Double-edged sword: The evolutionary consequences of the epigenetic silencing of transposable elements

Abstract

Transposable elements (TEs) are genomic parasites that selfishly replicate at the expense of host fitness. Fifty years of evolutionary studies of TEs have concentrated on the deleterious genetic effects of TEs, such as their effects on disrupting genes and regulatory sequences. However, a flurry of recent work suggests that there is another important source of TEs' harmful effects-epigenetic silencing. Host genomes typically silence TEs by the deposition of repressive epigenetic marks. While this silencing reduces the selfish replication of TEs and should benefit hosts, a picture is emerging that the epigenetic silencing of TEs triggers inadvertent spreading of repressive marks to otherwise expressed neighboring genes, ultimately jeopardizing host fitness. In this Review, we provide a long-overdue overview of the recent genome-wide evidence for the presence and prevalence of TEs' epigenetic effects, highlighting both the similarities and differences across mammals, insects, and plants. We lay out the current understanding of the functional and fitness consequences of TEs' epigenetic effects, and propose possible influences of such effects on the evolution of both hosts and TEs themselves. These unique evolutionary consequences indicate that TEs' epigenetic effect is not only a crucial component of TE biology but could also be a significant contributor to genome function and evolution.

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

“…This observation raises the possibility that dynamic TEs form part of the regulation of genes in the vicinity as cis-regulatory sequences or as a consequence of changes in the chromatin conformation (Le Rouzic, et al 2007;Hollister and Gaut 2009;Huang, et al 2012;Szitenberg, et al 2016;Choi and Lee 2020). Furthermore, this could explain the maintenance of dynamic TEs in V. dahliae, as the TE suppression of these elements could negatively affect the expression levels of neighboring genes, favoring their co-localization.…”

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

“…The effects upon local genomic architecture often are not limited to the TE sequences but can extend, in terms of both DNA methylation and heterochromatin formation, up to several kilobases away. Thus, TE accumulation and/or their silencing may spread into adjacent regions, possibly driving a feedback of extending recombination suppression and the further favoring of TE accumulation in those regions (Willing et al ., 2015; Kent et al ., 2017; Choi & Lee, 2020). In addition, repeat‐induced point mutation (RIP), a mechanism specifically mutating repeated sequences in fungi, also has the consequence to decrease recombination rates, because it decreases similarity between homologous genomic regions containing repeats and because it induces the formation of constitutive heterochromatin (Aramayo & Selker, 2013).…”

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

“…Furthermore, species-specific families of repeats can induce lagging chromatin at cell division during early embryogenesis (when heterochromatin is first established), leading to chromosome mis-segregation and F2 hybrid embryo death [52]. In the context of the refugium hypothesis, it is important to consider that new and active TEs are one of the main targets of heterochromatinization [53,54], and SLCs could be a source for both sex-specific and species-specific heterochromatin differences.…”