Abstract

BackgroundPolyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants. The duplication among the parental genomes (subgenomes) often leads to one subgenome becoming dominant over the other(s), resulting in subgenome asymmetry in gene content and expression. Polyploid wheats are allopolyploids with most genes present in two (tetraploid) or three (hexaploid) functional copies, which commonly show subgenome expression asymmetry. It is unknown whether a similar subgenome asymmetry exists during translation. We aim to address this key biological question and explore the major contributing factors to subgenome translation asymmetry.ResultsHere, we obtain the first tetraploid wheat translatome and reveal that subgenome expression asymmetry exists at the translational level. We further perform in vivo RNA structure profiling to obtain the wheat RNA structure landscape and find that mRNA structure has a strong impact on translation, independent of GC content. We discover a previously uncharacterized contribution of RNA structure in subgenome translation asymmetry. We identify 3564 single-nucleotide variations (SNVs) across the transcriptomes between the two tetraploid wheat subgenomes, which induce large RNA structure disparities. These SNVs are highly conserved within durum wheat cultivars but are divergent in both domesticated and wild emmer wheat.ConclusionsWe successfully determine both the translatome and in vivo RNA structurome in tetraploid wheat. We reveal that RNA structure serves as an important modulator of translational subgenome expression asymmetry in polyploids. Our work provides a new perspective for molecular breeding of major polyploid crops.

Highlights

  • Polyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants

  • Polysome profiling reveals translational subgenome asymmetry in wheat To uncover the translational landscape in wheat, we performed polysome profiling on the tetraploid durum wheat cultivar, Kronos (2n = 4x = 28, BBAA), by subjecting polysome-associated RNAs to deep sequencing (Fig. 1a, and Additional file 1: Figure S1A, B and C)

  • Our result showed that translational efficiencies of mRNAs in wheat were partially associated with their transcriptional levels

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Summary

Introduction

Polyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants. Accumulated evidence indicates that these induced genetic and epigenetic changes in allopolyploids may help overcome incompatibilities and offer a reservoir of novel phenotypes, facilitating their ecological diversification and adaptation to new niches [4, 5]. Of these changes, gene expression subgenome dominance is a common feature of allopolyploids and may have played crucial roles in their adaptation and evolution [6,7,8]. These duplicated genes of polyploid wheat are subject to dynamic selections during domestication and environmental adaptation [11,12,13]

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