (in press)Google Scholar
  23. Duthie SM, Nesterova TB, Formstone EJ, Keohane AM, Turner BM, Zakian SM, Brockdorff N (1999) Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum Mol Genet 8:195–204CrossRefPubMedGoogle Scholar
  24. Eissenberg JC, Elgin SCR (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10:204–210CrossRefPubMedGoogle Scholar
  25. Fischer C, Ozouf-Costaz C, Roest Crollius H, Dasilva C, Jaillon O, Bouneau L, Bonillo C, Weissenbach J, Bernot A (2000) Karyotype and chromosomal location of characteristic tandem repeats in the pufferfish Tetraodon nigroviridis. Cytogenet Cell Genet 88:50–55CrossRefPubMedGoogle Scholar
  26. Gilbert DM (2002) Replication timing and transcriptional control: beyond cause and effects. Curr Opin Cell Biol 14:377–383CrossRefPubMedGoogle Scholar
  27. Goto T, Monk M (1998) Regulation of X-chromosome inactivation in development in mice and human. Microbiol Mol Biol Evol 62:362–378Google Scholar
  28. Hansen RS (2003) X inactivation-specific methylation of LINE-1 elements by the DNMT3b: implications for the Lyon repeat hypothesis. Hum Mol Genet 12:2559–2567CrossRefPubMedGoogle Scholar
  29. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080CrossRefPubMedGoogle Scholar
  30. Kasahara S, Dutrillaux B (1983) Chromosome banding patterns of four species of bats, with special reference to a case of X-autosome translocation. Ann Genet 26:197–201PubMedGoogle Scholar
  31. King M (1993) Species evolution: the role of chromosomal change. Cambridge University, CambridgeGoogle Scholar
  32. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120CrossRefPubMedGoogle Scholar
  33. Lifschytz E, Lindsley DL (1972) The role of X-chromosome inactivation during spermatogenesis. Proc Natl Acad Sci USA 69:182–189PubMedGoogle Scholar
  34. Lin CC, Sasi R, Fan YS, Chen ZQ (1991) New evidence for tandem chromosome fusions in the karyotypic evolution of Asian muntjacs. Chromosoma 101:19–24PubMedGoogle Scholar
  35. Lyon MF (1961) Gene action in the X chromosome of the mouse (Mus musculus L.). Nature 190:372–373Google Scholar
  36. Lyon MF (2000) LINE-1 elements and X chromosome inactivation: a function for “junk” DNA? Proc Natl Acad Sci USA 97:6248–6249CrossRefPubMedGoogle Scholar
  37. Metcalfe CJ, Eldridge MCB, Toder R, Jonhston PG (1998) Mapping the distribution of the teloméric sequence (T2AG3) in the Macropodidae (Marsupilia) by fluorescence in situ hybridization. I. The swamp wallaby, Wallabia bicolor. Chromosome Res 6:603–610CrossRefPubMedGoogle Scholar
  38. Metzler-Guillemain C, Luciani J, Depetris D, Guichaoua MR, Mattei MG (2003) HP1b and HP1g, but not HP1a, decorate the entire XY body during human male meiosis. Chromosome Res 11:73–81CrossRefPubMedGoogle Scholar
  39. Mulligan G, Jacks T (1998) The retinoblastoma gene family: cousins with overlapping interests. Trends Genet 14:223–226CrossRefPubMedGoogle Scholar
  40. Neitzel H (1982) Karyotypenevolution und deren Bedeutung für den Speciationprozess der Cerviden (Cervidae, Artiodactyla, Mammalia). PhD thesis. University of BerlinGoogle Scholar
  41. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O’Caroll D, Firestein R, Cleary M, Jenuwein T, Herrera RE, Kouzarides T (2001) Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561–565CrossRefPubMedGoogle Scholar
  42. Parish DA, Vise P, Wichman HA, Bull JJ, Baker RJ (2002) Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 96:191–197CrossRefPubMedGoogle Scholar
  43. Peters AHFM, Mermoud JE, O’Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T (2002) Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 30:77–80CrossRefPubMedGoogle Scholar
  44. Quack B, Speed RM, Luciani JM, Noel B, Guichaoua M, Chandley AC (1988) Meiotic analysis of two human reciprocal X-autosome translocations. Cytogenet Cell Genet 48:43–47PubMedGoogle Scholar
