Eggs, embryos and the evolution of imprinting: insights from the platypus genome
Marilyn B. Renfree A B E , Anthony T. Papenfuss A C , Geoff Shaw A B and Andrew J. Pask A B DA ARC Centre of Excellence for Kangaroo Genomics.
B Department of Zoology, The University of Melbourne, Melbourne, Vic. 3010, Australia.
C Bioinformatics Division, The Walter and Eliza Hall Institute, 1G Royal Parade, Parkville, Vic. 3052, Australia.
D Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA.
E Corresponding author. Email: m.renfree@unimelb.edu.au
Reproduction, Fertility and Development 21(8) 935-942 https://doi.org/10.1071/RD09092
Submitted: 11 April 2009 Accepted: 28 August 2009 Published: 30 October 2009
Abstract
Genomic imprinting is widespread in eutherian and marsupial mammals. Although there have been many hypotheses to explain why genomic imprinting evolved in mammals, few have examined how it arose. The host defence hypothesis suggests that imprinting evolved from existing mechanisms within the cell that act to silence foreign DNA elements that insert into the genome. However, the changes to the mammalian genome that accompanied the evolution of imprinting have been hard to define due to the absence of large-scale genomic resources from all extant classes. The recent release of the platypus genome sequence has provided the first opportunity to make comparisons between prototherian (monotreme, which show no signs of imprinting) and therian (marsupial and eutherian, which have imprinting) mammals. We compared the distribution of repeat elements known to attract epigenetic silencing across the genome from monotremes and therian mammals, particularly focusing on the orthologous imprinted regions. Our analyses show that the platypus has significantly fewer repeats of certain classes in the regions of the genome that have become imprinted in therian mammals. The accumulation of repeats, especially long-terminal repeats and DNA elements, in therian imprinted genes and gene clusters therefore appears to be coincident with, and may have been a potential driving force in, the development of mammalian genomic imprinting. Comparative platypus genome analyses of orthologous imprinted regions have provided strong support for the host defence hypothesis to explain the origin of imprinting.
Additional keywords: eutherians, genomic imprinting, host defence hypothesis, mammals, marsupials, monotremes, repeats.
Acknowledgements
Our research was supported by the ARC Centre of Excellence in Kangaroo Genomics; A.T.P. was supported by an NHMRC Fellowship; A.J.P. was supported by an NHMRC R.D.Wright Fellowship; and M.B.R. by an ARC Federation Fellowship.
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