Abstract
A comprehensive, domain-wide comparative analysis of genomic imprinting between mammals that imprint and those that do not can provide valuable information about how and why imprinting evolved. The imprinting status, DNA methylation, and genomic landscape of the Dlk1-Dio3 cluster were determined in eutherian, metatherian, and prototherian mammals including tammar wallaby and platypus. Imprinting across the whole domain evolved after the divergence of eutherian from marsupial mammals and in eutherians is under strong purifying selection. The marsupial locus at 1.6 megabases, is double that of eutherians due to the accumulation of LINE repeats. Comparative sequence analysis of the domain in seven vertebrates determined evolutionary conserved regions common to particular sub-groups and to all vertebrates. The emergence of Dlk1-Dio3 imprinting in eutherians has occurred on the maternally inherited chromosome and is associated with region-specific resistance to expansion by repetitive elements and the local introduction of noncoding transcripts including microRNAs and C/D small nucleolar RNAs. A recent mammal-specific retrotransposition event led to the formation of a completely new gene only in the eutherian domain, which may have driven imprinting at the cluster.
Highlights
Genomic imprinting is a process that causes genes to be expressed according to their parental origin and is evident in plants and mammals
A fraction of mammalian genes, is subject to imprinting—a chemical modification that marks a gene according to its parental origin, so that one parent’s copy is expressed while the other parent’s copy is silenced
We have shown that all the genes in one genomic region, Delta-like homologue 1 (Dlk1)-Dio3, which are imprinted in placental mammals such as mouse and human, are not imprinted in marsupial or monotreme mammals
Summary
Genomic imprinting is a process that causes genes to be expressed according to their parental origin and is evident in plants and mammals. Many imprinted genes are located in clusters regulated by a single imprinting control element, whose function across the whole imprinted domain depends on DNA methylation acquired differentially in the male and the female germlines [1]. It is not known how or why mammalian imprinting evolved; its emergence is associated with the evolution of a placenta [2,3], and the correct dosage of imprinted genes is important in prenatal growth, postnatal metabolism [4], and neurodevelopment [5]. The orthologues of four genes imprinted in mouse and human are clearly imprinted in marsupials [7,8,9,10], and no evidence of imprinting has been found in monotremes, only three genes have been tested to date [8,11,12]
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