  45. Ratomponirina C, Viegas-Péquignot E, Dutrillaux B, Petter F, Rumpler Y (1986) Synaptonemal complexes in Gerbillidae: probable role of intercaled heterochromatin in gonosome–autosome translocations. Cytogenet Cell Genet 43:161–167PubMedGoogle Scholar
  46. Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599CrossRefPubMedGoogle Scholar
  47. Ringrose L, Paro R (2001) Cycling silence. Nature 412:493–494CrossRefPubMedGoogle Scholar
  48. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972CrossRefGoogle Scholar
  49. Searle JB (1993) Chromosomal hybrid zones in Eutherian Mammals. In: Harrison H (ed) Hybrid zones and the evolutionary process. Oxford University, Oxford, pp 309–353Google Scholar
  50. Sharp AJ, Spotswood HT, Robinson DO, Turner BM, Jacobs PA (2002) Molecular and cytogenetic analysis of the spreading of X inactivation in X:autosome translocations. Hum Mol Genet 11:3145–3146CrossRefPubMedGoogle Scholar
  51. Shi L, Yang F, Kumamoto A (1991) The chromosomes of tufted deer (Elaphodus cephalophus). Cytogenet Cell Genet 56:189–192CrossRefPubMedGoogle Scholar
  52. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45CrossRefPubMedGoogle Scholar
  53. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306PubMedGoogle Scholar
  54. Vassart T (1994) Evolution et diversité génétique chez les gazelles (Gazella): apports de l’électrophorèse des protéines, de la cytogénétique et des microsatellites. PhD thesis. Université de Paris XI, OrsayGoogle Scholar
  55. Vaute O, Nicolas E, Vandel L, Trouche D (2002) Functional and physical interaction between the histone methyltransferase Suv39H1 and histone deacetylases. Nucl Acid Res 30:475–481CrossRefGoogle Scholar
  56. Vidal A, Koff A (2000) Cell-cycle inhibitors: three families united by a common cause. Gene 247:1–15CrossRefPubMedGoogle Scholar
  57. Viegas-Péquignot E, Dutrillaux B (1978) Une méthode simple pour obtenir des prophases et des prométaphases. Ann Genet 21:122–125Google Scholar
  58. Viegas-Péquignot E, Benazzou T, Dutrillaux B, Petter F (1982) Complex evolution of sex chromosomes in Gerbillidae (Rodentia). Cytogenet Cell Genet 34:158–167PubMedGoogle Scholar
  59. Volobouev V, Granjon L (1996) A finding of the XX/XY1Y2 sex-chromosome system in Taterillus arenarius (Gerbillinae, Rodentia) and its phylogenetic implications. Cytogenet Cell Genet 75:45–48PubMedGoogle Scholar
  60. Watson JM, Spencer JA, Riggs AD, Graves JAM (1991) Sex chromosome evolution: Platypus gene mapping suggests that part of the human X chromosome was originally autosomal. Proc Natl Acad Sci USA 88:11256–11260PubMedGoogle Scholar
  61. White MJD (1973) Animal cytology and evolution, 3rd edn. Cambridge University, CambridgeGoogle Scholar
  62. White WM, Willard HF, Van Dyke DL, Wolffe DJ (1998) The spreading of X inactivation into autosomal material of an X-autosome translocation: evidence for a difference between autosomal and X-chromosomal DNA. Am J Hum Genet 63:20–28CrossRefPubMedGoogle Scholar
  63. Yang F, O’Brien PCM, Wienberg J, Ferguson-Smith MA (1997) A reappraisal of the tandem fusion theory of karyotype evolution in the Indian muntjac using chromosome painting. Chromosome Res 5:109–117CrossRefPubMedGoogle Scholar
  64. Zhang P (1999) The cell cycle and development: redundant roles of cell cycle regulators. Curr Opin Cell Biol 11:655–662CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • G. Dobigny
    • 1
    • 2
    • 3
  • C. Ozouf-Costaz
    • 2
  • C. Bonillo
    • 2
  • V. Volobouev
    • 1
  1. 1.Laboratoire Origine, Structure et Evolution de la BiodiversitéMuséum National d’Histoire NaturelleParisFrance
  2. 2.Service de Systématique MoléculaireMNHNParisFrance
  3. 3.Evolutionary Genomics Group, Department of ZoologyUniversity of StellenboschMatielandSouth Africa

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