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

Interspecific hybridization and allopolyploidization merge evolutionarily distinct parental genomes (subgenomes) into a single nucleus. A frequent observation is that one subgenome is "dominant" over the other subgenome, having a greater number of retained genes and being more highly expressed. Which subgenome becomes dominantly expressed in allopolyploids remains poorly understood. Here we "replayed the evolutionary tape" with six isogenic resynthesized Brassica napus (rapeseed) allopolyploid lines and investigated subgenome dominance patterns over the first ten generations post merger. We found that the same subgenome was consistently more dominantly expressed in all lines and generations and that >70% of biased gene pairs showed the same dominance patterns across all lines and an in silico hybrid of the parents. Gene network analyses indicated an enrichment for network interactions and several biological functions for the Brassica oleracea derived 'BnC' subgenome biased pairs, but no enrichment was identified for Brassica rapa derived 'BnA' subgenome biased pairs. Furthermore, DNA methylation differences between subgenomes mirrored the observed gene expression bias towards the 'BnC' subgenome in all lines and generations. These methylation patterns were consistent with those previously associated with higher expression, but differ from proposed mechanisms from recent conceptual models and with observations in other polyploid systems that exhibit subgenome dominance. Many of these differences in gene expression and methylation were also found when comparing the progenitor genomes, suggesting subgenome dominance is partly related to parental genome differences rather than just a byproduct of allopolyploidization. These findings demonstrate that "replaying the evolutionary tape" in an allopolyploid results in largely repeatable and predictable subgenome expression dominance patterns, partly due to preexisting genetic differences among the parental species.