Retrotransposon silencing by DNA methylation contributed to the evolution of placentation and genomic imprinting in mammals

The evolution of two mammalian-specific traits, viviparous reproduction with a placenta and genomic imprinting, have been addressed by multiple studies of two retrotransposon derived, mammalian-specific genes. These gene targeting experiments in mice, together with recent comparative genomic analyse...

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Bibliographic Details
Published in:Development, growth & differentiation growth & differentiation, 2010-08, Vol.52 (6), p.533-543
Main Authors: Kaneko-Ishino, Tomoko, Ishino, Fumitoshi
Format: Article
Language:English
Subjects:
Animals
Biological Evolution
DNA Methylation
Female
Gene Silencing - physiology
Genetic Drift
genomic imprinting
Genomic Imprinting - genetics
Germ Cells - cytology
mammalian evolution
Mice
placenta
Placentation - genetics
Pregnancy
Retroelements - genetics
retrotransposon
Selection, Genetic
viviparity
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Summary:The evolution of two mammalian-specific traits, viviparous reproduction with a placenta and genomic imprinting, have been addressed by multiple studies of two retrotransposon derived, mammalian-specific genes. These gene targeting experiments in mice, together with recent comparative genomic analyses among three mammalian groups, suggest that extremely rare events; namely exaptations from retrotransposons, made crucial contributions to the establishment and diversification of mammals via placental formation. We propose that nearly neutral evolution, as well as Darwinian evolution (natural selection), plays an important role in the exaptation process. Comparative genomic analysis of various imprinted regions has also revealed that an imprinting control element essential for parent-of-origin specific monoallelic expression of imprinted genes emerged in each of the imprinted regions, possibly by the insertion of exogenous DNAs, such as retrotransposons. In both cases, DNA methylation in germ cells must have been of critical importance to repress the exogenous DNAs inserted into the genomes of mammalian ancestors. We propose that the ability of germ line DNA methylation enabled the emergence of certain mammalian-specific features during the course of evolution.
ISSN:0012-1592
1440-169X
DOI:10.1111/j.1440-169X.2010.01194.x