Atypical E2F transcription factors couple Polycomb Repressive Complex 2 to endosperm cell division and...

Flowering plant endosperm and mammalian placenta represent convergent evolutionary products sharing conserved developmental programmes, embryonic nutrient transport and genomic imprinting. Polycomb Repressive Complex 2 (PRC2)-mediated H3K27me3 silencing restricts precocious tissue overproliferation in both lineages, yet the underlying molecular mechanism remains undefined. Here we show that mutations in ancestral maize ZmFIE2, not its derived paralogue ZmFIE1, abrogates global H3K27me3 levels, resulting in aberrant cell proliferation, impaired differentiation in early endosperm and seed lethality. ZmFIE2 physically interacts with the ancient atypical E2F transcription factor ZmE2F12 to recruit PRC2, depositing H3K27me3 at G1/S-phase and differentiation genes via E2F motifs in their promoters and repressing their expression. Codepletion of ZmE2F12 and its close paralogue ZmE2F13 abolishes this epigenetic repression and induces excessive endosperm cell proliferation. The orthologous DEL1-FIE complex functions equivalently in Arabidopsis endosperm. Collectively, our findings delineate a conserved E2F-PRC2 epigenetic module that restricts G1/S-phase progression to maintain endosperm developmental homeostasis.