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Paternally expressed imprinted genes under positive Darwinian selection in Arabidopsis thaliana

Tuteja, Reetu; McKeown, Peter C.; Ryan, Pat; Morgan, Claire C.; Donoghue, Mark T.A.; Downing, Tim; O'Connell, Mary J.; Spillane, Charles

Authors

Reetu Tuteja

Peter C. McKeown

Pat Ryan

Claire C. Morgan

Mark T.A. Donoghue

Tim Downing

Charles Spillane



Abstract

Genomic imprinting is an epigenetic phenomenon where autosomal genes display uniparental expression depending on whether they are maternally or paternally inherited. Genomic imprinting can arise from parental conflicts over resource allocation to the offspring, which could drive imprinted loci to evolve by positive selection. We investigate whether positive selection is associated with genomic imprinting in the inbreeding species Arabidopsis thaliana. Our analysis of 140 genes regulated by genomic imprinting in the A. thaliana seed endosperm demonstrates they are evolving more rapidly than expected. To investigate whether positive selection drives this evolutionary acceleration, we identified orthologs of each imprinted gene across 34 plant species and elucidated their evolutionary trajectories. Increased positive selection was sought by comparing its incidence among imprinted genes with non-imprinted controls. Strikingly, we find a statistically significant enrichment of imprinted paternally expressed genes (iPEGs) evolving under positive selection, 50.6% of the total, but no such enrichment for positive selection among imprinted maternally expressed genes (iMEGs). This suggests that maternally- and paternally-expressed imprinted genes are subject to different selective pressures. Almost all positively selected amino acids were fixed across 80 sequenced A. thaliana accessions, suggestive of selective sweeps in the A. thaliana lineage. The imprinted genes under positive selection are involved in processes important for seed development including auxin biosynthesis and epigenetic regulation. Our findings support a genomic imprinting model for plants where positive selection can affect paternally-expressed genes due to continued conflict with maternal sporophyte tissues, even when parental conflict is reduced in predominantly inbreeding species.

Citation

Tuteja, R., McKeown, P. C., Ryan, P., Morgan, C. C., Donoghue, M. T., Downing, T., …Spillane, C. (2019). Paternally expressed imprinted genes under positive Darwinian selection in Arabidopsis thaliana. Molecular Biology and Evolution, 36(6), 1239–1253. https://doi.org/10.1093/molbev/msz063

Journal Article Type Article
Acceptance Date Feb 21, 2019
Online Publication Date Mar 26, 2019
Publication Date 2019-06
Deposit Date Mar 13, 2019
Publicly Available Date Mar 28, 2024
Journal Molecular Biology and Evolution
Print ISSN 0737-4038
Electronic ISSN 1537-1719
Publisher Oxford University Press (OUP)
Peer Reviewed Peer Reviewed
Volume 36
Issue 6
Pages 1239–1253
DOI https://doi.org/10.1093/molbev/msz063
Keywords Genomic imprinting; Genomic conflict; Positive Darwinian selection; Endosperm; Plant evolution
Public URL https://nottingham-repository.worktribe.com/output/1636575
Publisher URL https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msz063/5380439

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