Control of transposon activity by a histone H3K4 demethylase in rice

Abstract

Transposable elements (TEs) are ubiquitously present in plant genomes and often account for significant fractions of the nuclear DNA. For example, roughly 40% of the rice genome consists of TEs, many of which are retrotransposons, including 14% LTR-and ∼1% non-LTR retrotransposons. Despite their wide distribution and abundance, very few TEs have been found to be transpositional, indicating that TE activities may be tightly controlled by the host genome to minimize the potentially mutagenic effects associated with active transposition. Consistent with this notion, a growing body of evidence suggests that epigenetic silencing pathways such as DNA methylation, RNA interference, and H3K9me2 function collectively to repress TE activity at the transcriptional and posttranscriptional levels. It is not yet clear, however, whether the removal of histone modifications associated with active transcription is also involved in TE silencing. Here, we show that the rice protein JMJ703 is an active H3K4-specific demethylase required for TEs silencing. Impaired JMJ703 activity led to elevated levels of H3K4me3, the misregulation of numerous endogenous genes, and the transpositional reactivation of two families of non-LTR retrotransposons. Interestingly, loss of JMJ703 did not affect TEs (such as Tos17) previously found to be silenced by other epigenetic pathways. These results indicate that the removal of active histone modifications is involved in TE silencing and that different subsets of TEs may be regulated by distinct epigenetic pathways. R etrotransposons are RNA-mediated transposable elements (TEs), which are abundant in the genomes of both plants and animals (1, 2). Retrotransposons are classified into long terminal repeat (LTR) or non-LTR types, and they are mobilized in a "copy and paste" manner (3-5). The integration of a newly transposed copy might disrupt local gene structure and affect the expression of nearby genes. In humans, misregulation of retrotransposons causes numerous diseases (3, 6, 7).Although transposition of TEs is a major driving force for genome evolution, host genomes have evolved diverse mechanisms to limit harmful mobilization (1, 7). DNA methylation and histone methylation are two reversible epigenetic modifications that control transposon activity (8-13). In plants, histone H3 that is dimethylated at residue K9 (H3K9me2) associates with methylated DNA sequences such as CpG, CHG, and CHH (where H = A, T, or C) and correlates with gene silencing, whereas H3 trimethylated at K4 (H3K4me3) is linked to active transcription (14-16). Histone methylation is highly dynamic. Lysine methylation is catalyzed by SET domain group (SDG) proteins and reversed by a family of Jumonji C (JmjC) domain-containing proteins, which use Fe (II) and α-ketoglutarate (αKG) as cofactors (17,18). In Arabidopsis, JMJ25/IBM1 (increase in BONSAI methylation) encodes an H3K9 demethylase (19,20). Mutation of IBM1 results in increased levels of H3K9me2 and DNA methylation in genes but not in transposons, indicating that IBM1 disti...

Regulation of Histone Methylation and Reprogramming of Gene Expression in the Rice Inflorescence Meristem

“…The jmj703 mutation resulted in a change of a relatively small portion of genome-wide H3K4me3 (Figure 5F), which confirmed previously published data (Cui et al, 2013), but led to a loss of 2957 and a gain of 2447 H3K27me3-marked genes in IM ( Figure 5E). Comparison of differentially marked genes in jmj703 and SDG711 RNAi plants revealed that 2307 out of 2952 (i.e., 2307 + 645) (78%) genes that lost H3K27me3 in jmj703 overlapped with those that lost the mark in SDG711 RNAi plants, 50% of which (1172/2307) corresponded to the genes that gained the mark in wild-type IM ( Figures 5A and 5E).…”

Six-Rowed Spike3 (VRS3) Is a Histone Demethylase That Controls Lateral Spikelet Development in Barley

“…Moreover, JmjCmediated histone demethylation at the FLC locus at elevated temperature is known to prevent premature early flowering (Gan et al, 2014). In rice, the JMJ703, a histone H3 Lys 4 (H3K4) demethylase, is required for stem elongation and transposon silencing (Chen et al, 2013;Cui et al, 2013). The barley VRS3 is similar to the JMJD2 group II of Lys demethylases and exhibits a high similarity to the rice JMJ706, which encodes for a histone H3 Lys 9 di-and tri-(H3K9me2 and H3K9me3) demethylase (Sun and Zhou, 2008).…”

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.…”