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 nonimprinted 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.
Highlights
Rapid evolution under Positive Selection (PS) is a feature of many reproductive proteins in both plants and animals, occurring either as a result of adaptive radiation or of sexual conflict within and between genomes (Clark, et al 2006)
To determine the selective pressures acting on imprinted genes, while avoiding these confounding scenarios, we focused our analyses on those genes with strong evidence for uniparental expression in seeds due to imprinting
We classified these as genes identified from RNA-seq-based studies (Gehring, et al 2011; Hsieh, et al 2011; Wolff, et al 2011) which are expressed from the paternal genome, and which cannot be due to contamination from maternal tissues; and those imprinted maternally expressed genes (iMEGs) for which experimental validation of monoallelic expression and/or epigenetic regulation in the endosperm has been performed in planta (Vielle-Calzada, et al 1999; Kinoshita, et al 2004; Köhler, et al 2005; Tiwari, et al 2008; Gehring, et al 2009; Hsieh, et al 2011; McKeown, et al 2011; Shirzadi, et al 2011; Wolff, et al 2011)
Summary
Rapid evolution under Positive Selection (PS) is a feature of many reproductive proteins in both plants and animals, occurring either as a result of adaptive radiation or of sexual conflict within and between genomes (Clark, et al 2006). Tests of selective pressure have shown that genes expressed in the highly reduced male gametophyte of flowering plants (the pollen grain) display elevated PS (Arunkumar, et al 2013; Gossmann, et al 2014) These increased levels of PS are observed in genes expressed in the pollen tube but not the sperm cell, and are interpreted to be a consequence of conflict driven by competition between pollen grains for access to ovules (Bernasconi, et al 2004). Genomic imprinting is widely considered to have evolved due to conflict between parentally[80] derived genomes over resource allocation to developing offspring which lead to genes evolving different optimal expression levels depending upon whether they are maternally- or paternally-derived (Willson and Burley 1983; Wilkins and Haig 2003b; Haig 2004). Kin conflict between iPEGs and iMEGs in plants is expected to arise from differences in the optimal level of offspring resource allocation, and resulting offspring size, between the maternal and paternal genomes as selection on the maternal genome favours equal provision to all offspring (and iMEGs near-equal provision; see (Trivers 1974)) while the paternal genome promotes growth of its own offspring alone (Haig 2000; Costa, et al 2012; Haig 2013; Willi 2013)
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