Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus

One of the parental diploid genomes (subgenomes) in an allopolyploid often exhibits higher gene expression levels compared to the other subgenome(s) in the nucleus. However, the genetic basis and deterministic fate of subgenome expression dominance remains poorly understood. We examined the establishment of subgenome expression dominance in six isogenic resynthesized Brassica napus (rapeseed) allopolyploid lines over the first ten generations, and uncovered consistent expression dominance patterns that were biased towards the Brassica oleracea 9C9 subgenome across each of the independent lines and generations. The number and direction of gene dosage changes from homoeologous exchanges (HEs) was highly variable between lines and generations, however, we recovered HE hotspots overlapping with those in multiple natural B. napus cultivars. Additionally, we found a greater number of 9C9 subgenome regions replacing 9A9 subgenome regions among resynthesized lines with rapid reduction in pollen counts and viability. Furthermore, DNA methylation differences between subgenomes mirrored the observed gene expression bias towards the 9C9 subgenome in all lines and generations. Gene-interaction network analysis indicated an enrichment for network interactions and several biological functions for 9C9 subgenome biased pairs, but no enrichment was observed for 9A9 subgenome biased pairs. These findings demonstrate that "replaying the evolutionary tape" in allopolyploids results in repeatable and predictable subgenome expression dominance patterns based on preexisting genetic differences among the parental species.