Repression of FLOWERING LOCUS T Chromatin by Functionally Redundant Histone H3 Lysine 4 Demethylases in Arabidopsis

Jae Hong Seol,Hae-Ryong Song,Ju-Hee Jeong,Young Eun Kwon,Young-Min Jeong,Richard M Amasino,Yoo-Sun Noh,Jong-Hyun Ko,Mohammed Bendahmane,Bosl Noh

doi:10.1371/journal.pone.0008033

Jae Hong Seol, Hae-Ryong Song + Show 8 more

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https://doi.org/10.1371/journal.pone.0008033

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Abstract

FLOWERING LOCUS T (FT) plays a key role as a mobile floral induction signal that initiates the floral transition. Therefore, precise control of FT expression is critical for the reproductive success of flowering plants. Coexistence of bivalent histone H3 lysine 27 trimethylation (H3K27me3) and H3K4me3 marks at the FT locus and the role of H3K27me3 as a strong FT repression mechanism in Arabidopsis have been reported. However, the role of an active mark, H3K4me3, in FT regulation has not been addressed, nor have the components affecting this mark been identified. Mutations in Arabidopsis thaliana Jumonji4 (AtJmj4) and EARLY FLOWERING6 (ELF6), two Arabidopsis genes encoding Jumonji (Jmj) family proteins, caused FT-dependent, additive early flowering correlated with increased expression of FT mRNA and increased H3K4me3 levels within FT chromatin. Purified recombinant AtJmj4 protein possesses specific demethylase activity for mono-, di-, and trimethylated H3K4. Tagged AtJmj4 and ELF6 proteins associate directly with the FT transcription initiation region, a region where the H3K4me3 levels were increased most significantly in the mutants. Thus, our study demonstrates the roles of AtJmj4 and ELF6 as H3K4 demethylases directly repressing FT chromatin and preventing precocious flowering in Arabidopsis.

Highlights

Flowering, a critical developmental transition in plants, is controlled by both environmental cues and internal developmental signals
The double-mutant plants flowered earlier than either single mutants as well as the wt Col plants both in long days (LD) and short days (SD) (Figures 5A–5C). Because both EARLY FLOWERING6 (ELF6) and Arabidopsis thaliana Jumonji4 (AtJmj4) have repressive roles in the photoperiod pathway, we evaluated the mRNA levels of genes acting in the photoperiod pathway, namely GI, CO and FLOWERING LOCUS T (FT), using RNAs isolated from SD-grown plants. mRNA levels of GI and CO were similar among wt, the elf6-4 and atjmj4-1 single mutants, and the elf6-4 atjmj4 double mutants at ZT4 and ZT11 (Figure 5D)
Recent studies have shown that the expression of some key flowering genes, such as FLOWERING LOCUS C (FLC) and FT, are regulated through chromatin modifications and have identified many of the factors involved in the chromatin modification processes [44,45]

Summary

Introduction

A critical developmental transition in plants, is controlled by both environmental cues and internal developmental signals. Generation of the photoperiodic floral induction signal in the leaves is mediated by light and circadian-clock signaling and relayed through the photoperiod pathway. GIGANTEA (GI) [1,2] and CONSTANS (CO) [3] act as upstream activators of FLOWERING LOCUS T (FT) [4,5] in the photoperiod pathway. FT acts as a component in the photoperiod pathway and as a floral integrator that combines the perception of inductive photoperiods and the FLC-mediated floral repression signal. FT protein, as a graft-transmissible signal, is translocated from the vascular tissue of leaves to the shoot apex [7], where it interacts with FD and stimulates the floral transition [8,9]

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