PWWP-DOMAIN INTERACTOR OF POLYCOMBS1 Interacts with Polycomb-Group Proteins and Histones and Regulates Arabidopsis Flowering and Development

Abstract

Polycomb-group (PcG) proteins mediate epigenetic gene regulation by setting H3K27me3 via Polycomb Repressive Complex 2 (PRC2). In plants, it is largely unclear how PcG proteins are recruited to their target genes. Here, we identified the PWWP-DOMAIN INTERACTOR OF POLYCOMBS1 (PWO1) protein, which interacts with all three <i>Arabidopsis thaliana</i> PRC2 histone methyltransferases and is required for maintaining full H3 occupancy at several Arabidopsis genes. PWO1 localizes and recruits CURLY LEAF to nuclear speckles in <i>Nicotiana benthamiana</i> nuclei, suggesting a role in spatial organization of PcG regulation. <i>PWO1</i> belongs to a gene family with three members having overlapping activities: <i>pwo1 pwo2 pwo3</i> triple mutants are seedling lethal and show shoot and root meristem arrest, while <i>pwo1</i> single mutants are early flowering. Interestingly, the PWWP domain of PWO1 confers binding to histones, which is reduced by a point mutation in a highly conserved residue of this domain and blocked by phosphorylation of H3S28. PWO1 carrying this mutation is not able to fully complement the <i>pwo1 pwo2 pwo3</i> triple mutant, indicating the requirement of this domain for PWO1 in vivo activity. Thus, the PWO family may present a novel class of histone readers that are involved in recruiting PcG proteins to subnuclear domains and in promoting Arabidopsis development.