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

Radhika Das, Nathan Anderson, MaryEllen I. Koran, Jennifer R. Weidman, Tarjei S. Mikkelsen, Michael Kamal, Susan K. Murphy, Kerstin Linblad-Toh, John M. Greally, Randy L. Jirtle

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Abstract

Background: Genomic 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.Results: L3MBTL 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.Conclusions: The 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.

Original languageEnglish (US)
Article number394
JournalBMC Genomics
Volume13
Issue number1
DOIs
StatePublished - Aug 16 2012

Fingerprint

Monodelphis
Genomic Imprinting
Opossums
Marsupialia
Histone Code
Genes
Resource Allocation
Genetic Promoter Regions
Epigenomics
Histones
Introns
Lysine
Mammals
Gene Expression

Keywords

  • Eutherians
  • Genomic imprinting
  • Marsupials

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

Cite this

Das, R., Anderson, N., Koran, M. I., Weidman, J. R., Mikkelsen, T. S., Kamal, M., ... Jirtle, R. L. (2012). Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica. BMC Genomics, 13(1), [394]. https://doi.org/10.1186/1471-2164-13-394

Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica. / Das, Radhika; Anderson, Nathan; Koran, MaryEllen I.; Weidman, Jennifer R.; Mikkelsen, Tarjei S.; Kamal, Michael; Murphy, Susan K.; Linblad-Toh, Kerstin; Greally, John M.; Jirtle, Randy L.

In: BMC Genomics, Vol. 13, No. 1, 394, 16.08.2012.

Research output: Contribution to journalArticle

Das, R, Anderson, N, Koran, MI, Weidman, JR, Mikkelsen, TS, Kamal, M, Murphy, SK, Linblad-Toh, K, Greally, JM & Jirtle, RL 2012, 'Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica', BMC Genomics, vol. 13, no. 1, 394. https://doi.org/10.1186/1471-2164-13-394
Das R, Anderson N, Koran MI, Weidman JR, Mikkelsen TS, Kamal M et al. Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica. BMC Genomics. 2012 Aug 16;13(1). 394. https://doi.org/10.1186/1471-2164-13-394
Das, Radhika ; Anderson, Nathan ; Koran, MaryEllen I. ; Weidman, Jennifer R. ; Mikkelsen, Tarjei S. ; Kamal, Michael ; Murphy, Susan K. ; Linblad-Toh, Kerstin ; Greally, John M. ; Jirtle, Randy L. / Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica. In: BMC Genomics. 2012 ; Vol. 13, No. 1.
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abstract = "Background: Genomic 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.Results: L3MBTL 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.Conclusions: The 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.",
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AU - Mikkelsen, Tarjei S.

AU - Kamal, Michael

AU - Murphy, Susan K.

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AB - Background: Genomic 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.Results: L3MBTL 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.Conclusions: The 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.

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