Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor

Abstract

Transposable elements (TEs) have a major impact on genome evolution, but they are potentially deleterious, and most of them are silenced by epigenetic mechanisms, such as DNA methylation. Here, we report the characterization of a TE encoding an activity to counteract epigenetic silencing by the host. In Arabidopsis thaliana, we identified a mobile copy of the Mutator‐like element (MULE) with degenerated terminal inverted repeats (TIRs). This TE, named Hiun (Hi), is silent in wild‐type plants, but it transposes when DNA methylation is abolished. When a Hi transgene was introduced into the wild‐type background, it induced excision of the endogenous Hi copy, suggesting that Hi is the autonomously mobile copy. In addition, the transgene induced loss of DNA methylation and transcriptional activation of the endogenous Hi. Most importantly, the trans‐activation of Hi depends on a Hi‐encoded protein different from the conserved transposase. Proteins related to this anti‐silencing factor, which we named VANC, are widespread in the non‐TIR MULEs and may have contributed to the recent success of these TEs in natural Arabidopsis populations.

Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids

“…The new Hi copies induce transdemethylation, mediated by the Hi-encoded VANC protein, having a high specificity for VANDAL21 family elements and being more pronounced at non-CG sites (18). In our material, Hi was hypomethylated in met1 at all cytosine contexts and associated with strong non-CG hypomethylation in F1 epihybrids (SI Appendix, Fig.…”

“…A specific VANDAL21 element, Hi, transposes in ddm1 and met1 mutants (16,18). The new Hi copies induce transdemethylation, mediated by the Hi-encoded VANC protein, having a high specificity for VANDAL21 family elements and being more pronounced at non-CG sites (18).…”

“…Deficiencies in DDM1 induce drastic hypomethylation of heterochromatin at all cytosine contexts, resulting in transcriptional up-regulation of some heterochromatic genes, a massive activation of TE transcription, and mobilization of various TEs (10,[13][14][15][16][17][18]. Elimination of MET1 in null met1 mutants causes a near-complete loss of CG methylation at genes and TEs, which is associated with misexpression of numerous protein-coding genes and broad transcriptional activation of TEs (3)(4)(5)8).…”

Mutator and MULE Transposons

“…A few putatively autonomous elements been demonstrated to be transpositionally active. This include those identified in rice (Os777 and Os3378) (117), Fusarium oxysporum (Hop) (118), and arabidopsis (AtMu1, Hiun ) (119,120). Of these, only Hiun has been unambiguously demonstrated to be an autonomous element.…”

Creating Order from Chaos: Epigenome Dynamics in Plants with Complex Genomes

“…Similarly, many MITE transposons are exceptionally AT-rich and sometimes prefer to insert into AT-rich regions (Le et al, 2000;Naito et al, 2009). Furthermore, at least some TEs are competent to combat silencing by inactivating systems that have evolved to recognize them (Fu et al, 2013;McCue et al, 2013).…”