Plants differ from animals in their capability to easily regenerate fertile adult individuals from terminally differentiated cells [1]. 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 [2,3]. However, it is not currently known if this developmental reprogramming is coupled to a global epigenomic resetting, or what impact it has on the phenotype of the clonal progeny. Here we show that plants asexually propagated via induction of a zygotic developmental program do not fully reset 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 cellspecific epigenetic marks during asexual propagation.
Main Text:Compared to animals, somatic cells of plants can be much more easily coaxed into regenerating entire individuals. Asexual reproduction is therefore much more common in plants than in animals, and this has been traditionally exploited by humans for the clonal propagation and genetic manipulation of many economically important plant species [4].Although clonal propagation provides ecological and evolutionary benefits, the resulting restricted genetic variation could be detrimental to fitness [5,6]. Notably, clonally propagated plants are not always phenotypically identical to their parents; a phenomenon often attributed to the accumulation of genetic mutations. Yet there is little direct evidence that genetic changes are solely responsible for this phenotypic variation, thus we hypothesized that the phenotypic diversity apparent in clonal plants may have epigenetic underpinnings. Because plants can reproduce asexually from below-ground and above-ground organs, which are known to be epigenetically distinct [7,8] we took advantage of this situation to determine to what extent the epigenome could influence clonal plant phenotypes. Specifically, we created somatic embryos from distinct root (Root Origin, RO) and leaf (Leaf Origin, RO) tissues of Arabidopsis thaliana (Col-0 strain) by the controlled expression of a RWP-RK zygotic factor [9] ( Supplementary Fig. 1), in order to mimic naturally-occurring events associated with asexual propagation [2, 10]. We collected seeds from independently regenerated G0 individuals after self-pollination and further propagated each line by selfing for over three 3 consecutive generations (G1-G3) (Fig. 1a). Visual examination revealed no obvious morphological differences between RO and LO plants. To determine any potential differences at the molecular level, we performed whole-genome transcriptome analyses in five randomly selected G2 lines. Only 13 differentially expressed genes (DEGs; FDR < 0.05) distinguished roots of LO and RO plan...