Polycomb Silencing of KNOX Genes Confines Shoot Stem Cell Niches in Arabidopsis

Most plant organs develop postembryonically from stem cells in the shoot and root meristems [1]. In Arabidopsis, Class I KNOTTED-like homeobox (KNOX) transcription factors are specifically expressed in shoot meristems and play a primary role in the maintenance of meristem function [2,3]. Although suppression of KNOX was shown to associate with histone H3K27-methylation [4], the molecular mechanism underlying this suppression is not well understood. Here, we provide genetic, molecular, and functional evidence that an Arabidopsis POLYCOMB REPRESSIVE COMPLEX1 (PRC1)-like complex acts in conjunction with PRC2 in KNOX suppression. We identified AtRING1a and AtRING1b as homologs of the animal PRC1 core component RING1. Loss-of-function mutant Atring1a(-/-)Atring1b(-/-) shows release of KNOX suppression and ectopic-meristem formation. AtRING1a and AtRING1b proteins are localized in the nucleus. AtRING1a binds to itself and to AtRING1b, to CURLY LEAF (CLF), a PRC2 core component catalyzing H3K27-methylation [4, 5], and to LIKE HETEROCHROMATIN PROTEIN1 (LHP1), a chromodomain protein binding trimethyl-H3K27 [6-8]. We further show that clf(-/-) and lhp1(-/-) enhance Atring1a(-/-)Atring1b(-/-) in release of KNOX suppression and mutant phenotypes. We propose a model in which AtRING1a, AtRING1b, and LHP1 form a PRC1-like complex, which binds trimethyl-H3K27 marked by the CLIF-containing PRC2, resulting in transcriptional suppression of KNOX.