Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

The gene balance hypothesis proposes that selection acts on the dosage (i.e. copy number) of genes within dosage-sensitive portions of networks, pathways, and protein complexes to maintain balanced stoichiometry of interacting proteins, because perturbations to stoichiometric balance can result in reduced fitness. This selection has been called dosage balance selection. Dosage balance selection is also hypothesized to constrain expression responses to dosage changes, making dosage-sensitive genes (those encoding members of interacting proteins) experience more similar expression changes. In allopolyploids, where whole-genome duplication involves hybridization of diverged lineages, organisms often experience homoeologous exchanges that recombine, duplicate, and delete homoeologous regions of the genome and alter the expression of homoeologous gene pairs. Although the gene balance hypothesis makes predictions about the expression response to homoeologous exchanges, they have not been empirically tested. We used genomic and transcriptomic data from 6 resynthesized, isogenic Brassica napus lines over 10 generations to identify homoeologous exchanges, analyzed expression responses, and tested for patterns of genomic imbalance. Groups of dosage-sensitive genes had less variable expression responses to homoeologous exchanges than dosage-insensitive genes, a sign that their relative dosage is constrained. This difference was absent for homoeologous pairs whose expression was biased toward the B. napus A subgenome. Finally, the expression response to homoeologous exchanges was more variable than the response to whole-genome duplication, suggesting homoeologous exchanges create genomic imbalance. These findings expand our knowledge of the impact of dosage balance selection on genome evolution and potentially connect patterns in polyploid genomes over time, from homoeolog expression bias to duplicate gene retention.

Automated summary

The gene balance hypothesis suggests that selection acts on gene dosage within dosage-sensitive parts of networks, pathways, and protein complexes to maintain balanced stoichiometry, due to the fitness cost of imbalanced stoichiometry. This selection is known as dosage balance selection. It is also hypothesized that dosage balance selection constrains expression responses to changes in dosage, resulting in similar expression changes among genes encoding interacting proteins. In this study, researchers tested the gene balance hypothesis by analyzing genomic and transcriptomic data from resynthesized Brassica napus lines. They found that dosage-sensitive genes had less variable expression responses to homoeologous exchanges, indicating that their relative dosage is constrained. Additionally, the expression response to homoeologous exchanges was more variable than the response to whole-genome duplication, suggesting that homoeologous exchanges create genomic imbalance.