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Chromosome Research

, Volume 26, Issue 4, pp 317–332 | Cite as

The methylation and telomere landscape in two families of marsupials with different rates of chromosome evolution

  • Emory D. Ingles
  • Janine E. DeakinEmail author
Original Article

Abstract

Two marsupial families exemplify divergent rates of karyotypic change. The Dasyurid family has an extremely conserved karyotype. In contrast, there is significant chromosomal variation within the Macropodidae family, best exemplified by members of the genus Petrogale (rock-wallabies). Both families are also distinguished by their telomere landscape (length and epigenetics), with the dasyurids having a unique telomere length dimorphism not observed in other marsupials and hypothesised to be regulated in a parent-of-origin fashion. Previous work has shown that proximal ends of chromosomes are enriched in cytosine methylation in dasyurids, but that the chromosomes of a macropod, the tammar wallaby, have DNA methylation enrichment of pericentric regions. Using a combination of telomere and 5-methylcytosine immunofluorescence staining, we investigated the telomere landscape of four dasyurid and three Petrogale species. As part of this study, we also further examined the parent-of-origin hypothesis for the regulation of telomere length dimorphism in dasyurids, using epigenetic modifications known to differentiate the active maternal X chromosome, including 5-methylcytosine methylation and histone modifications H3K4me2, H3K9ac and H4Kac. Our results give further support to the parent-of-origin hypothesis for the regulation of telomere length dimorphism in dasyurids, where the paternally derived X chromosome in females was associated with long telomeres and the maternally derived with short telomeres. In contrast to the tammar wallaby, rock-wallabies demonstrated a similar 5-methylcytosine staining pattern across all chromosomes to that of dasyurids, suggesting that DNA methylation of telomeric regions is not responsible for differences in the rates of chromosome evolution between these two families.

Keywords

Telomere DNA methylation Chromosome Marsupial 

Abbreviations

BSA

Bovine serum albumin

DAPI

4′,6-diamidino-2-phenylindole dichloride

FCS

Fetal calf serum

FISH

Fluorescence in situ hybridisation

H3K4me2

Histone H3 dimethylation on lysine 4

H3K9ac

Histone H3 acetylation on lysine 9

H4Kac

Histone H4 acetylation

KERV

Kangaroo endogenous retrovirus

PBS

Phosphate-buffered saline

PBST

Phosphate-buffered saline Tween 20

PNA

Peptide nucleic acid

prdm9

PR domain containing 9

Notes

Acknowledgements

We would like to thank Andrew Pask for providing us with the fat-tailed dunnart sample, Julie Old and Corrine Letendre for providing us with red-tailed phascogale sample and Anne-Maree Pearse from the Tasmanian Government Department of Primary Industries, Parks, Water and Environment for devil chromosome slides. This work was supported by Research Training Scheme funding from the Institute for Applied Ecology and an Australian Research Council Discovery Grant (DP 160100187) awarded to J.E.D., Jason Bragg, Mark Eldridge, Craig Moritz, Mark Kirkpatrick.

Author contributions

EDI and JED conceived and designed research. EDI conducted experiments. EDI and JED analysed data and wrote the manuscript.

Funding

This study was partly funded by the Australian Research Council (DP160100187).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Supplementary material

10577_2018_9593_MOESM1_ESM.pdf (104 kb)
Supplementary Fig. 1 Telomere staining on a tammar wallaby, Macropus eugenii. Telomere staining is not apparent at actual telomeres, presumably due to a masking effect by the large centromeric telomeric signals. (PDF 103 kb)

