Imprinted gene OsFIE1 modulates rice seed development by influencing nutrient metabolism and modifying genome H3K27me3

Imprinted Polycomb group (PcG) genes play a critical role in seed development in Arabidopsis. However, the role of the imprinted gene in cereal plants remains obscure. Here, a transgenic approach was conducted to study the function of the imprinted gene Oryza sativa Fertilization-Independent Endosperm 1 (OsFIE1) during seed development in rice (Oryza sativa ssp. japonica ZhongHua11'). RNAi of OsFIE1 and homozygous T-DNA insertion mutant osfie1 led to smaller seeds, delayed embryo development, smaller aleurone layer cells, and decreased seed set rate. OsFIE1 was specifically expressed in endosperm, and mRNA of OsFIE1 was also enriched in the inner seed coat together with the corresponding PcG members OsiEZ1 and OsCLF. Meanwhile, the contents of seed storage proteins and Ile, Leu, and Val were decreased, accompanied by the down-regulation of multiple transcription factors, storage protein synthesis and amino acid metabolism-related genes in OsFIE1-RNAi lines and osfie1. Western blot analysis showed that the complex OsFIE1-PcG in endosperm regulated the expression of target genes by genome H3K27me3 modification. We conclude that the OsFIE1-PcG complex, which was enriched in the inner seed coat and endosperm linked the development of embryo and endosperm by influencing transcription factors and nutrient metabolism and induced a highly differential effect when compared with the OsFIE2-PcG complex. Significance Statement Imprinted Polycomb group genes play a critical role in seed development in Arabidopsis, but the roles of imprinted genes in cereals remain obscure. Here, we characterize a rice endosperm-specific Polycomb group gene OsFIE1, which influences transcription factor expression and nutrient metabolism in rice.