A Companion Cell–Dominant and Developmentally Regulated H3K4 Demethylase Controls Flowering Time in Arabidopsis via the Repression of FLC Expression

Abstract

Flowering time relies on the integration of intrinsic developmental cues and environmental signals. FLC and its downstream target FT are key players in the floral transition in Arabidopsis. Here, we characterized the expression pattern and function of JMJ18, a novel JmjC domain-containing histone H3K4 demethylase gene in Arabidopsis. JMJ18 was dominantly expressed in companion cells; its temporal expression pattern was negatively and positively correlated with that of FLC and FT, respectively, during vegetative development. Mutations in JMJ18 resulted in a weak late-flowering phenotype, while JMJ18 overexpressors exhibited an obvious early-flowering phenotype. JMJ18 displayed demethylase activity toward H3K4me3 and H3K4me2, and bound FLC chromatin directly. The levels of H3K4me3 and H3K4me2 in chromatins of FLC clade genes and the expression of FLC clade genes were reduced, whereas FT expression was induced and the protein expression of FT increased in JMJ18 overexpressor lines. The early-flowering phenotype caused by the overexpression of JMJ18 was mainly dependent on the functional FT. Our findings suggest that the companion cell–dominant and developmentally regulated JMJ18 binds directly to the FLC locus, reducing the level of H3K4 methylation in FLC chromatin and repressing the expression of FLC, thereby promoting the expression of FT in companion cells to stimulate flowering.

Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC

“…The isolated chromatin was incubated with anti-GFP (ab290) and pulled out by salmon sperm DNA-coated Protein A agarose (Millipore). DNA was purified and analyzed as previously described (49). The Pol II ChIP was performed as described in ref.…”

Jumonji demethylases moderate precocious flowering at elevated temperature via regulation of FLC in Arabidopsis

“…Although FLC expression is low in WT plants that lack a functional FRIGIDA (FRI) 38 , expression analyses are still able to detect basal FLC expression, which gradually decreases during vegetative development (Fig. 1c) 27 . To determine whether FLC temporal expression level is affected by elevated temperatures, we analysed FLC expression in plants grown at 22°C and 29°C under LD conditions at 5, 9 and 13 days-after-germination (DAG) before the plants undergo the bolting process.…”

“…There are 21 JUMONJI (JMJ) genes in Arabidopsis, which can be categorized into five groups, namely the KDM5/JARID1, KDM4/JHDM3/ JMJD2, KDM3/JHDM2, JMJD6 and JmjC domain-only group, based on their JmjC domain sequences and domain architectures 22,23 . Members from the same group show similar target specificity for histone modifications [24][25][26][27][28][29][30][31][32] . One of the histone modifications, the repressive PcG-mediated H3K27me3, plays a key role in gene repression and developmental regulation, and is actively and dynamically deposited and removed in plants 33 .…”

Jumonji C Domain Protein JMJ705-Mediated Removal of Histone H3 Lysine 27 Trimethylation Is Involved in Defense-Related Gene Activation in Rice

“…Plant jmjC proteins are generally conserved with yeast and animal homologs, while there exist a subgroup of more divergent jmjC proteins (Sun and Zhou, 2008). Members of this subgroup (i.e., Arabidopsis JMJ14, JMJ15, and JMJ18 and rice JMJ703) have been reported to be H3K4 demethylases and to regulate diverse aspects of chromatin function and plant development (Deleris et al, 2010;Lu et al, 2010;Searle et al, 2010;Yang et al, 2012aYang et al, , 2012bChen et al, 2013;Cui et al, 2013). Conversely, the JMJD3/UTX (ubiquitously transcribed tetratricopeptide repeat, X chromosome) subgroup proteins, which exhibit H3K27 demethylase activities in mammalian cells, are not found in plants.…”