Dynamic regulation of Polycomb group activity during plant development

Polycomb group (PcG) complexes play important roles in phase transitions and cell fate determination in plants and animals, by epigenetically repressing sets of genes that promote either proliferation or differentiation. The continuous differentiation of new organs in plants, such as leaves or flowers, requires a highly dynamic PcG function, which can be induced, modulated, or repressed when necessary. In this review, we discuss the recent advance in understanding PcG function in plants and focus on the diverse molecular mechanisms that have been described to regulate and counteract PcG activity in Arabidopsis.

Introduction

Polycomb group (PcG) proteins are major regulators of gene expression in both plants and animals. The highly conserved and well-characterized Polycomb Repressive Complex 2 (PRC2) represses gene expression in an epigenetic manner by catalyzing the trimethylation of histone H3 at lysine 27 (H3K27me3). Both in plants and animals, the complex consists of four core members, which together are sufficient to generate the H3K27me3 mark, associated with repressive chromatin, in vitro [1]. The Drosophila PRC2 complex contains the core subunits Enhancer of zeste [E(z)], a histone methyltransferase, Suppressor of zeste 12 [Su(z)12], a Zinc finger protein, and the WD40 domain proteins Extra sex combs (Esc) and Nucleosome remodeling factor 55 (Nurf55). While in Drosophila all but one subunit are encoded by a single gene [1, 2], most of the Arabidopsis PRC2 core subunits are encoded by small gene families. MEDEA (MEA), CURLY LEAF (CLF) and SWINGER (SWN) are homologs of E(z), FERTILIZATION INDEPENDENT SEED2 (FIS2), VERNALIZATION2 (VRN2) and EMBRYONIC FLOWER2 (EMF2) are homologs of Su(z)12, while MULTICOPY SUPPRESSOR OF IRA1-5 (MSI1-5) are the five homologs of Nurf55. In contrast to Drosophila, where Esc and Esc-like share this function [2], the Esc homolog FERTILIZATION INDEPENDENT ENDOSPERM (FIE) is single copy in the Arabidopsis genome [1, 3, 4]. PRC2 complexes of distinct flavor can be formed by combining these different subunits. The complexes EMF-PRC2, VRN-PRC2 and FIS-PRC2 have been confirmed in planta and have both overlapping and independent functions [5].

A second PcG complex, which only to some extent is conserved in plants and animals, is the Polycomb Repressive Complex 1 (PRC1). The core Drosophila PRC1 complex consists of the proteins Polycomb (Pc), Posterior sex combs (Psc), Polyhomeotic (Ph) and dRING1, and binds to the H3K27me3 histone mark generated by PRC2 [6]. PRC1 catalyses the monoubiquitination of histone H2A at lysine 119 (H2AK119ub), thereby compacting the chromatin further and stabilizing the repressed state [7]. Recently, RING-finger homologs able to catalyze H2AK119 monoubiquitination have been identified in plants, as well as other proteins with a PRC1-like function [4, 8•]. The function of the PRC1-like proteins in plants is further discussed below.

In both the animal and plant kingdoms, PcG complexes play important roles in phase transitions during development, cell fate determination and cellular differentiation, by repressing sets of genes that regulate either proliferation or differentiation. In contrast to animals, where the entire body plan is formed during embryogenesis, plants differentiate organs, such as leaves, flowers or lateral roots, throughout their life span and maintain the ability to initiate new pools of stem cells. This requires highly dynamic PcG function, and the ability to induce, modulate, or repress PcG in response to developmental or environmental signals. In this review, we discuss the recent advance in our understanding of PcG function in plants and focus on the various molecular mechanisms that have been found to regulate and counteract PcG activity in Arabidopsis.