Abstract
Transposable elements (TEs) make up the majority of many plant genomes. Their transcription and transposition is controlled through siRNAs and epigenetic marks including DNA methylation. To dissect the interplay of siRNA–mediated regulation and TE evolution, and to examine how TE differences affect nearby gene expression, we investigated genome-wide differences in TEs, siRNAs, and gene expression among three Arabidopsis thaliana accessions. Both TE sequence polymorphisms and presence of linked TEs are positively correlated with intraspecific variation in gene expression. The expression of genes within 2 kb of conserved TEs is more stable than that of genes next to variant TEs harboring sequence polymorphisms. Polymorphism levels of TEs and closely linked adjacent genes are positively correlated as well. We also investigated the distribution of 24-nt-long siRNAs, which mediate TE repression. TEs targeted by uniquely mapping siRNAs are on average farther from coding genes, apparently because they more strongly suppress expression of adjacent genes. Furthermore, siRNAs, and especially uniquely mapping siRNAs, are enriched in TE regions missing in other accessions. Thus, targeting by uniquely mapping siRNAs appears to promote sequence deletions in TEs. Overall, our work indicates that siRNA–targeting of TEs may influence removal of sequences from the genome and hence evolution of gene expression in plants.
Highlights
While transposable elements (TEs) constitute a large fraction of plant, animal and human genomes [1,2,3], their contribution to genome size can change rapidly during evolutionary time
Twenty-four nt long short interfering RNAs (siRNAs) are associated with most Transposable elements (TEs) as part of a ‘double-lock’ mechanism of siRNA-mediated DNA methylation that controls transposition via transcriptional repression, with a reinforcement loop between DNA methylation, histone methylation and siRNAs [reviewed in 9]. siRNAs are a robust proxy for DNA methylation at TEs, with unmethylated TEs generally lacking matching 24 nt siRNAs [10,11,12,13]
The reference coordinates of TEs and genes were projected onto these genome templates, and variation in TEs and genes was determined based on single nucleotide polymorphisms (SNPs), 1 to 3 bp insertions/deletions and larger deletions of 4 to 11,464 bp
Summary
While transposable elements (TEs) constitute a large fraction of plant, animal and human genomes [1,2,3], their contribution to genome size can change rapidly during evolutionary time. TEs have been responsible for two-fold differences in genome size that arose over a few million years or less These rapid fluctuations, which may be due to TEs being either more active or more efficiently deleted in certain species, indicate that control of TEs can differ greatly between closely related plant species [4,5,6,7]. SiRNAtargeted, methylated TEs are, on average, located farther away from expressed genes than TEs that are not strongly methylated or associated with siRNAs [13,15] As expected from this correlation, siRNA-targeted TEs have more effects on nearby gene expression than those without [14,15]
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