eQTL Mapping of Transposon Silencing Reveals a Position-Dependent Stable Escape from Epigenetic Silencing and Transposition of AtMu1 in the Arabidopsis Lineage

Abstract

Transposons are massively abundant in all eukaryotic genomes and are suppressed by epigenetic silencing. Transposon activity contributes to the evolution of species; however, it is unclear how much transposition-induced variation exists at a smaller scale and how transposons are targeted for silencing. Here, we exploited differential silencing of the AtMu1c transposon in the Arabidopsis thaliana accessions Columbia (Col) and Landsberg erecta (Ler). The difference persisted in hybrids and recombinant inbred lines and was mapped to a single expression quantitative trait locus within a 20-kb interval. In Ler only, this interval contained a previously unidentified copy of AtMu1c, which was inserted at the 39 end of a protein-coding gene and showed features of expressed genes. By contrast, AtMu1c(Col) was intergenic and associated with heterochromatic features. Furthermore, we identified widespread natural AtMu1c transposition from the analysis of over 200 accessions, which was not evident from alignments to the reference genome. AtMu1c expression was highest for insertions within 39 untranslated regions, suggesting that this location provides protection from silencing. Taken together, our results provide a species-wide view of the activity of one transposable element at unprecedented resolution, showing that AtMu1c transposed in the Arabidopsis lineage and that transposons can escape epigenetic silencing by inserting into specific genomic locations, such as the 39 end of genes.

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

“…If a TE inserts into an exon or otherwise disrupts the gene's activity, this allele may be selected against, and this may result in the allele's disappearance from the population. Alternatively, a TE may escape silencing altogether by inserting into the 39 untranslated region of an essential gene (Kabelitz et al, 2014), which could provide a safe-haven location that the cell cannot afford to silence. Ultimately, the majority of intragenic TEs do not remain complete or active, as the selection for proper gene activity leads to TE silencing (discussed further below) and/or TE sequence deletion.…”

A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis

“…The degree of reactivation correlated with the magnitude of JMJ24 overexpression. The analysis of unspliced AtMu1c transcripts (Kabelitz et al, 2014) in jmj24-2 and 35S::JMJ24 plants (Supplemental Fig. S2) suggests that the release of silencing occurs at the level of transcription (i.e.…”

“…For AtMu1, it was shown that it is targeted by several epigenetic silencing pathways, including RdDM (Lippman et al, 2003;Bäurle et al, 2007), and AtMu1 transposition was found in DNA methylation-deficient backgrounds and in the vegetative nucleus of pollen, where global reactivation of TEs occurs (Singer et al, 2001;Slotkin et al, 2009). AtMu1c is the most active of the three AtMu1 copies (Kabelitz et al, 2014). At the phylogenetic level, AtMu1c transposition was found in the Arabidopsis lineage (Kabelitz et al, 2014).…”

“…AtMu1c is the most active of the three AtMu1 copies (Kabelitz et al, 2014). At the phylogenetic level, AtMu1c transposition was found in the Arabidopsis lineage (Kabelitz et al, 2014). AtMu1c contains two highly homologous terminal inverted repeats (TIRs) and a conserved transposase gene.…”

The many faces of plant chromatin: Meeting summary of the 4th European workshop onplantchromatin 2015, Uppsala, Sweden

“…This in general suggested that specific genomic locations and chromatin environments may favor escape of TEs from epigenetic silencing. 24 Within the nucleus, silent heterochromatin regions are visible as densely stained chromocenters that in Arabidopsis mainly comprise centromeric and pericentromeric heterochromatin. Chromocenters de-condense during imbibition and seed germination and progressively reform during the first days of post-germination seedling growth, following extensive chromatin rearrangements.…”