Silencing of active transposable elements in plants

Abstract

In plant genomes the vast majority of transposable elements (TEs) are found in a transcriptionally silenced state that is epigenetically propagated from generation to generation. Although the mechanism of this maintenance of silencing has been well studied, it is now clear that the pathways responsible for maintaining TEs in a silenced state differ from the pathways responsible for initially targeting the TE for silencing. Recently, attention in this field has focused on investigating the molecular mechanisms that initiate and establish TE silencing. Here we review the current models of how TEs are triggered for silencing, the data supporting each model, and the key future questions in this fast moving field.

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

“…The initial methylation of an intragenic TE likely occurs through RdDM. Exactly how RdDM is initially targeted to an unmethylated active TE is still unclear (reviewed in Fultz et al, 2015); however, most intragenic TEs are subject to a feed-forward loop combining RdDM, maintenance methylation, and H3K9me2 deposition (Figure 2). If unchecked, this reinforcement of chromatin modification can spread into the surrounding gene leading to gene silencing or epiallele formation (Saze and Kakutani, 2007), similar to the TEs near genes discussed in the previous section.…”

“…The constitutive heterochromatic silencing of the pericentromere, knob, and TE islands is thought of as the end point in a series of mechanisms to initiate, establish, and maintain TE silencing (Fultz et al, 2015), and this end-point silencing is stable across many plant generations (Becker et al, 2011). The silenced state of constitutive heterochromatin at TE islands is perpetuated through cell division and, in plants, through generations, thus defining these TEs as being epigenetically silenced on a transgenerational basis.…”

Retrotransposons are specified as DNA replication origins in the gene-poor regions of Arabidopsis heterochromatin

“…Moreover, the ±100 nt region around the ORI in euchromatin tends to be depleted of CG methylation (7), which suggests that ORI specification and activity may depend on low levels of methylation. TEs are heavily methylated in C residues of the three sequence contexts, and their methylation is actively maintained by RNA-directed DNA methylation (RdDM) and siRNAs (40,41). However, TEs may differ in their methylation state depending on the type, size or location (14,42).…”

Exogenous Transposable Elements Circumvent Identity-Based Silencing, Permitting the Dissection of Expression-Dependent Silencing

“…Pol V generates nascent RNAs from methylated DNA regions to act as scaffolding transcripts, tethering the siRNA-bound AGO4 or AGO6 to this region of chromatin by an RNA:RNA interaction (Wierzbicki et al, 2009) and triggering DNA methylation through DRM1/2 (Cao et al, 2003). Pol IV-RdDM occurs independently of Pol II expression and has been theorized to function as an identity sensor, using the 24-nucleotide siRNAs produced from silenced TEs to target similar sequences across the genome for RdDM (Fultz et al, 2015).…”