Hybridization and genome doubling shape codon usage landscapes in the subgenomes of bread wheat

The success of allopolyploids is partly attributable to their ability to resolve deadly genomic conflicts in early generations. Codon usage patterns are genomic signatures, and codon usage bias is thought to play a key role in shaping patterns of gene expression and cellular function through its effects on diverse processes. To date, little is known about the mechanism by which subgenomic conflicts in codon usage are resolved within allopolyploids. Here, we characterized changes in codon usage from wild progenitors to bread wheat. Our results indicated that evolutionarily divergent genomes in bread wheat have the same codon usage patterns, and the codon usage patterns of bread wheat are distinct from those of its wild progenitors, which tend to have a high GC content in the third codon site (GC3). The direct cause of the above phenomenon might be asymmetries in the increase in subgenome GC3 from wild progenitors to bread wheat. Increases in GC3 might also stem from sharp decreases in the average number of transcripts per GC3-poor genes from wild progenitors to bread wheat. Finally, we found that both hybridization and genome doubling can resolve genomic conflicts in codon usage during bread wheat allopolyploidization. Genome doubling induces increases in GC3, which results in a GC3-rich codon bias in bread wheat. The results of this study provide novel insights into the occurrence and consequences of allopolyploidization-induced genomic changes.