Auxin regulates endosperm cellularization in Arabidopsis

The endosperm is an ephemeral tissue serving as nutrient source for the developing embryo, similarly to the placenta in mammals. It is derived after fertilization of the central cell in the female gametophyte. In most angiosperms the endosperm starts to develop as syncytium, where nuclear divisions are not followed by cytokinesis. The timing of endosperm cellularization largely varies between species and the event triggering this transition remains unknown. Here we show that increased auxin biosynthesis in the endosperm prevents endosperm cellularization, leading to seed arrest. Auxin overproducing seeds phenotypically resemble paternal excess triploid seeds derived from hybridizations of diploid maternal plants with tetraploid pollen donors. We demonstrate that auxin biosynthesis and signaling genes are strongly overexpressed in triploid seeds, correlating with increased auxin activity. Reduced auxin biosynthesis and signaling can restore endosperm cellularization in triploid seeds and restore triploid seed viability, highlighting a causal role of increased auxin levels in preventing endosperm cellularization. We propose that auxin levels determine the time of endosperm cellularization and uncovered a central role of auxin in establishing hybridization barriers by changing the timing of endosperm cellularization.