The First Rule of Plant Transposable Element Silencing: Location, Location, Location

Abstract

Transposable elements (TEs) are mobile units of DNA that comprise large portions of plant genomes. Besides creating mutations via transposition and contributing to genome size, TEs play key roles in chromosome architecture and gene regulation. TE activity is repressed by overlapping mechanisms of chromatin condensation, epigenetic transcriptional silencing, and targeting by small interfering RNAs. The specific regulation of different TEs, as well as their different roles in chromosome architecture and gene regulation, is specified by where on the chromosome the TE is located: near a gene, within a gene, in a pericentromere/TE island, or at the centromere core. In this Review, we investigate the silencing mechanisms responsible for inhibiting TE activity for each of these chromosomal contexts, emphasizing that chromosomal location is the first rule dictating the specific regulation of each TE.

Figure 1.

The Four TE Chromosomal Contexts Discussed in This Review. TEs are shown as red, pink, and orange triangles, gene exons as green boxes, and tandem repeats as yellow triangles.

Figure 2.

RdDM and Maintenance TE Silencing Mechanisms. (A) TEs near and within genes are targeted by RdDM. RNA Pol IV is recruited to TE templates via H3K9me2 (Law et al., 2013). Pol V is recruited to TEs via DNA methylation (Johnson et al., 2014; Liu et al., 2014). The Pol IV/RDR2 complex generates double-stranded RNAs that are cleaved by DCL3 into 24-nucleotide siRNAs. These 24-nucleotide siRNAs are incorporated into and guide an AGO family protein to target the Pol V scaffold transcript, resulting in DRM2-mediated DNA methylation of cytosines in all sequence contexts. See text for details. (B) TEs are maintained in a silenced state by maintenance DNA methyltransferases (MET1, CMT3, and CMT2). MET1 acts after DNA synthesis to propagate CG methylation to the new DNA strand. CMT3 and CMT2 operate in a positive feedback loop of H3K9me2 and CHG/CHH context DNA methylation with the histone methyltransferase proteins KYP/SUVH4, SUVH5, and SUVH6. Protein sizes not to scale.

Figure 3.

Silencing at TE Edges. (A) The KYP/CMT cycle and/or RdDM function to spread H3K9me2 and cytosine DNA methylation outward from TEs toward neighboring genes. IBM1 and ROS1 remove methylation from H3K9me2 and DNA, respectively, stopping their spread into surrounding genes. JMJ14, LDL1, and LDL2 remove the genic mark of H3K4 methylation out of the silenced TEs. These mechanisms produce a sharp euchromatin-to-heterochromatin boundary or edge compared with the interior of the TE or flanking gene, represented here by the CHH methylation profile (green) of the TE and surrounding region. (B) The methylstat model of ROS1 regulation. The RdDM of an upstream TE spreads into the Ros1 promoter region. This spread of methylation activates Ros1 expression. The ROS1 protein prunes DNA methylation from its own promoter and limits the spread of methylation out of the TE. In this manner, ROS1 regulates its own expression and can potentially gauge and respond to the genome-wide activity level of RdDM.

Figure 4.

Punctuated Bursts of Different TE Lineages from the Same Plant Genome. Phylogenetic reconstructions of TE activity demonstrate that amplification of different TE lineages (green, orange, dark blue, light blue, and purple) within the same genome did not occur at the same time. Branch points represent TE transposition events, and branch length represents TE divergence. These data and model, adapted from Daron et al. (2014), refutes the “genome shock” hypothesis where the silencing pressure inhibiting all TEs is simultaneously released, and many or all TEs undergo a coordinated burst of activity. Rather, these data suggest that TE activity and genome expansion in plants are due to the ability of preexisting individual elements to separately circumvent silencing and go through a boom period of activity before resilencing. MYA, million years ago.

Figure 5.

Two Mutually Exclusive Mechanisms of CHH Methylation. TE CHH methylation either occurs via RdDM (left) or CMT2-mediated maintenance methylation (right) (Stroud et al., 2014; Li et al., 2015; McCue et al., 2015). RdDM acts at small TEs near genes on the euchromatic chromosome arms (green arrow), while CMT2 acts at TEs in pericentromeres, knobs, and TE islands (red arrows). Both of these pathways rely on existing H3K9me2, but how this one mark is differentially interpreted for either RdDM or CMT2-based maintenance methylation (but not both at the same time) is currently a critical question in the field. Protein sizes not to scale.