Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140 year old naturally established neo-allopolyploid monkeyflower.

The importance and applications of polyploidy have long been recognized, from shaping the evolutionary success of flowering plants to improving agricultural productivity. Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. How quickly one subgenome dominates within a newly formed polyploid, if immediate or after millions of years, and the genomic features that determine which genome dominates remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and that subgenome expression dominance significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within transposons in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and submissive subgenomes in the natural allopolyploid. Our analyses reveal that the subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following the hybridization. These findings not only provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events, but may also contribute to uncovering the mechanistic basis of heterosis and subgenomic dominance.