Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding

Abstract

BackgroundRetrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding. To ensure genome integrity several silencing mechanisms have evolved to repress retrotransposon mobility. Even though retrotransposons fully depend on transcriptional activity of the host RNA polymerase II (Pol II) for their mobility, it was so far unclear whether Pol II is directly involved in repressing their activity.ResultsHere we show that plants defective in Pol II activity lose DNA methylation at repeat sequences and produce more extrachromosomal retrotransposon DNA upon stress in Arabidopsis and rice. We demonstrate that combined inhibition of both DNA methylation and Pol II activity leads to a strong stress-dependent mobilization of the heat responsive ONSEN retrotransposon in Arabidopsis seedlings. The progenies of these treated plants contain up to 75 new ONSEN insertions in their genome which are stably inherited over three generations of selfing. Repeated application of heat stress in progeny plants containing increased numbers of ONSEN copies does not result in increased activation of this transposon compared to control lines. Progenies with additional ONSEN copies show a broad panel of environment-dependent phenotypic diversity.ConclusionsWe demonstrate that Pol II acts at the root of transposon silencing. This is important because it suggests that Pol II can regulate the speed of plant evolution by fine-tuning the amplitude of transposon mobility. Our findings show that it is now possible to study induced transposon bursts in plants and unlock their use to induce epigenetic and genetic diversity for crop breeding.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1265-4) contains supplementary material, which is available to authorized users.

Low temperature triggers genome-wide hypermethylation of transposable elements and centromeres in maize

“…Destabilization of the de novo RdDM pathway at the transcriptional level is also observed in our experiment, including this of RNA polymerase II-related genes, and may also participate in reactivating TEs, as observed in Arabidopsis RNA polymerase II (Thieme et al 2017). Further analysis of TE transcription will help decipher whether some TEs are transcriptionally reactivated in our experiment.…”

Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks

“…Another interesting example is the retrotransposon ONSEN in Arabidopsis [56]. Thieme et al [57] showed that following heat stress-dependent mobilization of ONSEN, the progenies of the treated plants contain up to 75 new ONSEN insertions. Progenies with additional ONSEN copies show a broad panel of environment-dependent phenotypic diversity.…”

The diversifying field of plant epigenetics

“…For example, Vítek Latzel found that repeated spraying of established plants with azacytidine reduced methylation in a way that is similar to germinating seeds directly in the chemical, but with fewer side effects. Etienne Bucher (INRA Anger, France) developed an approach to induce a targeted activation of stress‐responsive TEs (called jumping TEs) with a combination of zebularine and alpha‐amanitin treatment (Thieme et al ., ). This approach greatly reduced methylation, and led to an activation of TEs via the inhibition of DNA polymerase II (Pol II).…”