Maternally expressed OsFERTILIZATION INDEPENDENT ENDOSPERM1 regulates seed dormancy and aleurone development in rice

Abstract Seed dormancy, an essential trait for plant adaptation, is determined by the embryo itself and the surrounding tissues. Here, we found that rice (Oryza sativa) FERTILIZATION INDEPENDENT ENDOSPERM1 (OsFIE1) regulates endosperm-imposed dormancy and the dorsal aleurone thickness in a manner dependent on the parent of origin. Maternally expressed OsFIE1 suppresses gibberellin (GA) biosynthesis in the endosperm by depositing trimethylation of lysine 27 on histone H3 (H3K27me3) marks on GA biosynthesis-related genes, thus inhibiting germination and aleurone differentiation. Knockout of rice GA 20-oxidase1 (OsGA20ox1) alleviated the phenotypic defects in osfie1. The aleurone-positive determinant Crinkly 4 (OsCR4) is another target of the OsFIE1-containing Polycomb repressive complex 2 (PRC2). We found that OsFIE1 plays an important role in genomic imprinting in the endosperm of germinating seeds, particularly for paternally expressed genes associated with H3K27me3. The increased aleurone thickness of osfie1 substantially improved grain nutritional quality, indicating that the osfie1 gene may be utilized for breeding nutrient-enriched rice. The findings provide insights into the essential roles of PRC2-mediated H3K27me3 methylation in the acquisition of seed dormancy and endosperm cell differentiation in rice.