Abstract
Allopolyploidy involves the hybridization of two evolutionary diverged species and the doubling of genomic material. Allopolyploids often exhibit homoeologous exchanges (HEs) that recombine, duplicate, or delete homoeologous regions. These changes to gene dosage are hypothesized to be constrained by selection to maintain balanced gene dosage. However, the dynamics of this dosage constraint in response to HEs or in the context of biased subgenome expression is poorly understood. We used genomic and transcriptomic data for six independently resynthesized, isogenic Brassica napus lines in the first, fifth, and tenth generation to identify HEs. We modified a recently developed method (polyploid response variance, PRV) to analyze HE events, which we call homoeologous exchange response variance (HERV), and tested HEs for gene expression dynamics reflective of gene dosage constraint. Results from the HERV analyses showed that dosage-sensitive groups of genes (GO terms) had a less variable expression response to HEs than dosage-insensitive genes; thus, HEs showed a sign of selective constraint for balanced gene dosage. We also discovered this dosage constraint is present for homoeologous pairs where expression is biased toward the dominant BnC subgenome, but not the BnA subgenome. A PRV analysis of the expression response to polyploidy and an integrated PRV/HERV analysis confirmed this pattern of dosage constraint. These findings expand our knowledge of the prevalence of dosage constraint and the interplay of dosage constraints and biased subgenome expression. We speculate how these results connect evolutionary patterns in polyploids over time; from homoeolog expression bias to biased fractionation and reciprocal retention.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
We substantially revised our methodology for detecting expression responses to homoeologous exchange and provided additional analyses to address concerns of expression differences among dosage-sensitive and dosage-insensitive genes We also addressed the lack of clarity or detail in several aspects of the methodology and in doing so expanded the supplementary material to now include 8 supplemental figures and a supplementary dataset that contains the data underlying the main figures. In addition, we clarified our main points with an updated title and more focused abstract, introduction and discussion. We also added both classic and recent references on homoeologous exchanges and subgenome dominance to put this research into a historical context with respect to the published literature. Finally, we added a new concluding paragraph about future directions to connect this research to a broader audience.
