Modeling Interactions between Transposable Elements and the Plant Epigenetic Response: A Surprising Reliance on Element Retention

Abstract

Transposable elements (TEs) compose the majority of angiosperm DNA. Plants counteract TE activity by silencing them epigenetically. One form of epigenetic silencing requires 21–22 nt small interfering RNAs that act to degrade TE mRNA and may also trigger DNA methylation. DNA methylation is reinforced by a second mechanism, the RNA-dependent DNA methylation (RdDM) pathway. RdDM relies on 24 nt small interfering RNAs and ultimately establishes TEs in a quiescent state. These host factors interact at a systems level, but there have been no system level analyses of their interactions. Here, we define a deterministic model that represents the propagation of active TEs, aspects of the host response and the accumulation of silenced TEs. We describe general properties of the model and also fit it to biological data in order to explore two questions. The first is why two overlapping pathways are maintained, given that both are likely energetically expensive. Under our model, RdDM silenced TEs effectively even when the initiation of silencing was weak. This relationship implies that only a small amount of RNAi is needed to initiate TE silencing, but reinforcement by RdDM is necessary to efficiently counter TE propagation. Second, we investigated the reliance of the host response on rates of TE deletion. The model predicted that low levels of deletion lead to few active TEs, suggesting that silencing is most efficient when methylated TEs are retained in the genome, thereby providing one explanation for the large size of plant genomes.

Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes

“…In addition to this “sheltering” effect of TEs considered as deleterious or quasi neutral elements, it is also possible that those TEs that are retained in the long term have acquired a functional beneficial role for their host genome (being “domesticated”), thus making their removal deleterious in itself. It is unclear how frequent this phenomenon might be, but several clear examples of such domestication have been reported in the literature, including the regulation of stress-response genes by acquisition of response elements carried by some TEs (Capy et al 2000; Makarevitch et al 2015) or the production of siRNAs that trigger the trans-silencing of active relatives and therefore contribute to immune memory (Lisch 2009; Bousios and Gaut 2016; Roessler et al 2018). A recent study however showed that TE exaptation for regulatory function is rare, and is mostly associated with “old” TEs, suggesting a model in which TE-derived sequences are initially repressed, after which a small fraction acquires and retains enhancer activity (Simonti et al 2017).…”

Where the Wild Things Are: Transposable Elements as Drivers of Structural and Functional Variations in the Wheat Genome

“…We suggest that integration site selection together with epigenetic mechanisms leading to equilibrium in TEs copy numbers might explain these interesting phenomena. New insights regarding the underlying mechanisms for TE equilibrium in genomes might arrive from the implementation of mathematical and physical models on experimental data (Roessler et al, 2018;Bourgeois and Boissinot, 2019;Bousios et al, 2020).…”

“…In light of the recent developments in wheat genomics, the examination of new models based on whole genome sequencing, epigenetic, and 3D analysis (Concia et al, 2020) is now technically possible for newly synthesized allopolyploids. Studies of TE dynamics in newly synthesized wheat allopolyploids might deepen our understanding of the effect of perturbation on host: TE dynamics (Roessler et al, 2018) and on the possible effect of the 3D genome organization on TEs insertion sites and propagation across the nucleus (Bousios et al, 2020).…”

Integrating transposable elements in the 3D genome

“…There is a clear gap in the experimental and theoretical work on understanding the impact of genome architecture on integration of TEs. Models of TE amplification dynamics have traditionally been based on populationbased approaches [40], which typically set up systems of (stochastic) ordinary differential equations accounting for generic competing elements during TE expansion [41][42][43]. Few works, instead, have considered the 1D distribution of nucleosomes along the genome in order to predict preferential sites of HIV integration [44].…”