References

  1. Alsop AE, Miethke P, Rofe R, Koina E, Sankovic N, Deakin JE, Haines H, Rapkins RW, Graves JAM (2005) Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosom Res 13:627–636CrossRefGoogle Scholar
  2. Artandi SE, DePinho RA (2010) Telomeres and telomerase in cancer. Carcinogenesis 31:9–18CrossRefGoogle Scholar
  3. Beliveau BJ et al (2015) Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes. Nat Commun 6:13CrossRefGoogle Scholar
  4. Bender HS et al (2012) Extreme telomere length dimorphism in the Tasmanian devil and related marsupials suggests parental control of telomere length. PLoS One 7:10Google Scholar
  5. Benetti R, Garcia-Cao M, Blasco MA (2007) Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet 39:243–250CrossRefGoogle Scholar
  6. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD (2013) Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 24:196–205CrossRefGoogle Scholar
  7. Bolzan AD (2017) Interstitial telomeric sequences in vertebrate chromosomes: origin, function, instability and evolution. Mutat Res Rev Mutat Res 773:51–65CrossRefGoogle Scholar
  8. Bosco N, de Lange T (2012) A TRF1-controlled common fragile site containing interstitial telomeric sequences. Chromosoma 121:465–474CrossRefGoogle Scholar
  9. Brown JD, O'Neill RJ (2009) The mysteries of chromosome evolution in gibbons: methylation is a prime suspect. PLoS Genet 5:2CrossRefGoogle Scholar
  10. Bulazel KV, Ferreri GC, Eldridge MDB, O'Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:15CrossRefGoogle Scholar
  11. Canfield PJ, Cunningham AA (1993) Disease and mortality in Australasian marsupials held at London Zoo, 1872-1972. J Zoo Wildl Med 24:158–167Google Scholar
  12. Canfield PJ, Hartley WJ, Reddacliff GL (1990) Spontaneous proliferations in Australian marsupials - a survey and review .2. Dasyurids and bandicoots. J Comp Pathol 103:147–158CrossRefGoogle Scholar
  13. Carbone L et al (2009) Evolutionary breakpoints in the gibbon suggest association between cytosine methylation and karyotype evolution. PLoS Genet 5:10CrossRefGoogle Scholar
  14. Carvalho BD, Oliveira LFB, Nunes AP, Mattevi MS (2002) Karyotypes of nineteen marsupial species from Brazil. J Mammal 83:58–70CrossRefGoogle Scholar
  15. Choudhury SR, Cui Y, Narayanan A, Gilley DP, Huda N, Lo CL, Zhou FC, Yernool D, Irudayaraj J (2016) Optogenetic regulation of site-specific subtelomeric DNA-methylation. Oncotarget 7:50380–50391PubMedPubMedCentralGoogle Scholar
  16. Creighton HB, McClintock B (1931) A correlation of cytological and genetical crossing-over in Zea mays. Proc Natl Acad Sci U S A 17:492–497CrossRefGoogle Scholar
  17. Deakin JE (2018) Chromosome evolution in marsupials. Genes 9:72Google Scholar
  18. Deakin JE, Kruger-Andrzejewska M (2016) Marsupials as models for understanding the role of chromosome rearrangements in evolution and disease. Chromosoma 125:633–644CrossRefGoogle Scholar
  19. Deakin JE, Bender HS, Pearse AM, Rens W, O’Brien PCM, Ferguson-Smith MA, Cheng Y, Morris K, Taylor R, Stuart A, Belov K, Amemiya CT, Murchison EP, Papenfuss AT, Marshall Graves JA (2012) Genomic restructuring in the Tasmanian devil facial tumour: chromosome painting and gene mapping provide clues to evolution of a transmissible tumour. PLoS Genet 8:e1002483CrossRefGoogle Scholar
  20. Deakin JE, Delbridge ML, Koina E, Harley N, Alsop AE, Wang CW, Patel VS, Graves JAM (2013) Reconstruction of the ancestral marsupial karyotype from comparative gene maps. BMC Evol Biol 13:258CrossRefGoogle Scholar
