The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons

MADS-box transcription factors (TFs) are ubiquitous among eukaryotes, and classified into two groups: type I or SRF (Serum Response Factor)-like, and type II or MEF2 (Myocyte Enhancing Factor2)-like. In flowering plants, type I MADS-box TFs are associated with reproductive development and many are active in the endosperm, a nutritive tissue supporting the embryo. Deregulation of these genes has been frequently linked to failure of endosperm development and seed inviability, both in the Brassicaceae, and in crop species like tomato and rice. Nevertheless, a mechanistic explanation for these observations, clarifying the role of MADS-box TFs in endosperm development, remains to be established. Here we show that the imprinted Arabidopsis thaliana MADS-box TF PHERES1 (PHE1) has a central role in endosperm development as a master regulator of imprinted gene expression, especially of paternally expressed genes (PEGs), which have been previously implicated in endosperm development. Control of imprinted gene expression by PHE1 is mediated by parental asymmetry of epigenetic modifications in PHE1 DNA-binding sites, conferring different accessibilities to maternal and paternal alleles. Importantly, we show that the CArG-box-like DNA-binding motifs used by PHE1 to access gene promoters are carried by RC/Helitron transposable elements (TEs), providing an example of molecular domestication of these elements. Hence, this work shows that TEs are intrinsically linked to imprinting: not only by enforcing specific epigenetic landscapes, but also by serving as important sources of cis-regulatory elements. Moreover, it provides an example of how TEs can widely distribute TF binding sites in a plant genome, allowing to recruit crucial endosperm regulators into a single transcriptional network.