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Open Access Research article

Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica

Radhika Das1, Nathan Anderson2, MaryEllen I Koran1, Jennifer R Weidman1, Tarjei S Mikkelsen2, Michael Kamal2, Susan K Murphy3, Kerstin Linblad-Toh24, John M Greally5 and Randy L Jirtle6*

Author Affiliations

1 Department of Radiation Oncology, Duke University Medical Center, Box 3433, Durham, NC, 27710, USA

2 Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA

3 Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, 27708, USA

4 Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, 75123, Sweden

5 Department of Medicine (Hematology) and Molecular Genetics, Albert Einstein College of Medicine, Bronx, NY, 10461, USA

6 McArdle Laboratory for Cancer Research, Department of Oncology University of Wisconsin-Madison, 1400 University Avenue, Madison,, WI 53706, USA

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BMC Genomics 2012, 13:394  doi:10.1186/1471-2164-13-394

Published: 16 August 2012

Abstract

Background

Genomic imprinting is an epigenetic phenomenon resulting in parent-of-origin specific monoallelic gene expression. It is postulated to have evolved in placental mammals to modulate intrauterine resource allocation to the offspring. In this study, we determined the imprint status of metatherian orthologues of eutherian imprinted genes.

Results

L3MBTL and HTR2A were shown to be imprinted in Monodelphis domestica (the gray short-tailed opossum). MEST expressed a monoallelic and a biallelic transcript, as in eutherians. In contrast, IMPACT, COPG2, and PLAGL1 were not imprinted in the opossum. Differentially methylated regions (DMRs) involved in regulating imprinting in eutherians were not found at any of the new imprinted loci in the opossum. Interestingly, a novel DMR was identified in intron 11 of the imprinted IGF2R gene, but this was not conserved in eutherians. The promoter regions of the imprinted genes in the opossum were enriched for the activating histone modification H3 Lysine 4 dimethylation.

Conclusions

The phenomenon of genomic imprinting is conserved in Therians, but the marked difference in the number and location of imprinted genes and DMRs between metatherians and eutherians indicates that imprinting is not fully conserved between the two Therian infra-classes. The identification of a novel DMR at a non-conserved location as well as the first demonstration of histone modifications at imprinted loci in the opossum suggest that genomic imprinting may have evolved in a common ancestor of these two Therian infra-classes with subsequent divergence of regulatory mechanisms in the two lineages.

Keywords:
Genomic imprinting; Marsupials; Eutherians