Epigenetic divergence is sufficient to trigger heterosis in Arabidopsis thaliana

Despite the importance and wide exploitation of heterosis in commercial crop breeding, the molecular mechanisms behind this phenomenon are not well understood. Interestingly, there is growing evidence that beside genetic also epigenetic factors contribute to heterosis. Here we used near-isogenic but epigenetically divergent parents to create epigenetic F1 hybrids (epiHybrids) in Arabidopsis, allowing us to quantify the contribution of epigenetics to heterosis. We measured traits such as leaf area (LA), growth rate (GR), flowering time (FT), main stem branching (MSB), rosette branching (RB) and final plant height (HT) and observed several strong positive and negative heterotic phenotypes among the epiHybrids. For LA and HT mainly positive heterosis was observed, while FT and MSB mostly displayed negative heterosis. Heterosis for FT, LA and HT could be associated with several heritable, differentially methylated regions (DMRs) in the parental genomes. These DMRs contain 35 (FT and LA) and 14 (HT) genes, which may underlie the heterotic phenotypes observed. In conclusion, our study indicates that epigenetic divergence can be sufficient to cause heterosis.