Marsupial Centomeres and Telomeres: Dynamic Chromosome Domains



What has become clear from a synthesis of work on marsupial chromosomes over the last 100 years is that the centromere is more than simply an architectural feature of the chromosome. Rather, it has been participant, either directly or indirectly, in the evolution of the diversity of karyotypes observed in marsupials. Across marsupial lineages, a family of model species stands out as an ideal system in which to study centromere function and evolution: macropodines (kangaroos and wallabies). This chapter focuses on the study of centromeres in marsupials, as both a region critical to ensuring the distribution of sister chromatids to daughter cells during cell division and a chromosomal domain involved in karyotypic stability and evolution. We will explore the role played by elements found at centromeres and telomeres in cell division and karyotypic change as supported by both historic and current experimental evidence.


Centromere Telomere Small RNA Retroelement KERV 


  1. Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937.PubMedCrossRefGoogle Scholar
  2. Archer M (1984) Evolution of arid Australia and its consequences for vertebrates. In: Archer M, Clayton G (eds) Vertebrate Zoogeography and Evolution in Australasia. Southwood Press, Marrickville.Google Scholar
  3. Bailey JA, Baertsch R, Kent WJ, Haussler D, Eichler EE (2004) Hotspots of mammalian chromosomal evolution. Genome Biol 5:R23.PubMedCrossRefGoogle Scholar
  4. Baverstock PR, Krieg M, Birrell J (1990) Evolutionary Relationships of Australian Marsupials and Assessed by Albumin Immunology. Aust J Zool 37:273–287.CrossRefGoogle Scholar
  5. Bourque G, Pevzner PA (2002) Genome-scale evolution: reconstructing gene orders in the ancestral species. Genome Res 12:26–36.PubMedGoogle Scholar
  6. Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci USA 103:8709–8714.PubMedCrossRefGoogle Scholar
  7. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322:1387–1392.PubMedCrossRefGoogle Scholar
  8. Bulazel K, Metcalfe C, Ferreri G, Yu J, Eldridge M, O’Neill R (2006) Cytogenetic and molecular evaluation of centromere-associated DNA sequences from a marsupial (Macropodidae: Macropus rufogriseus) X chromosome. Genetics 172:1129–1137.PubMedCrossRefGoogle Scholar
  9. Bulazel KV, Ferreri GC, Eldridge MD, O’Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:R170.PubMedCrossRefGoogle Scholar
  10. Burk A, Springer M (2000) Intergeneric relationships among Macropodoidea (Metatheria: Diprotodontia) and the chronicle of kangaroo evolution. J Mammal Evol 7:213–237.CrossRefGoogle Scholar
  11. Cambareri EB, Aisner R, Carbon J (1998) Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol Cell Biol 18:5465–5477.PubMedGoogle Scholar
  12. Carone DM, Longo MS, Ferreri GC, et al. (2009) A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 118:113–125.PubMedCrossRefGoogle Scholar
  13. Carvalho BD, Mattevi MS (2000) (T2AG3)n telomeric sequence hybridization suggestive of centric fusion in karyotype marsupials evolution. Genetica 108:205–210.PubMedCrossRefGoogle Scholar
  14. Cheng Z, Dong F, Langdon T, et al. (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704.PubMedCrossRefGoogle Scholar
  15. Clarke L (1990) Centromeres of budding and fission yeasts. Trends Genet 6:150–154.PubMedCrossRefGoogle Scholar
  16. Coffin JM, Hughes SH, Varmus HE (1997) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  17. Csink AK, Henikoff S (1998) Something from nothing: the evolution and utility of satellite repeats. Trends Genet 14:200–204.PubMedCrossRefGoogle Scholar
  18. Danilevskaya ON, Arkhipova IR, Traverse KL, Pardue ML (1997) Promoting in tandem: the promoter for telomere transposon HeT-A and implications for the evolution of retroviral LTRs. Cell 88:647–655.PubMedCrossRefGoogle Scholar
  19. Dennis ES, Dunsmuir P, Peacock WJ (1980) Segmental amplification in a satellite DNA: restriction enzyme analysis of the major satellite of Macropus rufogriseus. Chromosoma 79:179–198.PubMedCrossRefGoogle Scholar
  20. Dunn CA, Romanish MT, Gutierrez LE, van de Lagemaat LN, Mager DL (2006) Transcription of two human genes from a bidirectional endogenous retrovirus promoter. Gene 366:335–342.PubMedCrossRefGoogle Scholar
