Both mechanism and age of duplications contribute to biased gene retention patterns in plants

Abstract

BackgroundAll extant seed plants are successful paleopolyploids, whose genomes carry duplicate genes that have survived repeated episodes of diploidization. However, the survival of gene duplicates is biased with respect to gene function and mechanism of duplication. Transcription factors, in particular, are reported to be preferentially retained following whole-genome duplications (WGDs), but disproportionately lost when duplicated by tandem events. An explanation for this pattern is provided by the Gene Balance Hypothesis (GBH), which posits that duplicates of highly connected genes are retained following WGDs to maintain optimal stoichiometry among gene products; but such connected gene duplicates are disfavored following tandem duplications.ResultsWe used genomic data from 25 taxonomically diverse plant species to investigate the roles of duplication mechanism, gene function, and age of duplication in the retention of duplicate genes. Enrichment analyses were conducted to identify Gene Ontology (GO) functional categories that were overrepresented in either WGD or tandem duplications, or across ranges of divergence times. Tandem paralogs were much younger, on average, than WGD paralogs and the most frequently overrepresented GO categories were not shared between tandem and WGD paralogs. Transcription factors were overrepresented among ancient paralogs regardless of mechanism of origin or presence of a WGD. Also, in many cases, there was no bias toward transcription factor retention following recent WGDs.ConclusionsBoth the fixation and the retention of duplicated genes in plant genomes are context-dependent events. The strong bias toward ancient transcription factor duplicates can be reconciled with the GBH if selection for optimal stoichiometry among gene products is strongest following the earliest polyploidization events and becomes increasingly relaxed as gene families expand.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3423-6) contains supplementary material, which is available to authorized users.

Multiple large-scale gene and genome duplications during the evolution of hexapods

“…This biased pattern was also found among WGD paralogs in an outgroup species, Ixodes scapularis (deer tick), and suggests that it may be consistent across arthropods. Previous studies in plants have found that similar functional categories of genes have been maintained following different genome duplication events Rody et al 2017) , although there are o en idiosyncratic patterns observed across families (Maere et al 2005;Barker et al 2008;Li et al 2016;Mandáková et al 2017) . The 20 insect transcriptomes included in our GO category analyses represent diverse hexapod (SI 10 .…”

“…A common signature of paleopolyploidy is the biased retention and loss of some categories of genes relative to the background pattern of gene turnover. Surviving paralogs from ancient WGDs are o en enriched with idiosyncratic gene ontology (GO) categories in plants (Barker et al 2008;De Smet et al 2013;Li et al 2016;Mandáková et al 2017;Rody et al 2017) , yeasts (Papp et al 2003;Conant 2014) , and animals (Berthelot et al 2014;Lien et al 2016;Session et al 2016) . Among the many hypotheses to explain the retention of paralogs (Kondrashov and Kondrashov 2006;Freeling 2009;Hahn 2009) , the dosage balance hypothesis (DBH) is the only hypothesis that predicts the parallel retention and loss of 7 .…”

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

“…Previous studies reported a bias in the probability of post-WGD retention for different functional categories (Seoighe and Wolfe 1999;McGrath, Gout, Johri, et al 2014;Rody, et al 2017). We assigned Gene Ontology (GO) terms to genes in the P. aurelia complex and the two outgroup species using the panther pipeline (Mi, et al 2013).…”

Phylogenomic analysis of UDP‐dependent glycosyltransferases provides insights into the evolutionary landscape of glycosylation in plant metabolism

“…The large disparities in genome size and gene numbers could be due to differences in the abundance of DNA repeats and polyploidy [allopolyploidy and autopolyploidy/whole‐genome duplication (WGD)] in various plant lineages (Pellicer et al ., ). In addition, tandem duplications also play a role in modulating genome size and gene content, for example, 34% of genes occur in tandem duplications in Eucalyptus grandis (Myburg et al ., ; Rody et al ., ). It has been proposed that retention after tandem duplications contributes to the expansion of enzyme families in plant specialized metabolism, which likely increases gene dosage and metabolic activities (Chae et al ., ; Moghe and Last, ).…”