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

Abstract

Background: All 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.

Results: We 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.

Conclusions: Both 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.

Keywords: Biased gene retention; Polyploidy; Transcription factors; Whole-genome duplication.

Fig. 1

Ks age distributions (a and b) and SiZer maps (c to e) of five plant species. a Brown bars, all paralogs (background); black bars, WGD-derived paralogs predicted by DAGchainer; yellow bars, paralogs annotated as transcription factor activity (GO:0003700). b Brown bars, background; gray bars, tandem-derived paralogs predicted by DAGchainer. SiZer maps for c All paralogs; d WGD-derived paralogs; e Transcription factor paralogs

Fig. 2

Heat maps of GO categories across 25 plant species. a The 10 most frequent GO categories overrepresented among WGD-derived paralogs. b Transcription factor activity category (GO:0003700) enrichment analysis for WGD-derived paralogs. c The 10 most frequent GO categories overrepresented among tandem-derived paralogs. Color gradient represents the Corrected P value calculated by the ErmineJ software: brown colors, significant over-representation (P < 0.05); yellow colors, reduced or non-significant enrichment; and gray color, no enrichment

Fig. 3

Phylogenetic distribution of transcription factor retention biases among 25 plant species. The phylogenetic tree was adapted from PLAZA 3.0. Symbol code: Black circles on the tree branches, all known WGD events we also identified in this study; Open circles, suggested ancient WGD events we did not examine; triangles, species with WGD-derived transcription factor paralogs significantly overrepresented; pentagons and stars, species with transcription factor paralogs significantly overrepresented in range 1.5 < Ks ≤ 2 and range 1 < Ks ≤ 2, respectively