DNA methylation and imprinting

Imprinting is a preferential expression pattern of genes according to their maternal and paternal allele origin. When the preferential expression comes from the mother, the genes are called maternally expressed genes (MEG), when from the father, paternally expressed genes (PEG) (Batista & Köhler, 2020). Epigenetic modifications in DNA methylation, histone modifications, or chromatin composition might be directly favoring the activity of one allele over another (Dong et al., 2018; P. R. V. Satyaki & Gehring, 2017). This epigenetic phenomenon is exclusive for flowering plants, suggesting an independent evolution among plant species of different periods in time (Batista & Köhler, 2020).

Imprinting is detected mostly in the endosperm, an analog of the placenta of mammals. Even though the endosperm surrounds the embryo and supplies nutrients to it from the maternal parent, little is known of imprinted genes in the embryo (Fig. 8) (Batista & Köhler, 2020; Law & Jacobsen, 2010; P. R. V. Satyaki & Gehring, 2017). What we know is that a small number of genes are differentially methylated and silenced in male and female tissues. This is regulated by de novo methylation, maintenance methylation, and demethylation, with demethylation dominating the process (Batista & Köhler, 2020; P. R. V. Satyaki & Gehring, 2017). This is suggested by DME activity and the presence of DML2-3 and ROS1 in the central cell and the vegetative nucleus of the male and female gametophyte in Arabidopsis and rice (Batista & Köhler, 2020). The reason for this massive active demethylation in vegetative gametophyte tissue may be the protection through hypermethylation of the DNA in the haploid egg and sperm cells. In the germline, active transposons could produce much damage. The active demethylation of TEs leads to their transcription and the production of small interfering RNAs (siRNAs) in the tissue surrounding the egg and sperm cells. From their, siRNAs are thought to be transported into the egg and sperm cells, leading to hypermethylation of their homolog sequences throughout the RdDM pathway and thereby effectively hindering the activation of TEs in the germline (Fig. 8B) (Batista & Köhler, 2020; Law & Jacobsen, 2010). However, how the siRNAs are exported to adjacent compartments is yet unknown (Law & Jacobsen, 2010).

So, hypermethylation of the embryo DNA is most likely caused by the demethylation of the surrounding vegetative tissue. However, this is not yet imprinting because it does not yet include a preference of the maternal of the parental allele. What is needed here, ist that not only the egg but also the endosperm is fertilized, which is the case in flowering plants (Fig. 8). Now it is principally possible that only the male or the female allele is transcribed in the endosperm, leading to allele-specific gene expression in the endosperm. This is realized, for example, via the accumulation of the histone H3K27me3 on the maternal allele of the MADS-box transcription factor PHERES 1, after demethylation through DME in the central cell of the endosperm. The maternal allele is silenced through this accumulation. In the parental allele, a 3’ sequence is methylated, which is thought to prevent H3K27me3 accumulation. Consequently, only the parental allele of PHERES 1 can be expressed in the endosperm (Batista & Köhler, 2020).

In many plant species such as Arabidopsis thaliana, maize, rice, and sorghum between the 40 to 50% of maternal expressed imprinted genes (MEGs) and 60% of parental expressed imprinted genes (PEGs) are associated with epigenetic marks in gene bodies and flanking regions in the endosperm (Batista & Köhler, 2020; Satyaki & Gehring, 2017). There is little information about well-identified imprinted genes and their regulation mechanism in Plants. One of the most studiest genes is the FLOWERING WAGENINGEN (FWA) gene in Arabidopsis, which encodes a transcription factor related to delayed flowering. FWA is tissue-specific activated by DNA demethylation in the female gamete and endosperm (Fujimoto et al., 2008; Meyer, 2011). The FWA gene is rich in tandem repeats and a SINE-related sequence which are direct targets for the methylation machinery, and it is sufficient for imprinting and vegetative silencing (Fujimoto et al., 2008; Meyer, 2011).

To summarize, a combination of epigenetic mechanisms is responsible for parent-of-origin expressed genes. However, it seems so far that plant species contain differ in their regulating systems hampering the general understanding of this phenomenon. Therefore, the development of new molecular tools probably is needed.