Abstract
Among mammals, only eutherians and marsupials are viviparous and have genomic imprinting that leads to parent-of-origin-specific differential gene expression. We used comparative analysis to investigate the origin of genomic imprinting in mammals. PEG10 (paternally expressed 10) is a retrotransposon-derived imprinted gene that has an essential role for the formation of the placenta of the mouse. Here, we show that an orthologue of PEG10 exists in another therian mammal, the marsupial tammar wallaby (Macropus eugenii), but not in a prototherian mammal, the egg-laying platypus (Ornithorhynchus anatinus), suggesting its close relationship to the origin of placentation in therian mammals. We have discovered a hitherto missing link of the imprinting mechanism between eutherians and marsupials because tammar PEG10 is the first example of a differentially methylated region (DMR) associated with genomic imprinting in marsupials. Surprisingly, the marsupial DMR was strictly limited to the 5′ region of PEG10, unlike the eutherian DMR, which covers the promoter regions of both PEG10 and the adjacent imprinted gene SGCE. These results not only demonstrate a common origin of the DMR-associated imprinting mechanism in therian mammals but provide the first demonstration that DMR-associated genomic imprinting in eutherians can originate from the repression of exogenous DNA sequences and/or retrotransposons by DNA methylation.
Highlights
Genomic imprinting, or parent-of-origin-specific gene silencing, has been observed in both eutherian and marsupial, but not monotreme mammals
Genomic imprinting is controlled by differential methylation of the DNA
By comparing the genome of all three extant classes of mammals, we have investigated the evolution of PEG10, a retrotransposon-derived imprinted gene that is essential for the formation of the placenta in the mouse
Summary
Parent-of-origin-specific gene silencing, has been observed in both eutherian and marsupial, but not monotreme mammals. It has been hypothesized that genomic imprinting arose as a by-product of a DNA methylation mechanism that silences foreign DNAs [10], such as retrotransposons [11,12]. Transgenes can become methylated, depending on parent of origin, further supporting a link between genomic imprinting and silencing of foreign DNAs [13,14,15]. Investigating the origin of the retrotransposon-derived PEG10 locus would clarify the relationship between retrotransposon (or exogenous DNA sequence) insertion and genomic imprinting. We examined the PEG10 locus in two Australian mammals by isolating bacterial artificial chromosome (BAC) clones from a marsupial, the tammar wallaby, and from a monotreme, the platypus.
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