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.