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Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators

M. Wołoszyńska,Sabine Le Gall,P. Neyt,T. M. Boccardi,Marion Grasser,G. Längst,S. Aesaert,Griet Coussens,Stijn Dhondt,Eveline Van De Slijke,L. Bruno,Jorge Fung-Uceda,P. Más,M. Van Montagu,D. Inzé,Kristiina Himanen,G. De Jaeger,K. Grasser,M. Van Lijsebettens

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance In eukaryotes, the genomic DNA is organized in chromatin that consists of nucleosomal units formed by histone proteins. The accessibility of genes for RNA polymerase II transcription by the dynamic modification of histone tails during the transcript elongation phase is emerging as an important regulatory mechanism. Here, we show that RNA-binding proteins, together with the conserved HISTONE MONOUBIQUITINATION1–HISTONE MONOUBIQUITINATION2 complex that mediates histone H2B monoubiquitination at the circadian clock, and flowering time-regulatory genes during transcript elongation are required for the processing of their pre-mRNA and antisense RNA, respectively. HISTONE MONOUBIQUITINATION1 (HUB1) and its paralog HUB2 act in a conserved heterotetrameric complex in the chromatin-mediated transcriptional modulation of developmental programs, such as flowering time, dormancy, and the circadian clock. The KHD1 and SPEN3 proteins were identified as interactors of the HUB1 and HUB2 proteins with in vitro RNA-binding activity. Mutants in SPEN3 and KHD1 had reduced rosette and leaf areas. Strikingly, in spen3 mutants, the flowering time was slightly, but significantly, delayed, as opposed to the early flowering time in the hub1-4 mutant. The mutant phenotypes in biomass and flowering time suggested a deregulation of their respective regulatory genes CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and FLOWERING LOCUS C (FLC) that are known targets of the HUB1-mediated histone H2B monoubiquitination (H2Bub). Indeed, in the spen3-1 and hub1-4 mutants, the circadian clock period was shortened as observed by luciferase reporter assays, the levels of the CCA1α and CCA1β splice forms were altered, and the CCA1 expression and H2Bub levels were reduced. In the spen3-1 mutant, the delay in flowering time was correlated with an enhanced FLC expression, possibly due to an increased distal versus proximal ratio of its antisense COOLAIR transcript. Together with transcriptomic and double-mutant analyses, our data revealed that the HUB1 interaction with SPEN3 links H2Bub during transcript elongation with pre-mRNA processing at CCA1. Furthermore, the presence of an intact HUB1 at the FLC is required for SPEN3 function in the formation of the FLC-derived antisense COOLAIR transcripts.

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