  21. Dunsmuir P (1976) Satellite DNA in the kangaroo Macropus rufogriseus. Chromosoma 56: 111–125.PubMedCrossRefGoogle Scholar
  22. Eichler EE (1999) Repetitive conundrums of centromere structure and function. Hum Mol Genet 8:151–155.PubMedCrossRefGoogle Scholar
  23. Eldridge MD, Close RL (1992) Taxonomy of rock wallabies, Petrogale (Marsupialia: Macropodidae). I: a revision of the eastern Petrogale with the description of three new species. Aust J Zool 40:605–624.CrossRefGoogle Scholar
  24. Eldridge MD, Close RL (1993) Radiation of chromosome shuffles. Curr Opin Genet Dev 3: 915–922.PubMedCrossRefGoogle Scholar
  25. Elizur A, Dennis ES, Peacock WJ (1982) Satellite DNA sequences in the red kangaroo (Macropus rufus). Aust J Biol Sci 35:313–325.PubMedGoogle Scholar
  26. Ferreri GC, Marzelli M, Rens W, O’Neill RJ (2004) A centromere-specific retroviral element associated with breaks of synteny in macropodine marsupials. Cytogenet Genome Res 107:115–118.PubMedCrossRefGoogle Scholar
  27. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811.PubMedCrossRefGoogle Scholar
  28. Flannery TF (1989) Phylogeny of the Macropodoidea; a study in convergence. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, Wallabies and Rat-Kangaroos. Surrey Beatty and Sons, Chipping Norton.Google Scholar
  29. Fry K, Poon R, Whitcome P, et al. (1973) Nucleotide sequence of HS-beta satellite DNA from kangaroo rat Dipodomys ordii. Proc Natl Acad Sci USA 70:2642–2646.PubMedCrossRefGoogle Scholar
  30. Fukagawa T, Nogami M, Yoshikawa M, et al. (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791.PubMedCrossRefGoogle Scholar
  31. Garagna S, Broccoli D, Redi CA, Searle JB, Cooke HJ, Capanna E (1995) Robertsonian metacentrics of the house mouse lose telomeric sequences but retain some minor satellite DNA in the pericentromeric area. Chromosoma 103:685–692.PubMedCrossRefGoogle Scholar
  32. Garagna S, Zuccotti M, Redi CA, Capanna E (1997) Trapping speciation. Nature 390:241–242.PubMedCrossRefGoogle Scholar
  33. Graves JAM, Wakefield MJ, Renfree MB, Cooper DW, Speed T, Lindblad-Toh K, Lander ES, Wilson RK (2003) Proposal to Sequence the Genome of the Model Marsupial Macropus eugenii (Tammar Wallaby). http://wwwgenomegov/Pages/Research/Sequencing/SeqProposals/WallabySEQpdf
  34. Greig GM, Warburton PE, Willard HF (1993) Organization and evolution of an alpha satellite DNA subset shared by human chromosomes 13 and 21. J Mol Evol 37:464–475.PubMedCrossRefGoogle Scholar
  35. Greig GM, England SB, Bedford HM, Willard HF (1989) Chromosome-specific alpha satellite DNA from the centromere of human chromosome 16. Am J Hum Genet 45:862–872.PubMedGoogle Scholar
  36. Grigg GC, Jarman P, Hume ID (1989) Kangaroos, Wallabies and Rat-Kangaroos. Surrey Beatty & Sons, Chipping Norton.Google Scholar
  37. Haaf T, Willard HF (1997) Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma 106:226–232.PubMedCrossRefGoogle Scholar
  38. Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–109.CrossRefGoogle Scholar
  39. Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296.PubMedCrossRefGoogle Scholar
  40. Hayman DL, Rofe RH, Sharp PJ (1987) Chromosome evolution in marsupials. Chromosomes Today 9:91–102.CrossRefGoogle Scholar
  41. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102.PubMedCrossRefGoogle Scholar
  42. Horvath JE, Gulden CL, Bailey JA, et al. (2003) Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of human centromeric segmental duplications. Mol Biol Evol 20:1463–1479.PubMedCrossRefGoogle Scholar
  43. Jiang J, Nasuda S, Dong F, et al. (1996) A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci USA 93:14210–14213.PubMedCrossRefGoogle Scholar
  44. John B (1988) Heterochromatin Molecular and Structural Aspects. Cambridge University Press, Cambridge, MA.Google Scholar
  45. Kanellopoulou C, Muljo SA, Kung AL, et al. (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19:489–501.PubMedCrossRefGoogle Scholar
  46. Karlseder J, Cooper JP (2007) Of wombats and whales: telomere tales in Madrid. Conference on telomeres and telomerase. EMBO Rep 8:542–546.PubMedCrossRefGoogle Scholar
