Dynamic regulation and function of histone monoubiquitination in plants

Abstract

Polyubiquitin chain deposition on a target protein frequently leads to proteasome-mediated degradation whereas monoubiquitination modifies target protein property and function independent of proteolysis. Histone monoubiquitination occurs in chromatin and is in nowadays recognized as one critical type of epigenetic marks in eukaryotes. While H2A monoubiquitination (H2Aub1) is generally associated with transcription repression mediated by the Polycomb pathway, H2Bub1 is involved in transcription activation. H2Aub1 and H2Bub1 levels are dynamically regulated via deposition and removal by specific enzymes. We review knows and unknowns of dynamic regulation of H2Aub1 and H2Bub1 deposition and removal in plants and highlight the underlying crucial functions in gene transcription, cell proliferation/differentiation, and plant growth and development. We also discuss crosstalks existing between H2Aub1 or H2Bub1 and different histone methylations for an ample mechanistic understanding.

Keywords: Arabidopsis thaliana; chromatin; epigenetics; histone monoubiquitination; plant development; transcription regulation; ubiquitin.

FIGURE 1

A proposed model for deposition and removal of histone H2B monoubiquitination in transcriptional activation of FLC and MAFs in flowering time regulation. In this model, HUB1 and HUB2 form a heterotetramer and recruit UBC1 or UBC2 to FLC/MAFs chromatin, leading to transfer of a ubiquitin (ub) monomer from UBC1 or UBC2 onto H2B. H2Bub1 formation enhances H3K4me3 deposition by methyltransferases, together promoting transcription initiation. UBP26 removes ubiquitin on H2B, favoring H3K36me3 deposition in promoting transcription elongation. Active transcription of FLC/MAFs represses Arabidopsis flowering, a transition from vegetative to reproductive plant development.

FIGURE 2

Proposed models for histone H2A monoubiquitination deposition in transcriptional repression of varied target genes. The Arabidopsis PRC1-like RING-finger proteins AtRING1a/b (RING1) and AtBMI1a/b/c (BMI1) have the E3 ligase activity in catalyzing H2A monoubiquitination (H2Aub1). Comparable to the classical model of sequential PRC2 then PRC1 action in Polycomb silencing in animal cells, the Arabidopsis PRC1-like protein LHP1 binds H3K27me3 pre-deposited by the evolutionarily conserved PRC2 complexes and recruits RING1, BMI1 and possibly also EMF1 through protein–protein interactions (A). This combinatorial action by PRC2 then PRC1 likely plays a broad role in suppression of numerous genes, including the key stem cell regulatory KNOX genes that need to be stably repressed during lateral organ development. The transcription factor VAL is involved in recruitment of BMI1 and RING1 in suppression of embryonic trait genes in somatic cells (B). AL proteins bind BMI1 and RING1 and play important roles in suppression of several key seed dormancy regulatory genes to promote germination (C). H3K27me3 deposition at embryonic/seed genes is enhanced by VAL/AL-PRC1 (B,C), unraveling a non-canonical crosstalk between H3K27me3 and H2Aub1. The question marks indicate that H2Aub1 deposition in the specified target gene chromatin still requires future investigation.