Abstract
BackgroundGenomic 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.ResultsL3MBTL 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.ConclusionsThe 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.
Highlights
Genomic imprinting is an epigenetic phenomenon resulting in parent-of-origin specific monoallelic gene expression
We identified a novel differentially methylated region (DMR) within IGF2R, but DMRs were not present near or within the other genes imprinted in the opossum
We focused on six known imprinted genes in mouse that had a high level of genomic sequence conservation in eutherians, namely MEST [8,30], COPG2 [31], HTR2A [32], L3MBTL [33], IMPACT [34,35] and PLAGL1 [36]
Summary
Genomic imprinting is an epigenetic phenomenon resulting in parent-of-origin specific monoallelic gene expression. Imprinted genes have not been identified in prototherian (i.e. platypus and echidna) and avian (i.e. chicken) species [6,13] To explain this unique phylogenetic distribution of imprinted genes, the “Conflict Hypothesis” proposes that genomic imprinting evolved in placental mammals in response to polygamy, viviparity, and multiple births [14,15]. This theory is based on maximizing competitive fitness of the father’s progeny while preserving the ability of the mother to provide care to all her offspring, regardless of paternity. A corollary to this hypothesis is that paternally and maternally expressed genes will enhance and inhibit growth, respectively
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