  47. Kennerdell JR, Carthew RW (2000) Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 18:896–898.PubMedCrossRefGoogle Scholar
  48. Kidwell MG, Kidwell JF (1976) Selection for male recombination in Drosophila melanogaster. Genetics 84:333–351.PubMedGoogle Scholar
  49. Kirsch JA (1977) The comparative serology of Marsupialia, and a classification of marsupials. Aust J Zool Suppl Ser 52:1–152.CrossRefGoogle Scholar
  50. Kirsch JA, Lapointe F, Springer MS (1997) DNA-Hybridization Studies of Marsupials and their Implications for Metatherian Classification. Aust J Zool 45:211–280.CrossRefGoogle Scholar
  51. Klattenhoff C, Theurkauf W (2008) Biogenesis and germline functions of piRNAs. Development 135:3–9.PubMedCrossRefGoogle Scholar
  52. Lee Y, Ahn C, Han J, et al. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419.PubMedCrossRefGoogle Scholar
  53. Liscinsky DM, Ferreri GC, Mack JA, Eldridge MD, O’Neill RJ (2005) Retention of latent centromeres in the Mammalian genome. J Hered 96:217–224.PubMedCrossRefGoogle Scholar
  54. Longo MS, Carone DM, Program NC, Green ED, O’Neill MJ,O’Neill RJ (2009) Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty. BMC Genomics 10:334.PubMedCrossRefGoogle Scholar
  55. Lowry PS, Eldridge MDB, Johnston PG (1994) Genetic analysis of a female macropodid hybrid (Macropus agilis × M. rufogriseus) and her backcross offspring. Aust Mamm 18: 79–82.Google Scholar
  56. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1:e79.PubMedCrossRefGoogle Scholar
  57. McClintock B (1987) The Discovery and Characterization of Transposable Elements. Garland Publishing, Inc., New York, NY.Google Scholar
  58. Metcalfe CJ (2002) Telomeres and Chromosome Evolution in Marsupials. Biological Sciences, Macquarie University, Sydney.Google Scholar
  59. Metcalfe CJ, Eldridge MD, Toder R, Johnston PG (1998) Mapping the distribution of the telomeric sequence (T2AG3)n in the Macropodoidea (Marsupialia), by fluorescence in situ hybridization. I. The swamp wallaby, Wallabia bicolor. Chromosome Res 6:603–610.PubMedCrossRefGoogle Scholar
  60. Metcalfe CJ, Eldridge MD, Johnston PG (2004) Mapping the distribution of the telomeric sequence (T2AG3)n in the 2n = 14 ancestral marsupial complement and in the macropodines (Marsupialia: Macropodidae) by fluorescence in situ hybridization. Chromosome Res 12:405–414.PubMedCrossRefGoogle Scholar
  61. Metcalfe CJ, Bulazel KV, Ferreri GC, et al. (2007) Genomic instability within centromeres of interspecific marsupial hybrids. Genetics 177:2507–2517.PubMedCrossRefGoogle Scholar
  62. Miller JT, Dong F, Jackson SA, Song J, Jiang J (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623.PubMedGoogle Scholar
  63. Murphy WJ, Larkin DM, Everts-van der Wind A, et al. (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617.PubMedCrossRefGoogle Scholar
  64. Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci USA 81:814–818.PubMedCrossRefGoogle Scholar
  65. Neumann P, Yan H, Jiang J (2007) The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics 176:749–761.PubMedCrossRefGoogle Scholar
  66. O’Neill RJ, O’Neill MJ, Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72.PubMedCrossRefGoogle Scholar
  67. O’Neill RJ, Eldridge MD, Graves JA (2001) Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids. Mamm Genome 12:256–259.PubMedCrossRefGoogle Scholar
  68. O’Neill RJ, Eldridge MD, Metcalfe CJ (2004) Centromere dynamics and chromosome evolution in marsupials. J Hered 95:375–381.PubMedCrossRefGoogle Scholar
  69. Pagnozzi JM, De Jesus Silva MJ, Yonenaga-Yassuda Y (2000) Intraspecific variation in the distribution of the interstitial telomeric (TTAGGG)n sequences in Micoureus demerarae (Marsupialia: Didelphidae). Chromosome Res 8:585–591.PubMedCrossRefGoogle Scholar
  70. Pagnozzi JM, Ditchfield AD, Yonenaga-Yassuda Y (2002) Mapping the distribution of the interstitial telomeric (TTAGGG)n sequences in eight species of Brazilian marsupials (Didelphidae) by FISH and the correlation with constitutive heterochromatin. Do ITS represent evidence for fusion events in American marsupials? Cytogenet Genome Res 98:278–284.PubMedCrossRefGoogle Scholar
  71. Peacock WJ, Dennis ES, Elizur A, Calaby JH (1981) Repeated DNA sequences and kangaroo phylogeny. Aust J Biol Sci 34:325–340.PubMedGoogle Scholar
