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...