  21. der-Sarkissian H, Bacchetti S, Cazes L, Londoño-Vallejo JA (2004) The shortest telomeres drive karyotype evolution in transformed cells. Oncogene 23:1221–1228CrossRefGoogle Scholar
  22. Eldridge MDB, Close RL (1992) Taxonomy of rock wallabies, Petrogale (Marsupialia, Macropodidae) .1. A revision of the eastern Petrogale with the description of 3 new species. Aust J Zool 40:605–625CrossRefGoogle Scholar
  23. Eldridge MDB, Johnston PG (1993) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia, Macropodidae) .8. An investigation of the nonrandom nature of karyotypic change. Genome 36:524–534CrossRefGoogle Scholar
  24. 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 107:115–118CrossRefGoogle Scholar
  25. Ferreri GC, Liscinsky DM, Mack JA, Eldridge MDB, O'Neill RJ (2005) Retention of latent centromeres in the mammalian genome. J Hered 96:217–224CrossRefGoogle Scholar
  26. Fumagalli M, Rossiello F, Clerici M, Barozzi S, Cittaro D, Kaplunov JM, Bucci G, Dobreva M, Matti V, Beausejour CM, Herbig U, Longhese MP, d’Adda di Fagagna F (2012) Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat Cell Biol 14:355–365CrossRefGoogle Scholar
  27. Gomes NMV, Ryder OA, Houck ML, Charter SJ, Walker W, Forsyth NR, Austad SN, Venditti C, Pagel M, Shay JW, Wright WE (2011) Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10:761–768CrossRefGoogle Scholar
  28. Gonzalo S, Jaco I, Fraga MF, Chen TP, Li E, Esteller M, Blasco MA (2006) DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat Cell Biol 8:416–U466CrossRefGoogle Scholar
  29. Grey C, Barthes P, Chauveau-Le Friec G, Langa F, Baudat F, de Massy B (2011) Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol 9:e1001176CrossRefGoogle Scholar
  30. Griner LA (1979) Neoplasms in Tasmanian devils (Sarcophilus-harrisii). J Natl Cancer Inst 62:589–595CrossRefGoogle Scholar
  31. Hayman DL (1990) Marsupial Cytogenetics. Aust J Zool 37:331–349CrossRefGoogle Scholar
  32. Hayman DL, Martin PG (1974) Mammalia I: Monotremata and Marsupialia. In: John B (ed) Animal Cytogenetics, vol 4. vol Chordata. Gebrüder Borntraeger, Berlin/StuttgartGoogle Scholar
  33. Ingles ED, Deakin JE (2015) Global DNA methylation patterns on marsupial and devil facial tumour chromosomes. Mol Cytogenet 8:74CrossRefGoogle Scholar
  34. Ingles ED, Deakin JE (2016) Telomeres, species differences, and unusual telomeres in vertebrates: presenting challenges and opportunities to understanding telomere dynamics. AIMS Genet 3:1–24CrossRefGoogle Scholar
  35. Koina E, Chaumeil J, Greaves IK, Tremethick DJ, Graves JAM (2009) Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosom Res 17:115–126CrossRefGoogle Scholar
  36. Link J, Jahn D, Schmitt J, Gob E, Baar J, Ortega S, Benavente R, Alsheimer M (2013) The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet 9:e1003261CrossRefGoogle Scholar
  37. Liu L, Blasco MA, Keefe DL (2002) Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles. EMBO Rep 3:230–234CrossRefGoogle Scholar
  38. Liu L, Franco S, Spyropoulos B, Moens PB, Blasco MA, Keefe DL (2004) Irregular telomeres impair meiotic synapsis and recombination in mice. Proc Natl Acad Sci U S A 101:6496–6501CrossRefGoogle Scholar
  39. Loebel DA, Johnston PG (1993) Analysis of DNase-1 sensitivity and methylation of active and inactive X-chromosomes of kangaroos (Macropus robustus) by in situ nick translation. Chromosoma 102:81–87CrossRefGoogle Scholar
