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

Abstract 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 ‘C’ 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 ‘C’ subgenome regions replacing ‘A’ 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 ‘C’ subgenome in all lines and generations. Gene-interaction network analysis indicated an enrichment for network interactions and several biological functions for ‘C’ subgenome biased pairs, but no enrichment was observed for ‘A’ 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. SignificanceInterspecific hybridization merges evolutionarily distinct parental genomes (subgenomes) into a single nucleus. A frequent observation is that one subgenome is “dominant” over the other subgenome(s) including higher gene expression levels. Which subgenome becomes dominantly expressed in allopolyploids remains poorly understood. Here we “replayed the evolutionary tape” with six isogenic resynthesized allopolyploid Brassica napus lines and investigated subgenome dominance patterns over the first ten generations. We found that the same parental subgenome was consistently more dominantly expressed in all lines and generations. This suggests that subgenome expression dominance is largely predetermined based on differences among the parental diploid genomes. These findings have major implications regarding the genotypic and phenotypic diversity observed following plant hybridization in both ecological and agricultural contexts.