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

Abstract

AbstractSeed development in flowering plants starts with a double fertilization event where two paternal gametes, the sperm cells, fertilize their maternal counterparts, egg cell and central cell. This leads to the formation of the embryo and the endosperm. These fertilization products are enveloped by the maternally-derived seed coat, the development of which is inhibited prior to fertilization by epigenetic regulator Polycomb Repressive Complex 2 (PRC2). This complex deposits the repressive histone mark H3K27me3, whose removal is necessary for seed coat formation. However, H3K27me3 marks are stable and PRC2 removal does not explain how seed coat genes become activated after fertilization. Here, we show that JUMONJI-type (JMJ) histone demethylases are expressed in the seed coats ofArabidopsis thaliana(Arabidopsis) and are necessary for its formation. We further propose that JMJ activity is coupled to Brassinosteroid (BR) function, as BR effectors have been shown to physically recruit JMJ proteins to target loci. Consistent with this hypothesis, we show that loss of BR function leads to seed coat defects, which can be rescued by depletion of H3K27me3. Finally, we reveal an additional pathway through which BRs directly regulate seed coat development, independently of H3K27me3 deposition. This discovery highlights the diverse functions of BRs in coordinating seed development, beyond their known roles in plant growth and development.