  40. Metcalfe CJ, Eldridge MDB, McQuade LR, Johnston PG (1997) Mapping the distribution of the telomeric sequence (T(2)AG(3))(n) in rock-wallabies, Petrogale (Marsupialia: Macropodidae), by fluorescence in situ hybridization .1 The penicillata complex. Cytogenet Cell Genet 78:74–80CrossRefGoogle Scholar
  41. Metcalfe CJ, Eldridge MDB, Toder R, Johnston PG (1998) Mapping the distribution of the telomeric sequence (T(2)AG(3))(n) in the Macropodoidea (Marsupialia), by fluorescence in situ hybridization. I. the swamp wallaby, Wallabia bicolor. Chromosom Res 6:603–610CrossRefGoogle Scholar
  42. Metcalfe CJ, Eldridge MDB, Johnston PG (2002) Mapping the distribution of the telomeric sequence (T(2)AG(3))(n) in rock wallabies, Petrogale (Marsupialia : Macropodidae), by fluorescence in situ hybridization - II. The lateralis complex. Cytogenet Genome Res 96:169–175CrossRefGoogle Scholar
  43. Metcalfe CJ, Eldridge MDB, Johnston PG (2004) Mapping the distribution of the telomeric sequence (T(2)AG(3))(n) in the 2n=14 ancestral marsupial complement and in the macropodines (Marsupialia : Macropodidae) by fluorescence in situ hybridization. Chromosom Res 12:405–414CrossRefGoogle Scholar
  44. Metcalfe CJ, Eldridge MDB, Johnston PG (2007) Mapping the distribution of the telomeric sequence (T(2)AG(3))(n) in the macropodoidea (marsupialia) by fluorescence in situ hybridization. II. The ancestral 2n=22 macropodid karyotype. Cytogenet Genome Res 116:212–217CrossRefGoogle Scholar
  45. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323:373–375CrossRefGoogle Scholar
  46. Mitelman F (2000) Recurrent chromosome aberrations in cancer. Mutat Res Rev Mutat Res 462:247–253CrossRefGoogle Scholar
  47. 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 98:278–284CrossRefGoogle Scholar
  48. Pearse AM, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439:549CrossRefGoogle Scholar
  49. Pearse AM, Swift K, Hodson P, Hua B, McCallum H, Pyecroft S, Taylor R, Eldridge MDB, Belov K (2012) Evolution in a transmissible cancer: a study of the chromosomal changes in devil facial tumor (DFT) as it spreads through the wild Tasmanian devil population. Cancer Genet 205(3):101–112CrossRefGoogle Scholar
  50. Potter S, Moritz C, Eldridge MDB (2015) Gene flow despite complex Robertsonian fusions among rock-wallaby (Petrogale) species. Biol Lett 11:5CrossRefGoogle Scholar
  51. Potter S, Bragg JG, Blom MPK, Deakin JE, Kirkpatrick M, Eldridge MDB, Moritz C (2017) Chromosomal speciation in the genomics era: disentangling phylogenetic evolution of rock-wallabies. Front Genet 8:10Google Scholar
  52. Putiri EL, Robertson KD (2011) Epigenetic mechanisms and genome stability. Clin Epigenetics 2:299–314CrossRefGoogle Scholar
  53. Reig OA, Gardner AL, Bianchi NO, Patton JL (1977) The chromosomes of the Didelphidae (Marsupialia) and their evolutionary significance. Biol J Linn Soc 9:191–216CrossRefGoogle Scholar
  54. Rens W, O'Brien PCM, Yang F, Graves JAM, Ferguson-Smith MA (1999) Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosom Res 7:461–474CrossRefGoogle Scholar
  55. Rens W, O'Brien PCM, Fairclough H, Harman L, Graves JAM, Ferguson-Smith MA (2003) Reversal and convergence in marsupial chromosome evolution. Cytogenet Genome Res 102:282–290CrossRefGoogle Scholar
  56. Rens W, Wallduck MS, Lovell FL, Ferguson-Smith MA, Ferguson-Smith AC (2010) Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc Natl Acad Sci U S A 107:17657–17662CrossRefGoogle Scholar
  57. Rofe R (1978) G-banded chromosomes and the evolution of Macropodidae. Aust Mammal 2:53–63Google Scholar
