Association of hybridization and genome doubling with codon usage landscapes in the subgenomes of bread wheat

The success of allopolyploids is partly attributable to their ability to resolve genomic conflicts during the early generations following allopolyploidization. Codon usage patterns represent important genomic signatures, and codon usage bias can influence gene expression and cellular function through multiple processes. However, little is known about how subgenomic conflicts in codon usage are resolved during allopolyploidization.

We characterized changes in codon usage from the wild progenitors of bread wheat to modern bread wheat. In addition, we generated full-length transcriptomes of Aegilops tauschii (male parent), Triticum durum (female parent), their triploid hybrids, and spontaneously doubled allohexaploid wheat to investigate changes in codon usage associated with hybridization and genome doubling.

The evolutionarily divergent subgenomes of bread wheat exhibited similar codon usage patterns, whereas the codon usage patterns of bread wheat differed markedly from those of its wild progenitors, which tended to have higher GC content at the third codon position (GC3). These differences were associated with asymmetric changes in subgenomic GC3 during the transition from the wild progenitors to bread wheat. Changes in GC3 were also associated with sharp decreases in the average number of transcripts from GC3-poor genes. Analysis of the synthetic allopolyploidization system further revealed distinct changes in codon usage during successive stages of bread wheat allopolyploidization, including hybridization and genome doubling. In particular, genome doubling was accompanied by an increase in GC3, contributing to the GC3-rich codon usage bias observed in bread wheat.

These findings reveal dynamic remodeling and convergence of codon usage patterns during wheat allopolyploidization and suggest that hybridization and genome doubling contribute differently to this process. Our results provide new insights into the evolution of codon usage landscapes in allopolyploids and may improve our understanding of subgenomic accommodation following allopolyploidization.