Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

In angiosperms, seed architecture is shaped by the coordinated development of three genetically different components: embryo, endosperm and maternal tissues. The relative contribution of these tissues to seed mass and nutrient storage varies considerably among species. The development of embryo, endosperm or nucellus maternal tissue as primary storage compartments defines three main typologies of seed architecture. It is still debated whether the ancestral angiosperm seed accumulated nutrients in the endosperm or the nucellus. During evolution, plants shifted repeatedly between these two storage strategies through molecular mechanisms that are largely unknown. Here, we characterize the regulatory pathway underlying nucellus and endosperm tissue partitioning in Arabidopsis. We show that Polycomb-group proteins repress nucellus degeneration before fertilization. A signal initiated in the endosperm by the AGAMOUS-LIKE 62 (AGL62) MADS box transcription factor relieves this Polycomb-mediated repression, and therefore allows nucellus degeneration. Further downstream in the pathway, the TRANSPARENT TESTA 16 (TT16) and GORDITA MADS box (GOA) transcription factors promote nucellus degeneration. Moreover, we demonstrate that TT16 mediates the crosstalk between nucellus and seed coat maternal tissues. Finally, we characterize the nucellus cell death program and its feedback role in timing endosperm development. Altogether, our data reveal the antagonistic development of nucellus and endosperm, in coordination with seed coat differentiation.