  58. Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet 39:40–50CrossRefGoogle Scholar
  59. Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138:90–103CrossRefGoogle Scholar
  60. Sharman GB (1961) The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust J Zool 9:38–60Google Scholar
  61. Sharman GB (1971) Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230:231–232CrossRefGoogle Scholar
  62. Silva C, de Andrade RA, de Souza EMS, Eler ES, da Silva MNF, Feldberg E (2017) Comparative cytogenetics of some marsupial species (Didelphimorphia, Didelphidae) from the Amazon basin. Comp Cytogenet 11:703–725CrossRefGoogle Scholar
  63. Slijepcevic P, Xiao Y, Dominguez I, Natarajan AT (1996) Spontaneous and radiation-induced chromosomal breakage at interstitial telomeric sites. Chromosoma 104:596–604CrossRefGoogle Scholar
  64. Smith TA, Martin MD, Nguyen M, Mendelson TC (2016) Epigenetic divergence as a potential first step in darter speciation. Mol Ecol 25:1883–1894CrossRefGoogle Scholar
  65. Stammnitz MR et al (2018) The origins and vulnerabilities of two transmissible cancers in Tasmanian devils. Cancer Cell 33:607–619.e615CrossRefGoogle Scholar
  66. Svartman M (2009) American marsupials chromosomes: why study them? Genet Mol Biol 32:675–687CrossRefGoogle Scholar
  67. Tardat M, Déjardin J (2018) Telomere chromatin establishment and its maintenance during mammalian development. Chromosoma 127:3–18CrossRefGoogle Scholar
  68. Toder R, Wienberg J, Voullaire L, Obrien PCM, Maccarone P, Graves JAM (1997) Shared DNA sequences between the X and Y chromosomes in the tammar wallaby - evidence for independent additions to eutherian and marsupial sex chromosomes. Chromosoma 106:94–98CrossRefGoogle Scholar
  69. Ujvari B, Pearse AM, Taylor R, Pyecroft S, Flanagan C, Gombert S, Papenfuss AT, Madsen T, Belov K (2012) Telomere dynamics and homeostasis in a transmissible cancer. PLoS One 7:e44085CrossRefGoogle Scholar
  70. Voet T, Liebe B, Labaere C, Marynen P, Scherthan H (2003) Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis. J Cell Biol 162:795–807CrossRefGoogle Scholar
  71. Wakefield MJ, Keohane AM, Turner BM, Graves JAM (1997) Histone underacetylation is an ancient component of mammalian X chromosome inactivation. Proc Natl Acad Sci U S A 94:9665–9668CrossRefGoogle Scholar
  72. Westerman M, Woolley PA (1990) Cytogenetics of some new Guinean dasyurids and genome evolution in the Dasyuridae (Marsupialia). Aust J Zool 37:521–531CrossRefGoogle Scholar
  73. Westerman M, Woolley PA (1993) Chromosomes and the evolution of dasyurid marsupials: an overview. Sci New Guin 19:123–130Google Scholar
  74. Yang J, Guo R, Wang H, Ye X, Zhou Z, Dan J, Wang H, Gong P, Deng W, Yin Y, Mao SQ, Wang L, Ding J, Li J, Keefe DL, Dawlaty MM, Wang J, Xu GL, Liu L (2016) Tet enzymes regulate telomere maintenance and chromosomal stability of mouse ESCs. Cell Rep 15:1809–1821CrossRefGoogle Scholar
  75. Young GJ, Graves JAM, Barbieri I, Woolley PA, Cooper DW (1982) The chromosomes of dasyurids (Masupialia). In: Archer M (ed) Carnivorous marsupials. Royal Zoological Society, NSW, Mosman, pp 783–795Google Scholar
  76. Zakharova IS, Shevchenko AI, Shilov AG, Nesterova TB, VandeBerg JL, Zakian SM (2011) Histone H3 trimethylation at lysine 9 marks the inactive metaphase X chromosome in the marsupial Monodelphis domestica. Chromosoma 120:177–183CrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institute for Applied EcologyUniversity of CanberraCanberraAustralia

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