Endosperm secretion remodels the maternal seed coat

Abstract

In flowering plants and mammals, maternal tissues must accommodate the growth of the offspring they enclose. The maternal seed coat expands around the developing embryo and endosperm. Endosperm pressure and hormonal signals coordinate seed-coat development1,2, but whether the endosperm directly promotes maternal cell elongation remains unclear. Here we show that the coenocytic Arabidopsis endosperm directly supplies cell-wall-loosening proteins to maternal seed-coat walls. The seed-size-regulating HAIKU-WRKY10 pathway activates an endosperm secretory programme enriched in cell-wall-associated proteins. These proteins spread through a shared extracellular domain across multiple inner seed-coat layers, revealing an extensive functional maternal-filial interface through which the endosperm reaches maternal cells it does not directly contact. Among these proteins, three expansins are necessary and sufficient for maternal cell elongation and seed growth. The endosperm therefore promotes its own growth by enabling expansion of the maternal tissues that enclose it. Paternal DNA methylation and maternal Polycomb activity jointly regulate this programme, with Polycomb also required for timely shutdown of expansin expression. These findings link parental epigenetic states to maternal tissue expansion through proteins supplied by the offspring. This cross-generational control of growth parallels epigenetically regulated signaling from mammalian extraembryonic tissues3, suggesting a shared strategy for adapting the maternal environment to offspring development.