Polycomb group proteins are required to couple seed coat initiation to fertilization

Seed development in flowering plants is initiated after a double fertilization event leading to the formation of zygotic embryo and endosperm tissues surrounded by the maternally derived seed coat. Although the seed coat does not take part in the fertilization process it develops immediately after fertilization, implicating a signaling mechanism from zygotic tissues to the surrounding maternal tissues. We addressed the question of the underlying mechanisms repressing seed coat development before fertilization and initiating seed coat development after fertilization by analyzing combinations of mutants that initiate seed development in the absence of fertilization. We discovered that seed coat development is actively repressed before fertilization by dosage-sensitive Polycomb group proteins acting in maternal tissues surrounding the female gametophyte. This repression is relieved after fertilization by a signal that is formed by the sexual endosperm. Fertilization is required for signal formation, as asexually formed endosperm fails to effectively initiate seed coat development in mutants with uncompromised maternal Polycomb group function. Mutants for the MADS-box transcription factor AGL62 initiate embryo and endosperm formation but fail to develop a seed coat, implicating AGL62 expression in the endosperm as a requirement for signal initiation. Together, our results provide evidence that fertilization of the central cell generates a signal that relieves Polycomb group-mediated repression in the surrounding maternal tissues to initiate seed coat formation.