Dynamic regulation of H3K27me3 to balance maize endosperm filling and development

Polycomb repressive complex 2 (PRC2)-mediated H3K27me3 deposition are vital for the cell fate determining during Arabidopsis endosperm development. Cereal endosperms have an entirely different post developmental process compared with Arabidopsis after the cellularization phase. OsFie1 and ZmFie1 are Fie homologs, and have a specific expression pattern during the endosperm filling but their functions are ambiguous. We applied CUT&Tag to map the H3K27me3 histone modification during maize endosperm development. We observed a genome-wide built of H3K27me3 before endosperm filling, followed by a quickly erasure after filling, the common regions named as Filling specific peaks (FSP), and regulated by ZmFie1. Knockout of ZmFie1 led to more zein proteins and increased cell numbers, but reduced starch content and kernel sizes. ZmFie1 suppresses premature expression of alpha-zein by directly adding H3K27me3 modifications at the Chromosome 4 tandem repeat gene loci of alpha-zein, and indirectly inhibits cell proliferation by adding H3K27me3 modifications at the ZmMADS loci, ultimately balancing endosperm development and filling. OsFie1 had the similar functions as ZmFie1. Our findings reveal the conserved function of H3K27me3 deposition mediated by ZmFie1/OsFie1 in cereal endosperm development.