Seed coat formation in Arabidopsis requires a concerted action of JUMONJI histone H3K27me3 demethylases and Brassinosteroid signaling

Seed development in angiosperms starts with double fertilization, where two paternal sperm cells fertilize the maternal gametes. This leads to the formation of the embryo and of the endosperm. These fertilization products are enveloped by the maternally-derived seed coat, the development of which is inhibited prior to fertilization by the Polycomb Repressive Complex 2 (PRC2). This complex deposits the repressive histone mark H3K27me3, whose removal is necessary for seed coat formation. Here, we show that JUMONJI-type (JMJ) histone demethylases are expressed in the seed coats of Arabidopsis thaliana (Arabidopsis) and are necessary for its formation. We propose that JMJ activity is coupled to Brassinosteroid (BR) function, as BR effectors physically recruit JMJ proteins to target loci. Consistent with this, we show that loss of BR biosynthesis and signaling leads to seed coat defects, and that loss of the main BR receptor, BRI1, results in H3K27me3 hypermethylation. Moreover, our data points to BRI1 mediating H3K27me3 removal independently of BRs, while a different receptor, BRL3, likely regulates seed coat formation in a BR-dependent manner. We thus propose a model where seed coat development relies on canonical and non-canonical functions of BR receptors.