Incomplete reprogramming of organ-specific epigenetic marks during plant asexual reproduction leads to heritable phenotypic variation

Plants differ from animals in their capability to easily regenerate fertile adult individuals from terminally differentiated cells. This unique developmental plasticity is commonly observed in nature where many species can reproduce asexually through the ectopic initiation of organogenic or embryogenic developmental programs. Limited epigenetic reprogramming taking place during sexual reproduction, it is not known whether the same reprogramming event happened during asexual propagation, and if not, whether this has phenotypic or physiological consequences for the clonal progeny. Here we show that plants asexually propagated via induction of a zygotic developmental program do not fully reprogram cell-specific epigenetic imprints. These imprints are instead inherited even over multiple rounds of sexual reproduction, becoming fixed in hybrids and resulting in heritable molecular and physiological phenotypes that depend on the founder cell used. Our results demonstrate how novel phenotypic variation in plants can be unlocked through the incomplete reprogramming of cell-specific epigenetic marks during asexual propagation.