Epigenetic targeting of transposon relics: beating the dead horses of the genome?

Abstract

Transposable elements (TEs) have been seen as selfish genetic elements that can propagate in a host genome. Their propagation success is however hindered by a combination of mechanisms such as mutations, selection, and their epigenetic silencing by the host genome. As a result, most copies of TEs in a given genome are dead relics: their sequence is too degenerated to allow any transposition. Nevertheless, these TE relics often, but not always, remain epigenetically silenced, and if not to prevent transposition anymore, one can wonder the reason for this phenomenon. The mere self-perpetuating loop inherent to epigenetic silencing could alone explain that even when inactive, TE copies remain silenced. Beyond this process, nevertheless, antagonistic selective forces are likely to act on TE relic silencing. Especially, without the benefit of preventing transposition, TE relic silencing may prove deleterious to the host fitness, suggesting that the maintenance of TE relic silencing is the result of a fine, and perhaps case-by-case, evolutionary trade-off between beneficial and deleterious effects. Ultimately, the release of TE relics silencing may provide a 'safe' ground for adaptive epimutations to arise. In this review, we provide an overview of these questions in both plants and animals.

DDM1-Mediated TE Silencing in Plants

“…More than any other epigenetic pathway combination, such as RNA interference plus RdDM, DDM1 and RdDM pathways synergistically mediate the epigenetic silencing of nearly all TEs in the plant genome [ 11 , 13 , 22 ]. A typical TE lifecycle begins from genome invasion to proliferation, degeneration and, eventually, TE senescence [ 77 , 78 ].…”

“…A typical TE lifecycle begins from genome invasion to proliferation, degeneration and, eventually, TE senescence [ 77 , 78 ]. This is further complicated by the TE silencing status, ranging from de novo methylation to maintenance and eventual release from epigenetic silencing [ 13 ]. In addition to the main TEs, TE relics are shorter but need to be silenced as they are preferentially close to protein-coding genes [ 79 ].…”

“…In addition to the main TEs, TE relics are shorter but need to be silenced as they are preferentially close to protein-coding genes [ 79 ]. TE relics are the TEs that have either lost their autonomous transposition ability or the capacity to promote the transposition of other elements [ 13 , 22 ]. The RdDM pathway targets newly inserted TEs, short active TEs, the edges of long active TEs and TE relics enriched in the chromosome arms [ 11 , 55 , 64 ].…”

“…The degree and speed at which these transpire can significantly vary depending on the TE activity and copy number [ 5 ]. Diverse epigenetically derived pathways regulate TE expression, mobility, replication and recombination in plants [ 12 , 13 ]. These pathways repress TE activity with different strategies, such as DNA methylation, histone modifications and RNA interference (RNAi) [ 11 , 12 , 14 , 15 , 16 ].…”

“…Mutations in both the RNA-directed DNA pathway (RdDM) and the DECREASE IN DNA METHYLATION 1 (DDM1) pathways lead to progressive changes in MET1, CMT2 and CMT3 DNA methylation marks [ 12 ]. However, the RdDM and DDM1 roles in TE silencing are regulated by different mechanisms, and their distinct roles may lead to a complex regulatory interplay at the whole-genome scale [ 13 , 22 ]. The RdDM utilises small RNAs to mediate DNA methylation in plants for TE and gene body silencing [ 12 ].…”