  72. Pevzner P, Tesler G (2003) Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Res 13:37–45.PubMedCrossRefGoogle Scholar
  73. Reinhart BJ, Bartel DP (2002) Small RNAs correspond to centromere heterochromatic repeats. Science 297:1831.PubMedCrossRefGoogle Scholar
  74. Rens W, O’Brien PC, Fairclough H, Harman L, Graves JAM, Ferguson-Smith MA (2003) Reversal and convergence in marsupial chromosome evolution. Cytogenet Genome Res 102:282–290.PubMedCrossRefGoogle Scholar
  75. Rofe R (1978) G-banded Chromosomes and the Evolution of Macropodidae. Aust Mamm 2:53–63.Google Scholar
  76. Rofe RH (1979) G-Banding and Chromosomal Evolution in Australian Marsupials. University of Adelaide, Adelaide.Google Scholar
  77. Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet 39:40–50.PubMedCrossRefGoogle Scholar
  78. Salser W, Bowen S, Browne D, et al. (1976) Investigation of the organization of mammalian chromosomes at the DNA sequence level. Fed Proc 35:23–35.PubMedGoogle Scholar
  79. Schibler L, Roig A, Mahe MF, et al. (2006) High-resolution comparative mapping among man, cattle and mouse suggests a role for repeat sequences in mammalian genome evolution. BMC Genomics 7:194.PubMedCrossRefGoogle Scholar
  80. Sharman GB, Close RL, Maynes M (1990) Chromosomal evolution, phylogeny and speciation of Rock Wallabies (Petrogale: Macropodidae). Aust J Zool 37:351–363.CrossRefGoogle Scholar
  81. She X, Horvath JE, Jiang Z, et al. (2004) The structure and evolution of centromeric transition regions within the human genome. Nature 430:857–864.PubMedCrossRefGoogle Scholar
  82. Singer MF (1982) Highly repeated sequences in mammalian genomes. Int Rev Cytol 76:67–112.PubMedCrossRefGoogle Scholar
  83. Southern EM (1970) Base sequence and evolution of guinea-pig alpha-satellite DNA. Nature 227:794–798.PubMedCrossRefGoogle Scholar
  84. Svartman M, Vianna-Morgante AM (1998) Karyotype evolution of marsupials: from higher to lower diploid numbers. Cytogenet Cell Genet 82:263–266.PubMedCrossRefGoogle Scholar
  85. Toder R, O’Neill RJ, Wienberg J, O’Brien PC, Voullaire L, Marshall-Graves JA (1997) Comparative chromosome painting between two marsupials: origins of an XX/XY1Y2 sex chromosome system. Mamm Genome 8:418–422.PubMedCrossRefGoogle Scholar
  86. Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA 101:15986–15991.PubMedCrossRefGoogle Scholar
  87. Ugarkovic D (2005) Functional elements residing within satellite DNAs. EMBO Rep 6: 1035–1039.PubMedCrossRefGoogle Scholar
  88. Valgardsdottir R, Chiodi I, Giordano M, Cobianchi F, Riva S, Biamonti G (2005) Structural and functional characterization of noncoding repetitive RNAs transcribed in stressed human cells. Mol Biol Cell 16:2597–2604.PubMedCrossRefGoogle Scholar
  89. Venolia L, Peacock WJ (1981) A highly repeated DNA from the genome of the wallaroo (Macropus robustus robustus). Aust J Biol Sci 34:97–113.PubMedGoogle Scholar
  90. Ventura M, Mudge JM, Palumbo V, et al. (2003) Neocentromeres in 15q24-26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Res 13:2059–2068.PubMedCrossRefGoogle Scholar
  91. Verdel A, Jia S, Gerber S (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676.PubMedCrossRefGoogle Scholar
  92. Verma RS (1999) Evolution of the centromeric alpha-satellite DNA sequences of human chromosome 22. Prenat Diagn 19:590–591.PubMedCrossRefGoogle Scholar
  93. Volpe T, Schramke V, Hamilton GL, et al. (2003) RNA interference is required for normal centromere function in fission yeast. Chromosome Res 11:137–146.PubMedCrossRefGoogle Scholar
  94. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837.PubMedCrossRefGoogle Scholar
  95. White M (1978) Modes of Speciation. WH Freeman and Co, San Francisco, CA.Google Scholar
  96. Wianny F, Zernicka-Goetz M (2000) Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol 2:70–75.PubMedCrossRefGoogle Scholar
  97. Willard HF (1990) Centromeres of mammalian chromosomes. Trends Genet 6:410–416.PubMedCrossRefGoogle Scholar
  98. Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Molecular and Cell BiologyCenter for Applied Genetics and Technology, University of ConnecticutStorrsUSA

Personalised recommendations