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

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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.

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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

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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.

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

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  1. Institute for Applied Ecology, University of Canberra, Canberra, ACT, 2617, Australia

    Emory D. Ingles & Janine E. Deakin

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  1. Emory D. Ingles
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EDI and JED conceived and designed research. EDI conducted experiments. EDI and JED analysed data and wrote the manuscript.

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Correspondence to Janine E. Deakin.

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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)

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Ingles, E.D., Deakin, J.E. The methylation and telomere landscape in two families of marsupials with different rates of chromosome evolution. Chromosome Res 26, 317–332 (2018). https://doi.org/10.1007/s10577-018-9593-0

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