Abstract
Transposable elements in crop plants are the powerful drivers of phenotypic variation that has been selected during domestication and breeding programs. In tomato, transpositions of the LTR (long terminal repeat) retrotransposon family Rider have contributed to various phenotypes of agronomical interest, such as fruit shape and colour. However, the mechanisms regulating Rider activity are largely unknown. We have developed a bioinformatics pipeline for the functional annotation of retrotransposons containing LTRs and defined all full-length Rider elements in the tomato genome. Subsequently, we showed that accumulation of Rider transcripts and transposition intermediates in the form of extrachromosomal DNA is triggered by drought stress and relies on abscisic acid signalling. We provide evidence that residual activity of Rider is controlled by epigenetic mechanisms involving siRNAs and the RNA-dependent DNA methylation pathway. Finally, we demonstrate the broad distribution of Rider-like elements in other plant species, including crops. Our work identifies Rider as an environment-responsive element and a potential source of genetic and epigenetic variation in plants.
Highlights
Transposable elements (TEs) replicate and move within host genomes
We determined the distribution of these Rider elements along the tomato chromosomes (Fig 1A) and estimated their age based on sequence divergence between 5’ and 3’ LTRs (Fig 1A)
Despite the relatively low proportion of euchromatic chromosomal regions in the tomato genome [32]), our de novo functional annotation of full-length Rider elements revealed preferential compartmentalization of recent Rider insertions within euchromatin compared to aged insertions
Summary
Transposable elements (TEs) replicate and move within host genomes. Based on their mechanisms of transposition, TEs are either DNA transposons that use a cut-and-paste mechanism or retrotransposons that transpose through an RNA intermediate via a copy-and-paste mechanism [1]. Chromosomal copies of transcriptionally silenced TEs are typically hypermethylated at cytosine residues and are associated with nucleosomes containing histone H3 di-methylated at lysine 9 (H3K9me2) They are targeted by 24-nt small interfering RNAs (24-nt siRNAs) that guide RNA-dependent DNA methylation (RdDM), forming a self-reinforcing silencing loop [6,7,8]. Interference with the activity of the chromatin remodelling factor DECREASE IN DNA METHYLATION 1 (DDM1), as well as various components of the RdDM pathway, leads to the activation of specific subsets of TEs in Arabidopsis These include DNA elements CACTA and MULE, as well as retrotransposons ATGP3, COPIA13, COPIA21, VANDAL21, EVADÉ and DODGER [14,15,16,17]. Loss of OsDDM1 genes in rice results in the transcriptional activation of TE-derived sequences [18]
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