Environmental and epigenetic regulation of Rider retrotransposons in tomato

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. Author summary Transposons are major constituents of plant genomes and represent a powerful source of internal genetic and epigenetic variation. For example, domestication of maize has been facilitated by a dramatic change in plant architecture, the consequence of a transposition event. Insertion of transposons near genes often confers quantitative phenotypic variation linked to changes in transcriptional patterns, as documented for blood oranges and grapes. In tomato, the most widely grown fruit crop and model for fleshy fruit biology, occurrences of several beneficial traits related to fruit shape and plant architecture are due to the activity of the transposon family Rider. While Rider represents a unique endogenous source of genetic and epigenetic variation, mechanisms regulating Rider activity remain unexplored. By achieving experimentally-controlled activation of the Rider family, we shed light on the regulation of these transposons by drought stress, signalling by phytohormones, as well as epigenetic pathways. Furthermore, we reveal the presence of Rider-like elements in other economically important crops such as rapeseed, beetroot and quinoa. This suggests that drought-inducible Rider activation could be further harnessed to generate genetic and epigenetic variation for crop breeding, and highlights the potential of transposon-directed mutagenesis for crop improvement.