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

• Published in: Genome biology and evolution Vol. 10; no. 3; pp. 803 - 815
• Main Authors: Roessler, Kyria, Bousios, Alexandros, Meca, Esteban, Gaut, Brandon S
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 01.03.2018
• Subjects: Arabidopsis - genetics; DNA Methylation - genetics; DNA Transposable Elements - genetics; Epigenesis, Genetic - genetics; Gene Expression Regulation, Plant; Gene Silencing; Genome, Plant - genetics; RNA, Messenger - genetics; RNA, Small Interfering - genetics
• ISSN: 1759-6653; 1759-6653
• DOI: 10.1093/gbe/evy043

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.