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

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.

Transcriptome-wide investigation of genomic imprinting in chicken

“…This phenomenon has been described in eutherian mammals, marsupials, plants and insects, but has never been observed in birds (1,2). …”

Post-natal imprinting: evidence from marsupials

“…However, germline DMRs are the main epigenetic mark distinguishing parental alleles of imprinted genes in the early embryo. Thus far, only three DMRs have been identified in marsupials in the promoters of PEG10, H19 and IGF2R Smits et al, 2008;Das et al, 2012). An additional two putative DMRs have also been identified in IGF2 and INS (Lawton et al, 2008;Stringer et al, 2012b, c).…”

“…Hence, human IGF2R is biallelically expressed (Yang et al, 2003;Vu et al, 2004). In marsupials, IGF2R is imprinted and possesses a novel DMR not present in eutherian mammals (Das et al, 2012). Interestingly, there is an allele-specific permissive histone modification (H3K4me2) at the IGF2R promoter (Das et al, 2012).…”

“…In marsupials, IGF2R is imprinted and possesses a novel DMR not present in eutherian mammals (Das et al, 2012). Interestingly, there is an allele-specific permissive histone modification (H3K4me2) at the IGF2R promoter (Das et al, 2012). Although the repressive mark H3K9me3 is absent, other modifications (for example, H3K27me3, H4K20me3) may be present and function to repress the paternal allele (Delaval et al, 2007;Henckel et al, 2009;Das et al, 2012).…”

“…Interestingly, there is an allele-specific permissive histone modification (H3K4me2) at the IGF2R promoter (Das et al, 2012). Although the repressive mark H3K9me3 is absent, other modifications (for example, H3K27me3, H4K20me3) may be present and function to repress the paternal allele (Delaval et al, 2007;Henckel et al, 2009;Das et al, 2012). Therefore, some DMRs are conserved between marsupials and eutherians at some loci, while at other loci epigenetic mechanisms have clearly diverged between these groups.…”